Plant LysM proteins: modules mediating symbiosis and immunity.

Microbial glycans, such as bacterial peptidoglycans, fungal chitin or rhizobacterial Nod factors (NFs), are important signatures for plant immune activation or for the establishment of beneficial symbioses. Plant lysin motif (LysM) domain proteins serve as modules mediating recognition of these different N-acetylglucosamine (GlcNAc)-containing ligands, suggesting that this class of proteins evolved from an ancient sensor for GlcNAc. During early plant evolution, these glycans probably served as immunogenic patterns activating LysM protein receptor-mediated plant immunity and stopping microbial infection. The biochemical potential of plant LysM proteins for sensing microbial GlcNAc-containing glycans has probably since favored the evolution of receptors facilitating microbial infection and symbiosis.

[1]  B. Lefebvre,et al.  Biochemical and phylogenetic analysis of CEBiP-like LysM domain-containing extracellular proteins in higher plants. , 2011, Plant physiology and biochemistry : PPB.

[2]  Gary Stacey,et al.  Molecular Evolution of Lysin Motif-Type Receptor-Like Kinases in Plants1[W][OA] , 2007, Plant Physiology.

[3]  Lauren S. Ryder,et al.  Effector-Mediated Suppression of Chitin-Triggered Immunity by Magnaporthe oryzae Is Necessary for Rice Blast Disease[C][W] , 2012, Plant Cell.

[4]  T. Boller,et al.  Specific perception of subnanomolar concentrations of chitin fragments by tomato cells: induction of extracellular alkalinization, changes in protein phosphorylation, and establishment of a refractory state , 1993 .

[5]  T. Boller,et al.  Molecular Sensing of Bacteria in Plants , 2003, The Journal of Biological Chemistry.

[6]  S. Spoel,et al.  How do plants achieve immunity? Defence without specialized immune cells , 2012, Nature Reviews Immunology.

[7]  H. Kouchi,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. , 2011, The Plant journal : for cell and molecular biology.

[8]  S. Thirup,et al.  LysM domains mediate lipochitin–oligosaccharide recognition and Nfr genes extend the symbiotic host range , 2007, The EMBO journal.

[9]  Y. Ren,et al.  Elicitation of Diterpene Biosynthesis in Rice (Oryza sativa L.) by Chitin. , 1992, Plant physiology.

[10]  S. Long.  Rhizobium symbiosis: nod factors in perspective. , 1996, The Plant cell.

[11]  A. Imberty,et al.  LysM domains of Medicago truncatula NFP protein involved in Nod factor perception. Glycosylation state, molecular modeling and docking of chitooligosaccharides and Nod factors. , 2006, Glycobiology.

[12]  P. Bakker,et al.  Deciphering the Rhizosphere Microbiome for Disease-Suppressive Bacteria , 2011, Science.

[13]  F. de Billy,et al.  Contribution of NFP LysM Domains to the Recognition of Nod Factors during the Medicago truncatula/Sinorhizobium meliloti Symbiosis , 2011, PloS one.

[14]  Kyutaro Kishimoto,et al.  Perception of the chitin oligosaccharides contributes to disease resistance to blast fungus Magnaporthe oryzae in rice. , 2010, The Plant journal : for cell and molecular biology.

[15]  T. Bisseling,et al.  Nod factor signaling genes and their function in the early stages of Rhizobium infection. , 2005, Current opinion in plant biology.

[16]  E. Blancaflor,et al.  Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis , 2009, BMC Plant Biology.

[17]  B. Thomma,et al.  The role of chitin detection in plant--pathogen interactions. , 2011, Microbes and infection.

[18]  M Bycroft,et al.  The structure of a LysM domain from E. coli membrane-bound lytic murein transglycosylase D (MltD). , 2000, Journal of molecular biology.

[19]  T. Bisseling,et al.  Identical accumulation and immobilization of sulfated and nonsulfated Nod factors in host and nonhost root hair cell walls. , 2003, Molecular plant-microbe interactions : MPMI.

[20]  Sophia Mersmann,et al.  Plant Pattern-Recognition Receptor FLS2 Is Directed for Degradation by the Bacterial Ubiquitin Ligase AvrPtoB , 2008, Current Biology.

[21]  M. Holsters,et al.  Nod factor structures, responses, and perception during initiation of nodule development. , 2002, Glycobiology.

[22]  Didier Reinhardt,et al.  Successful joint ventures of plants: arbuscular mycorrhiza and beyond. , 2011, Trends in plant science.

[23]  J. Downie,et al.  Coordinating nodule morphogenesis with rhizobial infection in legumes. , 2008, Annual review of plant biology.

[24]  G. Venema,et al.  Molecular cloning and nucleotide sequence of the gene encoding the major peptidoglycan hydrolase of Lactococcus lactis, a muramidase needed for cell separation , 1995, Journal of bacteriology.

[25]  M. Iriti,et al.  Chitosan as a MAMP, searching for a PRR , 2009, Plant signaling & behavior.

[26]  P. Rougé,et al.  The Medicago truncatula lysin [corrected] motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. , 2006, Plant physiology.

[27]  Klaus F. X. Mayer,et al.  Comparative Analysis of the Receptor-Like Kinase Family in Arabidopsis and Rice , 2004, The Plant Cell Online.

[28]  T. Boller,et al.  Specific, high affinity binding of chitin fragments to tomato cells and membranes. Competitive inhibition of binding by derivatives of chitooligosaccharides and a Nod factor of Rhizobium. , 1994, The Journal of biological chemistry.

[29]  G. Stacey,et al.  Chitin recognition in rice and legumes , 1997, Plant and Soil.

[30]  G. Martin,et al.  Methods to study PAMP-triggered immunity using tomato and Nicotiana benthamiana. , 2010, Molecular plant-microbe interactions : MPMI.

[31]  Anna Block,et al.  Plant targets for Pseudomonas syringae type III effectors: virulence targets or guarded decoys? , 2011, Current opinion in microbiology.

[32]  Alexandra M. E. Jones,et al.  The Lysin Motif Receptor-like Kinase (LysM-RLK) CERK1 Is a Major Chitin-binding Protein in Arabidopsis thaliana and Subject to Chitin-induced Phosphorylation*♦ , 2010, The Journal of Biological Chemistry.

[33]  Martin Parniske,et al.  Arbuscular mycorrhiza: the mother of plant root endosymbioses , 2008, Nature Reviews Microbiology.

[34]  Jean-Michel Ané,et al.  Tracing Nonlegume Orthologs of Legume Genes Required for Nodulation and Arbuscular Mycorrhizal Symbioses , 2006, Genetics.

[35]  Sally E. Smith,et al.  Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. , 2011, Annual review of plant biology.

[36]  Jonathan D. G. Jones,et al.  The plant immune system , 2006, Nature.

[37]  A. Joachimiak,et al.  B. subtilis ykuD protein at 2.0 Å resolution: Insights into the structure and function of a novel, ubiquitous family of bacterial enzymes , 2005, Proteins.

[38]  M. Mitsutomi,et al.  Direct Binding of a Plant LysM Receptor-like Kinase, LysM RLK1/CERK1, to Chitin in Vitro* , 2009, The Journal of Biological Chemistry.

[39]  P. D. de Wit,et al.  Fungal effector proteins. , 2009, Annual review of phytopathology.

[40]  J. Stougaard,et al.  The pea Sym37 receptor kinase gene controls infection-thread initiation and nodule development. , 2008, Molecular plant-microbe interactions : MPMI.

[41]  S. Tabata,et al.  Evolution and regulation of the Lotus japonicus LysM receptor gene family. , 2010, Molecular plant-microbe interactions : MPMI.

[42]  C. Zipfel,et al.  Activation of plant pattern-recognition receptors by bacteria. , 2011, Current opinion in microbiology.

[43]  T. Boller,et al.  A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. , 2009, Annual review of plant biology.

[44]  Y. Narusaka,et al.  CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis , 2007, Proceedings of the National Academy of Sciences.

[45]  K. Schleifer,et al.  Peptidoglycan types of bacterial cell walls and their taxonomic implications , 1972, Bacteriological reviews.

[46]  P. Gresshoff,et al.  Molecular analysis of legume nodule development and autoregulation. , 2010, Journal of integrative plant biology.

[47]  G. Stacey,et al.  Characterization of early, chitin-induced gene expression in Arabidopsis. , 2002, Molecular plant-microbe interactions : MPMI.

[48]  S. Chisholm,et al.  Host-Microbe Interactions: Shaping the Evolution of the Plant Immune Response , 2022 .

[49]  B. Poinssot,et al.  Priming: getting ready for battle. , 2006, Molecular plant-microbe interactions : MPMI.

[50]  D. Cook,et al.  Nod factor induction of reactive oxygen species production is correlated with expression of the early nodulin gene rip1 in Medicago truncatula. , 2002, Molecular plant-microbe interactions : MPMI.

[51]  S. Tabata,et al.  A receptor kinase gene of the LysM type is involved in legumeperception of rhizobial signals , 2003, Nature.

[52]  N. Beaudoin,et al.  Chitooligosaccharide sensing and downstream signaling: contrasted outcomes in pathogenic and beneficial plant–microbe interactions , 2010, Planta.

[53]  W. Broughton,et al.  Molecular Basis of Symbiotic Promiscuity , 2000, Microbiology and Molecular Biology Reviews.

[54]  P. Rougé,et al.  The Medicago truncatula Lysine Motif-Receptor-Like Kinase Gene Family Includes NFP and New Nodule-Expressed Genes1[W] , 2006, Plant Physiology.

[55]  Jonathan D. G. Jones,et al.  Plant pathogens and integrated defence responses to infection , 2001, Nature.

[56]  Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice , 2010, The Plant journal : for cell and molecular biology.

[57]  S. Shaw,et al.  The NFP locus of Medicago truncatula controls an early step of Nod factor signal transduction upstream of a rapid calcium flux and root hair deformation. , 2003, The Plant journal : for cell and molecular biology.

[58]  P. Bonfante,et al.  Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. , 2010, Nature communications.

[59]  B. Thomma,et al.  Fungal LysM effectors: extinguishers of host immunity? , 2009, Trends in microbiology.

[60]  S. Tabata,et al.  Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases , 2003, Nature.

[61]  C. Zipfel.  Pattern-recognition receptors in plant innate immunity. , 2008, Current opinion in immunology.

[62]  C. Janeway,et al.  Innate Immunity: The Virtues of a Nonclonal System of Recognition , 1997, Cell.

[63]  T. Bisseling,et al.  Medicago LYK3, an Entry Receptor in Rhizobial Nodulation Factor Signaling1[W] , 2007, Plant Physiology.

[64]  L. Piater,et al.  Innate immunity in plants and animals: striking similarities and obvious differences , 2004, Immunological reviews.

[65]  G. Stacey,et al.  A LysM Receptor-Like Kinase Plays a Critical Role in Chitin Signaling and Fungal Resistance in Arabidopsis[W][OA] , 2008, The Plant Cell Online.

[66]  R. Wing,et al.  LysM-Type Mycorrhizal Receptor Recruited for Rhizobium Symbiosis in Nonlegume Parasponia , 2011, Science.

[67]  F. Sánchez,et al.  Fast, transient and specific intracellular ROS changes in living root hair cells responding to Nod factors (NFs). , 2008, The Plant journal : for cell and molecular biology.

[68]  F. Ausubel,et al.  Innate Immune Responses Activated in Arabidopsis Roots by Microbe-Associated Molecular Patterns[W][OA] , 2010, Plant Cell.

[69]  Bart P. H. J. Thomma,et al.  Conserved Fungal LysM Effector Ecp6 Prevents Chitin-Triggered Immunity in Plants , 2010, Science.

[70]  Yoko Nishizawa,et al.  Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[71]  E. Minami,et al.  Oligosaccharide signalling for defence responses in plant , 2001 .

[72]  C. D. de Koster,et al.  The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species , 2008, Molecular microbiology.

[73]  C. Ponting,et al.  Eukaryotic signalling domain homologues in archaea and bacteria. Ancient ancestry and horizontal gene transfer. , 1999, Journal of molecular biology.

[74]  F. Katagiri,et al.  Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection , 2011, Proceedings of the National Academy of Sciences.

[75]  Anton Steen,et al.  LysM, a widely distributed protein motif for binding to (peptido)glycans , 2008, Molecular microbiology.

[76]  J. Cohn,et al.  Localization and Binding Characteristics of a High-Affinity Binding Site for N--Acetylchitooligosaccharide Elicitor in the Plasma Membrane from Suspension-Cultured Rice Cells Suggest a Role as a Receptor for the Elicitor Signal at the Cell Surface , 1996 .

[77]  N. Shibuya,et al.  Identification of a novel high‐affinity binding site for N‐acetylchitooligosaccharide elicitor in the membrane fraction from suspension‐cultured rice cells , 1993, FEBS letters.

[78]  E. Katoh,et al.  LysM Domains from Pteris ryukyuensis Chitinase-A , 2008, Journal of Biological Chemistry.

[79]  S. Tyerman,et al.  Ammonia and amino acid transport across symbiotic membranes in nitrogen-fixing legume nodules , 2001, Cellular and Molecular Life Sciences CMLS.

[80]  U. Schwarz,et al.  The composition of the murein of Escherichia coli. , 1988, The Journal of biological chemistry.

[81]  J. Rathjen,et al.  AvrPtoB Targets the LysM Receptor Kinase CERK1 to Promote Bacterial Virulence on Plants , 2009, Current Biology.

[82]  K. Hammond-Kosack,et al.  Analysis of Two in Planta Expressed LysM Effector Homologs from the Fungus Mycosphaerella graminicola Reveals Novel Functional Properties and Varying Contributions to Virulence on Wheat1[W][OA] , 2011, Plant Physiology.

[83]  S. Cannon,et al.  Evolutionary genomics of LysM genes in land plants , 2009, BMC Evolutionary Biology.

[84]  C. Gough,et al.  Lipo-chitooligosaccharide signaling in endosymbiotic plant-microbe interactions. , 2011, Molecular plant-microbe interactions : MPMI.

[85]  E. Kondorosi,et al.  How alfalfa root hairs discriminate between Nod factors and oligochitin elicitors. , 2000, Plant physiology.

[86]  T. Bisseling,et al.  Evolutionary origin of rhizobium Nod factor signaling , 2011, Plant signaling & behavior.

[87]  R. B. Day,et al.  Binding site for chitin oligosaccharides in the soybean plasma membrane. , 2001, Plant physiology.

[88]  M. Newman,et al.  Peptidoglycan and muropeptides from pathogens Agrobacterium and Xanthomonas elicit plant innate immunity: structure and activity. , 2008, Chemistry & biology.

[89]  Jean Dénarié,et al.  Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza , 2011, Nature.

[90]  G. Felix,et al.  Bacteria-derived Peptidoglycans Constitute Pathogen-associated Molecular Patterns Triggering Innate Immunity in Arabidopsis* , 2007, Journal of Biological Chemistry.

[91]  J. Willemse,et al.  LysM Domain Receptor Kinases Regulating Rhizobial Nod Factor-Induced Infection , 2003, Science.

[92]  M. Parniske,et al.  Plant biology: Locks, keys and symbioses , 2003, Nature.

[93]  M. Parniske,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. , 2011, The Plant journal : for cell and molecular biology.

[94]  B. Tyler.  Entering and breaking: virulence effector proteins of oomycete plant pathogens , 2009, Cellular microbiology.