Interaction of Medicago truncatula Lysin Motif Receptor-Like Kinases, NFP and LYK3, Produced in Nicotiana benthamiana Induces Defence-Like Responses

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Pietraszewska Bogiel, Anna ^a   Lefebvre, Benoit ^b   Koini, Maria A ^a   Klaus Heisen, Dörte ^b   Takken, Frank L W ^a   Geurts, René ^c   Cullimore, Julie V ^b   Gadella, Theodorus W J ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b LABORATOIRE DES INTERACTIONS PLANTES MICROORGANISMES LIPM   (France)

^c WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CHITIN; PHENOL DERIVATIVE; PHOSPHOTRANSFERASE; PROTEIN CERK1; PROTEIN LYK3; PROTEIN NFP; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARABIDOPSIS THALIANA; ARTICLE; BARREL MEDIC; BIOACCUMULATION; CELL DEATH; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SYNTHESIS; GENE EXPRESSION; INNATE IMMUNITY; MOLECULAR INTERACTION; NICOTIANA BENTHAMIANA; NODULATION; NONHUMAN; PLANT DEFENSE; PLANT LEAF; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION; SYMBIOSIS;

CELL DEATH; CHITIN; INTRACELLULAR SPACE; LIPOPOLYSACCHARIDES; MEDICAGO TRUNCATULA; PLANT LEAVES; PROTEIN BINDING; PROTEIN KINASES; SIGNAL TRANSDUCTION; TOBACCO;

ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); MEDICAGO TRUNCATULA; NICOTIANA BENTHAMIANA;

EID: 84878630564     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065055     Document Type: Article

References (84)

1. Masson-Boivin C, Giraud E, Perret X, Batut J, (2009) Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipies? Trends Microbiol 17: 458-466.
2. Downie JA, (2010) The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots. FEMS Microbiol Rev 34: 150-170.
3. Gust AA, Willmann R, Desaki Y, Grabherr HM, Nürnberger T, (2012) Plant LysM proteins: modules mediating symbiosis and immunity. Trends Plant Sci 17: 495-502.
4. Oldroyd GED, (2013) Speak friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nature 11: 252-263.
5. Madsen EB, Madsen LH, Radutoiu S, Olbryt M, Rakwalska M, et al. (2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425: 637-640.
6. Radutoiu S, Madsen LH, Madsen EB, Felle HH, Umehara Y, et al. (2003) Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425: 585-592.
7. El Yahyaoui FE, Küster H, Ben Amor B, Hohnjec N, Pühler A, et al. (2004) Expression profiling in Medicago truncatula identifies more than 750 genes differentially expressed during nodulation, including many potential regulators of the symbiotic program. Plant Physiol 136: 3159-3176.
8. Mitra RM, Shaw SL, Long SR, (2004) Six non-nodulating plant mutants defective for Nod factor-induced transcriptional changes associated with the legume-rhizobia symbiosis. Proc Natl Acad Sci U S A 101: 10217-10222.
9. Arrighi JF, Barre A, Ben Amor B, Bersoult A, Soriano LC, et al. (2006) The Medicago truncatula Lysin [corrected] motif-Receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol 142: 265-279.
10. Miwa H, Sun J, Oldroyd GED, Downie JA, (2006) Analysis of Nod-factor-induced calcium signalling in root hairs of symbiotically defective mutants of Lotus japonicus. Mol Plant Microbe Interact 19: 914-923.
11. Høgslund N, Radutoiu S, Krusell L, Voroshilova V, Hannah MA, et al. (2009) Dissection of symbiosis and organ development by integrated transcriptome analysis of Lotus japonicus mutant and wild-type plants. PLoS ONE 4: e6556.
12. Smit P, Limpens E, Geurts R, Fedorove E, Dolgikh E, et al. (2007) Medicago LYK3, an entry receptor in rhizobial nodulation factor signalling. Plant Physiol 145: 183-191.
13. Hayashi T, Banba M, Shimoda Y, Kouchi H, Hayashi M, et al. (2010) A dominant function of CCaMK in intracellular accommodation of bacterial and fungal endosymbionts. Plant J 63: 141-154.
14. Madsen LH, Tirichine L, Jurkiewicz A, Sullivan JT, Heckmann AB, et al. (2010) The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nature doi: 10.1038/ncomms1009.
15. Bensmihen S, de Billy F, Gough C, (2011) Contribution of NFP LysM domains to the recognition of Nod Factors during the Medicago truncatula/Sinorhizobium meliloti symbiosis. PloS ONE 6: e26114.
16. Limpens E, Mirabella R, Fedorova E, Franken C, Franssen H, et al. (2005) Formation of organelle-like N2-fixing symbiosomes in legume root nodules is controlled by DMI2. Proc Natl Acad Sci U S A 102: 10375-10380.
17. Mbengue M, Camut S, de Carvalho-Niebel F, Deslandes L, Froidure S, et al. (2010) The Medicago truncatula E3 ubiqutin ligase PUB1 interacts with the LYK3 symbiotic receptor and negatively regulates infection and nodulation. Plant Cell 22: 3474-3488.
18. Haney CH, Riely BK, Tricoli DM, Cook DR, Ehrhardt DW, et al. (2011) Symbiotic rhizobia bacteria trigger a change in localization and dynamics of the Medicago truncatula receptor kinase LYK3. Plant Cell 23: 2774-2787.
19. Broghammer A, Krusell L, Blaise M, Sauer J, Sullivan JT, et al. (2012) Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding. Proc Natl Acad Sci U S A 109: 13859-13864.
20. Klaus-Heisen D, Nurisso A, Pietraszewska-Bogiel A, Mbengue M, Camut S, et al. (2011) Structure-function similarities between a plant receptor-like kinase and the human Interleukin-1 Receptor-Associated Kinase-4. J Biol Chem 286: 11202-11210.
21. Madsen EB, Antolín-Llovera M, Grossmann C, Ye J, Vieweg S, et al. (2011) Autophosphorylation is essential for 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.
22. Lefebvre B, Klaus-Heisen D, Pietraszewska-Bogiel A, Hervé C, Camut S, et al. (2012) Role of N-glycosylation sites and CXC motifs in trafficking of Medicago truncatula Nod Factor Perception protein to the plasma membrane. J Biol Chem 287: 10812-10823.
23. Radutoiu S, Madsen LH, Madsen EB, Jurkiewicz A, Fukai E, et al. (2007) LysM domains mediate lipochitin-oligosaccharide recognition and Nfr genes extend the symbiotic host range. EMBO J 26: 3923-3935.
24. Oláh B, Brière C, Bécard G, Dénerié J, Gough C, (2005) 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.
25. Maillet F, Poinsot V, André O, Peuch-Pagès V, Haouy A, et al. (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469: 58-64.
26. Czaja LF, Hogekamp C, Lamm P, Maillet F, Andres Martinez E, et al. (2012) Transcriptional responses toward diffusible signals from symbiotic microbes reveal MtNFP- and MtDMI3-dependent reprogramming of host gene expression by arbuscular mycorrhizal fungal lipochitooligosaccharides. Plant Physiol 159: 1671-1685.
27. Rey T, Nars A, Bonhomme M, Bottin A, Huguet S, et al. (2013) NFP, a LysM protein controlling Nod Factor perception, also intervenes in Medicago truncatula resistance to pathogens. New Phytol 198: 875-886.
28. Streng A, Op den Camp R, Bisseling T, Geurts R, (2011) Evolutionary origin of Rhizobium Nod factor signalling. Plant Signal Behav 6: 1510-1514.
29. Boller T, Felix G, (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60: 379-406.
30. Thomma BPHJ, Nürnberger T, Joosten MHAJ, (2011) Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23: 4-15.
31. Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, et al. (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signalling in Arabidopsis. Proc Natl Acad Sci U S A 104: 19613-19618.
32. Wan J, Zhang XC, Neece D, Ramonell KM, Clough S, et al. (2008) A LysM receptor-like kinase plays a critical role in chitin signalling and fungal resistance in Arabidopsis. Plant Cell 20: 471-481.
33. Gimenez-Ibanez S, Hann DR, Ntoukakis V, Petutschnig E, Lipka V, et al. (2009) AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Curr Biol 19: 423-429.
34. Shimizu T, Nakano T, Takamizawa D, Desaki Y, Ishii-Minami N, et al. (2010) Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signalling in rice. Plant J 64: 204-214.
35. Willmann R, Lajunen HM, Erbs G, Newman MA, Kolb D, et al. (2011) Arabidopsis lysin-motif proteins LYM1 LYM3 and CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection. Proc Natl Acad Sci U S A 108: 19824-19829.
36. Liu B, Li JF, Ao Y, Qu J, Li Z, et al. (2012) Lysin motif-containing proteins LYP4 and LYP6 play dual roles in peptidoglycan and chitin perception in rice innate immunity. Plant Cell 24: 3406-3419.
37. Petutschnig EK, Jones AME, Serazetdinova L, Lipka U, Lipka V, (2010) 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.
38. Liu T, Liu Z, Song C, Hu Y, Han Z, et al. (2012) Chitin-induced dimerization activates a plant immune receptor. Science 336: 221-234.
39. Oh CS, Martin GB, (2010) Effector-triggered immunity mediated by the Pto kinase. Trends Plant Sci 16: 1360-1385.
40. Nguyen HP, Chakravarthy S, Velásquez AC, McLane HL, Zeng L, et al. (2010) Methods to study PAMP-triggered immunity using tomato and Nicotiana benthamiana. Mol Plant Microbe Interact 23: 991-999.
41. Lefebvre B, Timmers T, Mbengue M, Moreau S, Hervé C, et al. (2010) A remorin protein interacts with symbiotic receptors and regulates bacterial infection. Proc Natl Acad Sci U S A 107: 2343-2348.
42. van Ooijen G, Mayr G, Kasiem MM, Albrecht M, Cornelissen BJ, et al. (2008) Structure-function analysis of the NB-ARC domain of plant disease resistance proteins. J Exp Bot 59: 1383-1397.
43. Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, et al. (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nature 12: 1567-1572.
44. Kremers GJ, Goedhart J, van Munster EB, Gadella TW Jr, (2006) Cyan and yellow super fluorescent proteins with improved brightness, protein folding, and FRET Förster radius. Biochem 45: 6570-6580.
45. Endre G, Kereszt A, Kevei Z, Mihacea S, Kaló P, et al. (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417: 962-966.
46. Li J, Chory J, (1997) A putative leucine-rich repeat kinase involved in brassinosteroid signal transduction. Cell 90: 929-938.
47. Mur LA, Kenton P, Lloyd AJ, Ougham H, Prats E, (2008) The hypersensitive response; the centenary is upon us but how much do we know? J Exp Bot 59: 501-520.
48. Coll NS, Epple P, Dangl JL, (2011) Programmed cell death in the plant immune system. Cell Death Differ 18: 1247-1256.
49. Heese A, Hann DR, Gimenez-Ibanez S, Jones AM, He K, et al. (2007) The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci U S A 104: 12217-12222.
50. Taguchi F, Suzuki T, Takeuchi K, Inagaki Y, Toyoda K, et al. (2009) Glycosylation of flagellin from Pseudomonas syringae pv. tabaci 6605 contributes to evasion of host tobacco plant surveillance system. Physiol Mol Plant Pathol 74: 11-17.
51. Ranf S, Eschen-Lippold L, Pecher P, Lee J, Scheel D, (2011) Interplay between calcium signalling and early signalling elements during defence responses to microbe- or damage-associated molecular patterns. Plant J 68: 100-113.
52. Segonzac C, Feike D, Gimenez-Ibanez S, Hann DR, Zipfel C, et al. (2011) Hierarchy and roles of pathogen-associated molecular pattern-induced responses in Nicotiana benthamiana. Plant Physiol 156: 687-699.
53. Frei dit Frey N, Mbengue M, Kwaaitaal M, Nitsch L, Altenbach D, et al. (2012) Plasma membrane calcium ATPases are important components of receptor-mediated signalling in plant immune responses and development. Plant Physiol 159: 798-809.
54. Gust AA, Biswas R, Lenz HD, Rauhut T, Ranf S, et al. (2007) Bacteria-derived peptidoglycans constitute pathogen-associated molecular patterns triggering innate immunity in Arabidopsis. J Biol Chem 282: 32338-32348.
55. Erbs G, Silipo A, Aslam S, De Castro C, Liparoti V, et al. (2008) Peptidoglycan and muropeptides from pathogens Agrobacterium and Xanthomonas elicit plant innate immunity: structure and activity. Cell 15: 438-448.
56. Hamel LP, Beaudoin N, (2010) Chitooligosaccharide sensing and downstream signalling: contrasted outcomes in pathogenic and beneficial plant-microbe interactions. Planta 232: 787-806.
57. Cornelissen B, Horowitz J, van Kan JA, Goldberg RB, Bol JF, (1987) Structure of tobacco genes encoding pathogenesis-related proteins from the PR-1 group. Nucl Acid Res 15: 6799-6811.
58. Mucyn TS, Clemente A, Andriotis VME, Balmuth AL, Oldroyd GED, et al. (2006) The tomato NBARC-LRR protein Prf interacts with Pto kinase in vivo to regulate specific plant immunity. Plant Cell 18: 2792-2806.
59. Takahashi Y, Bin Nasir KH, Ito A, Kanzaki H, Matsumura H, et al. (2007) A high-throughput screen of cell-death-inducing factors in Nicotiana benthamiana identifies a novel MAPKK that mediates INF1-induced cell death signalling and non-host resistance to Pseudomonas cichorii. Plant J 49: 1030-1040.
60. Gao M, Wang X, Wang D, Xu F, Ding X, et al. (2009) Regulation of cell death and innate immunity by two receptor-like kinases in Arabidopsis. Cell 6: 34-44.
61. Kishi-Kaboshi M, Okada K, Kurimoto L, Murakami S, Umezawa T, et al. (2010) A rice fungal MAMP-responsive cascade regulates metabolic flow to antimicrobial metabolite synthesis. Plant J 63: 599-612.
62. Ditt RF, Kerr KF, de Figueiredo P, Delrow J, Comai L, et al. (2006) The Arabidopsis thaliana transcriptome in response to Agrobacterium tumefaciens. Mol Plant Microbe Interact 19: 665-681.
63. Bueno P, Soto MJ, Rodríguez-Rosales MP, Sanjuan J, Olivares J, et al. (2001) Time-course of lipoxygenase, antioxidant enzyme activities and H2O2 accumulation during the early stages of Rhizobium-legume symbiosis. New Phytol 152: 91-96.
64. den Hartog M, Musgrave A, Munnik T, (2001) 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.
65. Charron D, Pingret JL, Chabaud M, Journet EP, Barker DG, (2004) Pharmacological evidence that multiple phospholipid signalling 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.
66. Lohar DP, Sharopova N, Endre G, Peñuela S, Samac D, et al. (2006) Transcript analysis of early nodulation events in Medicago truncatula. Plant Physiol 140: 221-234.
67. Cárdenas L, Martinez A, Sánchez F, Quinto C, (2008) Fast, transient and specific intracellular ROS changes in living root hair cells responding to Nod factors (NFs). Plant J 56: 802-813.
68. Serna-Sanz A, Parniske M, Peck SC, (2011) Phosphoproteome analysis of Lotus japonicus roots reveals shared and distinct components of symbiosis and defense. Mol Plant Microbe Interact 24: 932-937.
69. Sieberer BJ, Chabaud M, Timmers AC, Monin A, Fournier J, et al. (2009) A nuclear-targeted cameleon demonstrates intranuclear Ca2+ spiking in Medicago truncatula root hairs in response to rhizobial Nodulation factors. Plant Physiol 151: 1197-1206.
70. Shaw SL, Long SR, (2003) Nod Factor elicits two separable calcium responses in Medicago truncatula root hair cells. Plant Physiol 131: 976-984.
71. den Hartog M, Verhoef N, Munnik T, (2003) Nod factor and elicitors activate different phospholipid signalling pathways in suspension-cultured alfalfa cells. Plant Physiol 132: 311-317.
72. Kwaaitaal M, Huisman R, Maintz J, Reinstädler A, Panstruga R, (2011) Ionotropic glutamate receptor (iGluR)-like channels mediate MAMP-induced calcium influx in Arabidopsis thaliana. Biochem J 440: 355-365.
73. Wan J, Tanaka K, Zhang XC, Son GH, Brechenmacher L, et al. (2012) LYK4, a lysine motif receptor-like kinase, is important for chitin signalling and plant innate immunity in Arabidopsis. Plant Physiol 160: 396-406.
74. Nakagawa T, Kaku H, Shimoda Y, Sugiyama A, Shimamura M, et al. (2010) 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.
75. Martinez-Abarca F, Herrera-Cervera JA, Bueno P, Sanjuan J, Bisseling T, et al. (1998) Involvement of salicylic acid in the establishment of the Rhizobium meliloti-alfalfa symbiosis. Mol Plant Microbe Interact 11: 153-155.
76. Peleg-Grosmann S, Golani Y, Kaye Y, Melamed-Book N, Levine A, (2009) NPR1 protein regulates pathogenic and symbiotic interactions between Rhizobium and legumes and non-legumes. PLoS ONE 4: e8399.
77. Capoen W, Oldroyd G, Goormachtig S, Holsters M, (2010) Sesbania rostrata: a case study of natural variation in legume nodulation. New Phytol 186: 340-345.
78. Zhang XC, Cannon SB, Stacey G (2009) Evolutionary genomics of LysM genes in land plants. BMC Evol Biol 9: doi:10.1186/1471-2148-9-183.
79. Murray J, Karas B, Ross L, Brachmann A, Wagg C, et al. (2006) Genetic suppressors of the Lotus japonicus har1-1 hypernodulation phenotype. Mol Plant Microbe Interact 19: 1082-1091.
80. Wang X, Kota U, He K, Blackburn K, Li J, et al. (2008) Sequential transphosphorylation of the BRI1/BAK1 receptor kinase complex impacts early events in brassinosteroid signalling. Cell 15: 220-235.
81. Lemmon MA, Schlessinger J, (2010) Cell signalling by receptor tyrosine kinases. Cell 141: 1117-1134.
82. Oh MH, Wang X, Clouse SD, Huber SC, (2012) Deactivation of the Arabidopsis Brassinosteroid Insensitive 1 (BRI1) receptor kinase by autophosphorylation within the glycine-rich loop. Proc Natl Acad Sci U S A 109: 327-332.
83. Chen L, Hamada S, Fujiwara M, Zhu T, Thao NP, et al. (2010) The Hop/Sti1-Hsp90 chaperone complex facilitates the maturation and transport of a PAMP receptor in rice innate immunity. Cell Host Microbe 7: 185-196.
84. Ke D, Fang Q, Chen C, Zhu H, Chen T, et al. (2012) The small GTPase ROP6 interacts with NFR5 and is involved in nodule formation in Lotus japonicus. Plant Physiol 159: 131-143.