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Proc Indian Natn Sci Acad 80 No. 5 December 2014 pp. 1013-1023
 Printed in India.
DOI: 10.16943/ptinsa/2014/v80i5/47970
Review Article
The Possible Overlap Between Salinity and Mechanical Challenges in
Porteresia coarctata
SONALI SENGUPTA
Division of Plant Biology, Bose Institute, P-1/12, CIT Scheme, VIIM, Kankurgachhi, Kolkata 700 054, India
(Received on 05 May 2014; Revised on 01 October 2014; Accepted on 30 October 2014)
In nature, certain abiotic stresses constitutively acting on plants often go unrecognized. Mechanical stress is one of such
stresses, which is manifested on a plant as low-spectrum pressure on the cell membrane due to wind, soil hindrance,
gravity or wave current. Although all plants face constant threats from mechanical stress, some ecosystems are more prone
to receive such stress. Mangrove vegetation is daily inundated by saline tidal waves that pose a serious threat to the soil
binding force of forest undergrowth. Porteresia coarctata is a mangrove rice, which being wild, is avaluable germplasm
for bioprospecting of genes and proteins that may confer salt-tolerance to domestic rice. However, P. coarctata is important
from ecological point of view as its salt and mechanical stress tolerance is an integral part of the mangrove ecosystem. It
is not possible to understand the basic biology of P. coarctata without an ecological perspective. The subterranean part of
Porteresia provides a high anchorage and binds soil, thus stabilizing the mangrove vegetation. The root system architecture
of Porteresia is unique, with a rhizome and rhizoid-like rootlets. The root system interacts with both salinity and mechanical
threat directly, and thus it is important to understand the molecular ecophysiology of Porteresia root and rhizomes to
understand the nature of overlap between salinity and mechanical stress in a mangrove ecosystem, which is still elusive.
Key Words: Porteresia coarctata; Salinity; Mechanical Stress; Mangrove; Rice
Introduction
Major environmental stresses that influence a plant’s
life often occur together in its natural habitat. Such
co-occurrence of stresses may elicit similar defence
reactions or adaptations and may express similar
group of transcription factors and shared group of
genes. Sometimes the stresses share physical or
chemical components as well. For convenience of
discussion, stress overlap can be reduced into certain
reaction types as shown in Fig. 1. For example,
salinity and dehydration may have a common physical
element of osmotic shift; that may be termed as
Interaction Tier A; sharing astress component.
Salinity may co-occur with submergence in coastal
ecosystem or industrial sewage washed cultivation
system, which is co-occurrence of unrelated
stressors, termed as Interaction Tier B (Fig. 1).
There is also a third type of reaction, wherein the
molecular response to one stress may use same
signalling pathways or cascades of reactions for one
or more biotic or abiotic stresses commonly known
as molecular cross talk and termed Interaction Tier
C in Fig. 1. In an ecological niche, all such
interactions shape a plant’s mode of survival and its
position in the ecosystem. Moreover, anthropogenic
inputs, such as cultivation or eradication could play
as an invasive pressure (Interaction Tier D in Fig.
1) at all levels of such interactions, and define
molecular ecophysiology of a plant.
This review will address all three tiers of
interactions between salinity and mechanical stress
with special reference to wild rice, Porteresia
*Author for Correspondence: E-mail: [email protected]
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Fig. 1: Interaction types in molecular ecophysiology of a plant. For
details, refer the text
coarctata. Porteresia, being a mangrove associate and
a salt-tolerant bioprospecting model for rice, is
extremely important in rice stress biology and
biotechnological improvement of rice.
Environment-Genotype Interactions in Mangrove
Vegetation
Mangrove plants occupy a special niche in the
ecosystem with plants of specialized adaptation. In a
mangrove habitat, the interactions among organism
and environment are critical for optimal survival. The
environmental forces operative on coastal or shoreline
mangrove forests are multifarious. They include
salinity, flooding and anaerobic condition.Mangrove
vegetation typically shows two types of plants, one
group represents the true mangroves, whereas the
other group consists of mangrove associates (Wang
et al., 2010).“Exclusive”, “obligate” or “true”
mangrove species are not able to grow outside the
mangrove environment whereas ‘nonexclusive’,
facultative or mangrove associates may occupy any
terrestrial or aquatic habitat outside the mangrove
ecosystem (Lacerda et al., 2002; Parani et al., 1998;
Tomlinson, 1986). Differences between them are not
well-defined and there are several fringe species with
debated position. Non-exclusive mangroves are
Sonali Sengupta
known to shift seamlessly between a saline and nonsaline environment.They may also show certain
energetically cheap adaptations compared to complex
anatomical adaptations found in true mangroves, for
example, vivipary and pneumatophores. Status of
Porteresia coarctatais somewhat ambiguous in this
regard. The Sunderban mangrove area is one of the
largest mangrove forests washed with the
distributaries of the Ganges, and forms the coast
fringe of Bay of Bengal. The soil of estuarine area is
highly saline and faces daily saline water
submergence from high and low tides. The major
vegetation of true mangrove trees and shrubs in
Sundarban area are accompanied by a large
proportion of the mangrove associates; which include
some monocots belonging to Cyperaceae and
Poaceae.
Porteresia coarctata, a Salt-Tolerant Wild Rice
Porteresia coarctata is a wild rice that has been
receiving great attention for its unique salt tolerance
quality and its close relation to rice. As proposed by
Sengupta et al. (2010), Porteresia is a potent model
for bioprospecting of genes and proteins for raising
salt tolerant rice through biotechnological
approaches. However, the domesticated rice Oryza
sativa and the wild rice Porteresia show significant
differences. The native Porteresia vegetation
flourishes in a range of 100 to 500mM of NaCl, which
is comparable to seawater. Many native landraces of
rice are also known to tolerate some extent of salinity,
but never establish in a mangrove eco-system.
Although suggested to be facultative, it has always
been difficult to establish a completely non-saline
formation of Porteresia and no such natural
establishment has been observed. This prompted us
to term Porteresia as salt loving rice or halophilic
rice, not a true facultative; and a fringe species in
context of mangrove-like property. We have observed
that Porteresia grows better in a saline soil, shows
greater vegetative growth and propagation, has a
higher biomass and a high photosynthetic rate, in
comparison to control (non-saline)conditions
(Sengupta and Majumder, 2009). It prefers vegetative
reproduction in the saline mode, and the occasional
spikelets produce almost no viable seeds. In absence
The Possible Overlap Between Salinity and Mechanical Challenges in Porteresia coarctata
of salt in soil, it is possible to force Porteresia to
enter in a sexual reproduction mode and to produce a
few viable seeds occasionally (Sengupta et al.,
unpublished) . In our previous observations,the
establishment of an endophytic fungus was seen
favourable for the establishment of a Porteresia
vegetation.
Ecological and Taxonomical Position of Porteresia
Porteresia is a tetraploid monotypic genus (2n = 4x
= 48) (Sengupta and Majumder, 2010). The largest
continuous vegetation of Porteresia occurs at
Sundarban delta that stretches along coastal West
Bengal and Bangladesh, covering about a million
hector of land. The majority of the flora are trees,
but the land is held by a large proportion of under
growth of shrubs and herbs. Porteresia forms a vast
population in the coastline, binds the soil and prevents
the coastline from erosion. Both the east and west
shore lines of India, including Orissa, Sundarban and
Chennai coast forests are manifested with Porteresia
coarctata. However, the vegetation is limited to the
soil that gets inundated twice a day with saline river
or seawater of 20 to 40 dSm-1 (Jagtap et al., 2006).
It is clearly indicated that Porteresia is a valuable
source of genes and proteins, that bear significant
homology to rice. Therefore, genomic, transcriptomic
and/or proteomic studies of Porteresia should offer
valuable bioresource for transgenic crop science.
However, the ambiguity in its physiology very often
contradicts part of its identity as a halophytic wild
(non-domesticated) model for rice which is curious.
Porteresia coarctata act as pioneer species in
the succession of mangrove formation along the
estuaries of India (Jagtap et al., 2006). Though of
great significance to estuarine and deltaic
environments, it is poorly understood ecologically.
The temporal and spatial patterns in the growth and
biomass production of P. coarctata were evaluated
at selected localities along the banks of Mandovi
estuary, Goa, India (Jagtap et al., 2006; Sengupta and
Majumder, 2010). Considering its ecological
significance i.e. tolerance to wide salinity range and
adaptability to sandy and muddy substrate, P.
coarctata is of a great value in protection,
conservation and restoration of estuarine and creek
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ecosystems in India. The habitat of this plant in India
has been categorized under ecologically sensitive
zone, and protected vide CRZ (Coastal Regulation
Zone) Act of 1990, along with mangroves. However,
Porteresia habitat continue to be under constant
threat from ever increasing anthropogenic demands,
and hence warrants strict implementation of CRZ rule
for their protection (Sengupta and Majumder, 2010).
Under such an ecological conditions, Porteresia faces
challenges from salt, physiological dehydration,
submergence and mechanical stress. Never
domesticated or cultivated, the anthropogenic input
to the vegetation is unclear. In the coastline population
of Sundarbans, it is widely used as a fodder which is
an important reason of its eradication. In the
coastlines of Sundarban area it is called Dhani ghas.
This plant shows an elaborate rhizomatous system
absent in other domestic rice species, but bears
similarity to the rhizomatous stem of a weedy rice,
Oryza longstaminata. Like Porteresia, weedy rice has
a robust vegetative growth, but it prefers a non-saline
habitat and the seeds of weedy rice are not dehiscent.
On the other hand, seeds of Porteresia are highly
dehiscent and not viable.
Oryza genome is made up of 24 species, of
which only two are cultivated and domesticated
(Table 1). There are 10 genome types, of which
diploids are AA through GG, and 4 are allote traploids.
The speciality of Porteresia lies in the fact that the
HHKK genome type in Porteresia is special, as none
of the genome complements (HH or KK)are present
in the diploid genome groups of rice. The taxonomical
position of P. coarctata Tateoka (= O. coarctata) is
discussed in detail by Sengupta and Majumder
(2010). The inclusion of this plant in Oryza species
is highly debated; though based on the genetic,
anatomical and morphological data, several scientists
have emphasized the positioning of Porteresia in the
Oryza genus (Tateoka, 1965; Flowers et al., 1990;
Finch et al., 1997; Garcia, 1992; Latha et al., 1998;
Ge et al., 1999). Though Ge et al. (1999) suggested a
more ancient origin of Porteresia than O. sativa, the
phylogenetic reconstruction of rice clearly shows that
the closest ancestral species to KK (P. coarctata)
genome are DD and HH genomes. Comparison of
Monoculm1 (MOC1) genomic regions suggests that
Sonali Sengupta
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Table 1: Origin and genome types of Oryza genus analysed so far (Adapted and modified from Ge et al., 1999)
S.No. Species
Genome
Accession
Habit
Status
Origin
1
P. coarctata (Syn. O. coarctata)
HHKK (?)
MSSR007
Halophyte
Wild
India
2
O. sativa
AA
IR64
Glycophyte
Domesticated
IRRI
3
O. glaberrima
AA
100792
Glycophyte
Domesticated
Senegal
4
O. nivara
AA
106185
Glycophyte
Wild
India
5
O. rufipogon
AA
105908
Glycophyte
Wild
Thailand
6
O. longistaminata
AA
103886
Glycophyte
Co-domesticated
Tanzania
7
O. punctata
BB
100937
Glycophyte
Wild
Ghana
8
O. officinalis
CC
101116
Glycophyte
Wild
Philippines
9
O. rhizomatis
CC
105448
Glycophyte
Wild
SriLanka
10
O. minuta
BBCC
100880
Glycophyte
Wild
Philippines
11
O. eichingeri
CC
105408
Glycophyte
Wild
SriLanka
12
O. malampuzhaensis
BBCC
105328
Glycophyte
Wild
India
13
O. alta
CCDD
100025
Glycophyte
Wild
Surinam
14
O. grandiglumis
CCDD
105156
Glycophyte
Wild
Brazil
15
O. latifolia
CCDD
105139
Glycophyte
Wild
Guatemala
16
O. australiensis
EE
105272
Glycophyte
Wild
Australia
17
O. brachyantha
FF
101232
Glycophyte
Wild
Sierraleone
18
O. longiglumis
HHJJ
105146
Glycophyte
Wild
Indonesia
19
O. ridleyi
HHJJ
100820
Glycophyte
Wild
Thailand
20
O. granulata
GG
101084
Glycophyte
Wild
Srilanka
21
O. meyeriana
GG
106473
Glycophyte
Wild
Philippines
22
O. indandamanica
unknown
105694
Glycophyte
Wild
India
O. coarctata (or P. coarctata) has a unique genome
type (Lu et al., 2009). Although most Oryza genome
types were determined by traditional genome or
molecular analysis (Li et al., 1964), O. coarctata was
designated as an HHKK genome type based solely
on its phylogenetic position (Ge et al., 1999). When
the HH subgenomes in O. coarctata (HHKK) and O.
ridleyi (HHJJ) were compared, no homology was
observed in the intergenic regions. These findings
contrast with other subgenome comparisons that show
homologous sequences and shared transposable
elements in intergenic regions, such as the BB and
CC genome types (Lu et al. 2009). Moreover, the
gene sequence differences between the predicted HH
subgenome types in O. coarctata and O. ridleyi were
more different from AA and BB genome types. Both
of these subgenomes were estimated to have diverged
from each other ~11 Ma. Hence, HH subgenomes in
O. coarctata and O. ridleyi are likely to belong to
different genome types. To avoid confusion Lu et al.
(2009) even suggested O. coarctata should be
designated as KKLL (Sengupta and Majumder,
2010).
Morphology of the Plant
To understand the relation of ecological status of
Porteresia to its genetic content, morphology of the
plant is noteworthy. Discussed in greater detail in our
earlier communication (Sengupta and Majumder,
2010), morphological uniqueness in Porteresia over
other rice plants briefly include salt hairs, elaborate
rhizomatous system, rhizoid like rootlets and
dehiscent seeds on scanty panicles. The morphology
and physiology of Porteresia are discussed in detail
in Sengupta and Majumder (2010) (Fig. 3). The root
The Possible Overlap Between Salinity and Mechanical Challenges in Porteresia coarctata
and rhizome architecture of Porteresia remains
largely unaddressed in literature,however it probably
represents the most significant part of the physiology
of Porteresia.
The Subterranean System of Porteresia
As mentioned previously, Porteresia has a distinctly
different underground system compared to that of
rice. The rhizomes are essentially runners (Fig. 3D),
with high deposition of mechanical tissue. From the
nodes of the rhizome, leaf buds arise that are the
progenitors of new leafy shoots (Fig. 3E). Scale leaves
cover and protect the nodal meristematic regions from
harsh environment as in salt-marsh grasses
(Cyperaceae). Thin rootlets emerge from nodes of
rhizomes (Fig. 3) which may serve the purpose of
absorption and feeble anchorage. The root system
hardly penetrates the soil deeper than a foot (roughly)
in Sundarban area, so we assume the roots may not
have a true root structure, and the rhizome has fullest
ability to absorb water and nutrients as well as
providing anchorage to the substratum. The root
system seems extremely important for the study of
the biology of this mangrove associate.
The plant exhibits a profound and special
system of salt exclusion from leaves, comparable to
salt marsh grasses. Originally described by Flowers
et al. (1990) and later detailed by Sengupta and
Majumder (2009), two types of salt hairs are present
on Porteresia leaves with different mechanisms of
salt exclusion. Both are unicellular trichomes, the
glands on the upper surface of leaf excrete salt, which,
at high concentrations of substrate salinity forms
crystals on the upper surface. On the other hand, hairs
on the lower surface are prone of shedding themselves
off at higher salt concentration, and regenerate at low
salt concentration. This is a typical salt-inundated
estuarine adaptation, where saline water level
constantly fluctuates. To keep at continuum with the
diurnal variation of salt concentration in the medium,
the mechanism of such shedding of glands and regrowing must be a very successful strategy. The
cellular sodium ion concentration and sodium:
potassium ratio in leaf remains low (Sengupta and
Majumder, 2009). According to Flowers et al. (1990),
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Porteresia plants accumulate Na+ and Cl-ions in
leaves, but maintain a Na:K ratio as low as 0.7 even
after 6 weeks of growth in 25% artificial saline water
(ASW) where the Na:K ratio was 34. This points
towards an ability to leach out the salts as well as an
ability to take up saline solution through soil (Bal
and Dutt, 1986). To achieve this, a very high root
pressure is required. To survive such high pressure,
root cells must have a much robust protection/
tolerance mechanism against salt. Unfortunately, root
adaptation against salt is relatively less covered in
previous research.
The Genomic and Proteomic Studies
The genomic and proteomic studies so far done in
Porteresia have been discussed by different workers
(Sengupta and Majumder, 2009; Garg et al., 2013).
Porteresia has been vigorously used as a valuable
bioresource for salt-tolerant gene pool in the last
decade (Majee et al., 2004; Sengupta et al., 2008).
The massive advancement of technology and the
integration of computation in biological sciences has
changed our concept and modified our scope of
looking at the plant from a holistic viewpoint. The
leaf proteome and EST profiles were analyzed in
detail (Sengupta and Majumder, 2009). Their research
shows that the plant can keep a normal, or even
vigorous growth profile under high salt stress. A
differential leaf proteomic profile was generated by
Sengupta and Majumder (2009) in which a very small
subset of proteins related to salt tolerance in
Porteresia were identified. Proteins identified were
involved in several processes such as : protection of
the photosystems from oxidative/hyperionic damage
and maintaining the ETS function; enhancing
available catalytic sites of the main carbonassimilating enzyme Rubis CO under low stromal
CO2 concentration; shunting some active oxygen
species to photorespiratory carbon oxidation (PCO)
cycle; savings of overall energy costs by favouring
low-energy pathways; synthesizing osmotically active
compounds; detoxifying the system by removing
stress-generated alcohols; controlling the
transcriptional regulatory network through stressinduced transcription factors; enhanced synthesis of
chaperones to uphold normal protein structure that
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can be altered during high-stress regime; maintaining
cellular integrity through supplying high amount of
cell wall components and thus retaining normal to
robust growth under stress (Sengupta and Majumder
2009). The identified proteins can well be
functionally related to the physiology of Porteresia
under stress (Fig. 2A, Sengupta and Majumder, 2009).
In a subtractive cDNA profiling, a vast metabolic
alteration in Porteresia leaves in the presence of salt
stress was indicated (Fig. 2B, unpublished data from
the laboratory). More recent next-generation
transcriptome enrichment (Garg et al., 2013) indicates
a close functional overlap of submergence and salinity
tolerance trait in Porteresia, as is expected of
mangrove habitat plants. However, Garg et al. (2013)
and Sengupta and Majumder (2009) made an
observation that the similarity of Porteresia
transcripts to rice transcripts was not very high.
Candidate gene based studies showed that a large
number of Porteresia genes are similar to Rice genes.
On the other hand, a more comprehensive scenario
obtained from proteomic and genomic studies
highlights the fact that many of the salt-stress induced
transcripts in Porteresia do not have any homologues
or orthologues in rice or wild rice; and they are not
even anotated (Sengupta et al., 2009; Garg et al.,
2013). It has also been shown by Sengupta et al. 2008
that genes like Inositol methyl Transferase, which has
not been reported to be present in rice, are present in
Porteresia. Many hypothetical proteins are identified
in Porteresia that may represent a completely
different cluster of genes absent in rice and also
important in salt-tolerance physiology of the plant.
We assume that these genes probably contribute
profoundly to the special physiological traits of the
plant, including high mechanical strength. The
biological processes and the anatomical specialties
are closely related to the restricted habitat of the plant;
and one may conclude that the unknown or
hypothetical proteins/transcripts belong to the KK
genome complement of Porteresia, that is of untraced
origin within rice genotypes.
The extended families of salt-induced
transcription factors reported by Garg et al., (2013)
are rather significant. Most of the TFs are upregulated
during salinity stress and the transcriptional activity
Sonali Sengupta
Fig. 2: A. A summary of proteomic responses of Porteresia coarctata
(adapted from Sengupta and Majumder, 2009).
Diagrammatic representation of the salt-induced molecular
functions and proteins identified through proteomic
analysis: in Porteresia coarctata to be upregulated under
salinity stress. The orange boxes and shapes represent the
proteins and functions identified. Major abbreviations used
are: UDPG UDP-glucose, sus: sucrose synthase, CS1:
cellulose synthase 1, GS1: glutamine synthase, SU IV subunit
IV, MIPS L-myo-inositol-1-P synthase, ADH:
alcoholdehydrogenase, HSP heat shock protein, FNR
ferredoxin-NADP oxidoreductase, FD ferredoxin, cp
chloroplast. B. Functional grouping of salt-induced ESTs
from Porteresia coarctata
is repressed under submergence stress (Garg et al.,
2013). Among the salinity upregulated transcription
factors, NAC, MYB and WRKY are indicated,
whereas among the submergence-upregulated
transcription factors, bZIP, bHLH, HSF and AP2EREBP families may play a major role. Incidentally
NAC and MYB are the most important TFs associated
with lignin deposition in plants and so are bZIP and
The Possible Overlap Between Salinity and Mechanical Challenges in Porteresia coarctata
B
A
C
D
E
H
F
G
I
J
K
Fig. 3: A-K A. Porteresia plant; B. IR-64 Rice potted plant; C.
Plantlets of Porteresia emerging from underground rhizomes
D. Plantlets maintained in culture. Black arrow shows the
rhizome. E. Multiple buds emerging from rhizome that
matures into shoots-shown by a black circle. F. Rice root
system G. Porteresia roots. H. Leaf transverse section of
Porteresia (figure not to scale) I, J. Light microscopic view
of salt hairs (figure not to scale), K. Scanning Electron
Microscope view of the salt hairs
bHLH (Dharmawardhana et al., 2010). A close link
can be assumed between the mechanical stress
tolerance, and saline submergence tolerance in this
plant which is discussed in the next section. Table 2
presents all the genes identified from Porteresia till
date, most of which are reported to be upregulated
during salt stress.
A Hitherto Unexplored Relation to Mechanical
Stress
Mechanical stress is considered a complex form of
pressure-induced stress. It has often been suggested
that the first mechanical stress early microorganisms
1019
faced was that of osmotic stress. In a mangrove
vegetation, the impact of tide is ecologically
enormous on the pioneering undergrowth species,
which remain under noticed. Species like Porteresia,
forms a dense rhizomatous mat and gives support to
soil, which helps in preventing soil erosion during
high and low tides of salt-water. Its rhizoid-like roots
are able to invade through comparatively restricted
air spaces present amongst the soil particles in
estuarine clay. They do not penetrate further in soil
as sea tides are the major source of water. Robust
vegetative propagation and high mechanical strength
of rhizomes is a prerequisite for such pioneering
species. Also, the subterranean part acclimatizes to
the interplay of salt, mechanical and submergence
stress, which seems to be Porteresia’s natural
ecological adaptation. Despite its high vegetative
growth ability, it has never been reported from a nonsaline ecosystem, unless artificially introduced. This
suggests that Porteresiais a natural halophile,
although not an obligate. Its unique rhizomatous
system may account both for its salinity and
mechanical stress tolerance, probably more than the
aerial parts. Unfortunately, the ecology of root and
rhizome system architecture was never studied with
respect to genetic basis in Porteresia coarctata, as
has been studied for the shoot system (Sengupta and
Majumder, 2009).
Overlap Between Salinity and Mechanical Stress
Cellular dehydration and osmotic adjustment brings
a decrease in ambient osmotic potential. This also
brings in mechanical stress, degree of which changes
with the volume of cell cytoplasm. Salt treated plant
cells show reorganization of cytoskeleton and changes
in abundance of several cytoskeletal and
cytoskeleton-associated proteins. Such structural
proteins also play a major role in maintaining
mechanical strength of plant cells. Proteins having
such shared role are actin, tubulin; profilin—an actinbinding protein involved in polymerization and
depolymerization of actin filaments; kinesin—a
microtubule motor involved in microtubuledependent transport processes, especially during cell
cycle and cytokinesis (Pang et al., 2010; Askari et
al., 2006; Wang et al., 2009; Dooki et al., 2006;
Sonali Sengupta
1020
Table 2. Genes/Loci so far reported from Porteresia coarctata in NCBI
Gene/Locus
Accession no.
Reference (Article/Gene)
Oryza coarctata Na+/H+ antiporter (NHX1)
Porteresia coarctata serine-rich protein (PcSrp)
Porteresia coarctata V-ATPase subunit c (PVA1)
Porteresia coarctata translational initiation factor eIF1
Porteresia coarctata inositol 1-phosphate synthase (PINO1)
JQ782416
AF110148
AF286464
AF380357
AF412340
Porteresia coarctata histone H3
AF109910
Porteresia coarctata homeobox protein
Porteresia coarctata metallothionein
Porteresia coarctata alcoholdehydrogenase I (Adh1)
Porteresia coarctata alcohol dehydrogenase II (Adh2)
Porteresia coarctata maturase (matK) gene
Porteresia coarctata fructose-1,6-bisphosphatase (PcCFR)
Porteresia coarctata catA
AF384375
AF257465
AF148593
AF148628
AF148669
AF218845
AB014455
Kizhakkedath P et al, 2003)
Mahalakshmi S et al., (2006) Planta 224(2), 347-359
Unpublished (Senthilkumar P et al., 2000)
Unpublished (Rangan L et al., 2001)
Majee et al., (2004) J. Biol. Chem. 279 (27),
28539-28552
Senthilkumar P et al., (1999) Plant Physiol. 119(2),
806
Rangan L et al., 2001
Padmanaban S et al., 2000
Ge et al., (1999) 96 (25), 14400-14405
Ge et al., (1999) 96 (25), 14400-14405
Ge et al., (1999) 96 (25), 14400-14405
Chatterjee J et al., (2013) PCTOC
Iwamoto M et al., (1999) Theor. Appl. Genet. 98, 853861
Goswami L. et al., 2008
Usha B et al., 2007
Guo YL and Ge, S Am. J. Bot. 92(9), 1548-1558
(2005)
Guo YL. and Ge, S. (2003)
Guo YL and Ge, S. Am. J. Bot. 92(9), 1548-1558
(2005)
Luo S et al., Mol. Biol. Evol. (2011) 28(1), 313-325
Oryza coarctata phosphoenolpyruvate carboxylase (PEPC) EU371116
Oryza coarctata metallothionein type 3 (MT3)
EU121847
Oryza coarctata tRNA-Leu (trnL)
AY792522
Oryza coarctata NADH dehydrogenase subunit 1 (nad1)
Oryza coarctata G protein alpha subunit (GPA1)
AY792545
Oryza coarctata Rp1-like protein pseudogene (OcRp1)
AY507935
AY792544,
GU733154
Porteresia coarctata inositol methyl transferase (PcIMT)
Oryza coarctata ubiquitin 2
EU240449
HQ340170
Oryza coarctata iron deficiency-responsive cis-acting
element-binding factor 1 (IDEF1)
Oryza coarctata inositol-1-phosphate synthase (INO1-1)
Oryza coarctata inositol-1-phosphate synthase (INO1-2)
Oryza coarctata triose phosphateisomerase
Oryza coarctata plastid NADH dehydrogenase (ndhF)
JN615010
Oryza coarctata plastid ribulose bisphosphate carboxylase
(rbcL)
Oryza coarctata Ycf3 protein (ycf3)
HE577876
Oryza coarctata tRNA-Gly (trnG)
FJ908510
Oryza coarctata PSII 10kDa phosphoprotein(psbH)
FJ908378
Oryza coarctata ATP synthase beta chain(atpB) gene
FJ908106
Monoculm1 locus (Clone a0295K14 Monoculm1,
Mlo family protein, aspartic proteinase nepenthesin-1
precursor, microtubule-associated protein MAP65-1a,
IQ calmodulin-binding motif family protein,EMB2261
putative, polygalacturonase precursor, exopolygalacturonase precursor, and putative RNA polymerase A(I)
large subunit genes)
FJ032636
FJ237299
FJ237300
EU371994
HE577878
FJ908683
Sengupta et al., 2008
Philip A et al., (2013) Plant Cell Rep. 32 (8), 11991210
Purohit D et al., (2011)
Ray S et al., (2010) Planta 231 (5), 1211-1227
Ray S et al., (2010) Planta 231 (5), 1211-1227
Sengupta S et al., (2008)
Aliscioni S et al., (2012) New Phytol. 193 (2),
304-312
Aliscioni S et al., (2012) New Phytol. 193 (2),
304-312
Tang L et al., (2010) Mol. Phylogenet. Evol. 54(1),
266-277
Tang L et al., (2010) Mol. Phylogenet. Evol. 54 (1),
266-277
Tang L et al., (2010) Mol. Phylogenet. Evol. 54 (1),
266-277
Tang L et al., (2010) Mol. Phylogenet. Evol. 54 (1),
266-277
Lua F et al., PNAS (2009) 106 (6) 2071–2076
The Possible Overlap Between Salinity and Mechanical Challenges in Porteresia coarctata
Fatehi et al., 2012; Sobhanian et al., 2010; Du et al.,
2010). In salt stressed rice roots, a plant specific
Myosin VIII heavy chain is upregulated that links
cytoskeleton to cell wall linker and also activates
callose synthase complexes in plasma membrane
(Cheng et al., 2009). Remorin, is another plantspecific plasma membrane/lipid raft-associated
filamentous protein which might play an important
role in cytoskeleton reorganization under salt and
mechanical stress (Cheng et al., 2009). A common
adaptation towards salinity is enhanced cellulose
synthase found in salt-treated Porteresia. This
indicates a requirement of plasticity to adapt to an
enhanced osmotic pressure (Sengupta and Majumder,
2009) Similarly, an increased level of β-dglucanexohydrolase was found in creeping bentgrass
(Xu et al., 2010). Cell-wall associated glycine-rich
proteins (GRP) reveal both mechanical and defence
properties (Dooki et al., 2006; Du et al., 2010).
Changes in cytoskeletal as well as plasma-membrane
associated proteins with mechanical functions
indicate profound alterations in both intracellular and
cell wall architecture of plant cells facing the impacts
of an osmotic stress. It is expected that at high tide,
Porteresia rhizome and roots would display an array
of proteins that will increase the mechanical strength
of the subterranean part alongwith providing an
osmotic protection. No studies till date has been done
with Porteresia growing in its native habitat, in high
and low tidal conditions. No effort has been made to
identify the effect of mechanical stress on this wild
rice. It is important to start such studies and look for
mechanical sensors and shared response pathways
for coupled salt and mechanical stress in Porteresia
coarctata. The knowledge thus obtained can be
transferred to cultivated rice for agricultural benefits.
Conclusion
Under high salinity, or mechanical obstruction, rice
root bends away from the saline zone and scans the
rhizosphere for a stress-free area (Unpublished data
from the laboratory). Regulated by combined function
of ethylene and auxin on root growth, such bending
is a characteristic of the root system of a plant, and
can be used as a tolerance index (unpublished data).
1021
In a saline-water-washed ecosystem, however,
bending and escaping is not a feasible route. It is
necessary for the subterranean cells to maintain their
osmotic pressure. The plant has to survive salinity
and the pressure exerted by high and low tides, and
thus, the rhizome cells must show osmotic tolerance,
and must be mechanically very strong. There are
needs of lignification and secondary tissue
development in the root. The future research needs
to address the rhizome biology of Porteresia; from a
genomic, transcriptomic and proteomic aspect and
also needs to correlate that with the physiology.
Porteresia in its native habitat, i.e. growing as a
mangrove undergrowth, covers all the interaction
types discussed in Fig. 1. High anthropogenic input
without attempts to domesticate renders Porteresia
as ecologically vulnerable species. Being the only
salt-tolerant wild rice, Porteresia represents a
valuable source of genes that may confer stability
and tolerance to high-yield sensitive rice and increase
the viable agricultural area in the coasts. In our recent
work, we observed that the bending and directional
growth of rice roots is similar in salt and mechanical
stress, with a large set of co-expressing transcripts
(Unpublished data from laboratory, Adak et al.). It
will be of great interest to know what is the bending
and structural alteration pattern that Porteresia root
and rhizomes may exhibit in a mangrove ecosystem
during high and low tides. It will be of further interest
to determine what are the common molecular
determinants that dictate the specific physiological
characteristics and help the plant to survive the
combined salinity, submergence and mechanical
challenges in nature. Mechanical stress and salinity,
probably has more shared characteristic than
acknowledged so far. A mangrove associate like
Porteresia present us with ample scope to evaluate
such hypothesis. In our earlier work (Sengupta and
Majumder, 2009), we dissected the molecular
physiology of this plant. Molecular ecophysiology
of Porteresia coarctata will provide a more rational
insight into the biology of the system and help
understand the interplay of mechanical and salinity
stress.
Sonali Sengupta
1022
Acknowledgement
I thank the Department of Biotechnology and
Department of Science and Technology, Govt. of
India for financial support, and Indian National
Science Academy for presenting me an opportunity
to contribute to the Proceedings. I also thank Prof.
Arun Lahiri Majumder for critical reading of the
manuscript.
References
Aliscioni S et al. (2012) New grass phylogeny resolves deep
evolutionary relationships and discovers C4 origins. New
Phytol 193(2) 304-312
Askari H, Edqvist J, Hajheidari M, Kafi M and Salekdeh GH
(2006) Effects of salinity levels on proteome of Suaeda
aegyptiaca leaves. Proteomics 6 2542-2554
Bal AR and Dutt SK (1986) Mechanisms of salt tolerance in
wild rice (Oryza coarctata Roxb. Plant and Soil 92 399404
Cheng Y, Qi Y, Zhu Q, Chen X, Wang N, Zhao X, Chen H, Cui
X, Xu L and Zhang W (2009) New changes in the plasmamembrane-associated proteome of rice roots under salt
stress. Proteomics 9 3100-3114
Dharmawardhana P, Brunner AM and Strauss SH (2010)
Genome-wide transcriptome analysis of the transition from
primary to secondary stem development in Populust
richocarpa. BMC Genomics 11 150. doi: 10.1186/14712164-11-150
Dooki AD, Mayer-Posner FJ, Askari H, Zaiee AA and Salekdeh
GH (2006) Proteomic responses of rice young panicles to
salinity. Proteomics 6 6498-6507
Du CX, Fan HF, Guo SR, Tezuka T and Li J (2010) Proteomic
analysis of cucmber seedling roots subjected to salt stress.
Phytochemistry 71 1450-1459
Fatehi F, Hosseinzadeh A, Alizadeh H, Brimavandi T and Struik
PC (2012) The proteome response of salt-resistant and
salt-sensitive barley genotypes to long-term salinity stress.
Mol Biol Rep 39 6387-6397
Finch RP, Mcroberts N and Balakrishna P (1997) Molecular
analysis of diversity in Porteresia coarctata. Rice
Biotechnology Quarterly 29 10-15
Flowers TJ, Flowers SA, Hajibagheri MA and Yeo AR (1990)
Salt tolerance in the halophytic wild rice, Porteresia
coarctata. T New Phytol 114 675-684
Gao C, wang Y, Liu G, Yang C, Jiang J and Li H (2008) Expression
profiling of salinity alkali stress responses by large-scale
expressed sequence tag analysis in Tamarix hispid. Plant
MolBiol 66(3) 245-258
Garcia A (1992) Salt tolerance in the halophytic wild rice,
Porteresia coarctata Tateoka. Ph.D. Thesis, University of
Sussex
Garg R, Verma M, Agrawal S, Shankar R, Majee M and Jain M
(2013) Deep Transcriptome Sequencing of Wild Halophyte
Rice, Porteresia coarctata, Provides Novel Insights into
the Salinity and Submergence Tolerance Factors
doi:10.1093/dnares/dst042
Ge S, Sang T, Lu B and Hong D (1999) Phylogeny of rice
genomes with emphasis on origins of allotetraploid species.
Proc Natl Acad Sci USA 96(25) 14400-14405
Ghosh Dastider K, Maitra S, Goswami L, Roy D, Das KP and
Majumder AL (2006) An insight into the molecular basis
of salt-tolerance of L-myo inositol 1-phosphate synthase
(PcINO1) from Porteresia coarctata (Roxb.) Tateoka, a
halophytic wild rice. Plant Physiol 140 1279-1296
Goswami L, Nandy P, Ray S, Sengupta S, Patra B and Lahiri
Majumder A Isolation and cloning of a partial cDNA
sequence encoding phosphoenol pyruvate carboxylase
from Porteresia coarctata (Roxb). Tateoka. Unpublished
Guo YL and Ge S (2005) Molecular phylogeny of Oryzeae
(Poaceae) based on DNA sequences from chloroplast,
mitochondrial, and nuclear genomes. Am J Bot 92(9) 15481558
GuoYL and Ge S The utility of mitochondrial nad1 intron in the
phylogenetic study of Oryzeae. Unpublished
Iwamoto M, Nagashima H, Nagamine T, Higo H and Higo K
(1999) p-SINE1-like intron of the CatA catalase homologs
and phylogenetic relationships among AA-genome Oryza
and related species. Theor Appl Genet 98 853-861
Jagtap TG, Bhosale S and Singh C (2006) Characterization of
Porteresia coarctata beds along the Goa coast, India.
Aquatic Botany 84 37-44
Kizhakkedath P, Venkataraman G and Parida A (unpublished as
article) Isolation, characterization and overexpression of
a diurnally regulated vacuolar NHX-type antiporter from
the halophytic wild rice Porteresia coarctata (Roxb.)
Lacerda LD, Conde JE, Kjerfve B et al. American mangroves.
In: Lacerda LD, editor.Mangrove Ecosystems: Function
and Management. Berlin, Germany: Springer; 2002. p.162
Latha R, Rao CS, Subramaniam HMS, Eganathan P and
Swaminathan MS (2004) Approaches to breeding for
salinity tolerance—a case study on Porteresia coarctata.
Ann Appl Biol 144(2) 177-184
Lu F, Ammiraju JS, Sanyal A, Zhang S, Song R, Chen J, Li G,
Sui Y, Song X, Cheng Z, de Oliveira AC, Bennetzen JL,
The Possible Overlap Between Salinity and Mechanical Challenges in Porteresia coarctata
Jackson SA, Wing RA and Chen M (2009) Comparative
sequence analysis of MONOCULM1-orthologous regions
in 14 Oryza genomes. Proc Natl Acad Sci USA 106(6)
2071-2076
Luo S, Peng J, Li K, Wang M and Kuang H(2011) Contrasting
evolutionary patterns of the Rp1 resistance gene family in
different species of poaceae. Mol Biol Evol 28(1) 313325
Mahalakshmi S, Christopher GS, Reddy TP, Rao KV and Reddy
VD (2006) Isolation of a cDNA clone (PcSrp) encoding
serine-rich-protein from Porteresia coarctata T. and its
expression in yeast and finger millet (Eleusine coracana
L.) affording salt tolerance. Planta 224(2) 347-359.
Majee M, Maitra S, Ghose Dastidar K, Pattanaik S, Chatterjee
A, Hait N, Das KP and Majumder AL (2004) A novel salttolerant L-myo-inositol-1-phosphate synthase from
Porteresia coarctata (Roxb.) Tateoka, a halophytic wild
rice. J Biol Chem 279(27) 28539-2855
Padmanaban S, Madasamy P and Parida A Cloning and
characterization of a metallothione in gene from the
mangrove species Porteresia coarctata Tateoka
Unpublished
Pang Q, Chen S, Dai S, Chen Y, Wang Y and Yan X (2010)
Comparative proteomics of salt tolerance in Arabidopsis
thaliana and Thellungiella halophila. J Proteome Res 9
2584-2599
Parani M, Lakshmi M, Senthilkumar P et al. (1998) Molecular
phylogeny of mangroves V Analysis of genome
relationships in mangrove species using RAPD and RFLP
markers. Theor Appl Genet 97 617-25
Philip A, Syamaladevi DP, Chakravarthi M, Gopinath K and
Subramonian N (2013) 5' Regulatory region of ubiquitin
2 gene from Porteresia coarctata makes efficient
promoters for transgene expression in monocots and dicots.
Plant Cell Rep 32(8) 1199-1210
Purohit D, George S, Sankararamasubramanian H and Parida A
Idef1 transcript expression is regulated by iron deficiency
combined with salt treatment in the halophytic wild rice
relative Porteresia coarctata. Unpublished
Rangan L, Bennett J and Hosseini S (Unpublished as article)
Molecular cloning and expression of stress-responsive
eIF1 gene in Porteresia coarctata Tateoka
1023
halophytic rice, Porteresia coarctata Planta 231(5) 12111227
Sengupta S, Patra B, Ray S and Majumder AL (2008) Inositol
methyl tranferase from ahalophytic wild rice, Porteresia
coarctata Roxb. (Tateoka): regulation of pinitol
synthesisunder abiotic stress. Plant cell Environ 31(10)
1442-1459
Sengupta S and Majumder AL (2009) Insight into the salt
tolerance factors of wild halophytic rice, Porteresia
coarctata: a physiological and proteomic approach. Planta
229(4) 911-929
Sengupta S and Majumder AL (2010) Porteresia coarctata (Roxb.)
Tateoka, a wild rice: a potential model for studying saltstress biology in rice. Plant, Cell & Environment 33(4)
526-542
Senthilkumar P, Parani M and Parida A (Unpublished as article)
V-ATPase subunit c from a salt tolerant wild rice Porteresia
coarctata. Unpublished
Senthilkumar P, Parani M, Lakshmi M, Jithesh MN and Parida A
(1999) Histone H3 gene from Porteresia coarctata. Plant
Physiol 119(2) 806
Sobhanian H, Razavizadeh R, Nanjo Y, Ehsanpour AA, Jazii FR,
Motamed N and Komatsu S (2010) Proteome analysis of
soybean leaves, hypocotyls and roots under salt stress.
Proteome Sci 8 19
Tang L, Zou XH, Achoundong G, Potgieter C, Second G, Zhang
DY and Ge S (2010) Phylogeny and biogeography of the
rice tribe (Oryzeae): evidence from combined analysis of
20 chloroplast fragments. Mol Phylogenet Evol 54(1) 266277
Tateoka T (1965) Porteresia, a new genus of Graminae. Bulletin
of National Science Museum, Tokyo 8 405-406
Tomlinson PB The Botany of Mangroves. Cambridge, UK:
Cambridge University Press; 1986
Usha B, Nisha SK, Jithesh MN and Parida A Characterization of
type 3 metallothionein from a mangrove associate,
Porteresia coarctata Unpublished
Wang L, Meirong Mu M, Li X, Lin P and Wang W (2010)
Differentiation between true mangroves and mangrove
associates based on leaf traits and salt contents. J Plant
Ecol .doi:10.1093/jpe/rtq008
Rangan L, Bennett J and Hosseini SG. Homeobox gene from
Porteresia coarctata induced by salinity stress.
Unpublished
Wang X, Fan P, Song H, Chen X, Li X and Li Y (2009)
Comparative proteomic analysis of differentially expressed
proteins in shoots of Salicorniaeuropaea under different
salinity. J Proteome Res 8 3331-3345
Ray S, Patra B, Das-Chatterjee A, Ganguli A and Majumder AL
(2010) Identification and organization of chloroplastic and
cytosolic L-myo-inositol 1-phosphate synthase coding
gene(s) in Oryzasativa: comparison with the wild
Xu C, Sibicky T and Huang B (2010) Protein profile analysis of
salt-responsive proteins in leaves and roots in two cultivars
of creeping bentgrass differing in salinity tolerance. Plant
Cell Rep 29 595-615.