Plants establish beneficial associations with nitrogen-fixing bacteria and with arbuscular mycorrhizal fungi (AMF) to facilitate the acquisition of nutrients that are limiting to plant growth. These symbiotic associations must be newly established in each plant, and this involves the recognition of diffusible lipochitooligosaccharide (LCO) signals called nodulation factors (Nod factors) and mycorrhizal factors (Myc factors), produced by rhizobia and AMF, respectively.
Receptors containing oligosaccharide-binding LysM domains are involved in the recognition of LCOs from microbial symbionts. Two such receptors, Nod factor receptor 1 (NFR1) and NFR5, have been shown to bind Nod factors directly.
Recognition of a range of microbial oligosaccharides involves LysM-containing receptor complexes. These receptors can be involved in the promotion of symbiont infection or the restriction of pathogen colonization.
A common symbiosis signalling pathway is involved in the promotion of rhizobial and mycorrhizal associations. This signalling pathway uses oscillations in calcium as a secondary messenger. Despite the commonality in signalling in these symbiosis pathways, specificity must be maintained to ensure appropriate responses to each symbiont.
The production of symbiont-induced calcium oscillations involves a cation channel (or channels) that is most probably associated with potassium flow, a SERCA-type calcium pump and an as-yet-undefined calcium channel. Modelling suggests that these three components are sufficient for self-sustaining calcium oscillations.
Recognition of calcium oscillations involves calcium- and calmodulin-dependent serine/threonine protein kinase (CCaMK), which associates with and phosphorylates a transcriptional regulator. Autoactivation of this calcium-signalling complex is sufficient to promote symbiotic responses.
Transcription factor complexes involving a variety of GRAS domain-containing proteins are involved in regulating symbiotic gene expression. The specificity of symbiosis signalling seems to be defined by differential complexes of GRAS domain proteins, and these different complexes have specific roles in the regulation of plant gene expression associated with either rhizobia or AMF.
Plants associate with a wide range of microorganisms, with both detrimental and beneficial outcomes. Central to plant survival is the ability to recognize invading microorganisms and either limit their intrusion, in the case of pathogens, or promote the association, in the case of symbionts. To aid in this recognition process, elaborate communication and counter-communication systems have been established that determine the degree of ingress of the microorganism into the host plant. In this Review, I describe the common signalling processes used by plants during mutualistic interactions with microorganisms as diverse as arbuscular mycorrhizal fungi and rhizobial bacteria.
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Akiyama, K., Matsuzaki, K. & Hayashi, H. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435, 824–827 (2005). This paper defines strigolactones as signals that promote hyphal branching of AMF.
Besserer, A. et al. Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol. 4, 1239–1247 (2006).
Gomez-Roldan, V. et al. Strigolactone inhibition of shoot branching. Nature 455, 189–194 (2008).
Long, S. R. & Staskawicz, B. J. Prokaryotic plant parasites. Cell 73, 921–935 (1993).
Chabaud, M., Venard, C., Defaux-Petras, A., Becard, G. & Barker, D. G. Targeted inoculation of Medicago truncatula in vitro root cultures reveals MtENOD11 expression during early stages of infection by arbuscular mycorrhizal fungi. New Phytol. 156, 265–273 (2002).
Kosuta, S. et al. A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiol. 131, 952–962 (2003).
Kosuta, S. et al. Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes. Proc. Natl Acad. Sci. USA 105, 9823–9828 (2008).
Olah, B., Briere, C., Becard, G., Denarie, J. & Gough, C. Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signalling pathway. Plant J. 44, 195–207 (2005).
Dénarié, J., Debelle, F. & Prome, J.-C. Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu. Rev. Biochem. 65, 503–535 (1996).
Oldroyd, G. & Downie, A. Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu. Rev. Plant Biol. 59, 519–546 (2008).
Oldroyd, G. E. & Downie, J. A. Calcium, kinases and nodulation signalling in legumes. Nature Rev. Mol. Cell Biol. 5, 566–576 (2004).
Oldroyd, G. E. D., Murray, J. D., Poole, P. S. & Downie, J. A. The rules of engagement in the legume-rhizobial symbiosis. Annu. Rev. Genet. 45, 119–144 (2011).
Miller, J. B. & Oldroyd, G. E. D. The role of diffusible signals in the establishment of rhizobial and mycorrhizal symbioses. Signal. Commun. Plants 10, 1–30 (2012).
Roche, P. et al. Molecular basis of symbiotic host specificity in Rhizobium meliloti: nodH and nodPQ genes encode the sulfation of lipo-oligosaccharide signals. Cell 67, 1131–1143 (1991). An article that elucidates the genetic basis for the specificity of rhizobial recognition.
Downie, J. A. & Walker, S. A. Plant responses to nodulation factors. Curr. Opin. Plant Biol. 2, 483–489 (1999).
Giraud, E. et al. Legumes symbioses: absence of Nod genes in photosynthetic bradyrhizobia. Science 316, 1307–1312 (2007).
Pawlowski, K. & Bisseling, T. Rhizobial and actinorhizal symbioses: what are the shared features? Plant Cell 8, 1899–1913 (1996).
Kucho, K., Hay, A. E. & Normand, P. The determinants of the actinorhizal symbiosis. Microbes Environ. 25, 241–252 (2010).
Gherbi, H. et al. SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria. Proc. Natl Acad. Sci. USA 105, 4928–4932 (2008). This work shows that the pathway for the recognition of Frankia spp. shares genetic components with the pathway for the recognition of rhizobia in legumes.
Hocher, V. et al. Transcriptomics of actinorhizal symbioses reveals homologs of the whole common symbiotic signaling cascade. Plant Physiol. 156, 700–711 (2011).
Markmann, K., Giczey, G. & Parniske, M. Functional adaptation of a plant receptor-kinase paved the way for the evolution of intracellular root symbioses with bacteria. PLoS Biol. 6, 497–506 (2008).
Maillet, F. et al. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469, 58–63 (2011). This study demonstrates that AMF produce LCOs that are similar to the Nod factors of rhizobial bacteria.
Perret, X., Staehelin, C. & Broughton, W. J. Molecular basis of symbiotic promiscuity. Microbiol. Mol. Biol. Rev. 64, 180–201 (2000).
Amor, B. B. et al. The NFP locus of Medicago truncatula controls an early step of Nod factor signal transduction upstream of a rapid calclium flux and root hair deformation. Plant J. 34, 495–506 (2003).
Madsen, E. B. et al. A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425, 637–640 (2003).
Radutoiu, S. et al. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425, 585–592 (2003). This work reveals the identity of the Nod factor receptors.
Arrighi, J. F. et al. The Medicago truncatula lysine motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol. 142, 265–279 (2006).
Buist, G., Steen, A., Kok, J. & Kuipers, O. R. LysM, a widely distributed protein motif for binding to (peptido)glycans. Mol. Microbiol. 68, 838–847 (2008).
Limpens, E. et al. LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 302, 630–633 (2003).
Zhang, X. C. et al. Molecular evolution of lysin motif-type receptor-like kinases in plants. Plant Physiol. 144, 623–636 (2007).
Mulder, L., Lefebvre, B., Cullimore, J. & Imberty, A. LysM domains of Medicago truncatula NFP protein involved in Nod factor perception. Glycosylation state, molecular modeling and docking of chitooligosaccharides and Nod factors. Glycobiology 16, 801–809 (2006).
Radutoiu, S. et al. LysM domains mediate lipochitin–oligosaccharide recognition and Nfr genes extend the symbiotic host range. EMBO J. 26, 3923–3935 (2007).
Broghammer, A. et al. Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding. Proc. Natl Acad. Sci. USA 109, 13859–13864 (2012).
Oldroyd, G., Mitra, R. M., Wais, R. & Long, S. Evidence for structurally specific negative feedback in the Nod factor signal transduction pathway. Plant J. 28, 191–199 (2001).
Madsen, E. B. et al. Autophosphorylation is essential for the in vivo function of the Lotus japonicus Nod factor receptor 1 and receptor-mediated signalling in cooperation with Nod factor receptor 5. Plant J. 65, 404–417 (2011).
Bensmihen, S., de Billy, F. & Gough, C. Contribution of NFP LysM domains to the recognition of Nod factors during the Medicago truncatula/Sinorhizobium meliloti symbiosis. PLoS ONE 6, e26114 (2011).
Gust, A. A. et al. Bacteria-derived peptidoglycans constitute pathogen-associated molecular patterns triggering innate immunity in Arabidopsis. J. Biol. Chem. 282, 32338–32348 (2007).
Schwessinger, B. & Ronald, P. C. Plant innate immunity: perception of censerved microbial signatures. Annu. Rev. Plant Biol. 63, 451–482 (2012).
Shibuya, N. & Minami, E. Oligosaccharide signalling for defence responses in plant. Physiol. Mol. Plant Pathol. 59, 223–233 (2001).
Chinchilla, D. et al. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448, 497–500 (2007).
Heese, A. et al. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc. Natl Acad. Sci. USA 104, 12217–12222 (2007).
Schwessinger, B. et al. Phosphorylation-dependent differential regulation of plant growth, cell death, and innate immunity by the regulatory receptor-like kinase BAK1. PLoS Genet. 7, e1002046 (2011).
Roux, M. et al. The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Plant Cell 23, 2440–2455 (2011).
Endre, G. et al. A receptor kinase gene regulating symbiotic nodule development. Nature 417, 962–966 (2002).
Stracke, S. et al. A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417, 959–962 (2002).
Young, N. D. et al. The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480, 520–524 (2011). This paper reports the genome sequence of the model legume M. truncatula , a plant that is central to the dissection of symbiotic associations.
den Camp, R. O. et al. LysM-type mycorrhizal receptor recruited for rhizobium symbiosis in nonlegume Parasponia. Science 331, 909–912 (2011).
Dolgikh, E. A. et al. Genetic dissection of Rhizobium-induced infection and nodule organogenesis in pea based on ENOD12A and ENOD5 expression analysis. Plant Biol. 13, 285–296 (2011).
Ehrhardt, D. W., Wais, R. & Long, S. R. Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85, 673–681 (1996). This investigation discovers the calcium oscillations that have since been shown to be a central signalling component in the symbiosis signalling pathway.
Charron, D., Pingret, J. L., Chabaud, M., Journet, E. P. & Barker, D. G. Pharmacological evidence that multiple phospholipid signaling pathways link rhizobium nodulation factor perception in Medicago truncatula root hairs to intracellular responses, including Ca2+ spiking and specific ENOD gene expression. Plant Physiol. 136, 3582–3593 (2004).
den Hartog, M., Musgrave, A. & Munnik, T. Nod factor-induced phosphatidic acid and diacylglycerol pyrophosphate formation: a role for phospholipase C and D in root hair deformation. Plant J. 25, 55–65 (2001).
Engstrom, E. M., Ehrhardt, D. W., Mitra, R. M. & Long, S. R. Pharmacological analysis of Nod factor-induced calcium spiking in Medicago truncatula. Evidence for the requirement of type IIA calcium pumps and phosphoinositide signaling. Plant Physiol. 128, 1390–1401 (2002).
Kevei, Z. et al. 3-hydroxy-3-methylglutaryl coenzyme A reductase 1 interacts with NORK and is crucial for nodulation in Medicago truncatula. Plant Cell 19, 3974–3989 (2007).
Chen, T. et al. A MAP kinase kinase interacts with SymRK and regulates nodule organogenesis in Lotus japonicus. Plant Cell 24, 823–838 (2012).
Ane, J. M. et al. Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303, 1364–1367 (2004).
Capoen, W. et al. Nuclear membranes control symbiotic calcium signaling of legumes. Proc. Natl Acad. Sci. USA 108, 14348–14353 (2011).
Charpentier, M. et al. Lotus japonicus CASTOR and POLLUX are ion channels essential for perinuclear calcium spiking in legume root endosymbiosis. Plant Cell 20, 3467–3479 (2008). A study defining the role of the cation channels in symbiotic signalling.
Imaizumi-Anraku, H. et al. Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature 433, 527–531 (2005).
Riely, B. K., Lougnon, G., Ane, J. M. & Cook, D. R. The symbiotic ion channel homolog DMI1 is localized in the nuclear membrane of Medicago truncatula roots. Plant J. 49, 208–216 (2007).
Venkateshwaran, M. et al. The recent evolution of a symbiotic ion channel in the legume family altered ion conductance and improved functionality in calcium signaling. Plant Cell 24, 2528–2545 (2012).
Sieberer, B. J. et al. A nuclear-targeted cameleon demonstrates intranuclear Ca2+ spiking in Medicago truncatula root hairs in response to rhizobial nodulation factors. Plant Physiol. 151, 1197–1206 (2009).
Granqvist, E. et al. Buffering capacity explains signal variation in symbiotic calcium oscillations. Plant Physiol. 160, 2300–2310 (2012).
Levy, J. et al. A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303, 1361–1364 (2004).
Mitra, R. M., Shaw, S. L. & Long, S. R. Six nonnodulating plant mutants defective for Nod factor-induced transcriptional changes associated with the legume-rhizobia symbiosis. Proc. Natl Acad. Sci. USA 101, 10217–10222 (2004).
Gleason, C. et al. Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition. Nature 441, 1149–1152 (2006).
Tirichine, L. et al. Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development. Nature 441, 1153–1156 (2006). Together with reference 65, this work reveals that autoactivation of CCaMK leads to spontaneous nodule formation.
Takeda, N., Maekawa, T. & Hayashi, M. Nuclear-localized and deregulated calcium- and calmodulin-dependent protein kinase activates rhizobial and mycorrhizal responses in lotus japonicus. Plant Cell 24, 810–822 (2012).
Hayashi, T. et al. A dominant function of CCaMK in intracellular accommodation of bacterial and fungal endosymbionts. Plant J. 63, 141–154 (2010).
Madsen, L. H. et al. The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nature Commun. 1, 10 (2010).
Shimoda, Y. et al. Rhizobial and fungal symbioses show different requirements for calmodulin binding to calcium calmodulin-dependent protein kinase in Lotus japonicus. Plant Cell 24, 304–321 (2012).
Singh, S. & Parniske, M. Activation of calcium- and calmodulin-dependent protein kinase (CCaMK), the central regulator of plant root endosymbiosis. Curr. Opin. Plant Biol. 15, 444–453 (2012).
Liao, J. et al. Negative regulation of CCaMK is essential for symbiotic infection. Plant J. 72, 572–584 (2012).
Horvath, B. et al. Medicago truncatula IPD3 is a member of the common symbiotic signaling pathway required for rhizobial and mycorrhizal symbioses. Mol. Plant Microbe Interact. 24, 1345–1358 (2011).
Messinese, E. et al. A novel nuclear protein interacts with the symbiotic DMI3 calcium and calmodulin dependent protein kinase of Medicago truncatula. Mol. Plant Microbe Interact. 20, 912–921 (2007).
Ovchinnikova, E. et al. IPD3 controls the formation of nitrogen-fixing symbiosomes in pea and Medicago spp. Mol. Plant Microbe Interact. 24, 1333–1344 (2011).
Yano, K. et al. CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc. Natl Acad. Sci. USA 105, 20540–20545 (2008).
Catoira, R. et al. Four genes of Medicago truncatula controlling components of a Nod factor transduction pathway. Plant Cell 12, 1647–1665 (2000). One of the papers to define the genetics of the common symbiosis signalling pathway.
Sieberer, B. J., Chabaud, M., Fournier, J., Timmers, A. C. & Barker, D. G. A switch in Ca2+ spiking signature is concomitant with endosymbiotic microbe entry into cortical root cells of Medicago truncatula. Plant J. 69, 822–830 (2012).
Kalo, P. et al. Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 308, 1786–1789 (2005).
Smit, P. et al. NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308, 1789–1791 (2005).
Devers, E. A., Branscheid, A., May, P. & Krajinski, F. Stars and symbiosis: microRNA- and microRNA*-mediated transcript cleavage involved in arbuscular mycorrhizal symbiosis. Plant Physiol. 156, 1990–2010 (2011).
Lauressergues, D. et al. The microRNA miR171h modulates arbuscular mycorrhizal colonization of Medicago truncatula by targeting NSP2. Plant J. 72, 512–522 (2012).
Oldroyd, G. E. & Long, S. R. Identification and characterization of nodulation-signaling pathway 2, a gene of Medicago truncatula involved in Nod factor signaling. Plant Physiol. 131, 1027–1032 (2003).
Liu, W. et al. Strigolactone biosynthesis in Medicago truncatula and rice requires the symbiotic GRAS-type transcription factors NSP1 and NSP2. Plant Cell 23, 3853–3865 (2011).
Hirsch, S. et al. GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell 21, (2009). A study that uncovers the role of the symbiotic transcription factors.
Marsh, J. F. et al. Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase. Plant Physiol. 144, 324–335 (2007).
Middleton, P. H. et al. An ERF transcription factor in Medicago truncatula that is essential for Nod factor signal transduction. Plant Cell 19, 1221–1234 (2007).
Cerri, M. R. et al. Medicago truncatula ERN transcription factors: regulatory interplay with NSP1/NSP2 GRAS factors and expression dynamics throughout rhizobial infection. Plant Physiol. 160, 2155–2172 (2012).
Gobbato, E. et al. A GRAS-type transcription factor with a specific function in mycorrhizal signaling. Curr. Biol. 22, 2236–2241 (2012). This research identifies a mycorrhiza-specific GRAS domain transcription factor.
Wang, E. et al. A common signaling process that promotes mycorrhizal and oomycete colonization of plants. Curr. Biol. 22, 2242–2246 (2012).
Marie, C., Plaskitt, K. A. & Downie, J. A. Abnormal bacteroid development in nodules induced by a glucosamine synthase mutant of Rhizobium leguminosarum. Mol. Plant Microbe Interact. 7, 482–487 (1994).
Capoen, W., Goormachtig, S., De Rycke, R., Schroeyers, K. & Holsters, M. SrSymRK, a plant receptor essential for symbiosome formation. Proc. Natl Acad. Sci. USA 102, 10369–10374 (2005).
Limpens, E. et al. Formation of organelle-like N2-fixing symbiosomes in legume root nodules is controlled by DMI2. Proc. Natl Acad. Sci. USA 102, 10375–10380 (2005).
Kosuta, S. et al. Lotus japonicus symRK-14 uncouples the cortical and epidermal symbiotic program. Plant J. 67, 929–940 (2011).
Ardourel, M. et al. Rhizobium meliloti lipooligosaccharide nodulation factors: different structural requirements for bacterial entry into target root hair cells and induction of plant symbiotic developmental responses. Plant Cell 6, 1357–1374 (1994).
Smit, P. et al. Medicago LYK3, an entry receptor in rhizobial nodulation factor signaling. Plant Physiol. 145, 183–191 (2007).
Mbengue, M. et al. The Medicago truncatula E3 ubiquitin ligase PUB1 interacts with the LYK3 symbiotic receptor and negatively regulates infection and nodulation. Plant Cell 22, 3474–3488 (2010).
Haney, C. H. et al. Symbiotic rhizobia bacteria trigger a change in localization and dynamics of the Medicago truncatula receptor kinase LYK3. Plant Cell 23, 2774–2787 (2011).
Haney, C. H. & Long, S. R. Plant flotillins are required for infection by nitrogen-fixing bacteria. Proc. Natl Acad. Sci. USA 107, 478–483 (2010).
Lefebvre, B. et al. A remorin protein interacts with symbiotic receptors and regulates bacterial infection. Proc. Natl Acad. Sci. USA 107, 2343–2348 (2010).
Markmann, K. & Parniske, M. Evolution of root endosymbiosis with bacteria: how novel are nodules? Trends Plant Sci. 14, 77–86 (2009).
Wang, B. et al. Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonization of land by plants. New Phytol. 186, 514–525 (2010).
Banba, M. et al. Divergenec of evolutionary ways among common sym genes: Castor and CCaMK show functional conservation between two symbiosis systems and constitute the root of a common signaling pathway. Plant Cell Physiol. 49, 1659–1671 (2008).
Gutjahr, C. et al. Arbuscular mycorrhiza-specific signaling in rice transcends the common symbiosis signaling pathway. Plant Cell 20, 2989–3005 (2008). This paper reports the most complete characterization of the common symbiosis signalling pathway in cereals and its role in the association with AMF.
Heckmann, A. B. et al. Lotus japonicus nodulation requires two GRAS domain regulators, one of which is functionally conserved in a non-legume. Plant Physiol. 142, 1739–1750 (2006).
Pumplin, N. et al. Medicago truncatula Vapyrin is a novel protein required for arbuscular mycorrhizal symbiosis. Plant J. 61, 482–494 (2010).
Murray, J. D. et al. Vapyrin, a gene essential for intracellular progression of arbuscular mycorrhizal symbiosis, is also essential for infection by rhizobia in the nodule symbiosis of Medicago truncatula. Plant J. 65, 244–252 (2011).
Ivanov, S. et al. Rhizobium–legume symbiosis shares an exocytotic pathway required for arbuscule formation. Proc. Natl Acad. Sci. USA 109, 8316–8321 (2012).
Sanchez, L. et al. Pseudomonas fluorescens and Glomus mosseae trigger DMI3-dependent activation of genes related to a signal transduction pathway in roots of Medicago truncatula. Plant Physiol. 139, 1065–1077 (2005).
Li, J. et al. Specific ER quality control components required for biogenesis of the plant innate immune receptor EFR. Proc. Natl Acad. Sci. USA 106, 15973–15978 (2009).
Robatzek, S., Chinchilla, D. & Boller, T. Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev. 20, 537–542 (2006).
Zipfel, C. Early molecular events in PAMP-triggered immunity. Curr. Opin. Plant Biol. 12, 414–420 (2009).
Kaku, H. et al. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc. Natl Acad. Sci. USA 103, 11086–11091 (2006).
Miya, A. et al. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc. Natl Acad. Sci. USA 104, 19613–19618 (2007).
Wan, J. R. et al. A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20, 471–481 (2008).
Shimizu, T. et al. Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J. 64, 204–214 (2010).
Willmann, R. et al. Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection. Proc. Natl Acad. Sci. USA 108, 19824–19829 (2011).
Gimenez-Ibanez, S. et al. AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Curr. Biol. 19, 423–429 (2009).
Liu, T. et al. Chitin-induced dimerization activates a plant immune receptor. Science 336, 1160–1164 (2012).
Iizasa, E., Mitsutomi, M. & Nagano, Y. Direct binding of a plant LysM receptor-like kinase, LysM RLK1/CERK1, to chitin in vitro. J. Biol. Chem. 285, 2996–3004 (2010).
Petutschnig, E. K., Jones, A. M. E., Serazetdinova, L., Lipka, U. & Lipka, V. The lysin motif receptor-like kinase (LysM-RLK) CERK1 is a major chitin-binding protein in Arabidopsis thaliana and subject to chitin-induced phosphorylation. J. Biol. Chem. 285, 28902–28911 (2010).
Nakagawa, T. et al. From defense to symbiosis: limited alterations in the kinase domain of LysM receptor-like kinases are crucial for evolution of legume–Rhizobium symbiosis. Plant J. 65, 169–180 (2011).
Lohmann, G. V. et al. Evolution and regulation of the Lotus japonicus LysM receptor gene family. Mol. Plant Microbe Interact. 23, 510–521 (2010).
Guimil, S. et al. Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proc. Natl Acad. Sci. USA 102, 8066–8070 (2005).
Skamnioti, P. & Gurr, S. J. Magnaporthe grisea cutinase2 mediates appressorium differentiation and host penetration and is required for full virulence. Plant Cell 19, 2674–2689 (2007).
Mendoza-Mendoza, A. et al. Physical-chemical plant-derived signals induce differentiation in Ustilago maydis. Mol. Microbiol. 71, 895–911 (2009).
Barrett, L. G. & Heil, M. Unifying concepts and mechanisms in the specificity of plant-enemy interactions. Trends Plant Sci. 17, 282–292 (2012).
Bozkurt, T. O., Schornack, S., Banfield, M. J. & Kamoun, S. Oomycetes, effectors, and all that jazz. Curr. Opin. Plant Biol. 15, 1–10 (2012).
Feng, F. & Zhou, J.-M. Plant-bacterial pathogen interactions mediated by type III effectors. Curr. Opin. Plant Biol. 15, 469–476 (2012).
Deakin, W. J. & Broughton, W. J. Symbiotic use of pathogenic strategies: rhizobial protein secretion systems. Nature Rev. Microbiol. 7, 312–320 (2009).
Kloppholz, S., Kuhn, H. & Requena, N. A. Secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr. Biol. 21, 1204–1209 (2011).
Plett, J. M. et al. A secreted effector protein of Laccaria bicolor is required for symbiosis development. Curr. Biol. 21, 1197–1203 (2011).
Jones, J. D. & Dangl, J. L. The plant immune system. Nature 444, 323–329 (2006).
Yang, S., Tang, F., Gao, M., Krishnan, H. B. & Zhu, H. R gene-controlled specificity in the legume–rhizobia symbiosis. Proc. Natl Acad. Sci. USA 107, 18735–18740 (2010).
Genre, A. et al. Prepenetration apparatus assembly precedes and predicts the colonization patterns of arbuscular mycorrhizal fungi within the root cortex of both Medicago truncatula and Daucus carota. Plant Cell 20, 1407–1420 (2008).
Parniske, M. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nature Rev. Microbiol. 6, 763–775 (2008).
Groth, M. et al. NENA, a Lotus japonicus homolog of Sec13, is required for rhizodermal infection by arbuscular mycorrhiza fungi and rhizobia but dispensable for cortical endosymbiotic development. Plant Cell 22, 2509–2526 (2010).
Kanamori, N. et al. A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc. Natl Acad. Sci. USA 103, 359–364 (2006).
Saito, K. et al. NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus. Plant Cell 19, 610–624 (2007).
The author thanks A. Downie and J. Murray for critical reading of the manuscript.
The author declares no competing financial interests.
- Arbuscular mycorrhizal fungi
(AMF). Fungi from the phylum Glomeromycota. These fungi have the ability to associate with plant roots, leading to invasion of the root and the formation of arbuscules in root cortical cells.
A varied group of plants that includes peas and beans. The ability to associate with nitrogen-fixing bacteria is a widespread (although not ubiquitous) feature of the family.
- Rhizobial bacteria
Bacteria that can enter a nitrogen-fixing symbiosis with legumes or Parasponia spp. This ability has been acquired by a wide range of bacteria through horizontal gene transfer.
Highly branched fungal hyphal networks that develop in root cells and act as the point of nutrient exchange between the mycorrhizal fungus and the host root.
The soil environment surrounding the plant root. The microbial communities within this environment are strongly influenced by the plant.
Terpenoid plant hormones with a function in the suppression of shoot branching. These hormones are also released by the plant root to signal to the mycorrhizal fungus. Parasitic plants, such as Striga spp., have learnt to recognize strigolactones as a signal for the proximity of a potential plant host root.
A group of polyhydroxy polyphenol plant secondary metabolites with diverse functions. Legumes release flavonoids from their roots to signal rhizobia and promote the production of nodulation factors.
- Actinorhizal plants
A group of plants with the ability to associate with Frankia spp. bacteria. This association results in the production of nitrogen-fixing nodules colonized by the bacteria.
- Pathogen-associated molecular pattern
(PAMP). A molecule (or part of a molecule) that is present on or in or produced by a pathogen and is recognized by the host organism as a signal of that invading pathogen.
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Oldroyd, G. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11, 252–263 (2013). https://doi.org/10.1038/nrmicro2990
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