Download Plant–Microbe Communications for Symbiosis

Plant–Microbe Communications for Symbiosis
Masayoshi Kawaguchi1 and Kiwamu Minamisawa2
1Division
of Symbiotic Systems, National Institute for Basic Biology, Okazaki, Japan
School of Life Sciences, Tohoku University, Sendai, Japan
2Graduate
Symbiosis is a biological phenomenon involving dynamic
changes in the genome, metabolism and signaling network,
and a multidirectional comprehension of these interactions is
required when studying symbiotic organisms. In plant–microbe
interactions, two symbiotic systems have been actively studied
for many years. One is arbuscular mycorrhizal (AM) symbiosis
and the other is root nodule (RN) symbiosis. AM symbiosis is
probably the most widespread interaction between plants
and microbes, in the context of phylogeny and ecology (Kistner
and Parniske 2002, Bonfante and Genre 2010). More than 80%
of all land plant families are thought to have a symbiotic
relationship with AM fungi that belong to the Glomeromycota.
The origin of AM symbiosis is thought to be in the early
Devonian period, approximately 400 million years ago. Thus,
AM symbiosis is also called the mother of plant root endosymbioses (Parniske 2008). On the other hand, RN symbiosis
involves morphogenesis and is formed by communication
between plants and nitrogen-fixing bacteria.
Plant nutrient transporters for AM symbiosis
AM fungi absorb minerals, including phosphate and nitrogen,
via extraradical hyphae and supply them to the plant, possibly
via highly branched structures inside root cells known as
arbuscules (Harrison 1999, Parsnike 2008). The arbuscules are
enveloped in plant-derived membranes, the periarbuscular
membrane. To absorb phosphate, mycorrhiza-induced phosphate transporter genes, such as MtPT4, are predominantly or
exclusively up-regulated in plant root cells containing arbuscules. Some of these genes have been shown to be required for
AM symbiosis as well as the acquisition of phosphate delivered
by the AM fungus (Javot et al. 2007). Interestingly, in addition
to phosphate, AM fungi transfer substantial amounts of nitrogen to the host plants (Javot et al. 2007). Nitrogen sources such
as ammonium and amino acids are translocated to the plant
via fungal hyphae. Several ammonium transporters (AMTs)
have been identified in plants, and it will be interesting to
determine their precise expression patterns and subcellular
location. Kobae et al. report in this issue that GmAMT4.1
identified from the soybean genome database shows specific
expression in arbusculated cortical cells. Moreover, they
show that GmAMT4.1 is localized on the branch domains of
periarbuscular membranes, indicating that arbuscule branches
are active sites for ammonium transport (Kobae et al. 2010).
Plant factors in RN symbiosis
RN symbiosis in legumes involves host-specific recognition
and post-embryonic development of a nitrogen-fixing organ,
the root nodule. Compared with our extensive knowledge of
the bacterial factors required for RN symbiosis, such as Nod
factors, lipo- and exopolysaccharides (Jones et al. 2007), little is
known about the symbiotic factors in terms of the plant.
Molecular genetics and genomics of two model legumes, Lotus
japonicus and Medicago truncatula, have made a significant
contribution to the identification of a number of plant factors
and to an understanding of the molecular basis of nodule
initiation, rhizobial infection, organogenesis, nitrogen fixation,
senescence and feedback regulation (Sandal et al. 2006, Oldroyd
and Downie 2008, Kouchi et al. 2010). Among these phenomena, nodule senescence, namely regulation of nodule lifespan,
is uncharted territory but would gain in importance when our
aim is to achieve long-term nitrogen-fixing activity in legumes.
D’haeseleer et al. analyzed the nodule senescence up-regulated
gene M. truncatula ATB2. The MtATB2 gene encodes a bZIP
transcription factor and is regulated by sucrose and light conditions as well as during nodule senescence. For nodule function,
carbon is provided mainly as sucrose derived from photosynthesis and transported via the phloem. These authors show
that the MtATB2 transcripts occur in and around the vascular
tissue of nodules and roots and in the nodule apex (D’haeseleer
et al. 2010).
Leguminous plants strictly control nodule numbers, because
nodulation and nitrogen fixation are an energy drain on the
host. To maintain the symbiotic balance with rhizobia, plants
have evolved negative feedback systems known as autoregulation of nodulation (AON). AON involves long-distance signaling via shoot–root communication and is mediated by
CLAVATA1-like receptor kinases such as L. japonicus HAR1,
Glycine max NARK and M. truncatula SUNN (Oka-Kira and
Kawaguchi 2006, Ferguson et al. 2010). In L. japonicus, grafting
experiments have shown that HAR1 and KLAVIER function in
the shoot to restrict the nodule number while TML functions in
the root. In this issue, Yoshida et al. report the characteristics of
Plant Cell Physiol. 51(9): 1377–1380 (2010) doi:10.1093/pcp/pcq125, available online at www.pcp.oxfordjournals.org
© The Author 2010. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists.
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Plant Cell Physiol. 51(9): 1377–1380 (2010) doi:10.1093/pcp/pcq125 © The Author 2010.
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a novel root-regulated hypernodulating mutant in L. japonicus
named plenty. Unlike TML, PLENTY appears to act independently of HAR1-mediated long-distance control of nodulation
and mediates nitrate signaling (Yoshida et al. 2010). Thus,
plenty is invaluable for dissecting the complex web of negative
regulatory systems in nodulation.
NSP1 and NSP2, which encode a GRAS family transcription
factor, are required for nodule initiation and act as components
of the Nod factor signaling pathway downstream of Ca2+
spiking (Oldroyd and Downie 2008, Kouchi et al. 2010).
The homologs are widely conserved in non-leguminous
plants but their functions are unknown. Yokota et al. isolated
homologs of NSP1/2 from the monocot rice, OsNSP1 and
OsNSP2, and introduced these genes into nsp1 and nsp2
non-nodulating mutants in L. japonicus, respectively. Transformation with OsNSP1 and OsNSP2 fully rescued the mutant
phenotypes such as nodule development and nitrogenase
activity, indicating that these rice transcription factors can
potentially mediate Nod factor signaling in L. japonicus
(Yokota et al. 2010). Precise expression and functional analyses
of NSP1/2 homologs in rice would shed light on their original
function in plants.
Bacterial factors in RN symbiosis
In response to stimulation by flavonoids exuded from legume
roots into soil, rhizobia synthesize signaling molecules that are
responsible for nodule formation. These signaling molecules,
named Nod factors, have been identified as lipochitooligosaccharides decorated with diverse chemical substitutions
(Spaink 1995). Nod factors are certainly a key trigger for legume
symbiotic signaling and nodule organogenesis (Kouchi et al.
2010). However, other rhizobial systems such as exopolysaccharide excretion (Skorupska et al. 2006), ethylene biosynthesis
regulation (Okazaki et al. 2004, Gresshoff et al. 2009), protein
secretion systems (Deakin and Broughton 2009) and BacA
(LeVier et al. 2000) are often required for the establishment of
symbiosis with legumes, probably because they are involved in
bacterial release into the host cytoplasm and bacteroid
development.
BacA protein, a cytoplasmic membrane protein conferring
resistance to peptide antibiotics, was the first bacterial
factor identified as essential for bacteroid development in
Sinorhizobium meliloti (LeVier et al. 2000). Interestingly,
a homolog of BacA in Brucella abortus, an animal pathogen,
is required for effective survival in murine macrophages
(LeVier et al. 2000). In this special issue, Maruya and Saeki
(2010) examine the physiological functions of the BacA
homolog in Mesorhizobium loti. From study of a bacA mutant,
they found that BacA is dispensable for M. loti symbiosis with
L. japonicus. However, the M. loti bacA gene partially restored
the symbiosis-defective phenotype of a S. meliloti bacA mutant
by genetic complementation. These results raise the question
of why BacA is not absolutely required for symbiosis with
M. loti but it is required for that with S. meliloti. Recently, other
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legume–rhizobium partners were examined for their BacA
requirement for symbiosis (Karumakaran et al. 2010). One
fascinating explanation is that BacA is exclusively required in
galegoid legumes producing defensin-type antimicrobial
peptides (NCR peptides).
Changes in plant-associated microbial
communities
Our knowledge of the molecular interplay between plant and
AM and RN symbionts has developed over the past decade
(Oldroyd and Downie 2008, Parniske 2008, Kouchi et al. 2010).
Diverse microbes are able to associate with plants in natural
habitats as endophytes and epiphytes (Mano and Morisaki
2008, Saito et al. 2007). The cellular signaling networks that
determine RN and AM symbioses overlap in legumes, suggesting that the molecular components of the legume-specific
networks are shared with other plant-associated microbes.
In this special issue, Ikeda et al. (2010) report the microbial
community shifts of field-grown soybeans with different nodulation genotypes and nitrogen levels, suggesting that soybean
accommodates a taxonomically characteristic microbial community by a system of autoregulation of nodulation involving
symbiotic signal networks. A unique procedure of bacterial
enrichment from plant tissues assisted this study significantly,
although profiling techniques currently used to assess the
microbial community structure in environmental microbiology
required further development (Saito et al. 2007). These efforts
could provide platforms for dissecting the organization and
functions of rhizosphere and phyllosphere microbial communities, and for identifying the plant loci that contribute to their
formation (Bisseling 2009). In addition, a deeper understanding
of plant-associated microbial communities offers exciting
opportunities for controlling crop growth in sustainable agricultural settings.
Valuable input from genomics and bioresources
The genomics of both partners (legumes and rhizobia) and
their bioresources have been crucial in the facilitation of recent
progress in the study of legume and microbe interactions.
In particular, the activities of the Kazusa DNA Research
Institute and the M. truncatula genome sequence consortium
have contributed significantly to our understanding of plant–
microbe interactions, which may be summarized as follows:
(i) Information has been generated on the majority of genome
sequence from euchromatic regions and corresponding
genetic markers for model legumes (Young et al. 2005,
Sato et al. 2008). Web databases have been constructed
for the L. japonicus genome database, miyakogusa.jp
(http://www.kazusa.or.jp/lotus/) and M. truncatula
sequencing resources (http://www.medicago.org/genome/),
to provide detailed information on L. japonicus and
M. truncatula genomes and markers (Young et al. 2005,
Plant Cell Physiol. 51(9): 1377–1380 (2010) doi:10.1093/pcp/pcq125 © The Author 2010.
Sato et al. 2008). This greatly facilitates the identification of
causal genes of symbiotic mutants in the model legumes
(Sandal et al. 2006, Oldroyd and Downie 2008, Parniske
2008, Kouchi et al. 2010).
(ii) Complete genome sequences have been obtained of the
endosymbionts Mesorhizobium loti MAFF303099 (Kaneko
et al. 2000), Sinorhizobium meliloti 1021 (Galibert et al. 2001)
and Bradyrhizobium japonicum USDA110 (Kaneko et al.
2002), and the endophyte Azospirillum sp. B510 (Kaneko
et al. 2010), and comprehensive web databases for these
bacteria have been constructed: RhizoBase (http://genome
.kazusa.or.jp/rhizobase/) and RhizoGATE (http://www
.cebitec.uni-bielefeld.de/CeBiTec/rhizogate/).
(iii) Several analysis tools and post-genomic data for S. meliloti
have been well integrated in RhizoGATE (http://www
.cebitec.uni-bielefeld.de/CeBiTec/rhizogate/). A large-scale
protein–protein interaction database for M. loti using
the yeast two-hybrid system is available (Shimoda et al.
2008a). In addition, a mutant library of M. loti has been
constructed using the signature-tagged mutagenesis technique, covering 3,680 non-redundant M. loti genes (51%
of the total genes) (Shimoda et al. 2008b), which is distributed worldwide via the NBRP (http://www.legumebase
.brc.miyazaki-u.ac.jp/).
This information together with the mutant material will
enable significant progress in this field in the next decade.
This special collection of articles highlights some of the recent
progress made in understanding plant–microbe symbiosis and
its contribution to the plant and microbial worlds.
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