Leguminous Plants: Inventors of Root Nodules to Accommodate Symbiotic Bacteria

Suzaki, Takuya; Yoro, Emiko; Kawaguchi, Masayoshi

doi:10.1016/bs.ircmb.2015.01.004

Cited by 120 publications

(95 citation statements)

References 198 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Legume nodules represent a unique environmental niche derived from differentiated cortical root cells where both symbiotic and nonsymbiotic bacteria are allowed accommodation and proliferation. Laboratory studies with single WT or mutant symbiotic strains demonstrated a stepwise, hostcontrolled colonization process ensuring symbiont selection (34). By contrast, little is known about the extent or the diversity of nodule and root colonization by nonsymbionts (35).…”

Section: Resultsmentioning

confidence: 99%

Root nodule symbiosis in Lotus japonicus drives the establishment of distinctive rhizosphere, root, and nodule bacterial communities

Zgadzaj

Garrido‐Oter

Jensen

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

269

217

View full text Add to dashboard Cite

Lotus japonicus has been used for decades as a model legume to study the establishment of binary symbiotic relationships with nitrogen-fixing rhizobia that trigger root nodule organogenesis for bacterial accommodation. Using community profiling of 16S rRNA gene amplicons, we reveal that in Lotus, distinctive noduleand root-inhabiting communities are established by parallel, rather than consecutive, selection of bacteria from the rhizosphere and root compartments. Comparative analyses of wild-type (WT) and symbiotic mutants in Nod factor receptor5 (nfr5), Nodule inception (nin) and Lotus histidine kinase1 (lhk1) genes identified a previously unsuspected role of the nodulation pathway in the establishment of different bacterial assemblages in the root and rhizosphere. We found that the loss of nitrogen-fixing symbiosis dramatically alters community structure in the latter two compartments, affecting at least 14 bacterial orders. The differential plant growth phenotypes seen between WT and the symbiotic mutants in nonsupplemented soil were retained under nitrogen-supplemented conditions that blocked the formation of functional nodules in WT, whereas the symbiosis-impaired mutants maintain an altered community structure in the nitrogen-supplemented soil. This finding provides strong evidence that the root-associated community shift in the symbiotic mutants is a direct consequence of the disabled symbiosis pathway rather than an indirect effect resulting from abolished symbiotic nitrogen fixation. Our findings imply a role of the legume host in selecting a broad taxonomic range of root-associated bacteria that, in addition to rhizobia, likely contribute to plant growth and ecological performance.Lotus japonicus | microbiota | symbiosis | 16S | nitrogen fixation

show abstract

Section: Resultsmentioning

confidence: 99%

Root nodule symbiosis in Lotus japonicus drives the establishment of distinctive rhizosphere, root, and nodule bacterial communities

Zgadzaj

Garrido‐Oter

Jensen

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

269

217

View full text Add to dashboard Cite

show abstract

“…Autoregulation of nodulation (AON) is a conserved mechanism observed among diverse leguminous species by which plants restrict the number of root nodules, the symbiotic organs containing nitrogen-fixing rhizobia, to conserve energy related to nodulation (Caetano-Anolles and Gresshoff 1991;Oka-Kira and Kawaguchi 2006;Suzaki et al 2015). The basic concept of AON is as follows.…”

Section: Introductionmentioning

confidence: 99%

Expression of the CLE-RS3 gene suppresses root nodulation in Lotus japonicus

et al. 2016

Self Cite

View full text Add to dashboard Cite

Cell-to-cell communication, principally mediated by short- or long-range mobile signals, is involved in many plant developmental processes. In root nodule symbiosis, a mutual relationship between leguminous plants and nitrogen-fixing rhizobia, the mechanism for the autoregulation of nodulation (AON) plays a key role in preventing the production of an excess number of nodules. AON is based on long-distance cell-to-cell communication between roots and shoots. In Lotus japonicus, two CLAVATA3/ESR-related (CLE) peptides, encoded by CLE-ROOT SIGNAL 1 (CLE-RS1) and -RS2, act as putative root-derived signals that transmit signals inhibiting further nodule development through interaction with a shoot-acting receptor-like kinase HYPERNODULATION ABERRANT ROOT FORMATION 1 (HAR1). Here, an in silico search and subsequent expression analyses enabled us to identify two new L. japonicus CLE genes that are potentially involved in nodulation, designated as CLE-RS3 and LjCLE40. Time-course expression patterns showed that CLE-RS1/2/3 and LjCLE40 expression is induced during nodulation with different activation patterns. Furthermore, constitutive expression of CLE-RS3 significantly suppressed nodule formation in a HAR1-dependent manner. TOO MUCH LOVE, a root-acting regulator of AON, is also required for the CLE-RS3 action. These results suggest that CLE-RS3 is a new component of AON in L. japonicus that may act as a potential root-derived signal through interaction with HAR1. Because CLE-RS2, CLE-RS3 and LjCLE40 are located in tandem in the genome and their expression is induced not only by rhizobial infection but also by nitrate, these genes may have duplicated from a common gene.

show abstract

“…Soil-dwelling bacteria from the Rhizobiaceae family form a species-specific symbiosis with their legume hosts that is characterized by the formation of a plant organ known as a nodule (Cooper 2007;Jones et al 2007;Suzaki et al 2015). In developing nodules, bacteria undergo metamorphosis into bacteroids, which fix atmospheric nitrogen into ammonium.…”

mentioning

confidence: 99%

Sinorhizobium meliloti Chemotaxis to Multiple Amino Acids Is Mediated by the Chemoreceptor McpU

Webb

Compton

Campo

et al. 2017

MPMI

View full text Add to dashboard Cite

The legume symbiont Sinorhizobium meliloti is chemoattracted to compounds exuded by germinating seeds of its host alfalfa. This response is mainly mediated by the S. meliloti chemoreceptor McpU. McpU also has a prominent contribution in sensing a synthetic amino acid (aa) mixture mimicking the amounts and composition observed in seed exudate. Here, we used the hydrogel capillary assay to quantify chemotactic responses of S. meliloti to individual aa exuded by germinating alfalfa seeds and to define the role of McpU in this behavior. S. meliloti exhibited positive chemotaxis responses to all proteinogenic aa, except for aspartate, and to citrulline, cystine, gamma-aminobutyric acid, and ornithine. Wild-type responses were diverse in intensity, while a strain lacking mcpU displayed strongly diminished responses. Differential scanning fluorimetry demonstrated interaction of the purified periplasmic region of McpU (McpU-PR) with the aa, except glutamate and aspartate. We additionally tested organic acids and sugars, but there were no significant interactions with the McpU ligand-binding domain, except for citrate. Using ligand displacement, we confirmed the interaction of McpU-PR with aa representing strong and weak attractants. Our results show that S. meliloti McpU is a broad-range aa receptor mediating differential responses to individual attractants, which does not bind negatively charged aa.

show abstract

Leguminous Plants: Inventors of Root Nodules to Accommodate Symbiotic Bacteria

Cited by 120 publications

References 198 publications

Root nodule symbiosis in Lotus japonicus drives the establishment of distinctive rhizosphere, root, and nodule bacterial communities

Root nodule symbiosis in Lotus japonicus drives the establishment of distinctive rhizosphere, root, and nodule bacterial communities

Expression of the CLE-RS3 gene suppresses root nodulation in Lotus japonicus

Sinorhizobium meliloti Chemotaxis to Multiple Amino Acids Is Mediated by the Chemoreceptor McpU

Contact Info

Product

Resources

About