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Supplementary File 5: Written description of the functions of the predicted genes in
the context of LEA gene function.
LEA gene annotated as being "Similar to Heat-shock protein precursor."
(LOC_Os12g32986; Os12g0514500).
The LEA gene annotated as being "Similar to Heat-shock protein precursor."
(LOC_Os12g32986; Os12g0514500) was found to share 17 common promoter motifs
with a gene annotated as “Phosphatidylinositol 3- and 4-kinase, catalytic domain
containing protein" (LOC_Os06g17290; Os06g0283400). These kinases are part of the
Phosphatidylinositol (PI) signaling pathway in plants. This signaling pathway has been
demonstrated to be critical in signal transduction processes such as cell differentiation,
transduction of intracellular signaling molecules, control of cell responses to
environmental factors, regulation of ion-channel gating, energy metabolism and
rearrangement of cytoskeleton (Munnik et al., 1998). These kinases are responsible for
the phosphorylation of intermediates in this pathway resulting in the generation of two
important second messenger molecules, Ins(1,4,5)P3 and diacylglycerol (DAG), which
can stimulate Ca2+ release from internal calcium stores and activate related protein
kinases for regulation of downstream pathways or cellular responses.
The PI 3-kinase (PI3K) and PI 4-kinase (PI4K), synthesize PI 3-phosphate (PI3P) and PI
4-phosphate (PI4P) respectively. The plant PI3K has been suggested to be involved in
root nodule development, plant growth and development, vesicle trafficking from Golgi
to vacuoles, and regulation of the transcriptional process (Hong & Verma, 1994) (Welters
et al., 1994; Bunney et al., 2000) (Kim et al., 2001a). Arabidopsis IP3K (AtIpk2α and
AtIpk2β) is expressed in stem, leaf, stigma, siliques, and fast-growing regions including
root tips and root hairs (Xia et al., 2003) (Xu et al., 2005), which implied that
Arabidopsis IP3K may play important roles in plant growth and development.
Mammalian IP3Ks are involved in a range of processes including brain development
(Mailleux et al., 1991), embryogenesis (Frederick et al., 2005) memory and learning
(Kim et al., 2004), membrane traffic and Ca2+ homoeostasis (Soriano et al., 1997) and
oxidative stress resistance (Monnier et al., 2002).
PI4K catalyzes the production of PI4P, the only known precursor of PI45P, which can be
cleaved into inositol 1,4,5-trisphosphate (IP3) and diacylglycerol by phospholipase
C; therefore, it represents a critical point of regulation of PI-dependent pathways. In
mammalian and yeast cells, PI4Ks also are important for membrane biogenesis and
vesicle trafficking from the ER to the Golgi and the plasma membrane (Roth, 1999). In
yeast, PI4K is required for the maintenance of vacuole morphology, cell wall integrity,
and cytoskeletal organization, particularly during osmotic stress. In plant cells, two PI4K
genes have been cloned (Stevenson et al., 2000). Previous studies have localized enzyme
activity of these PI4Ks to the plasma membrane, nucleus, cytosol, and cytoskeleton
(Drobak et al., 1999), their functions remain poorly understood. In Arabidopsis
protoplasts knock outs in the AtPI4K gene resulted in a 50% reduction in Vesicular
trafficking indicating that PPI species play a role in the turnover of intracellular
membrane compartments (Kim et al., 2001a).
Phosphoinositide metabolism has been shown to play important roles in abscisic acid
(ABA)–induced cytosolic calcium concentration changes and stomatal closing (Gilroy et
al., 1990) (Staxen, I et al., 1999). In addition, endogenous PI monophosphate (PIP)
levels, the product of the PI-kinases, were found to change rapidly in guard cells in
response to treatment with ABA (Lee et al., 1996) and the products of the PI -3 and -4
kinases PI3P and PI4P were found to be involved in inducing ABA-induced stomatal
closure in Vicia faba guard cells by increasing cytosolic Ca levels (Jung et al., 2002).
The LEA gene annotated as being "Similar to Heat-shock protein precursor."
(LOC_Os12g32986; Os12g0514500) was also found to share 18 promoter motifs in
common with the gene annotated as "Transcription factor jumonji, JmjN domain
containing protein" (LOC_Os05g10770; Os05g0196500). The jumonji (jmj) gene was
initially identified using a mouse gene trap approach and is characterized as essentual
nuclear factor involved in mouse embryonic development (Takeuchi, 1997). Jmj has been
shown to play important roles in cardiovascular development, neural tube fusion
processes, hematopoiesis, and liver development in mouse embryos (Jung et al., 2005).
In many diverse species including bacteria, fungi, plants, and animals, there are many
jumonji family proteins. Recently, Jmj protein was found to be a transcriptional
repressor. Several proteins in the jumonji family are involved in transcriptional repression
and/or chromatin regulation (Takeuchi et al., 2006).
Interesting, along with a number of LEA and heat shock encoding genes, a Jumunji class
transcription factor was present in a water stress deficit cDNA library in the peanut plant.
In the peanut plant the expression of a jumunji transcription factor protein was
determined to be upregulated in response to water deficit and the expression of the
homolog of this protein was also found to be induced in water deprived wildtype N.
benthamiana plants. Additionally, inhibition of expression of this Jumonji protein by
virus-induced gene silencing (VIGS) resulted in increased membrane damage following
water deprivation in Nicotiana benthamiana (Senthil-Kumar et al., 2007).
The sequence, secondary-structure and active-site similarities between JmjC domains and
cupins strongly indicate that JmjC domains represent a previously unrecognized branch
of the cupin family with mostly enzymatic functions (Clissold & Ponting, 2001).
Similarities between cupins and several transcription factors had previously been noted
and wer subsequently identified to contain JmjC domains, such as rat testis-specific
protein A (a hairless paralogue) and a DNA-binding protein (ENBP1) from Vicia sativa
(Clissold & Ponting, 2001) (Dunwell, 1998).
This LEA gene also shared 17 promoter motifs with “Ribulose bisphosphate carboxylase,
small chain family protein” (LOC_Os11g19250.1; Os11g0298400). Ribulose-1,5biphosphate carboxylase/oxygenase (Rubisco) is the most abundant protein in nature and
is the primary enzyme in photosynthetic carbon fixation and the likely rate limiting factor
for photosynthesis under light saturated conditions and atmospheric CO2 pressures
(Makino et al., 1985). In the monocot Hordeum vulgare (barley) protein levels of the
small subunit of Rubisco was found to decrease in abundance during seed development
and maturation (Finnie et al., 2002) and in rice seedlings ABA has been shown to reduce
rubisco levels in a time dependent manner (Rakwal & Komatsu, 2004). Further, in rice
leaves mRNA transcripts and the syntheis of rubisco subunits was drastically reduced in
response to cold stress (Hahn & Walbot, 1989). Oxidative conditions have been shown
to cause fragmentation and degredation of Rubisco (Penarrubia & Moreno, 1990) (Ishida
et al., 1999). It has been suggested that ROS may modify Rubisco sulfhydryl groups from
critical cysteine residues whose oxidation renders the enzyme sensitive to proteases
(Penarrubia & Moreno, 1990) (Moreno et al., 1995). Further, in tobacco, both a decrease
in the levels of mRNA encoding the small subunit of Rubisco (Kawaguchi R, 2003), and
a decreased amount of Rubisco protein and have been observed in response to water
stress conditions.
Abscisic acid (ABA) treatment and water stress have been commonly reported to induce
stomatal closure and an inhibition of leaf photosynthesis (Downton et al., 1985)
(Terashima et al., 1988). Evidence indicates that stomatal closure is responsible for the
reduction in photosynthesis following water stress due to the limited CO2 diffusion from
the atmosphere to the site of carboxylation (Chaves & Oliveira, 2004) (Flexas et al.,
2004) .
The decline in intracellular CO2 levels results in the over-reduction of components within
the electron transport chain and the electrons get transferred to oxygen at photosystem I
(PS I). This generates ROS including superoxide, hydrogen peroxide (H2O2) and
hydroxyl radicals (Lorento et al., 1995). Plants need to respond quickly to prevent the
photosynthetic machinery from suffering from irreversible oxidative damage. Since most
studies on drought-induced changes indicate that the amount and activity of rubisco
primarily controls photosynthetic carbon assimilation, the reduction in rubisco levels may
contribute to the shut down of photosynthesis and thus help prevent the generation of
ROS and damage to the photosynthetic machinery during water deprivation.
This LEA gene was also found to share 17 promoter motifs with a gene annotated as
"Peptidase A1, pepsin family protein" (LOC_Os07g34920.1; Os07g0533600). Aspartic
proteinases (APs ) have been extensively studied and characterized and are widely
distributed among vertebrates, plants, yeast, nematodes, parasites, fungi and viruses
(Davies, 1990) (Dunn, 2002). Plant APs are widely distributed in the plant kingdom and
have been extensively detected in monocotyledonous (Asakura et al., 1995) (Sarkkinen et
al., 1992) and dicotyledonous (Hiraiwa et al., 1997) (Mutlu et al., 1998) plants. The
majority of plant APs belongs to the A1 family. In common with other members of the
A1 family, plant APs are active at acidic pH, are specifically inhibited by pepstatin and
have two aspartic acid residues responsible for the catalytic activity (Dunn, 2002). In situ
hybridization demonstrated that A1-protease genes are expressed in many cells of the
seeds and developing seed pods.
Plant APs have been implicated in general protein processing and/or degradation in
numerous organs and processes including senescence, stress responses, programmed cell
death and reproduction (Simoes & Faro, 2004). In situ hybridization demonstrated that
A1-protease genes are expressed in many cells of the seeds and developing seed pods.
Participation of plant APs in storage protein degradation during the mobilization of
reserve proteins in seed germination has been proposed for rice and wheat since the
distribution of APs was co-localised with seed storage proteins (Doi et al., 1980).
Additionally, AP was able to hydrolyse the main wheat storage protein gliadin
(Belozersky et al., 1989). Based on experimental evidence a role for plant APs in
proteolytic processing and maturation of seed storage proteins has also been proposed
(Mutlu et al., 1998; Runeberg-Roos et al., 1994).
This LEA gene was also found to share 17 promoter motifs with a gene annotated as
"DEAD/DEAH box helicase N-terminal domain containing protein”
(LOC_Os07g43980.1; Os07g0633500). DNA repair genes are included among genes
that are induced by abiotic stresses since these types of stresses often result in DNA
damage. Since the stresses affect the cellular gene expression machinery, it is possible
that molecules involved in nucleic acid metabolism including helicases are likely to be
affected (Vashisht & Tuteja, 2006). Most helicases are members of DEAD-box protein
superfamily and play essential roles in basic cellular processes such as DNA replication,
repair, recombination, transcription, ribosome biogenesis and translation initiation
(Matson et al., 1994) (West, 1996). It was proposed that helicases might play an
important role in regulating plant growth and development under stress conditions by
regulating some stress-induced pathways (Vashisht & Tuteja, 2006).
There are reports of abiotic induced induction of DEAD-box helicases in a number of
plant species (Vashisht & Tuteja, 2006). In barley a salt responsive transcript HVD1
(Hordeum vulgare DEAD-box protein), encoding a putative ATP-dependent DEAD-box
RNA helicase was reported to be increased under salt stress, cold stress and ABA
treatment (Nakamura et al., 2004). In Arabidosis plantsa a DEAD-box RNA helicase
was identified to be expressed during cold stress (Seki et al., 2001). In Pea a DNA
helicase 45 (PDH45), was found to be induced in pea seedling in response to high salt
(NaCl) and other abiotic stresses including dehydration, wounding and low temperature
(Sanan-Mishra et al., 2005). The induction of PDH45 transcript was observed to be
induced by ABA, which suggested that the stress effect may be mediated through ABAmediated pathways.
LEA gene “Similar to Dehydrin DHN1 (M3) (RAB-17 protein)”
(LOC_Os11g26570.1; Os11g0451700).
The LEA gene annotated to be “Similar to Dehydrin DHN1 (M3) (RAB-17 protein)” was
found to share 9 promoter motifs with a gene annotated as being “Similar to Heat shock
protein STI (Stress inducible protein) (GmSTI)" (LOC_Os02g43020.1; Os02g0644100)
that contains tetratricopeptide regions (TPR).
This gene was first identified in yeast where its transcript levels were determined to be
induced by heat shock (named STI 1). Additionally, the STI gene product is required for
optimal growth of yeast cells at both low and high temperatures (Nicolet & Craig, 1989).
In soybean, a protein named GmSTI was found too share high sequence identity to the
yeast STI1 stress-inducible protein which has a TPR elements (Hernandez et al., 1995).
The GmSTI gene was found to be heat-inducible and was the first evidence for the
existence of plant genes coding for proteins which belong to the TPR family. STI1, IEF
SSP 3521 and GMSTI all contain a number of 34-aa TPR which are proposed to be
important for intra- and intermolecular protein interactions (Lamb et al., 1995). In yeast
and humans both STI1 and IEF SSP 3521 have been identified as components of
multiprotein chaperone complexes involving the heat shock proteins, Hsp70 and Hsp90
(Smith et al., 1993) (Chang & Lindquist, 1994) (Schumacher et al., 1994) and evidence
indicates that STI may play a role in mediating the heat shock response of some HSP70
genes (Nicolet & Craig, 1989). The STI proteins are also referred to as Hop (hsp70- and
hsp90-organizing protein) based on their functions as adapter or cochaperone proteins
that can bind to both hsp90 and hsp70 simultaneously, bringing them into close proximity
(Chen & Smith, 1998). The Arabidopsis genome sequence has been examined for Hoplike sequences, and three genes encoding Hop-like proteins were identified (Krishna &
Gloor, 2001), confirming the presence of a multigene family for this protein in plants.
The HSP proteins are a stereotypical set of proteins that have been shown to be
synthesized in response to increased temperature in cells from nearly every organism thus
far tested (Nicolet & Craig, 1989). The synthesis of these proteins is also induced by a
number of other stress conditions indicating that they are involved in general cellular
stress responses. The most abundant and highly conserved of the heat shock proteins
found after a temperature increase is called hsp70. Analysis of thermoregulation of
HSP70 genes, and of other heat shock genes from a number of organisms, has led to the
hypothesis that the primary function of the heat shock proteins is to protect cells from
damage caused by an abrupt shift in environmental conditions. Hsp70 protects cells from
stress by binding partially unfolded proteins preventing protein aggregation and prion
formation (Tutar, 2006). Thus, the identification of a stress inducible cochaperone to
share common promoter motifs with a stress inducible LEA gene is consistent with these
products being co-regulated since they are both involved in protecting cellular
components when adverse conditions are encountered.
This LEA gene was also found to share 9 promoter motifs with a gene annotated as
“Serine/threonine-protein kinase SAPK4 (EC 2.7.1.37) (Osmotic stress/abscisic acidactivated protein kinase 4)." (LOC_Os01g64970.1; Os01g0869900)
The SAPK4 kinase, which is annotated as an osmotic stress/ABA–activated protein
kinase (Kobayashi et al., 2004) belongs too a large group of plant kinases called the
sucrose nonfermenting 1–related protein kinase (SnRK) that were named based on
similarities to the classical SNF1-type kinases from yeast. The SnRKs in turn belong to
a superfamily of calcium-dependent protein kinase (CDPKs)-SnRK which includes seven
types of serine-threonine protein kinases (Hrabak et al., 2003). The SnRKs have been
divided into three subgroups in plants based on domain organisations and they have been
named SnRK1, SnRK2, and SnRK3 (Halford & Hardie, 1998). The SAP4 kinase
belongs to the SnRK2 family and 10 genes that encode SnRK2 family protein kinases
have been identified in the rice genome. These protein kinases were designated SAPK1
through SAPK10 (Kobayashi et al., 2004). In rice SAPK4 has shown to be upregulated
by hyperosmotic stress and ABA. The osmotic and ABA-induced activation of SAPKs
has been shown to mediate phosphorylation of the ABA-induced transcription factor
TRAB1 which in turn binds to ABRE-elements in gene promoters modulating expression
of ABA-regulated genes. Since ABA is known to be critically involved in water
deficiency responses in plants and a know regulator of LEA gene expression the potential
co-regulation of this gene with the LEA gene makes sense.
This LEA protein also shared 9 promoter motifs with a protein annotated as a “STAT
protein family protein” (LOC_Os01g07140; Os01g0165200) with transcription factor and
signal transducer activity. The Signal Transducers and Activators of Transcription
(STAT) family of proteins are known in many non-plant species, and act as intracellular
intermediaries between extracellular ligands and the transcription and activation of genes
(Richards et al., 2000). It has been suggested that STAT proteins are related to GRAS
proteins in plants which are a recently discovered family of plant-specific proteins that
play important regulatory roles in diverse aspects of plant development (Richards et al.,
2000). These proteins were identified to share similarities in their domain structures
rather than complete amino acid sequences. Several of the motifs present in the GRAS
proteins suggest that they function as transcription factors, although homology-searching
programs have revealed no significant similarity to any non-plant proteins (Richards et
al., 2000). It is interesting that this annotated STAT protein that shares domain
similarities to GRAS proteins that are involved in plant development shares common
promoter motifs with a LEA gene that is also know to be expressed during seed
development.
This LEA protein also shares 9 promoter motifs with a "Cupin 4 family protein"
(Os04g0659150). The cupin superfamily consists of a functionally diverse family of
proteins that contain a conserved a β-barrel structural core domain (Dunwell et al., 2000).
They were originally discovered using a conserved motif that was present in germin
proteins from higher plants which are unusual thermostable proteins produced during the
early phase of germination in wheat embryos (Dunwell, 2003). This similarity was then
extended to a group of germin-like proteins (GLPs) in dicotyledonous plants, and
subsequent comparative sequence analysis noted a much weaker, though consistent, level
of similarity to the major globulin storage proteins such as the desiccation-tolerant
vicilins and legumins from plant seeds and spores. Although members of the cupin
superfamily posses very low levels of overall sequence identity, members have highly
conserved structures and include; enzymes as well as proteins that bind different sugars
(Rocha et al., 2007), transcription factors, seed storage proteins, auxin binding proteins
and stress-related proteins such as spherulins and germin-like proteins (Dunwell et al.,
2000; Dunwell et al., 2001). Many of these functions involve aspects of sugar
metabolism and cell wall synthesis and are concerned with responses to abiotic stress
such as heat, desiccation, or starvation. Cupins have been found in a variety of different
organisms that inhabit a spectrum of extreme environments including thermophilic
bacteria, plants and animals (Dunwell, 1998). It has been proposed that the presence of
the conserved β-barrel structure in both pro- and eukaryotic cupin proteins provides a
stable architecture that allows these proteins to survive and remain active under an array
of extreme environmental conditions (Thompson & Eisenberg, 1999). Some members of
the cupin family including the germins and GLPs have been shown to be expressed
during embryogenesis (Domon et al., 1995; Neutelings et al., 1998) and in response to a
range of biotic (Thordahl-Christensen et al., 1997) and abiotic stresses, including salt
(Hurkman & Tanaka, 1996) and temperature variation (Vallelian-Bindschedler et al.,
1998). Additionally, the germins and GLPs, contain conserved enzymatic domains that
posses superoxide dismutase activity that is thought to function in protecting plants from
oxidative stresses that are induced by various biotic and abiotic stresses (Khuri et al.,
2001). Similarly, some LEA proteins have also been found to have anti-oxidant
properties and function to reduce oxidative stress in dehydrating cells (Hara et al., 2004).
Thus, although the function of this predicted “cupin 4” annotated gene is not know, the
identification of a thermally stable cupin that can maintain function in extreme stress
conditions and shares a high number of potential regulatory motifs with four different
LEA genes that are induced in response to abiotic stresses including temperature
variations is consistent with this protein being co-regulated with LEA gene expression.
This LEA gene was also found to share 9 promoter motifs with a gene annotated as being
“similar to Avr9/Cf-9 induced kinase 1” (LOC_Os02g53750; Os02g0777800). The
Avr9/Cf-9 gene encodes type I transmembrane glycoproteins carrying extracytoplasmic
Leu-rich repeats (LRRs), a single pass membrane-spanning region, and a short
cytoplasmic domain that has no similarity to known signaling domains (Thomas et al.,
1998). These proteins are involved in R-gene mediated resistance to virulent pathogens.
The recognition of a Avr9 race-specific elicitor in Cf-9-expressing solanaceous plants,
was found to induce rapid changes in ion flux (Piedras et al., 1998; Blatt et al., 1999),
the production of ROS (Piedras et al., 1998), the activation of the mitogen activated
protein kinases (MAPKs) such as wound inducible protein kinase (WIPK) and salicylic
acid-inducible protein kinase (SIPK) (Romeis et al., 2000), and the activation of calciumdependent protein kinases(Romeis et al., 2001). Additionally, a gene with a similar
annotation, termed “Avr9/Cf-9 rapidly elicited protein”, was found to be induced by
salinity stress in the salt-tolerant rice genotype FL478 (Walia et al., 2005).
LEA gene “Seed maturation protein domain containing protein, category III”
(LOC_Os03g53610.1, Os03g0747400).
The above LEA gene shares 27 promoter motifs with a gene annotated as being a ‘FAR1
domain containing protein, category III” (LOC_Os02g33750.1, LOC_Os02g33750.2,
Os02g0542200) that is involved in transcription factor activity. It has been shown that
FHY3, together with FAR1, define a key role in a signaling network underlying phyAmediated FR light responses (Wang & Deng, 2002). Hudson(Hudson et al., 2003)
demonstrated that the FAR1 protein is capable of activating transcription in Arabidopsis,
indicating that it may define a type of transcriptional regulator specific requirement for
FAR1 in phyA signal transduction.
The above LEA gene also shares 27 promoter motifs in common with a protein annotated
as being “Similar to Dual-specific kinase DSK1, category II” (LOC_Os01g65940.1,
LOC_Os01g65940.2, Os01g0881966) that is involved in protein kinase activity. Dual
specificity protein kinases have been reported in Arabidopsis (Ali et al., 1994) and
soybean (Feng et al., 1993). Kiegerl (Kiegerl et al., 2000) demonstrated that the saltinduced activation of SIMK (salt stress induced mitogen-activated protein kinases) was
mediated by the dual-specificity protein kinase (SIMKK). Further, Cardinale (Cardinale
et al., 2002) showed that plants respond to biotic and abiotic stresses by inducing
overlapping sets of mitogen-activated protein kinases (MAPKs) and response genes. In
addition, Rudrabhatla and Rajasekharan (Rudrabhatla & Rajasekharan, 2002) reported
the involvement of a non-MAP kinase cascade that involved a dual-specificity kinase,
Ser/Thr/Tyr (STY) kinase, which is distinct from other kinases, involved in abiotic stress
response
and
seed
development.
These
authors
also
demonstrated
that
Serine/threonine/tyrosine (STY) protein kinase from peanut is developmentally regulated
and is induced by abiotic stresses.
This LEA gene also shared 27 common promoter motifs with a protein being annotated
as being ‘Similar to 26s proteasome subunit RPN3a, categoty II” (LOC_Os08g43640;
Os08g0550100) involved in binding activity. The 26 S proteasome is a multisubunit
protease complex. It is responsible for degrading a wide range of intracelular proteins in
eukaryotes, especially those modified with polyubiquitin chains (Yang et al., 2004b). In
Arabidopsis, RPN12a is part of 26S proteasome and it controls the stability of one or
more of the factors involved in cytokinin regulation (Smalle et al., 2002). Further, Zang
and Komatsu (Zang & Komatsu, 2007) have demonstrated the response of a 26S
proteasome regulatory subunit to only osmotic stress in rice. In addition, (Cho et al.,
2006) have shown several possibilities of its involvement in a subset of physiological
responses to counteract dehydration and high-salinity stresses in transgenic Arabidopsis
seedlings.
This LEA gene also shared 27 common promoter motifs with a protein being annotated
as being ‘Peptidase A1, pepsin family protein, category III” (LOC_Os07g34920.1,
Os07g0533600) involved in pepsin A activity.
Peptidase family A1 contains
endopeptidases, most of which are most active at acidic pH. They contain peptidases that
were known as 'acid proteinases' or 'carboxyl proteinases'. Aspartic proteinases of the A1
family are widely distributed among plant species (Dunn, 2002). They are most active at
acidic pH (Simoes & Faro, 2004). Although their biological functions have not been
completely established, there is evidence of their involvement in protein processing or
degradation under different conditions and in different stages of plant development. The
majority of plant APs belongs to the A1 family, together with pepsin-like enzymes from
many different origins. In addition, there is evidence that it may function in late autolysis
of plant cells (Egas et al., 2000).
LEA gene annotated as being being “Late embryogenesis abundant (LEA) group 1
family protein category III” (LOC_Os04g49980.1, Os04g0589800).
The above LEA gene was found to share 21 promoter motifs in common with a protein
annotated as “Plant lipid transfer protein/ par allergen family protein, category III’
(LOC_Os08g03690.1, Os08g0131200) involved in lipid transport. Lipid transfer proteins
(LTPs) are ubiquitous plant lipid-binding proteins. They are associated with multiple
developmental and stress responses in plants (Bakan et al., 2006). Strong accumulation of
VULTP mRNA [LTP from cowpea (Vigna unguiculata)] has also been shown during
seed development (Carvalho et al., 2006). In addition, VULTP gene shows differential
expression in response to different stress. Liu and Lin (Liu & Lin, 2003) suggested that
Vrltps (Vigna radiata lipid transfer proteins) are specific to growing shoot tissues, and
may play an important role in plant acclimation to water stress. Further, high-temperature
stress causes abortive male reproductive development in many plant species. Microarray
analysis indicated that a series of genes, including a meiosis-specific gene Asy1 and
anther-specific lipid transfer protein genes, was up-regulated at an earlier stage in
developing anther cells in barley plant under high-temperature conditions (Oshino et al.,
2007).
This LEA gene was also found to share 21 promoter motifs in common with the
previously discussed protein annotated as being “Similar to Dual-specific kinase DSK1,
category II” (LOC_Os01g65940.1, LOC_Os01g65940.2, Os01g0881966)
LEA gene annotated as being “Drought induced, 19 family protein, category III”
(LOC_Os05g28980; Os05g0358000).
This LEA gene was found to share 16 common promoter motifs with a protein annotated
as a “Lipolytic enzyme, G-D-S-L family protein, category III” (LOC_Os05g11950,
Os05g0210100) involved in lipid metabolism. GDSL lipases play an important role in
plant growth and development (Ling et al., 2006). BnLIP2 probably plays an important
role in rapeseed germination, morphogenesis and flowering. The patatin, a potato tuber
storage protein is shown to have a lipolytic activity (Matos et al., 2001). They proposed
possible involvement of lipolytic enzyme VUPAT1 (Vigna unguiculata) in droughtinduced galactolipid degradation. In addition, it was demonstrated that AtLTL1 encodes a
putative lipase of the GDSL-motif family, which includes a very large number of plant
proteins. In Arabidopsis, AtLTL1 expression is rapidly induced by LiCl or NaCl (Naranjo
et al., 2006). It has also been observed that overexpression of AtLTL1 increases salt
tolerance in transgenic Arabidopsis plants, compared to non-transformed controls. It
allows germination of seeds in the presence of toxic concentrations of LiCl and NaCl,
and stimulates vegetative growth, flowering and seed set in the presence of NaCl.
This LEA gene also shared 15 common promoter motifs with a protein being annotated
as “Harpin-induced 1 domain containing protein, category III” (LOC_Os12g06260.1,
Os12g0159600) involved in harpin induction. It was suggested that HrpN(ea) induced
different signaling pathways in Arabidopsis(Reboutier et al., 2007). Further, it was
reported that HrpN activates abscisic acid (ABA) signalling to induce drought tolerance
(DT) in Arabidopsis thaliana plants grown with water stress(Dong et al., 2005). Wild
type plants sprayed with HrpN promoted stomatal closure decreased leaf transpiration
rate, increased moisture and proline levels in leaves, and alleviated extents of damage to
cell membranes and plant drought symptoms caused by water deficiency. In plants
treated with HrpN, ABA levels increased; expression of several ABA-signalling
regulatory genes and the important effector gene rd29B was induced or enhanced.
This LEA gene also shared 19 common promoter motifs with a protein being annotated
as being “Similar to Pathogenesis related protein 5 precursor (PR-5), category II”
(LOC_Os04g59370.1, Os04g0689900) involved in thaumatin pathogenesis related
activity. The family of pathogenesis-related (PR) 5 proteins are classified as thaumatins,
osmotins, and inhibitors of alpha-amylase or trypsin (Thompson et al., 2006). They have
diverse functions and some of them are involved in the acquired systemic resistance and
response to biotic stress. Many of the pathogenesis-related group 5 (PR5) plant proteins
have antimicrobial activity (Shatters, Jr. et al., 2006). Further, bioassays of transgenic
plants with the sheath blight pathogen, Rhizoctonia solani, indicated that over-expression
of TLP enhanced resistance compared to control plants (Datta et al., 1999). Additionally,
there are reports of the PR proteins also being upregulated by abiotic stresses such as
osmotic challenges.
This LEA gene also shared 19 common promoter motifs with a protein being annotated
as
being
a
“Cytidylyltransferase
domain
containing
protein,
category
III”
(LOC_Os11g03050.1, Os11g0123400) involved in biosynthesis and cytidylyltransferase
activity. Evidence from studies in animals, as well as in plants, suggests that the
intermediate step catalysed by cholinephosphate cytidylyltransferase (CPCT) during
phosphatidylcholine synthesis through CDP-choline pathway has a major control in
carbon flux to this lipid (Jones et al., 1998). Inatsugi (Inatsugi et al., 2002) observed that
Arabidopsis utilizes two distinct CCT isozymes (phosphorylcholine cytidylyltransferase )
for CDP-choline synthesis during cold acclimation. In addition, experiments conducted
by reverse transcriptase-PCR indicated that the expression of A. thaliana CCT is
regulated by temperature. The expression level of CCT increased during low temperature
treatment and returned to original level upon transfer to 22degrees C (Choi et al., 2001).
This LEA gene also shared 15 common promoter motifs with a protein being annotated
as being a “Curculin-like (mannose-binding) lectin domain containing protein category
III” (LOC_Os05g07450.1, Os05g0166600) involved in protein kinase. Curculin from
Curculigo latifolia is a unique sweet protein that exhibits both sweet-tasting and tastemodifying activities (Suzuki et al., 2004). These proteins often maintain possible
mannose binding sites.
LEA gene annotated as being “Embryonic abundant protein 1, category I”
(LOC_Os05g28210.1, Os05g0349800).
This LEA gene shared 19 common promoter motifs with a protein being annotated as a
“Homeodomain-like
containing
protein,
category
III”,
(LOC_Os02g07800.1,
Os02g0174300) involved in Myb, DNA-binding. In Arabidopsis thaliana, the ZFHD
recognition sequence (ZFHDRS) and NAC recognition sequence (NACRS) play an
important role in the dehydration-inducible expression of the Arabidopsis thaliana early
responsive to dehydration stress (ERD1) gene (Tran et al., 2007). In addition, microarray
analysis of transgenic plants over-expressing ZFHD1 revealed that several stressinducible genes were up regulated in the transgenic plants. It was observed that both
AtMYC2 and AtMYB2 proteins function as transcriptional activators in ABA-inducible
gene expression under drought stress in plants(Abe et al., 2003).
This LEA gene shared 19 common promoter motifs with a protein being annotated as
“2OG-Fe
(II)
oxygenase
domain
containing
protein,
category
III”
(LOC_Os06g08023.1,LOC_Os06g07923.2, Os06g0176500) involved in 2OG-Fe(II)
oxygenase activity.
Flavonol synthase was classified as a 2-oxoglutarate-dependent
dioxygenase converting natural (2R,3R)-dihydroflavonols (Lukacin et al., 2003). During
the biosynthesis of the tricyclic flavonoid natural products in plants, oxidative
modifications to the central C-ring are catalysed by Fe(ii) and 2-oxoglutarate dependent
oxygenases (Welford et al., 2005).
This LEA gene shared 19 common promoter motifs with a protein being annotated as a
“Heavy metal transport/detoxification domain containing protein, category III”
(LOC_Os02g57360.1, Os02g0819000) involved in metal ion transport. A heavy metal
transporter cDNA, ZNT1, was shown to mediate high-affinity Zn2+ uptake as well as lowaffinity Cd2+ uptake. It was found that this transporter is expressed at very high levels in
roots and shoots of the hyperaccumulator (Pence et al., 2000). In Arabidopsis, AtHMA4
plays an important role in metal detoxification at higher metal concentrations (Mills et
al., 2005). In addition, it was demonstrated that CdI19 plays an important role in the
maintenance of heavy metal homeostasis and also in detoxification(Suzuki et al., 2002).
Further, Roosens(Roosens et al., 2005) has shown that plant metallothioneins (MTs) are
extremely diverse in function and are involved in metal homeostasis or detoxification.
AtATM3, an ATP-binding cassette transporter of Arabidopsis, is a mitochondrial protein
involved in the biogenesis of iron-sulfur clusters and iron homeostasis in plants (Kim et
al., 2006a). Their research finding show that AtATM3 contributes to Cd resistance and it
may mediate transport of glutamine synthetase-conjugated Cd(II) across the
mitochondrial membrane.
LEA gene annotated as being “Similar to Cor14 b protein precursor, category II”
LOC_Os04g52110.1, Os04g0610600).
This LEA gene shared 21 common promoter motifs with a protein being annotated as a
“Glycosyl
transferase,
family
8
protein,
category
III”
(LOC_Os03g08600;
Os03g0184300) involved in carbohydrate biosynthesis. This family of protein includes
enzymes involved in the synthesis of plant cell walls (Lao et al., 2003). In addition,
Bouton (Bouton et al., 2002) demonstrated the possible involvement of a
glycosyltransferase of this family in the synthesis of pectic polysaccharides.
This LEA gene shared 21 common promoter motifs with a protein being annotated as a
“Peptidase M24A, methionine amino peptidase, subfamily 1 protein,category III”
(LOC_Os04g52100.1, Os04g0610500) involved in methionyl aminotransferase activity
and proteolysis. A cellular requirement for (methionine amino peptidase) MetAP activity
is likely due to dysfunction of MetAP substrates that require methionine removal for
proper protein function (Dummitt et al., 2005). Ross(Ross et al., 2005) have showed that
a minimal level of cytoplasmic MAP is required for normal development.
Late embryogenesis abundant protein (LOC_Os02g15250; Os02g0250600).
This LEA gene (Os02g0250600) has also been annotated as carbohydrate kinase
IPR002173 (Gramene). Carbohydrate kinases are involved in phosphorylation of sugars.
There is differential expression of UDP glucose phosphorylases during cold stress in
Populus (Meng et al., 2007). The overexpression of UDP glucose phosphorylase and
sucrose synthase have resulted in altered plant growth and metabolism in transgenic
tobacco plants (Coleman et al., 2006).
This LEA protein shares 19 common promoter motifs with a gene annotated as a
"Conserved hypothetical protein"(LOC_Os07g26210; Os07g0444000). that has been
annotated as a “phosphoenolpyruvate-dependent sugar phosphotransferase system”
GO:0009401 (Gramene). These proteins have been shown to be involved in sugar
transport in bacterial systems and phosphorylation of the enzymes is very important for
sugar transportation (Postma & Stock, 1980). Sugar has been implicated as an important
molecule in conferring desiccation tolerance. The importance of these proteins in enteric
bacteria has been reported (Mitchell, 1985). However such proteins have not been
identified from eukaryotic genomes which have been published (Barabote & Saier, Jr.,
2005).
The LEA protein also has 18 common promoter motifs with a gene annotated as
“Peptidoglycan-binding
LysM
domain
containing
protein”
(Os10g0524300;
LOC_Os10g38040.1). LysM Type Receptor-like Kinases form a distinct family in plants
whose function is not clearly understood (Zhang et al., 2007). However, LysM domains
of Medicago truncatula NFP protein was shown to be involved in Nod factor perception
(Mulder et al., 2006). LysM receptor kinases have been shown to regulate nod factor
induced infection (Limpens et al., 2003) and legume perception of rhizobial signals
(Madsen et al., 2003).
The LEA protein also has 17 common promoter motifs with a gene annotated as "Zinc
finger, C2H2-type domain containing protein." (Os10g0486300; LOC_Os10g34500.1).
A C2H2 type zinc finger protein has been reported to be involved in salt tolerance in rice
plants (Huang et al., 2007). SGR5, a C2H2-type zinc finger protein, was shown to be
involved in early events of gravitropism in Arabidopsis inflorescence stems (Morita et
al., 2006). SUF4, encoding a C2H2-Type zinc finger protein, represses flowering by
transcriptional activation of Arabidopsis FLOWERING LOCUS C (Kim et al., 2006b).
Another C2H2 type zinc finger protein is reported to be transiently expressed during cold
in rice (Huang et al., 2005). SCOF1, a zinc finger protein increases cold tolerance in
soyabean (Kim et al., 2001b). Similar proteins are also expressed during water stress in
Arabidopsis (Sakamoto et al., 2000).
The LEA protein also has 17 common promoter motifs with a gene annotated as a “No
apical
meristem
(NAM)
domain
containing
protein”
(Os10g0359500;
LOC_Os10g21560.1). Rice has a large family of NAC genes which includes the NAM
proteins and these proteins are important developmentally (Kikuchi et al., 2000).
Another protein ONAC300, a novel member of the NAC family is expressed at very
early developmental stages in the shoot, root and flower, as well as in the mature phloem
of vascular tissues in rice (Kusano et al., 2005).
The LEA protein also has 17 common promoter motifs with a gene annotated as a
"Citrate transporter family protein" (Os09g0109800; LOC_Os09g02214). Citrate
transporters play a critical role in Al-stimulated citrate efflux in rice bean (Yang et al.,
2006). Citrus sinensis citrate transporter 1 CsCit1 encoding a novel vacuolar
citrate/symporter is able to mediate the electroneutral co-transport of H(+) and citrate
ions (Shimada et al., 2006). Citrate carriers from mitochondria have been identified in
Maize plants (Genchi et al., 1999).
The LEA protein also has 17 common promoter motifs with a gene annotated as Histone
H3 (Os06g0159501; LOC_Os06g06460) involved in chromosome organization and
biogenesis and nucleosome assembly. Two histone chaperones have been shown to be
essential for post embryonic root growth in Arabidopsis (Zhu et al., 2006). A Histone
deacetylase from Arabidopsis was shown to be involved in abiotic stress response and is
regulator of abscissic acid response (Sridha & Wu, 2006). The role of a histone protein in
water stress has been studied in tomato (Scippa et al., 2000; Scippa et al., 2004). A pea
nuclear protein, p16 is expressed during seed dessication. The authors hypothesise that
the function of p16 may be related to the protection of chromatin structure against
desiccation during seed development (Castillo et al., 2000).
The LEA protein also has 17 common promoter motifs with a gene annotated as a
"Protein kinase domain containing protein" (Os05g0323800; LOC_Os05g25840;)
involved in phosphorylation of amino acids of proteins. Sugar signalling during abiotic
stress has signal transduction cascades that involve mitogen-activated protein kinases
(Gupta & Kaur, 2005).Two new maize bZIP transcription factors, EmBP-2 and ZmBZ-1
are involved in the expression of abscisic acid inducible genes such as rab28 and their
activity is modulated by ABA and by phosphorylation. ZmBZ-1 is abscisic acid-inducible
and accumulates during late embryogenesis. EmBP-2 and ZmBZ-1 are phosphorylated by
protein kinase CK2 and phosphorylation alters their DNA binding properties (Nieva et
al., 2005). MAPK cascades play an important role in plant stress responses(Nakagami et
al., 2005).
The LEA protein also has 17 common promoter motifs with a gene annotated as an
"Inositol polyphosphate related phosphatase domain containing protein" (Os03g0626500;
LOC_Os03g42810). Phosphatidylinositol signaling pathway is involved in multiple plant
responses to hormone and abiotic treatments as shown by expression studies (Lin et al.,
2004).
The LEA protein also has 17 common promoter motifs with a gene annotated as a
"Peptidase S14, ClpP family protein" (Os03g0411500; LOC_Os03g29810). In
Arabidopsis ClpR1 is suggested to be involved in plastid development (Sjogren et al.,
2006; Koussevitzky et al., 2007).
The LEA protein also has 17 common promoter motifs with a gene annotated as a "Zinc
finger, CCCH-type domain containing protein" (Os01g0174600; LOC_Os01g07930).
CCCH-type zinc finger proteins bind to AU-rich regions of RNA and are regulatory
(Brown, 2005). A CCCH-type zinc finger protein, OsDOS, localized in the nucleus is
shown to be involved in delaying leaf senescence in rice (Kong et al., 2006). HUA1
another CCCH-type zinc finger protein from Arabidopsis is a regulator of stamen and
carpel identities and is RNA binding (Li et al., 2001).
The LEA protein also has 17 common promoter motifs with a gene annotated as
LOC_Os01g04110 "Surfeit locus 5 family protein" (Os01g0132700; LOC_Os01g04110).
These proteins have been reported from animal systems and are thought to be
housekeeping genes. The Surfeit gene homologs are quite wide spread in invertebrate
genomes (Armes & Fried, 1996). Five of the SURF genes are tightly clustered and
conserved during evolutionary process (Colombo et al., 1992).
The LEA gene annotated as being “Late embryogenesis abundant (LEA) group 1
family protein” (LOC_Os06g21910.1; Os06g0324400).
The LEA gene annotated as being “Late embryogenesis abundant (LEA) group 1 family
protein” (LOC_Os06g21910.1; Os06g0324400) was found to share 22 promoter motifs
with a protein annotated as being" ATPase, P-type, K/Mg/Cd/Cu/Zn/Na/Ca/Na/Htransporter family protein” (LOC_Os07g12900.1; Os07g0232900).
Among several families of proteins involved in heavy metal transport across cellular
membranes is the type 1B subfamily of the P-type ATPases. The P-type ATPases
transport a variety of cations across cell membranes, and the superfamily can be divided
into many subfamilies on the basis of both sequence and functional similarities (Axelsen
& Palmgren, 1998). Type 1B heavy metal–transporting P-type ATPases have been
identified in prokaryotes and eukaryotes, including yeasts, insects, plants, and mammals.
In prokaryotes, the metal substrates of these transporters include Cu, Zn, Cd, Ag, Pb, and
Co ions, and in most cases, individual transporters confer tolerance to the metal ion
substrate through acting as an efflux pump (Rensing et al., 1999).
In plants and fungi the major ion pumps in the plasma membrane are P-type H+-ATPase
(proton pumps) (Morsomme & Boutry, 2000; Portillo, 2000). These pumps function to
energize the plasma membrane for nutrient uptake and signal transduction by generating
an electrical potential and chemical gradient across the membrane. Biochemical and
structural evidence indicates that proton pumps form multimeric structures (Scarborough,
2000). In plants, it is expected that proton pumps are also essential, although similar
analyses have not yet been reported. In addition, small changes in pump activity are
thought to be important for many aspects of plant growth and development. For example,
many studies have found changes in pump activity in response to a variety of
environmental conditions, including salt stress, hormones, light, and pathogens
(Assmann, 1993) (Mathieu et al., 1994) (Niu et al., 1993)
(Portillo, 2000). The
underlying mechanisms of action are not yet elucidated, but it has been observed that in
tobacco, the cosuppression of at least one H+ resulted in pleiotropic effects on sucrose
translocation, stomatal opening, growth, and fertility (Zhao et al., 2000). The gene
LOC_Os07g12900.1 being a P-type ATPase might have a role in stress response.
This LEA protein was also found to share 22 promoter motifs with a protein annotated as
being"
Similar
to
F22D16.14
protein
(RING
finger
family
protein)”
(LOC_Os07g47590.1; Os07g0673200). The F22D16.14 protein is a synonym used for
Arabidopsis gene AT1G02860.1 (http://www.arabidopsis.org), which has zinc finer
domain and has been linked with protein and zinc ion binding. In a recently published
study (April, 2007), the F22D16 clone was studied and the mutant of gene named NLA
(nitrogen limitation adaptation) was isolated and was assigned a role in adaptation
towards nitrogen deficiency.
The major inorganic nitrogen compound available to crop plants under most soil
conditions is nitrate, which is required in great abundance for optimal plant growth and
development (Crawford, 1995). It has been shown that when nitrate is insufficient, plants
can develop a set of adaptive responses to the nitrogen-limited growth condition (Diaz et
al., 2006) (Ding et al., 2005). Accumulating anthocyanin and reducing photosynthesis are
two important adaptive responses to nitrogen limitation, and are controlled by multiple
QTLs in Arabidopsis (Diaz et al., 2006).
In Arabidopsis, functional characterization of some RING-containing proteins such as
COP1 and SINATA5 suggests that the biological function of the RING domain is to
participate in ubiquitin-dependent protein degradation (Moon et al., 2004), and thus plays
a central and essential role in eukaryotic cellular regulation (Glickman & Ciechanover,
2002). Stone et al. (Stone et al., 2005) reported that the Arabidopsis genome encodes 469
putative RING-containing proteins, which can be grouped into eight types, and NLA
belongs to the RING-HCa type.
Based upon their analysis, Peng (Peng et al., 2007) proposed that NLA may be involved
in the ubiquitination-mediated degradation or modification of substrate protein(s), which
may function as the key negative regulator(s) in the nitrogen limitation sensing or
signalling pathway. In the nla mutant, the negative regulator(s) would not be degraded or
modified properly by the nla protein which lacks the RING domain. Consequently, the
nla plants grown with limited nitrogen nutrient cannot sense or signal the nitrogenlimiting conditions, and fail to develop the essential adaptive responses to nitrogen
limitation. The above study shows genes having RING finger domain are involved in
stress responses and the predicted gene might be assigned a role in stress response.
This LEA gene was also found to share 22 promoter motifs with a protein annotated as
being" Amino acid/polyamine transporter II family protein” (LOC_Os06g42720;
Os06g0633800). For amino acid transporters, a wide range of genes has been cloned
from higher plants which are divided into two major families: the amino acid transporter
family ATF and the amino acid-polyamine-choline transporter family APC (Williams &
Miller, 2001). The APC superfamily of transport proteins includes members that function
as solute/cation symporters and solute/solute antiporters. They occur in bacteria, archaea,
yeast, fungi, unicellular eukaryotic protists, slime molds, plants and animals.
In response to salt and osmotic stress, many plants accumulate proline as an
osmoprotective compound to balance the increased osmotic potential (Adams et al.,
1998). Proline is synthesized de novo from glutamate (Hasegawa et al., 2000) indicating
an increased nitrogen requirement in salt-stressed plants. Thus, maintenance of N
homeostasis by salt-dependent regulation of nitrogen and amino acid uptake and transport
systems in salt-stressed plants is a likely requirement. The amino acid transporters
McAAT1 and McAAT2 in Mesembryanthemum crystallinum L. were found to be involved
in stress responses. McAAT2 was abundant in most cell types in mature roots and
McAAT1 in the mesophyll and cells neighbouring xylem vessels in leaves. In response to
salt stress, expression of McAAT2 was stimulated in the root vasculature and McAAT1
signals increased in the leaf phloem. Growth of yeast mutants deficient in histidine
uptake was restored by McAAT2 whereas both McAAT1 and McAAT2 complemented a
yeast mutant carrying a defect in proline uptake (Popova et al., 2003).
The coordinated and cell-specific expressional regulation of transporters of these protein
families is involved in the import of nitrogenous compounds into plant roots, its transfer
into the xylem in roots and from the phloem into roots as well as cycling between xylem
and phloem, respectively, thus maintaining nitrogen supply and accumulation of proline
for osmotic adaptation in response to salt stress.
“Seed maturation protein domain containing protein” (LOC_Os06g23350.1;
Os06g0341300)
The LEA gene annotated as being “Seed maturation protein domain containing protein”
(LOC_Os06g23350.1; Os06g0341300) is a Late embryogenesis abundant protein and
was found to share 22 promoter motifs with a protein annotated as being" Similar to
Alanine aminotransferase 2” (LOC_Os09g26380.1; Os09g0433900). In several plant
species, including barley (Hordeum vulgare), corn (Zea mays), Panicum miliaceum, and
M. truncatula (Orzechowski et al., 1999; Ricoult et al., 2005), Alanine aminotransferase
(AlaAT) gene expression and the AlaAT fermentative reaction were stimulated in
hypoxic or anoxic tissues (Bray et al., 2002).
Flooding is one of the adverse environmental factors that severely harm germination,
seedling establishment, and plant development {Subbaiah and Sachs, 2003}. Gases
diffuse approximately 10 000 times more slowly in water than in air; as a consequence,
when soils are saturated with water, the flux of oxygen into plants becomes too slow to
support respiration, resulting in energy deficits and, eventually, death of cells and tissues
in non-adapted plants (Jackson & Armstrong, 1999; Gout et al., 2001). In hypoxic/anoxic
tissues, the pyruvate content increased and glycolytic (glyceraldehyde-3-phosphate
dehydrogenase) and fermentative enzymes [pyruvate decarboxylase (PDC), alcohol
dehydrogenase (ADH) and lactate dehydrogenase (LDH)] are induced as a consequence
of the need for increased glycolysis to compensate for the lower ATP yield due to the
inactivation of oxidative phosphorylation (Sato et al., 2002). Accumulation of pyruvate
under anaerobic conditions may shift the equilibrium of alanine aminotransferases
towards alanine accumulation; a rapid response of plants to anaerobic stress (Stewart &
Larher, 1980).
The role of alanine aminotrasferases in anaerobic stress is well
established and the predicted gene, which is similar to alanine aminotrasferase might also
have a similar role to play in rice under hypoxic conditions.
This LEA gene was also found to share 22 promoter motifs with a protein annotated as
being " Rieske [2Fe-2S] region domain containing protein” (LOC_Os03g59100.1;
Os03g0805700). Rieske (2Fe-2S) domain-containing protein is similar to cell death
suppressor protein lethal leaf spot 1 (Lls1) from maize. The gene, Lls1 from maize
functions as a cell death suppressor (Gray et al., 1997). It was determined that the Lls1
and its known ortholog in Arabidopsis, accelerated cell death 1 (Yang et al., 2004a), are
both genes that encode pheophorbide a oxygenase. Pheophorbide a oxygenase is an
enzyme necessary for the catabolism of chlorophyll b and removal of a phototoxic
intermediate in the pathway of chlorophyll degradation (Pruzinska et al., 2003).
Healthy plants must overcome many barriers to maintain homeostasis especially when
light-harvesting pigments and the generation of oxygen during photosynthesis create a
radical-rich environment (Reinbothe et al., 1996). Failure to remove the red chlorophyll
catabolite (RCC) results in the generation of toxic free radicals which can result in cell
death (Wuthrich et al., 2000) (Mach et al., 2001). The expression of the Lls1 gene in Zea
mays increased transiently upon wounding. This was correlated with the need to quickly
remove chlorophyll in damaged cells and was reflected in the chlorotic phenotype of
many diseased plants (Yang et al., 2004a). Thus, the presence of Rieske [2Fe-2S] region
domain in the predicted protein makes it a candidate for further investigation into its role
in stress response especially in response to wounding.
LEA
gene
annotated
as
being
“Conserved
hypothetical
protein”
(LOC_Os08g01370.1; Os08g0104400).
The
LEA
gene
annotated
as
being
“Conserved
hypothetical
protein”
(LOC_Os08g01370.1; Os08g0104400) is a Late embryogenesis abundant protein and
was found to share 21 promoter motifs with a protein annotated as being “Similar to
ReMembR-H2 protein JR700” (LOC_Os01g48310.1; Os01g0673900).
Animal, yeast, and plant cells have in common an organelle within their secretory
pathways that maintains an acidic pH and functions as a terminal degredative
compartment (Klionsky, 1990). Cells from the three types of organisms share a common
mechanism for delivery of soluble proteins to the lysosome/lytic vacuole: an integral
membrane receptor protein binds ligands at a relatively neutral pH in the Golgi/transGolgi network and delivers them to an endosomal/prevacuolar compartment, where the
presence of an acidic pH causes their release from the receptor protein (Robinson, 1997;
Jiang & Rogers, 1998). Interestingly, however, the three types of cells differ greatly in
the structures and ligand specificities of their lysosomal/vacuolar sorting receptors
(VSRs). The VSRs have receptor-like domains called ReMembR-H2 (for receptor–
transmembrane sequence–RING H2, abbreviated RMR) proteins, which are expressed in
mammals, birds, plants, and Schizosaccharomyces pombe and appear to traffic to
endosomal/prevacuolar compartments; their functions are unknown. The protein BP 80 is
a VSR and carries this domain. The drug Wortmannin has been found to cause a rapid
redistribution of BP80 from the prevacuolar compartment (PVC) to the vacuole in
tobacco (Nicotiana tabacum) leaf protoplasts. Thus, it was found that the overexpression
of wild-type BP80 molecules can restore vacuolar sorting quantitatively during
wortmannin stress (daSilva et al., 2006).
Although the functions of this domain are not very clear, but the protein like BP 80
carrying this domain has been found to react in response to drug response. Thus, this
predicted gene might serve as good target for evaluation as drug stress responsive gene.
This LEA gene was also found to share 20 promoter motifs with a protein annotated as
being
“Similar
to
Exo-1,3-beta-glucanase
precursor”
(LOC_Os01g48310.1;
Os08g0484100). Plants produce a variety of pathogenesis-related (PR) proteins in
response to stress or infection. The largest group of these proteins is the lytic enzymes
which is composed primarily of ß,1-3 glucanases (ßGlu) and chitinases (Chn). The ß-1,3glucanases are abundant, highly regulated enzymes widely distributed in seed-plant
species (Meins et al., 1992; Høj & Fincher, 1995; Simmons CR., 1994). Although the
major interest in ß-1,3-glucanases stems from their possible role in the response of plants
to microbial pathogens, there is strong evidence that these enzymes are also implicated in
diverse physiological and developmental processes in the uninfected plant including cell
division (Fulcher et al., 1976), pollen germination and tube growth (Meikle et al., 1991)
fertilization (Lotan et al., 1989) (Ori et al., 1990) and embryogenesis (Dong & Dunstan,
1997; Helleboid et al., 1998). In general, ßGlu and Chn are induced in plants infected
with viral, bacterial, and fungal pathogens. There is now compelling evidence that ßGlu
and Chn, acting alone and particularly in combination, can help defend plants against
fungus infection. It has been proposed that these glucanohydrolases act in at least two
different ways: directly, by degrading the cell walls of the pathogen; and, indirectly by
promoting the release of cell-wall derived materials that can act as elicitors of defense
reactions (Boller, 1997; Boller, 1995; Bowles, 1990). It is clear from above discussion
that glucanases are expressed in response to stress in plants, thus the predicted protein
being classified as a glucanase precursor can be classified as putative stress responsive
protein.
LEA gene annotated as being
“Similar to Heat-shock protein precursor”
(LOC_Os08g38086.1; Os08g0487800)
The LEA gene annotated as being
“Similar to Heat-shock protein precursor”
(LOC_Os08g38086.1; Os08g0487800) is a Late embryogenesis abundant protein and
was found to share 19 promoter motifs with a protein annotated as being " Protein kinaselike domain containing protein” (LOC_Os08g17320.1; Os08g0275200).
The kinase domain plays a role in cell surface recognition of a pathogen ligand and
subsequent activation of an intracellular defense response. The protein kinases are
activated in response to stressful environmental conditions, including starvation for key
nutrients and are involved in the response to osmotic stress (Maeda et al., 1994) and in
the response to glucose deprivation (Hardie et al., 1998), both in S. cerevisiae. Receptor-
like protein kinases (RLKs) in plants play major roles in cellular processes and stress
responses. A resistance gene, Rpg1, was identified in barley, which encodes a receptor
kinase-like protein with two tandem protein kinase domains, a novel structure for a plant
disease-resistance gene (Brueggeman et al., 2002).The presence of kinase domain points
towards that predicted genes might have a role in stress response.
This LEA gene was also found to share 19 promoter motifs with a protein annotated as
being “Similar to RNA helicase” (LOC_Os07g20580.1; Os07g0301200). RNA helicases
are the enzymes catalyze the structural rearrangements in the RNA structure and are
involved in all cellular processes involving RNA maturation viz., ribosome biogenesis,
RNA splicing, transport, and turnover, transcription, translation initiation, RNAi, RNA
editing, and development. RNA helicase expression or activity is regulated not only with
respect to participation in housekeeping processes such as those mentioned above, but
also in response to changes in specific environmental variables, including temperature,
light, oxygen and osmolarity (Owttrim, 2006).
The allelic Arabidopsis RNA helicase mutants, los4-1 and los4-2/cryophyte, reveal that
the LOS4 RNA helicase is an early regulator of CBF transcription factor expression in
response to plant chilling (Gong et al., 2005; Gong et al., 2002). LOS4 inactivation
renders the plants sensitive to chilling although the two mutants differentially affect the
CBF–COR cold response pathway; los4-1 reduces whereas los4-2 enhances the
expression of CBFs and their downstream target genes. This divergent response is
mediated through a differential effect on nuclear mRNA export that los4-1 inhibits and
los4-2 enhances at low temperature (Gong et al., 2005). This pleiotrophic phenotype
includes germination at temperatures that are generally inhibitory to wild-type seeds and
early flowering. These processes also involve the plant stress hormone, absisic acid
(ABA), to which the los4 mutants are sensitive. Inactivation of the cold responsive LOS4
helicase therefore also affects cellular ability to respond to the plant stress hormone.
Investigation of the effect on germination indicated that LOS4 appears to be required for
the formation of a germination inhibitor, an intriguing observation, as it suggests that
helicase activity is necessary for the formation of a protein that inhibits the environmental
sensing-signal transduction pathway required for germination (Gong et al., 2005). The
LOS4 helicase is therefore important in a range of physiological processes involving plant
development, in addition to or in conjunction with response to low temperature. Genomewide transcript analysis has identified additional Arabidopsis RNA helicase genes whose
expression is cold stress regulated. drh1 was initially observed to be moderately cold
induced (Seki et al., 2001).
This LEA gene was also found to share 19 promoter motifs in common with two different
proteins that are both annotated as being a
protein”
(LOC_Os04g13150.1;
“Cyclin-like F-box domain containing
Os04g0208400
and
LOC_Os02g18640.1;
Os02g0288000). Cyclins are eukaryotic proteins that play an active role in controlling
nuclear cell division cycles (Sayle et al., 2003), and regulate cyclin dependent kinases
(CDKs). Cyclins, together with the p34 (cdc2) or cdk2 kinases, form the Maturation
Promoting Factor (MPF). The F-box domain was first described as a sequence motif
found in cyclin-F that interacts with the protein SKP1 (Bai et al., 1996; Skowyra et al.,
1997). This relatively conserved structural motif is present in numerous proteins and
serves as a link between a target protein and a ubiquitin-conjugating enzyme.
An F-box protein, ORE9, has been found to be involved in the drought stress responses
and ethylene-induced enhanced senescence. This suggests that protein degradation may
play a role in the (Enhanced Disease Resistance1 (EDR1)) EDR1-mediated signal
transduction pathway since ORE9 has been shown to interact with ASK1, a component of
the SCF ubiquitin ligase complex, in vitro (Woo et al., 2001). Thus protein degradation
has been found to play a role in EDR1 regulation of drought stress responses and
ethylene-induced senescence (Tang et al., 2005). In a recently published study, at least 43
F-box protein-encoding genes have been found to be differentially expressed in rice
seedlings subjected to different abiotic stress conditions. F-box protein-encoding genes
displayed specific expression during various stages of panicle and seed development. In
addition, F-box proteins appear to serve as the key components of the machinery involved
in regulating plant growth and development throughout its life cycle and their expression
is influenced by light and abiotic stresses (Jain et al., 2007).
Protein degradation can be part of the normal cellular protein turnover process but can
also play an important role in the control of plant development and plant-microbe
interactions (Hellmann & Estelle, 2002) (Serino & Deng, 2003). Thus, cyclin-like F-box
proteins could be part of a ubiquitin ligase complex involved in signaling via protein
degradation. This explains the direct and indirect involvement of cyclin-like F-box
proteins in stress response.
This LEA gene was also found to share 19 promoter motifs in common with a gene
annotated as being " Similar to MAP kinase kinase” (LOC_Os02g54600.1;
Os02g0787300). In animals and yeast, MAP kinases are involved in differentiation, cell
division, and response to stress. The family of mammalian MAP kinases, including the
SAPK (stress activated protein kinase)/JNK (Jun N-terminal kinase)/p38, is activated by
various types of stress (Galcheva-Gargova et al., 1994; Han et al., 1994; Kyriakis et al.,
1994). Jonak (Jonak et al., 1996) also suggested that a specific MAP kinase pathway is
involved in signaling cold and drought stress in alfalfa plants.
The mitogen-activated protein (MAP) kinase (MAPK) cascades constitute a prominent
example for the cooperation of signaling pathways. Various MAP kinases has been
identified and MAPK 3, 4 and 6 have been linked to diverse stress responses (Nuhse et
al., 2000; Desikan et al., 2001b; Desikan et al., 2001a; Asai et al., 2002). MKP1 has
been associated with genotoxic stress signaling and it also interacts with MPKs 3, 4 and 6
and these have been reported to be involved in salt stress signaling (Mizoguchi et al.,
1996; Ichimura et al., 1998), and a microarray analysis revealed an increased mRNA
level of a Na+/H+-exchanger belonging to a family of proteins involved in salt stress
tolerance (Apse et al., 1999; Shi et al., 2000). The evidence to-date suggest that MAP
kinases are involved in the stress responses and the predicted gene LOC_Os02g54600.1
annotated as being “Similar to MAP kinase kinase” might have a role in stress response.
LEA gene annotated as being
“LEA-like protein” (LOC_Os05g46480.1;
Os05g0542500).
The LEA gene annotated as being “LEA-like protein” (LOC_Os05g46480.1;
Os05g0542500) is a Late embryogenesis abundant protein and was found to share 17
promoter motifs with a protein annotated as being " Similar to DAG protein, chloroplast
precursor” (LOC_Os08g04450.1; Os08g0139100). Membrane phospholipids constitute a
dynamic system that generates a multitude of signal molecules (e.g., DAG (diacyglycerol
pyrophosphate), PA (Phosphatidic acid) etc.) in addition to serving important structural
roles during stress responses. The phospholipid messengers may activate downstream
adaptive responses when expressed at low levels , whereas at high levels, phospholipidgenerated products may reflect stress damage or may be damaging.
Phospholipid signaling systems are typically grouped according to the phospholipases
that catalyze the formation of lipid and other messengers. There are also novel pathways
involving the formation of lipid messengers that are not the direct products of
phospholipases, such as diacylglycerol pyrophosphate (DGPP) and phosphatidylinositol
3,5-bisphosphate [PIP2] (Munnik & Meijer, 2001). The phospholipase C (PLC) pathway
has been the best characterized, particularly in nonplant systems. PLC catalyzes the
hydrolysis of phosphotidylinositol 4,5-bisphosphate (PIP2), generating the second
messengers inositol 1,4,5-trisphosphate (IP3) and diacylglycerol (DAG). IP3 releases Ca2+
from internal stores, whereas DAG activates protein kinase C. Several studies have
shown that in various plant systems IP3 levels rapidly increase in response to
hyperosmotic stress (Dewald et al., 2001; Drobak & Watkins, 2000; Heilmann et al.,
1999). IP3 levels also increased upon treatment with exogenous ABA in Vicia faba guard
cell protoplasts (Lee et al., 1996) and in Arabidopsis seedlings (Xiong et al., 2001). The
IP3 precursor, PIP2, is synthesized via phosphatidylinositol 4-phosphate 5-kinase. An
Arabidopsis gene encoding this enzyme, PIP5K, is induced by osmotic stress and ABA
(Mikami et al., 1998). Similarly, an Arabidopsis PLC gene, AtPLC1, is also induced by
salt and drought stress (Hirayama et al., 1997). Thus , the predicted gene being annotated
as DAG protein can be predicted to have a role in stress response.
This LEA gene was also found to share 16 promoter motifs with a protein annotated as
being" Ribosomal protein L14 domain containing protein” (LOC_Os04g43540.1;
Os04g0515300). Ribosomal proteins (r-proteins) have been identified in screens for
genes up-regulated in response to cold treatment (Kim et al, 2004b) or UV radiation
(Casati and Walbot, 2003) during various stages of development (Taylor et al., 1992; Van
Lijsebettens et al., 1994). Mechanical wounding, auxin and cytokinin treatments all
result in an increase in transcript levels of many r-protein genes. The stress hormone
abscisic acid causes a decrease in r-protein transcript levels in species as distantly related
as lupine (Cherepneva et al., 2003) and Arabidopsis (Hulm et al., 2005; McIntosh and
Bonham-smith, 2005). The changes in transcription levels of various r-protein genes have
also been observed in several plant species in response to physiological and
environmental changes. For example, transcription of numerous r-protein genes has been
found to increase in maize in response to UV-B radiation and in soybean in response to
cold treatment (McIntosh and Bonham-Smith, 2006). Thus, it has been observed in
literature that ribosomal proteins are involved in stress response.
LEA gene annotated as being “Cold acclimation protein COR413-TM1”
(LOC_Os05g49170.1; Os05g0566800).
The LEA gene annotated as being “Cold acclimation protein COR413-TM1”
(LOC_Os05g49170.1; Os05g0566800) is a Late embryogenesis abundant protein and
was found to share 22 promoter motifs with a protein annotated as being " ABC
transporter,
transmembrane
region,
type
1
domain
containing
protein”
(LOC_Os04g33700.1; Os04g0413000).
The ATP binding cassette (ABC) superfamily is probably the largest and most diverse
family of proteins that mediate ATP-dependent transfer of solutes across membranes in
species ranging from Escherichia coli to humans (Higgins 1992). They have been found
to be involved functionally in cellular detoxification (Rea et al. 1998) or in cell
elongation (Sidler et al. 1998). Interestingly, the accumulation of an ABC transcript in
plants can be correlated to stress conditions, suggesting a hormonal and environmental
regulation of these genes (Smart and Fleming 1996). It has been demonstrated that at
least one putative ABC protein interacts with an anion channel and abscisic acid (ABA)
hormonal signals in plants (Nathalie et al., 1999). The involvement of the ABC
transporters in signalling pathways and the responsive behaviour towards ABA supports
that the predicted protein LOC_Os04g33700.1 might have a stress related role to play in
rice as well.
This LEA gene was also found to share 22 promoter motifs with a protein annotated as
being "Similar to Cell wall invertase” (LOC_Os04g33720.1; Os04g0413200). Wounding
is a common event in the life time of a plant and elicits a spatially and temporally
complex series of responses. It is well established that mechanical wounding leads to an
induction of cell wall associated invertase (cwINV) gene expression and activity (Sturm
& Chrispeels, 1990) (Zhang et al., 1996) (Ohyama et al., 1998) and it has been proposed
that the hydrolysis of sucrose by cwINV generates hexoses which fulfil the energy and
carbon requirements of the wounded tissue (Sturm & Chrispeels, 1990). The hexose
sugars generated by cwINV activity have also been proposed to play an important
signalling role in leaves subject to biotic and abiotic stresses (Chou et al., 2000) (Roitsch
et al., 2003) (Roitsch & Gonzalez, 2004).
Plants contain multiple sugar signalling
pathways which can activate defence-related gene expression and repress photosynthetic
gene expression and there is extensive crosstalk between the sugar and wound/stress
signalling pathways (Gibson, 2004) (Halford & Paul, 2003) (Smeekens, 2000). The
involvement of cell wall invertase in wound related stress responses has also been
confirmed in Arabidopsis (Quilliam et al., 2006). The predicted gene being annotated as
cell wall inverstase could be assigned a role in stress response.
The LEA protein annotated as "Similar to Rab28 protein. “Seed maturation
protein". (LOC_Os03g06360; Os03g0159600). The Arabidopsis AtRab28 protein is
related to germination and may play a role in the ion cell balance during late
embryogenesis and germination as they show improved cation toxicity tolerance (Borrell
et al., 2002). This LEA protein shares 20 common promoter motifs with the following
proteins:
A "Protein kinase domain containing protein" (Os05g0323800; LOC_Os05g25840).
Sugar signaling during abiotic stress has signal transduction cascades that involve
mitogen-activated protein kinases (Gupta & Kaur, 2005). Two new maize bZIP
transcription factors, EmBP-2 and ZmBZ-1 are involved in the expression of abscisic
acid inducible genes such as rab28 and their activity is modulated by ABA and by
phosphorylation. ZmBZ-1 is abscisic acid-inducible and accumulates during late
embryogenesis. EmBP-2 and ZmBZ-1 are phosphorylated by protein kinase CK2 and
phosphorylation alters their DNA binding properties (Nieva et al., 2005). MAPK
cascades play an important role in plant stress responses (Nakagami et al., 2005).
A "TolB, C-terminal domain containing protein." WD40-like Beta Propeller"
(Os03g0840200; LOC_Os03g62370). TolB is periplasmic proteins involved in cell
envelop complex called Tol-Pal system in E.coli. They are involved in the translocation
of colicins which penetrate the membrane and kill the cells. WD proteins in general are
proteins with repeats which are found in all eukaryotes and these regulate various cellular
functions (Neer et al., 1994).
A
“Protein
prenyltransferase
domain
containing
protein"
(Os03g0159700;
LOC_Os03g06370). Protein prenyltransferases are involved in lipid modification of
proteins which are critical in many signaling pathways like apoptosis and vesicular
trafficking (Maurer-Stroh et al., 2003). Ubiquitin fold proteins are membrane bound and
show post translational prenylations (Downes et al., 2006).
A
"Heavy
metal
transport/detoxification
protein
domain
containing
protein"
(Os02g0819000; LOC_Os02g57360). LEA proteins are known to bind metal ions and
play a role in combating oxidative stress. Binding affinity studies for metal ions by group
2 LEA proteins show that Fe3+ has the highest affinity (Svensson et al., 2000). Kruger
(Kruger et al., 2002) has used iron binding techniques to purify some proteins similar to
LEA proteins.
A protein annotated as "Similar to H(+)-transporting ATP synthase (Os02g0750100;
LOC_Os02g51470). Experiments in barley have suggest that the hormone ABA regulate
the expression of the H (+)-pump and Na(+)/H(+) antiporter genes (Fukuda & Tanaka,
2006). Similar experiments in cucumber roots showed that ABA increased the activity of
proton pumps in membranes due to salinity (Janicka-Russak & Klobus, 2007). In rice a
mitochondrial ATPase was shown to be induced during salinity and osmotic stress
(Zhang et al., 2006). Another study has shown that in soyabean Aluminium induced
citrate secretion shows induction in the activity of plasma membrane H+-ATPase in
parallel (Shen et al., 2005). In an earlier group citrate transporters show motif similarity
with LEA gene, so this article may be relevant to show the interplay of citrate
transporters and H+ATPase.
The LEA protein annotated as "Late embryogenesis abundant protein repeat containing
protein”. (LOC_Os03g07180; Os03g0168100).shares 23 common promoter motifs with a
gene annotated as "Heavy metal transport/detoxification protein domain containing
protein" (Os02g0819000; LOC_Os02g57360). As mentioned previously LEA proteins
have been shown to bind to metal ions and combat oxidative stress.
This LEA protein also shares 22 common promoter motifs with a protein annotated as "Sadenosylmethionine synthetase 1; (Methionine adenosyltransferase 1) (AdoMet
synthetase 1)" (Os05g0135700; LOC_Os05g04510). Aluminium induced protein study in
Rice have shown that S-adenosylmethionine synthetase 2 is upregulated showing that this
protein plays a role in Al tolerance of rice (Yang et al., 2007). Salt stress has been shown
to induce the expression of S-adenosyl-L-methionine synthase in lignifying tissues of
tomato plants (Sanchez-Aguayo et al., 2004) and in tomato seedlings (Espartero et al.,
1994). Two S-adenosylmethionine synthetases from Rice (Lee et al., 1997) and three
enzymes from Catharanthus rosea (Schroder et al., 1997) have been functionally
characterized and all of these show induction during salt stress.
The LEA protein also shares 22 common promoter motifs with a protein annotated as a
“conserved hypothetical protein” (Os02g0168000; LOC_Os02g07150). This has been
annotated as a putative Urease accessory protein F (Gramene). Plant orthologs of the
bacterial urease accessory genes ureD and ureF, which are required for the insertion of
the nickel ion at the active site, have been isolated from soybean (Glycine max L. Merr.),
tomato (Lycopersicon esculentum) and Arabidopsis thaliana (Bacanamwo et al., 2002).
LEA protein annotated as “seed maturation protein” (LOC_Os03g53620;
Os03g0747500).
This LEA gene shares 19 common promoter motifs with a gene annotated as "GCN5related
N-acetyltransferase
domain
containing
protein"
(Os05g0376600;
LOC_Os05g31254) A GCN5 related N acetyltransferase domain containing protein was
identified as a part of the histoneacetyltransferase complex called elongator is involved in
cell proliferation (Nelissen et al., 2005).
The LEA protein also shares 17 common promoter motifs with a gene annotated as a
"Pyruvate kinase family protein" (Os04g0677300; LOC_Os04g58090). Pyruvate kinase
show differential expression during submergence stress in Rice (Umeda & Uchimiya,
1994). A pyruvate kinase-like gene was characterized which was among the 38 cold
acclimation-responsive genes from the extremophile hair grass Deschampsia antarctica
Desv (Gidekel et al., 2003).
LEA gene annotated as "Late embryogenesis abundant (LEA) group 1 family
protein." (LOC_Os06g02040; Os06g0110200)
This LEA gene shares 22 common promoter motifs with a gene annotated as "Similar to
Scl1 protein” (Os10g0551200; LOC_Os10g40390.1). Scl1 is a “streptococcal collagenlike proteins. These proteins triple helices similar to collagen (Xu et al., 2002). These
proteins were shown to interact with mammalian integrins (Humtsoe et al., 2005).
It also shares 22 common promoter motifs with a "Putative DNA helicase family protein"
(Os03g0586900; LOC_Os03g38990). A cold- and salinity stress-induced pea DNA
helicase 47 (PDH47) was characterized (Vashisht et al., 2005) and another DNA helicase
45 from pea was shown to confer salt tolerant (Sanan-Mishra et al., 2005). Helicases
might be playing an important role in regulating plant growth and development under
stress conditions by regulating some stress-induced pathways (Vashisht & Tuteja, 2006).
This LEA gene (LOC_Os06g02040) also shares 21 common promoter motifs with the
following proteins;
A
"Zinc
finger,
C2H2-type
domain
containing
protein."
(Os11g0169400;
LOC_Os11g06840). A C2H2 type zinc finger protein has been reported to be involved in
salt tolerance in rice plants (Huang et al., 2007). SGR5, a C2H2-type zinc finger protein,
was shown to be involved in early events of gravitropism in Arabidopsis inflorescence
stems (Morita et al., 2006). SUF4, encoding a C2H2-Type zinc finger protein, represses
flowering by transcriptional activation of Arabidopsis FLOWERING LOCUS C (Kim et
al., 2006b). Another C2H2 type zinc finger protein is reported to be transiently expressed
during cold in rice (Huang et al., 2005). SCOF1, a zinc finger protein increases cold
tolerance in soyabean (Kim et al., 2001b). Similar proteins are also expressed during
water stress in Arabidopsis (Sakamoto et al., 2000).
A "Pathogenesis-related transcriptional factor and ERF domain containing protein"
(Os01g0899800; LOC_Os01g67410). Proteins containing this domain have been shown
not only to enhance pathogen resistance but also induce osmotic stress tolerance (Zuo et
al., 2007) and salt tolerance (Jung et al., 2007). These proteins have been shown to be
expressed during cold acclimatization (Brautigam et al., 2005). One such protein
identified from Arabidopsis is induced by abscisic acid, cold, drought, mechanical
wounding and to a lesser extent, by high salinity treatment (Wei et al., 2005). A similar
cold responsive protein was also identified from Zea Mays (Qin et al., 2004). Thirteen
proteins with ERF/AP2 domain were identified in cDNA libraries from Poplar which
were induced by stress conditions. Some of them showed stress-responsive gene
expression (Nanjo et al., 2004).
A
"DREPP
plasma
membrane
polypeptide
family
protein"
(Os01g0233000;
LOC_Os01g13210). DREPP stands for developmentally regulated plasma membrane
polypeptide. A study conducted to identify putative plasma membrane proteins of
Arabidopsis leaves associated with cold acclimation showed that tobacco DREPP-like
protein to be expressed temporarily. The authors suggest that this protein may be
associated with Ca2+ signal transduction pathway at the early stage of cold acclimation
(Kawamura & Uemura, 2003).
A “Mannose-6-phosphate isomerase, type I" (Os01g0127900; LOC_Os01g03710).
Phosphomannose isomerases (PMI) (EC 5.3.1.8) are enzymes that catalyze the
interconversion of mannose-6-phosphate and fructose-6-phosphate and are involved in
bacterial and fungal cell wall synthesis. It belongs to the cupin family which includes
several seed storage proteins and a class of proteins called germins. Some germin
proteins are induced during abiotic stress (Dunwell et al., 2000).
The LEA protein annotated as "Similar to Galactinol synthase” “Glycosyl
transferase, family 8" (Os03g0316200; LOC_Os03g20120).
This LEA protein shares 17 common promoter motifs with the following genes:
A protein annotated as a "Heavy metal transport/detoxification protein domain containing
protein" (Os02g0819000; LOC_Os02g57360.1) LEA proteins are known to bind metal
ions. Binding affinity studies for metal ions by group 2 LEA proteins show that Fe3+ has
the highest affinity followed by Cu2+, Zn2+ Mn2+ and Fe2+ (Svensson et al., 2000).
Kruger (Kruger et al., 2002) has used iron binding techniques to purify some proteins
similar to LEA proteins. Purification of LEA proteins have been carried out using Cu2+
chromatography step (Herzer et al., 2003). Metal-binding capability of LEA proteins
helps in combating oxidative stress. Transition metal ions like Cu2+ can bind to group 2
LEA proteins (Svensson et al., 2000).
A gene annotated as “Phosphoserine phosphatase” (Os12g0502400; LOC_Os12g31820)
Environmental stresses, such as high salinity, flooding and low temperature, and induced
changes in mRNA levels of enzymes in the plastidic phosphorylated serine biosynthetic
pathway (Ho & Saito, 2001).
A gene annotated as a "Zinc finger, RING-type domain containing protein"
(Os10g0445400; LOC_Os10g30850). RING (really interesting new gene) zinc-finger
proteins have important regulatory roles in development. Upregulation of XERICO, a
RING zinc finger substantially increased cellular ABA levels. XERICO overexpressed
plants show tolerance to drought stress (Ko et al., 2006). OsRING-1, a novel RING-type
zinc finger protein is involved in many stress responses and in rice might play a role as a
transcription regulator in plant stress response signal transduction pathways (Meng et al.,
2006).
A gene annotated as a "Zinc finger, C2H2-type domain containing protein"
(Os09g0431900; LOC_Os09g26210). A C2H2 type zinc finger protein has been reported
to be involved in salt tolerance in rice plants (Huang et al., 2007). SGR5, a C2H2-type
zinc finger protein, was shown to be involved in early events of gravitropism in
Arabidopsis inflorescence stems (Morita et al., 2006). SUF4, encoding a C2H2-Type zinc
finger protein, represses flowering by transcriptional activation of Arabidopsis
FLOWERING LOCUS C (Kim et al., 2006b). Another C2H2 type zinc finger protein is
reported to be transiently expressed during cold in rice (Huang et al., 2005). SCOF1, a
zinc finger protein increases cold tolerance in soyabean (Kim et al., 2001b). Similar
proteins are also expressed during water stress in Arabidopsis (Sakamoto et al., 2000).
A gene annotated as "Protein kinase domain containing protein" (Os05g0550800;
LOC_Os05g47770). Sugar signalling during abiotic stress has signal transduction
cascades that involve mitogen-activated protein kinases (Gupta & Kaur, 2005). Two
maize bZIP transcription factors, EmBP-2 and ZmBZ-1 are involved in the expression of
abscisic acid inducible genes such as rab28 and their activity is modulated by ABA and
by phosphorylation. ZmBZ-1 is abscisic acid-inducible and accumulates during late
embryogenesis. EmBP-2 and ZmBZ-1 are phosphorylated by protein kinase CK2 and
phosphorylation alters their DNA binding properties (Nieva et al., 2005). MAPK
cascades play an important role in plant stress responses (Nakagami et al., 2005).
A gene annotated as an "IQ calmodulin-binding region domain containing protein"
(Os03g0161400;
LOC_Os03g06570).
Calmodulin-binding transcription
activators
(CAMTAs) comprise a conserved family of transcription factors in a wide range of
multicellular eukaryotes. Some of these were identified after screening expression
libraries derived from plants exposed to stress. The authors suggest that CAMTAs
possibly respond to calcium signaling by direct binding of calmodulin (Bouche et al.,
2002).
The
LEA
gene
annotated
to
be
"similar
to
Dehydrin
DHN1
(B8)."
(LOC_Os01g50700.1; Os01g0702500), known to be expressed during water stress, acts
at subcellular as an intracellular stabilizer with possible surfactant characteristics, is also
responsible for winter hardy in barley (Hordeum vulgare L.) and anthesis-silking in
maize (Zea mays L.), (Campbell Scott & Timothy J.Close, 1997), is induced by ABA and
stress conditions in Arabidospsis and was found to share 14 promoter motifs with a
protein annotated to be a "Protein kinase-like domain containing protein."
(LOC_Os05g51740.1; Os05g0595950). Protein kinase-like domain containing proteins
have protein Serine/threonine kinase activity. In bean (Phaseolus vulgaris) leaf a
serine/threonine kinase was exclusively expressed during senescence and was designated
senescence-associated receptor-like kinase (SARK) (Hajouj et al., 2000). Since leaf
senescence is associated with stress response, likely that the two above genes share the
same regulatory elements.
This LEA gene alo shares 14 promoter motifs with a protein annotated to be similar to a
"Heavy
metal
transport/detoxification
protein
domain
containing
protein."
(LOC_Os02g57360.1; Os02g0819000), shown to be involved in selective directed
movement of toxic Heavy metal using a carrier-mediated process. Heavy metal toxicity
in plant is an important stress factor. Plants respond to heavy metal toxicity in a number
of
ways.
Such
responses
include
immobilization,
exclusion,
chelation
and
compartmentalization of the metal ions, and the expression of more general stress
response mechanisms such as ethylene and stress proteins (Cobbett, 2000).
This LEA gene shares 13 promoter motifs with a protein annotated to be similar to
"Inositol
polyphosphate
related
phosphatase
domain
containing
protein."
(LOC_Os03g42810.2; Os03g0626500). Numerous studies have demonstrated that the
SH2-domain-containing inositol 5-phosphatase SHIP (referred hereto as SHIP-1) is
essential in termination of activation signals in the control of the immune response in
human and animals. A defective inhibitory feedback pathway results is autoimmunity and
overwhelming inflammation (Muraille et al., 1999). In arabidopsis inositol polyphosphate
1-phosphatase, was found to be involved in the regulation of ABA and stress signal
transduction in plants and their turnover was critical for attenuating ABA and stress
signalling (Xiong & Zhu, 2001).
This LEA gene also shares 13 promoter motifs with a protein annotated to be "Similar to
Subtilisin-like protease (Fragment)." (LOC_Os03g40830.1; Os03g0605300). Proteases
are responsive to stress and pathogen stimuli. Proteases are crucial for living cells and
play a role in plant cell adaptation to environmental conditions. They are involved in
plant defence against metal toxicity. Oxidative stress produced oxidized proteins which
are selectively degraded by proteases (Golldack et al., 2003; Pena et al., 2006). Their
functional role involves the negative regulation of enzyme activity.
The LEA gene annotated to be a "Late embryogenesis abundant protein repeat
containing protein."( LOC_Os01g50910.2; Os01g0705200) is induced by ABA and
stress conditions in Arabidosis and was found to share 14 promoter motifs with a protein
annotated to be "Similar to Alanine aminotransferase 2 (EC 2.6.1.2) (GPT) (Glutamic-pyruvic
transaminase
2)
(Glutamic--alanine
transaminase
2)
(ALAAT-2)."
(LOC_Os09g26380; Os09g0433900). Under anaerobic stress conditions, plants respond
rapidly by accumulation of pyruvate which shifts the equilibrium of alanine
aminotransferases towards alanine accumulation. The primary role of Alanine
aminotransferase is to breakdown excess alanine: Therefore, alanine aminotransferase is
crucial for the rapid conversion of alanine to pyruvate during recovery from low-oxygen
stress (Miyashita et al., 2007) (Streeter & Thompson, 1972).
This LEA gene shares 13 promoter motifs with a protein annotated as a "Cyclin-like Fbox domain containing protein" (Os12g0557900; LOC_Os12g37110). a conserved
structural motif that serves as a link between a target protein and a ubiquitin-conjugating
enzyme and plays a similar role as an E3 ligase in ubiquitin protein degradation pathway.
LEA gene annotated as a "Conserved hypothetical protein."(LOC_Os01g46600.1;
Os01g0654400).
This LEA gene shares 13 promoter motifs with a gene annotated as a "Root-specific
protein (RCc2 protein)." (LOC_Os10g40430.1; Os10g0551800). The NT16 gene from
tobacco, highly similar to the RCc2 gene from rice is specifically expressed in roots. Its
expression has been shown to be induced by MeJA (methyl Jasmonic acid). It is involved
in shoot and root formation and in wound-healing process by modifying cell wall
composition (Yasuda et al., 1997).
This LEA gene also shared 13 promoter motifs with the annotated protein "Similar to
Vacuolar ATP synthase subunit D (EC 3.6.3.14) (V-ATPase D subunit) (Vacuolar proton
pump D subunit)." (LOC_Os04g55040.2; Os04g0643100). In wheat roots, vacuolar
ATPase was shown to be induced by Aluminum stress. Its been suggested that during
Aluminum toxicity, ATPase is overexpressed since ATP is required for energy balance
within the cell (Hamilton et al., 2001).
This LEA gene also shared 13 promoter motifs with the annotated protein "Similar to
Ubiquitin-activating enzyme E1 3" (LOC_Os03g18380; Os03g0294900). In lens cell
oxidative stress induces overproduction of Ubiquitin-activating enzyme E1. The increases
in ubiquitin conjugation activity were associated with an increase in intracellular
proteolysis, suggesting that the enzyme may play a role in removal of damaged proteins
from the cells (Shang et al., 1997). Ubiquitin is involved in many cell processes. For
example, Ubiquitin is conjugated to the protein cyclin during the G1 phase of mitosis and
thus plays an important role in regulating the cell cycle. Ubiquitin conjugation is also
involved in DNA repair, embryogenesis, the regulation of transcription, and apoptosis
(programmed cell death) (Raasi et al., 2005).
This LEA gene also shared 13 promoter motifs with the annotated protein "Lipolytic
enzyme, G-D-S-L family protein."";category " (LOC_Os01g46080.2; Os01g0649200). It
is involved in lipid metabolism by hydrolase activity of ester bonds, an important process
in the maintenance of cell membrane integrity (Wang et al., 2006).
This LEA gene also shared 13 promoter motifs with the annotated protein "Similar to
Dimethylaniline
monooxygenase-like
protein
(Flavin-containing
monooxygenase
YUCCA)" (LOC_Os01g45760.2; Os01g0645400). Enhanced expression of the YUCCA
gene, a flavin-containing monooxygenase (FMO) gene from Arabidopsis leads to a
phenotype characterized by increased hypocotyl elongation, increased root thickness,
increased root hair development, increased lateral root initiation, increased apical
dominance, epinastic leaf growth, increased flowering node formation, increased fruit
yield, increased endogenous auxin levels, parthenocarpic fruit production, altered gene
expression, altered pathogen resistance, altered pest resistance, and altered herbicide
resistance (Tatiana et al 2006).
The LEA gene annotated as "Similar to Late embryogenesis abundant protein
Lea14-A." (LOC_Os01g12580.1; Os01g0225600) is induced by ABA and stress
conditions, shares 19 promoter motifs with a protein annotated as "Epoxide hydrolase
family protein." (Os01g0919700; LOC_Os01g69060). which is a salt stress induced
protein (Solanum commersonii and S. tuberosum). Transcripts were also induced by cold
and water stress but not ABA. This protein is crucial for plant stress tolerance (Massarelli
et al., 2006).
The
LEA
gene
annotated
as
a
"Conserved
hypothetical
protein."
(LOC_Os01g46600; Os01g0654400) is induced by ABA and stress conditions and
shares 21 promoter motifs with a protein annotated as "Similar to Type III chlorophyll
a/b-binding protein (Fragment)" (LOC_Os07g37550; Os07g0562700). Chlorophyll a/bbinding protein expression is induced transiently by various stress conditions. Its
suggested to play a role in protection of Chlorophyll damage from light stress (Andersson
et al., 2003).
This LEA gene also shares 19 promoter motifs with "Oxysterol-binding protein family
protein" (LOC_Os12g18770.1; Os12g0285600). It contains a Pleckstrin homology
domain, binds to intracellular lipid molecules and enables them in recruiting lipids to
different membranes (endocytosis) and maintenance of intracellular sterol-lipid
distribution. Incidentally, cellular membranes play a vital role in cellular stress
resistance/tolerance. Thus any biological process involving cellular membrane
biosynthesis is part of the stress response mechanism.
This LEA gene also shares 19 promoter motifs with the annotated protein "2OG-Fe(II)
oxygenase domain containing protein." (LOC_Os06g07923; Os06g0176500). In Human,
heme oxygenase-1 (HO-1) catalyzes the rate-limiting step in heme catabolism and is
involved in cellular iron homeostasis. It is induced by a variety of cellular stresses,
including oxygen deprivation and free radical-mediated stress (Panchenko et al., 2000).
This LEA gene also shares 19 promoter motifs with the annotated protein "Heavy metal
transport/detoxification protein domain containing protein." (LOC_Os02g57360.1;
Os02g0819000) It is involved in heavy metal ion binding and transporting.
This LEA gene also shares 19 promoter motifs with the annotated protein "FAR1 domain
containing protein." (LOC_Os02g33750.2; Os02g0542200). In yeast, this annotated gene
encodes a cyclin-dependent protein kinase inhibitor involved in cell cycle arrest in
response to ABA induction (Blondel et al., 2000; Wang et al., 1998). This probably
explains why/how plant growth is arrested during extreme stress conditions.
The Lea gene annotated as being “Dehydrin RAB 16B” (LOC_Os11g26780.1;
Os11g0454200) belongs to the rabl6 gene family of rice (Oryza sativa L.) that consists of
four tandemly arrayed genes, rabl6A to rabl6AD, which are highly expressed in embryos
during the late stage of seed development, and which respond to ABA and water stress in
vegetative tissues (Mundy & Chua, 1988; Yamaguchi-Shinozaki & Shinozaki, 1993b).
This LEA gene shared 14 promoter motifs with a protein annotated as “WD40-like
domain” (Os03g0625300; LOC_Os03g42710).
Secondary metabolism is not only a
protective mechanism against biotic and abiotic stresses but also part of the molecular
programs that contribute to normal plant growth and development. In this context,
secondary metabolism is intimately linked with other aspects of plant differentiation in
which transcription factors play a key coordinating role. Recent findings illustrated that
the complexity of regulatory networks controls flavonoid biosynthesis in Arabidopsis and
other species. They also underline the close relationship between secondary metabolism
and epidermal and seed differentiation in Arabidopsis and the central role played by
conserved WD40 domain proteins in regulating these processes (Broun, 2005). The
relationship between flavonoid metabolism and epidermal and seed differentiation in
Arabidopsis first became apparent with the discovery of the transparent testa glabra1
(ttg1) mutants (Koornneef, 1981; Koornneef et al., 1982; Galway et al., 1994). The ttg1
phenotype clearly indicates that the developmental fates of these structures and the
control of the flavonoid pathway are linked. Further evidence of this connection is
provided by the phenotype of Arabidopsis plants that overexpress the RED gene, which
encodes a basic helix-loop-helix (bHLH) transcription factor that regulates anthocyanin
biosynthesis in maize (Dellaporta et al., 1988; Ludwig et al., 1989). RED overexpression
is sufficient to correct all defects in the ttg1 mutant, restoring trichomes, root-hair
initiation, seed-coat development and flavonoid production (Lloyd et al., 1992; Lloyd et
al., 1994).
A complex of transcription factors that can include various members of the MYB, basic
helix–loop–helix (bHLH) and WD40 protein families have recently provided insight into
how this one complex regulates multiple cell fates and has therefore played a key role in
the evolution of cellular diversity in the plant epidermis. The plant epidermis is the first
point of contact between the sessile plant and its changing environment. As such, the
epidermis fulfils several distinct roles and this multi-functionality makes it an ideal
system for the study of evolution of morphological diversity. The plant epidermis
primarily provides an impermeable barrier to water, allowing organisms that evolved in
the sea to survive in a dehydrating terrestrial atmosphere (Ramsay & Glover, 2005).
Another annotated gene that shares 14 promoter motifs with this LEA gene is “BURP
domain containing protein” (LOC_Os02g18690.1, Os02g0288600). A gene, SCB1 (Seed
Coat BURP-domain protein 1), that is expressed specifically within the soybean (Glycine
max [L.] Merrill) seed coat early in its development. Northern blot analysis and mRNA in
situ hybridization revealed novel patterns of gene expression during seed development.
SCB1 mRNA accumulated first within the developing thick-walled parenchyma cells of
the inner integument and later in the thick- and thin-walled parenchyma cells of the outer
integument. This occurred prior to the period of seed coat maturation and seed filling and
before either of the layers started to degrade. SCB1 may therefore play a role in the
differentiation of the seed coat parenchyma cells. In addition, the protein product appears
to be located within cell walls. The SCB1 gene codes for a new member of a class of
modular proteins that possess a carboxy-terminal BURP domain and a variety of different
repeated sequences. The sequence of the genomic clone revealed the insertion of a Tgm
transposable element in the upstream promoter region but it is not certain whether it
contributes to the tissue-specific pattern of SCB1 expression (Batchelor et al., 2002).
Another annotated gene that shares 14 promoter motifs with a LEA gene is “Basic helixloop-helix dimerisation region bHLH domain containing protein” (LOC_Os10g39750.1;
Os10g0544200). Heisler (Heisler et al., 2001) described the role of the basic helix-loophelix transcription factor SPATULA (SPT) in the control of the germination of dormant
seeds by light and temperature. SPT is a multifunctional transcription factor, acting as a
light-stable repressor of GA3ox expression controlling seed responses to cold
stratification and to a lesser extent red light. SPT also acts as a key regulator of carpel
development (Heisler et al., 2001) and of the expansion of cotyledons and petals.
Penfield (Penfield et al., 2005) characterize the role of the related transcription factor
PIL5 in germination control and found that although it’s not required for seed dormancy
in the light, PIL5 is vital for the repression of germination in the dark after cold
stratification.
PIF3-Like 5 (PIL5/PIF1/bHLH015), a phytochrome-interacting bHLH protein, is a key
negative regulator of seed germination, and that light promotes seed germination partly
by inhibiting the function of PIL5 (Oh et al., 2004). Oh (Oh et al., 2006) demonstrated
that PIL5 mediates seed germination by simultaneously regulating the expression of GA
biosynthetic and catabolic genes, and also show that light inhibits PIL5 function by
activating the phytochrome-mediated degradation of the PIL5 protein.
The rd22 gene is a dehydration-responsive gene induced by the application of exogenous
ABA to Arabidopsis plants (Yamaguchi-Shinozaki & Shinozaki, 1993a).
Iwasaki
(Iwasaki et al., 1995) have shown that a 67-bp promoter region of rd22 can regulate
drought-inducible gene expression. There is a MYC and a MYB recognition site within
this 67-bp region. MYC and MYB recognition sites function as cis-acting elements in the
drought-induced expression of the rd22 gene (Abe et al., 1997).
The LEA gene annotated as being “Similar to Water-stress inducible protein
RAB21” (LOC_Os11g26790.1, Os11g0454300).
Godoy (Godoy et al., 1990) had characterized a new tomato cDNA, TAS14, inducible by
salt stress and abscisic acid (ABA). Its nucleotide sequence predicts an open reading
frame coding for a highly hydrophilic and glycine-rich (23.8%) protein of 130 amino
acids. Southern blot analysis of tomato DNA suggested that there is one TAS14 structural
gene per haploid genome. TAS14 mRNA accumulates in tomato seedlings upon
treatment with NaCl, ABA or mannitol. It is also induced in roots, stems and leaves of
hydroponically grown tomato plants treated with NaCl or ABA. TAS14 mRNA is not
induced by other stress conditions such as cold and wounding. The sequence of the
predicted TAS14 protein shows four structural domains similar to the rice RAB21, cotton
LEA D11 and barley and maize dehydrin genes.
A novel rice gene, called RAB 21, which is induced when plants are subjected to waterstress. This gene encodes a basic, glycine-rich protein (mol.wt 16 529) which has a
duplicated domain structure. Immunoblots probed with antibodies raised against
Bgalactosidase/RAB 21 fusion protein detect RAB 21 protein only in cytosolic cell
fractions. RAB 21 mRNA and protein accumulate in rice embryos, leaves, roots and
callus-derived suspension cells upon treatment with NaCl (200 mM) and/or the plant
hormone abscisic acid (10 μM ABA).
Another annotated gene that shares 10 promoter motifs with this LEA gene is “Similar to
DAG protein” (LOC_Os08g04450, Os08g0139100). The only Dof gene for which an
effect in plants has been so far convincingly demonstrated is DAG1, which have been
shown to be involved in seed germination in Arabidopsis. The knockout mutant in DAG1,
isolated from a T-DNA insertion collection, produces seeds that do not develop
dormancy and are capable of germinating in the dark (Papi et al., 2000). Seeds of several
annuals, including Arabidopsis, develop dormancy during the late stages of their
development: Although mature, they are not capable of germinating under favorable
conditions when freshly harvested or naturally detached from the mother plant. Seed
dormancy can be relieved by a period of dry storage referred to as “after ripening”; in
Arabidopsis, stored non dormant seeds need illumination with (red) light to germinate
(Koornneef & Karssen, 1994) (for review, see (Bewley, 1997)). Disruption of the Dof
gene DAG1 causes mutant seed to loose dormancy and dependence upon red light for
germination. In addition, this gene DAG1 is expressed only in the mother plant and not in
the seed at any stage of development.
Another annotated gene that shares 10 promoter motifs with a LEA gene is “Similar to
Ser-Thr protein” (LOC_Os03g51020.1; Os03g0719500). Plants respond to environmental
stress by activating “stress genes.” The plant hormone abscisic acid (ABA) plays an
important role in stress-responsive gene expression. Although Ca2+ serves as a common
second messenger in signaling stress and ABA, little is known about the molecular basis
of Ca2+ action in these pathways. Kim (Kim et al., 2003) have shown that CIPK3, a
Ser/Thr protein kinase that associates with a calcineurin B–like calcium sensor, regulates
ABA response during seed germination and ABA- and stress-induced gene expression in
Arabidopsis. The expression of the CIPK3 gene itself is responsive to ABA and stress
conditions, including cold, high salt, wounding, and drought. Disruption of CIPK3 altered
the expression pattern of a number of stress gene markers in response to ABA, cold, and
high salt. However, drought-induced gene expression was not altered in the cipk3 mutant
plants, suggesting that CIPK3 regulates select pathways in response to abiotic stress and
ABA. Their results have identified that CIPK3 as a molecular link between stress- and
ABA-induced calcium signal and gene expression in plant cells. Because the cold
signaling pathway is largely independent of endogenous ABA production, CIPK3
represents a cross-talk “node” between the ABA-dependent and ABA independent
pathways in stress responses.
Another annotated gene that shares 10 promoter motifs with a LEA gene is “RNAbinding region RNP-1” (LOC_Os08g38120; Os08g0488700). A perennial ryegrass
cDNA clone encoding a putative glycine-rich RNA binding protein (LpGRP1) was
isolated from a cDNA library constructed from crown tissues of cold-treated plants. A
significant increase in the mRNA level of LpGRP1 was detected in root, crown and leaf
tissues during the treatment of plants at 4°C, through which freezing tolerance is attained.
The increase in the mRNA level was prominent at least 2 h after the commencement of
the cold treatment, and persisted for at least 1 week. Changes in mRNA level induced by
cold treatment were more obvious than those due to treatments with abscisic acid (ABA)
and drought. The LpGRP1 protein was found to localise in the nucleus in onion
epidermal cells, suggesting that it may be involved in pre-mRNA processing. The
deduced polypeptide sequence consists of 107 amino acids with a single N-terminal RNA
recognition motif (RRM) and a single C-terminal glycine-rich domain. The sequence
showed extensive homology to glycine-rich RNA binding proteins previously identified
in other plant species. The best-characterised motif, RRM, contains two short sub-motifs
designated RNP-1 and RNP-2. There is a family of proteins that contain a glycine-rich
sequence (Sachetto-Martins et al., 2000).
The glycine-rich RNA-binding proteins are widely distributed in plants, including both
angiosperms and gymnosperms (Sachetto-Martins et al., 2000). An increase in gene
expression in response to environmental stresses such as cold, drought or wounding is
one of the typical features of plant glycine-rich RNA-binding proteins (Alba & Pages,
1998; Sachetto-Martins et al., 2000). Ribohomopolymer-binding assays showed that
glycine-rich RNA-binding proteins such as those from maize (MA16), (Ludevid et al.,
1992). It is also known that the expression of a glycine-rich RNA-binding protein in
Arabidopsis thaliana (AtGRP1) is regulated according to a circadian clock through
alternative pre-mRNA splicing (Staiger et al., 2003). The overall function of glycine rich
RNA-binding proteins is still unknown. However observations suggested that they are
involved in the control of RNA processing and/or mRNA stability in response to
environmental stimuli.
Another protein that shares 10 promoter motifs with this LEA gene is annotated as being
“Similar to Phytochrome A” (Os03g0719700). Imbibition-inducible (IMB1) is a nuclear
protein suggested by subcellular localization in onion epidermal cells using an IMB1yellow fluorescent protein (YFP) fusion protein. In Arabidopsis thaliana, IMB1, is
expressed at very low levels in dry seeds but is markedly induced during seed
imbibitions. In addition, IMB1 transcript levels are down regulated during germination.
Seeds of a loss-of-function mutant allele, imb1, shows impaired cotyledon greening
during germination in ABA and expressed higher levels of ABI5 protein than the wild
type (Duque & Chua, 2003). Moreover, imb1 seeds are deficient in the phytochrome A
(phyA)-mediated very-low-fluence response of germination.
The LEA gene annotated as a “Late embryogenesis abundant (LEA) group 1 family
protein” (Os06g0110200) was found to share 10 promoter motifs with the above LEA
gene. A late embryogenesis abundant (LEA) group 3 protein, a novel protein that is
named an anhydrin., a state by exposure to a moderate reduction in relative humidity
Strikingly, the predicted LEA and anhydrin proteins are highly hydrophilic and lack
significant secondary structure in the hydrated state. LEA proteins occur commonly in
plants and accumulate during seed maturation and desiccation stress; the presence of a
gene encoding an LEA protein in an anhydrobiotic nematode suggested that some
mechanisms of coping with water loss are conserved between plants and animals.
Another annotated gene that shares 10 promoter motifs with a LEA gene is known as
“Similar to Cytochrome c biogenesis protein” (LOC_Os12g04270.1; Os12g0137300).
Within the plant kingdom a very broad plasticity in primary metabolic function has
developed to cope with altered oxygen availability (Sachs et al., 1980; Subbaiah & Sachs,
2003). Some plant species exhibit extreme tolerance to prolonged anoxic conditions by
maintaining an energy charge through increased glycolysis and redistributed energy
allocation (Gibbs et al., 2000). Rice is one of the most anoxia-tolerant plant crop species
and its able to germinate and sustain early seedling growth in strictly anoxic solutions
under a high vacuum and can readily return to atmospheric or aerobic conditions without
substantial damage (Setter et al., 1997; Ushimaru et al., 1992; Shibasaka & Tsuji,
1988b). Under field conditions rice is often sown into anoxic mud in unstirred flooded
land and germinates to meet aerobic conditions as it grows upward (Setter & Ella, 1994).
On the return of anoxically grown rice seedlings to air there are a number of well
documented responses to sudden oxygen availability including increased respiratory rate
(Shibasaka & Tsuji, 1988b), elevation of antioxidant enzymes such as catalase, ascorbate
peroxidase, superoxide dismutase, dehydroascorbate/monohydroascorbate reductase, and
glutathione reductase (Ushimaru et al., 1992; Ushimaru et al., 1994; Boo & Jung, 1999)
and heightened levels of small molecule antioxidants such as glutathione, ascorbate and
α-tocopherol. Mitochondrial structures appeared to proliferate in rice seedlings even
when they are grown under anoxic conditions from dry seed. Cytochromes have been
shown to be present in anoxically grown rice but at lower levels than in aerobic controls
(Vartapetian et al., 1975) and the mitochondrial cytochrome content increases rapidly on
air adaptation from anoxia (Shibasaka & Tsuji, 1988a). Respiratory oxidase gene
expression has been reported to respond to oxygen deprivation and air adaptation in rice
(Tsuji et al., 2000).
Another annotated gene that shares 10 promoter motifs with a LEA gene is
“Quinonprotein
alcohol
dehydrogenase-like
domain
containing
protein”
(LOC_Os07g40030; Os07g0589400). Mutants able to germinate and perform early
growth in medium containing a high NaCl concentration were identified during the
course of two independent screenings and named salt resistant (sre) and salobreño (sañ)
(Gonzalez-Guzman et al., 2002). The sre and sañ mutants also were able to germinate in
high-osmoticum medium, indicating that they are osmotolerant in a germination assay.
Complementation analyses revealed that sre1-1, sre1-2, sañ3-1, and sañ3-2 were alleles
of the abscisic acid (ABA) biosynthesis ABA2 gene. A map-based cloning strategy
allowed the identification of the ABA2 gene and molecular characterization of four new
aba2 alleles. The ABA2 gene product belongs to the family of short-chain
dehydrogenases/reductases, which are known to be NAD- or NADP-dependent
oxidoreductases. Recombinant ABA2 protein produced in Escherichia coli exhibits a Km
value for xanthoxin of 19μM and catalyzes in a NAD-dependent manner the conversion
of xanthoxin to abscisic aldehyde as determined by HPLC–mass spectrometry. The ABA2
mRNA is expressed constitutively in all plant organs examined and is not upregulated in
response to osmotic stress. The results of this work are discussed in the context of
previous genetic and biochemical evidence regarding ABA biosynthesis, confirming the
xanthoxin abscisic aldehyde.
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