1932

Abstract

A classic view of the evolution of mutualism is that it derives from a pathogenic relationship that attenuated over time to a situation in which both partners can benefit. If this is the case for rhizobia, then one might uncover features of the symbiosis that reflect this earlier pathogenic state. For example, as with plant pathogens, it is now generally assumed that rhizobia actively suppress the host immune response to allow infection and symbiosis establishment. Likewise, the host has retained mechanisms to control the nutrient supply to the symbionts and the number of nodules so that they do not become too burdensome. The open question is whether such events are strictly ancillary to the central symbiotic nodulation factor signaling pathway or are essential for rhizobial host infection. Subsequent to these early infection events, plant immune responses can also be induced inside nodules and likely play a role in, for example, nodule senescence. Thus, a balanced regulation of innate immunity is likely required throughout rhizobial infection, symbiotic establishment, and maintenance. In this review, we discuss the significance of plant immune responses in the regulation of symbiotic associations with rhizobia, as well as rhizobial evasion of the host immune system.

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2017-04-28
2024-03-28
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Literature Cited

  1. Ade J, DeYoung BJ, Golstein C, Innes RW. 1.  2007. Indirect activation of a plant nucleotide binding site-leucine-rich repeat protein by a bacterial protease. PNAS 104:2531–36 [Google Scholar]
  2. Arthikala MK, Montiel J, Nava N, Santana O, Sánchez-López R. 2.  et al. 2013. PvRbohB negatively regulates Rhizophagusirregularis colonization in Phaseolus vulgaris. Plant Cell Physiol. 54:1391–402 [Google Scholar]
  3. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL. 3.  et al. 2002. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977–83 [Google Scholar]
  4. Ausubel FM.4.  2005. Are innate immune signaling pathways in plants and animals conserved?. Nat. Immunol. 6:973–79 [Google Scholar]
  5. Axtell MJ, Staskawicz BJ. 5.  2003. Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112:369–77 [Google Scholar]
  6. Baltrus DA, Nishimura MT, Romanchuk A, Chang JH, Mukhtar MS. 6.  et al. 2011. Dynamic evolution of pathogenicity revealed by sequencing and comparative genomics of 19 Pseudomonassyringae isolates. PLOS Pathog 7:e1002132 [Google Scholar]
  7. Bent AF, Mackey D. 7.  2007. Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu. Rev. Phytopathol. 45:399–436 [Google Scholar]
  8. Berrabah F, Bourcy M, Cayrel A, Eschstruth A, Mondy S. 8.  et al. 2014. Growth conditions determine the DNF2 requirement for symbiosis. PLOS ONE 9:e91866 [Google Scholar]
  9. Berrabah F, Bourcy M, Eschstruth A, Cayrel A, Guefrachi I. 9.  et al. 2014. A nonRD receptor-like kinase prevents nodule early senescence and defense-like reactions during symbiosis. New Phytol 203:1305–14 [Google Scholar]
  10. Berrabah F, Ratet P, Gourion B. 10.  2015. Multiple steps control immunity during the intracellular accommodation of rhizobia. J. Exp. Bot. 66:1977–85 [Google Scholar]
  11. Bigeard J, Colcombet J, Hirt H. 11.  2015. Signaling mechanisms in pattern-triggered immunity (PTI). Mol. Plant 8:521–39 [Google Scholar]
  12. Birker D, Heidrich K, Takahara H, Narusaka M, Deslandes L. 12.  et al. 2009. A locus conferring resistance to Colletotrichum higginsianum is shared by four geographically distinct Arabidopsis accessions. Plant J 60:602–13 [Google Scholar]
  13. Boch J, Bonas U, Lahaye T. 13.  2014. TAL effectors—pathogen strategies and plant resistance engineering. New Phytol 204:823–32 [Google Scholar]
  14. Boudsocq M, Willmann MR, McCormack M, Lee H, Shan L. 14.  et al. 2010. Differential innate immune signalling via Ca2+ sensor protein kinases. Nature 464:418–22 [Google Scholar]
  15. Bourcy M, Brocard L, Pislariu CI, Cosson V, Mergaert P. 15.  et al. 2013. Medicago truncatula DNF2 is a PI-PLC-XD-containing protein required for bacteroid persistence and prevention of nodule early senescence and defense-like reactions. New Phytol 197:1250–61 [Google Scholar]
  16. Brewin NJ.16.  1991. Development of the legume root nodule. Annu. Rev. Cell Biol. 7:191–226 [Google Scholar]
  17. Broughton WJ, Perret X. 17.  1999. Genealogy of legume-Rhizobium symbioses. Curr. Opin. Plant Biol. 2:305–11 [Google Scholar]
  18. Cao Y, Liang Y, Tanaka K, Nguyen CT, Jedrzejczak RP. 18.  et al. 2014. The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1. eLife 3:e03766 [Google Scholar]
  19. Cao Y, Tanaka K, Nguyen CT, Stacey G. 19.  2014. Extracellular ATP is a central signaling molecule in plant stress responses. Curr. Opin. Plant Biol. 20:82–87 [Google Scholar]
  20. Chen LQ, Hou BH, Lalonde S, Takanaga H, Hartung ML. 20.  et al. 2010. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468:527–32 [Google Scholar]
  21. Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nurnberger T. 21.  et al. 2007. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497–500 [Google Scholar]
  22. Chisholm ST, Coaker G, Day B, Staskawicz BJ. 22.  2006. Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–14 [Google Scholar]
  23. Choi J, Tanaka K, Cao Y, Qi Y, Qiu J. 23.  et al. 2014. Identification of a plant receptor for extracellular ATP. Science 343:290–94 [Google Scholar]
  24. Christian M, Cermak T, Doyle EL, Schmidt C, Zhang F. 24.  et al. 2010. Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186:757–61 [Google Scholar]
  25. Cohn M, Bart RS, Shybut M, Dahlbeck D, Gomez M. 25.  et al. 2014. Xanthomonas axonopodis virulence is promoted by a transcription activator-like effector-mediated induction of a SWEET sugar transporter in cassava. Mol. Plant-Microbe Interact. 27:1186–98 [Google Scholar]
  26. Collmer A, Badel JL, Charkowski AO, Deng WL, Fouts DE. 26.  et al. 2000. Pseudomonas syringae Hrp type III secretion system and effector proteins. PNAS 97:8770–77 [Google Scholar]
  27. Cui H, Tsuda K, Parker JE. 27.  2015. Effector-triggered immunity: from pathogen perception to robust defense. Annu. Rev. Plant Biol. 66:487–511 [Google Scholar]
  28. D'Haeze W, De Rycke R, Mathis R, Goormachtig S, Pagnotta S. 28.  et al. 2003. Reactive oxygen species and ethylene play a positive role in lateral root base nodulation of a semiaquatic legume. PNAS 100:11789–94 [Google Scholar]
  29. D'Haeze W, Holsters M. 29.  2002. Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 12:79R–105R [Google Scholar]
  30. Dai WJ, Zeng Y, Xie ZP, Staehelin C. 30.  2008. Symbiosis-promoting and deleterious effects of NopT, a novel type 3 effector of Rhizobium sp. strain NGR234. J. Bacteriol. 190:5101–10 [Google Scholar]
  31. Dangl JL, Jones JD. 31.  2001. Plant pathogens and integrated defence responses to infection. Nature 411:826–33 [Google Scholar]
  32. Dangl JL, McDowell JM. 32.  2006. Two modes of pathogen recognition by plants. PNAS 103:8575–76 [Google Scholar]
  33. Day RB, Okada M, Ito Y, Tsukada K, Zaghouani H. 33.  et al. 2001. Binding site for chitin oligosaccharides in the soybean plasma membrane. Plant Physiol 126:1162–73 [Google Scholar]
  34. Deakin WJ, Broughton WJ. 34.  2009. Symbiotic use of pathogenic strategies: rhizobial protein secretion systems. Nat. Rev. Microbiol. 7:312–20 [Google Scholar]
  35. Debellé F, Moulin L, Mangin B, Dénarié J, Boivin C. 35.  2001. Nod genes and Nod signals and the evolution of the rhizobium legume symbiosis. Acta Biochim. Pol. 48:359–65 [Google Scholar]
  36. Del Rio LA.36.  2015. ROS and RNS in plant physiology: an overview. J. Exp. Bot. 66:2827–37 [Google Scholar]
  37. Deslandes L, Olivier J, Theulieres F, Hirsch J, Feng DX. 37.  et al. 2002. Resistance to Ralstonia solanacearum in Arabidopsis thaliana is conferred by the recessive RRS1-R gene, a member of a novel family of resistance genes. PNAS 99:2404–9 [Google Scholar]
  38. DeYoung BJ, Qi D, Kim SH, Burke TP, Innes RW. 38.  2012. Activation of a plant nucleotide binding-leucine rich repeat disease resistance protein by a modified self protein. Cell. Microbiol. 14:1071–84 [Google Scholar]
  39. Dodds PN, Lawrence GJ, Catanzariti AM, Teh T, Wang CI. 39.  et al. 2006. Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. PNAS 103:8888–93 [Google Scholar]
  40. Dodds PN, Rathjen JP. 40.  2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11:539–48 [Google Scholar]
  41. Duodu S, Bhuvaneswari TV, Stokkermans TJ, Peters NK. 41.  1999. A positive role for rhizobitoxine in Rhizobium-legume symbiosis. Mol. Plant-Microbe Interact. 12:1082–89 [Google Scholar]
  42. Farkas A, Maroti G, Durgo H, Gyorgypal Z, Lima RM. 42.  et al. 2014. Medicago truncatula symbiotic peptide NCR247 contributes to bacteroid differentiation through multiple mechanisms. PNAS 111:5183–88 [Google Scholar]
  43. Faruque OM, Miwa H, Yasuda M, Fujii Y, Kaneko T. 43.  et al. 2015. Identification of Bradyrhizobium elkanii genes involved in incompatibility with soybean plants carrying the Rj4 allele. Appl. Environ. Microbiol 81:6710–17 [Google Scholar]
  44. Faulkner C, Petutschnig E, Benitez-Alfonso Y, Beck M, Robatzek S. 44.  et al. 2013. LYM2-dependent chitin perception limits molecular flux via plasmodesmata. PNAS 110:9166–70 [Google Scholar]
  45. Fliegmann J, Bono JJ. 45.  2015. Lipo-chitooligosaccharidic nodulation factors and their perception by plant receptors. Glycoconjug. J. 32:455–64 [Google Scholar]
  46. Flor HH.46.  1971. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9:275–96 [Google Scholar]
  47. Gage DJ.47.  2004. Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol. Mol. Biol. Rev. 68:280–300 [Google Scholar]
  48. Garcia K, Delaux PM, Cope KR, Ane JM. 48.  2015. Molecular signals required for the establishment and maintenance of ectomycorrhizal symbioses. New Phytol 208:79–87 [Google Scholar]
  49. Gassmann W, Bhattacharjee S. 49.  2012. Effector-triggered immunity signaling: from gene-for-gene pathways to protein-protein interaction networks. Mol. Plant-Microbe Interact. 25:862–68 [Google Scholar]
  50. Gassmann W, Hinsch ME, Staskawicz BJ. 50.  1999. The Arabidopsis RPS4 bacterial-resistance gene is a member of the TIR-NBS-LRR family of disease-resistance genes. Plant J 20:265–77 [Google Scholar]
  51. Ge YY, Xiang QW, Wagner C, Zhang D, Xie ZP, Staehelin C. 51.  2016. The type 3 effector NopL of Sinorhizobium sp. strain NGR234 is a mitogen-activated protein kinase substrate. J. Exp. Bot. 67:2483–94 [Google Scholar]
  52. Geurts R, Bisseling T. 52.  2002. Rhizobium Nod factor perception and signalling. Plant Cell 14:Suppl.S239–49 [Google Scholar]
  53. Gimenez-Ibanez S, Hann DR, Ntoukakis V, Petutschnig E, Lipka V, Rathjen JP. 53.  2009. AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Curr. Biol. 19:423–29 [Google Scholar]
  54. Giraud E, Moulin L, Vallenet D, Barbe V, Cytryn E. 54.  et al. 2007. Legumes symbioses: absence of Nod genes in photosynthetic bradyrhizobia. Science 316:1307–12 [Google Scholar]
  55. Gómez-Gómez L, Boller T. 55.  2000. FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell 5:1003–11 [Google Scholar]
  56. Gómez-Gómez L, Boller T. 56.  2002. Flagellin perception: a paradigm for innate immunity. Trends Plant Sci 7:251–56 [Google Scholar]
  57. Gough C, Cullimore J. 57.  2011. Lipo-chitooligosaccharide signaling in endosymbiotic plant-microbe interactions. Mol. Plant-Microbe Interact. 24:867–78 [Google Scholar]
  58. Gourion B, Berrabah F, Ratet P, Stacey G. 58.  2015. Rhizobium-legume symbioses: the crucial role of plant immunity. Trends Plant Sci 20:186–94 [Google Scholar]
  59. Govindarajulu M, Kim SY, Libault M, Berg RH, Tanaka K. 59.  et al. 2009. GS52 ecto-apyrase plays a critical role during soybean nodulation. Plant Physiol 149:994–1004 [Google Scholar]
  60. Gressent F, Cullimore JV, Ranjeva R, Bono JJ. 60.  2004. Radiolabeling of lipo-chitooligosaccharides using the NodH sulfotransferase: a two-step enzymatic procedure. BMC Biochem 5:4 [Google Scholar]
  61. Guefrachi I, Pierre O, Timchenko T, Alunni B, Barriere Q. 61.  et al. 2015. Bradyrhizobium BclA is a peptide transporter required for bacterial differentiation in symbiosis with Aeschynomene legumes. Mol. Plant-Microbe Interact 28:1155–66 [Google Scholar]
  62. Gully D, Gargani D, Bonaldi K, Grangeteau C, Chaintreuil C. 62.  et al. 2016. A peptidoglycan-remodeling enzyme is critical for bacteroid differentiation in Bradyrhizobium spp. during legume symbiosis.. Mol. Plant-Microbe Interact. 29:447–57 [Google Scholar]
  63. Hadwiger LA.63.  1999. Host-parasite interactions: elicitation of defense responses in plants with chitosan. EXS 87:185–200 [Google Scholar]
  64. Hamid R, Khan MA, Ahmad M, Ahmad MM, Abdin MZ. 64.  et al. 2013. Chitinases: an update. J. Pharm. Bioallied Sci. 5:21–29 [Google Scholar]
  65. Hayafune M, Berisio R, Marchetti R, Silipo A, Kayama M. 65.  et al. 2014. Chitin-induced activation of immune signaling by the rice receptor CEBiP relies on a unique sandwich-type dimerization. PNAS 111:E404–13 [Google Scholar]
  66. Hayashi M, Saeki Y, Haga M, Harada K, Kouchi H, Umehara Y. 66.  2012. Rj (rj) genes involved in nitrogen-fixing root nodule formation in soybean. Breed. Sci 61:544–53 [Google Scholar]
  67. Hayashi M, Shiro S, Kanamori H, Mori-Hosokawa S, Sasaki-Yamagata H. 67.  et al. 2014. A thaumatin-like protein, Rj4, controls nodule symbiotic specificity in soybean. Plant Cell Physiol 55:1679–89 [Google Scholar]
  68. Heese A, Hann DR, Gimenez-Ibanez S, Jones AM, He K. 68.  et al. 2007. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. PNAS 104:12217–22 [Google Scholar]
  69. Henry E, Yadeta KA, Coaker G. 69.  2013. Recognition of bacterial plant pathogens: local, systemic and transgenerational immunity. New Phytol 199:908–15 [Google Scholar]
  70. Herbert JM, Savi P. 70.  2003. P2Y12, a new platelet ADP receptor, target of clopidogrel. Semin. Vasc. Med. 3:113–22 [Google Scholar]
  71. Horvath B, Domonkos A, Kereszt A, Szucs A, Abraham E. 71.  et al. 2015. Loss of the nodule-specific cysteine rich peptide, NCR169, abolishes symbiotic nitrogen fixation in the Medicago truncatula dnf7 mutant. PNAS 112:15232–37 [Google Scholar]
  72. Indrasumunar A, Gresshoff PM. 72.  2010. Duplicated Nod-Factor Receptor 5 (NFR5) genes are mutated in soybean. Plant Signal. Behav. 5:535–36 [Google Scholar]
  73. Indrasumunar A, Searle I, Lin MH, Kereszt A, Men A. 73.  et al. 2011. Nodulation factor receptor kinase 1α controls nodule organ number in soybean (Glycine max L. Merr). Plant J 65:39–50 [Google Scholar]
  74. Jia Y, McAdams SA, Bryan GT, Hershey HP, Valent B. 74.  2000. Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J 19:4004–14 [Google Scholar]
  75. Jones JD, Dangl JL. 75.  2006. The plant immune system. Nature 444:323–29 [Google Scholar]
  76. Jones KM, Sharopova N, Lohar DP, Zhang JQ, VandenBosch KA, Walker GC. 76.  2008. Differential response of the plant Medicago truncatula to its symbiont Sinorhizobium meliloti or an exopolysaccharide-deficient mutant. PNAS 105:704–9 [Google Scholar]
  77. Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N. 77.  et al. 2006. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. PNAS 103:11086–91 [Google Scholar]
  78. Kamoun S.78.  2006. A catalogue of the effector secretome of plant pathogenic oomycetes. Annu. Rev. Phytopathol. 44:41–60 [Google Scholar]
  79. Karr DB, Emerich DW, Karr AL. 79.  1992. Accumulation of the phytoalexin, glyceollin, in root nodules of soybean formed by effective and ineffective strains of Bradyrhizobium japonicum. J. Chem. Ecol. 18:997–1008 [Google Scholar]
  80. Katsir L, Schilmiller AL, Staswick PE, He SY, Howe GA. 80.  2008. COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. PNAS 105:7100–5 [Google Scholar]
  81. Kawaharada Y, Kelly S, Nielsen MW, Hjuler CT, Gysel K. 81.  et al. 2015. Receptor-mediated exopolysaccharide perception controls bacterial infection. Nature 523:308–12 [Google Scholar]
  82. Keating DH, Willits MG, Long SR. 82.  2002. A Sinorhizobium meliloti lipopolysaccharide mutant altered in cell surface sulfation. J. Bacteriol. 184:6681–89 [Google Scholar]
  83. Kim JG, Stork W, Mudgett MB. 83.  2013. Xanthomonas type III effector XopD desumoylates tomato transcription factor SlERF4 to suppress ethylene responses and promote pathogen growth. Cell Host Microbe 13:143–54 [Google Scholar]
  84. Kim M, Chen Y, Xi J, Waters C, Chen R, Wang D. 84.  2015. An antimicrobial peptide essential for bacterial survival in the nitrogen-fixing symbiosis. PNAS 112:15238–43 [Google Scholar]
  85. Kim SH, Qi D, Ashfield T, Helm M, Innes RW. 85.  2016. Using decoys to expand the recognition specificity of a plant disease resistance protein. Science 351:684–87 [Google Scholar]
  86. Kim SY, Sivaguru M, Stacey G. 86.  2006. Extracellular ATP in plants. Visualization, localization, and analysis of physiological significance in growth and signaling. Plant Physiol 142:984–92 [Google Scholar]
  87. Krishnan HB.87.  2002. NolX of Sinorhizobium fredii USDA257, a type III-secreted protein involved in host range determination, is localized in the infection threads of cowpea (Vigna unguiculata [L.] Walp) and soybean (Glycine max [L.] Merr.) nodules. J. Bacteriol 184:831–39 [Google Scholar]
  88. Le Roux C, Huet G, Jauneau A, Camborde L, Tremousaygue D. 88.  et al. 2015. A receptor pair with an integrated decoy converts pathogen disabling of transcription factors to immunity. Cell 161:1074–88 [Google Scholar]
  89. Liang Y, Cao Y, Tanaka K, Thibivilliers S, Wan J. 89.  et al. 2013. Nonlegumes respond to rhizobial Nod factors by suppressing the innate immune response. Science 341:1384–87 [Google Scholar]
  90. Liang Y, Tóth K, Cao Y, Tanaka K, Espinoza C, Stacey G. 90.  2014. Lipochitooligosaccharide recognition: an ancient story. New Phytol 204:289–96 [Google Scholar]
  91. Libault M, Farmer A, Brechenmacher L, Drnevich J, Langley RJ. 91.  et al. 2010. Complete transcriptome of the soybean root hair cell, a single-cell model, and its alteration in response to Bradyrhizobium japonicum infection. Plant Physiol 152:541–52 [Google Scholar]
  92. Liu B, Li JF, Ao Y, Li Z, Liu J. 92.  et al. 2013. OsLYP4 and OsLYP6 play critical roles in rice defense signal transduction. Plant Signal. Behav. 8:e22980 [Google Scholar]
  93. Liu CW, Murray JD. 93.  2016. The role of flavonoids in nodulation host-range specificity: an update. Plants 5:33 [Google Scholar]
  94. Liu J, Elmore JM, Lin ZJ, Coaker G. 94.  2011. A receptor-like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor. Cell Host Microbe 9:137–46 [Google Scholar]
  95. Liu T, Liu Z, Song C, Hu Y, Han Z. 95.  et al. 2012. Chitin-induced dimerization activates a plant immune receptor. Science 336:1160–64 [Google Scholar]
  96. Lohmann GV, Shimoda Y, Nielsen MW, Jorgensen FG, Grossmann C. 96.  et al. 2010. Evolution and regulation of the Lotus japonicus LysM receptor gene family. Mol. Plant-Microbe Interact. 23:510–21 [Google Scholar]
  97. Long SR.97.  1996. Rhizobium symbiosis: Nod factors in perspective. Plant Cell 8:1885–98 [Google Scholar]
  98. López-Baena FJ, Monreal JA, Pérez-Montaño F, Guasch-Vidal B, Bellogín RA. 98.  et al. 2009. The absence of Nops secretion in Sinorhizobium fredii HH103 increases GmPR1 expression in Williams soybean. Mol. Plant-Microbe Interact 22:1445–54 [Google Scholar]
  99. Lopez-Gomez M, Sandal N, Stougaard J, Boller T. 99.  2012. Interplay of flg22-induced defence responses and nodulation in Lotus japonicus. J. Exp. Bot. 63:393–401 [Google Scholar]
  100. López-Lara IM, Blok-Tip L, Quinto C, Garcia ML, Stacey G. 100.  et al. 1996. NodZ of Bradyrhizobium extends the nodulation host range of Rhizobium by adding a fucosyl residue to nodulation signals. Mol. Microbiol 21:397–408 [Google Scholar]
  101. Lu D, Wu S, Gao X, Zhang Y, Shan L, He P. 101.  2010. A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. PNAS 107:496–501 [Google Scholar]
  102. Macho AP, Zipfel C. 102.  2014. Plant PRRs and the activation of innate immune signaling. Mol. Cell 54:263–72 [Google Scholar]
  103. Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL. 103.  2003. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112:379–89 [Google Scholar]
  104. Mackey D, Holt BF III, Wiig A, Dangl JL. 104.  2002. RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108:743–54 [Google Scholar]
  105. Madsen EB, Antolin-Llovera M, Grossmann C, Ye J, Vieweg S. 105.  et al. 2011. 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 65:404–17 [Google Scholar]
  106. Madsen EB, Madsen LH, Radutoiu S, Olbryt M, Rakwalska M. 106.  et al. 2003. A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425:637–40 [Google Scholar]
  107. Madsen LH, Tirichine L, Jurkiewicz A, Sullivan JT, Heckmann AB. 107.  et al. 2010. The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat. Commun. 1:10 [Google Scholar]
  108. Marino D, Andrio E, Danchin EG, Oger E, Gucciardo S. 108.  et al. 2011. A Medicago truncatula NADPH oxidase is involved in symbiotic nodule functioning. New Phytol 189:580–92 [Google Scholar]
  109. Martínez-Abarca F, Herrera-Cervera JA, Bueno P, Sanjuan J, Bisseling T, Olivares J. 109.  1998. Involvement of salicylic acid in the establishment of the Rhizobium meliloti-alfalfa symbiosis. Mol. Plant-Microbe Interact. 11:153–55 [Google Scholar]
  110. McHale L, Tan X, Koehl P, Michelmore RW. 110.  2006. Plant NBS-LRR proteins: adaptable guards. Genome Biol 7:212 [Google Scholar]
  111. Mengiste T.111.  2012. Plant immunity to necrotrophs. Annu. Rev. Phytopathol. 50:267–94 [Google Scholar]
  112. Mergaert P, Nikovics K, Kelemen Z, Maunoury N, Vaubert D. 112.  et al. 2003. A novel family in Medicago truncatula consisting of more than 300 nodule-specific genes coding for small, secreted polypeptides with conserved cysteine motifs. Plant Physiol 132:161–73 [Google Scholar]
  113. Miya A, Albert P, Shinya T, Desaki Y, Ichimura K. 113.  et al. 2007. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. PNAS 104:19613–18 [Google Scholar]
  114. Miyata K, Kozaki T, Kouzai Y, Ozawa K, Ishii K. 114.  et al. 2014. The bifunctional plant receptor, OsCERK1, regulates both chitin-triggered immunity and arbuscular mycorrhizal symbiosis in rice. Plant Cell Physiol 55:1864–72 [Google Scholar]
  115. Montiel J, Arthikala MK, Cárdenas L, Quinto C. 115.  2016. Legume NADPH oxidases have crucial roles at different stages of nodulation. Int. J. Mol. Sci. 17:680 [Google Scholar]
  116. Montiel J, Nava N, Cárdenas L, Sánchez-López R, Arthikala MK. 116.  et al. 2012. A Phaseolus vulgaris NADPH oxidase gene is required for root infection by rhizobia. Plant Cell Physiol 53:1751–67 [Google Scholar]
  117. Morbitzer R, Elsaesser J, Hausner J, Lahaye T. 117.  2011. Assembly of custom TALE-type DNA binding domains by modular cloning. Nucleic Acids Res 39:5790–99 [Google Scholar]
  118. Nakagawa T, Kaku H, Shimoda Y, Sugiyama A, Shimamura M. 118.  et al. 2011. 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 65:169–80 [Google Scholar]
  119. Narusaka M, Shirasu K, Noutoshi Y, Kubo Y, Shiraishi T. 119.  et al. 2009. RRS1 and RPS4 provide a dual Resistance-gene system against fungal and bacterial pathogens. Plant J. 60:218–26 [Google Scholar]
  120. Nelson MS, Sadowsky MJ. 120.  2015. Secretion systems and signal exchange between nitrogen-fixing rhizobia and legumes. Front. Plant Sci. 6:491 [Google Scholar]
  121. Okazaki S, Kaneko T, Sato S, Saeki K. 121.  2013. Hijacking of leguminous nodulation signaling by the rhizobial type III secretion system. PNAS 110:17131–36 [Google Scholar]
  122. Paparella C, Savatin DV, Marti L, De Lorenzo G, Ferrari S. 122.  2014. The Arabidopsis LYSIN MOTIF-CONTAINING RECEPTOR-LIKE KINASE3 regulates the cross talk between immunity and abscisic acid responses. Plant Physiol 165:262–76 [Google Scholar]
  123. Peleg-Grossman S, Volpin H, Levine A. 123.  2007. Root hair curling and Rhizobium infection in Medicago truncatula are mediated by phosphatidylinositide-regulated endocytosis and reactive oxygen species. J. Exp. Bot 58:1637–49 [Google Scholar]
  124. Perret X, Staehelin C, Broughton WJ. 124.  2000. Molecular basis of symbiotic promiscuity. Microbiol. Mol. Biol. Rev. 64:180–201 [Google Scholar]
  125. Pislariu CI, Murray JD, Wen J, Cosson V, Muni RR. 125.  et al. 2012. A Medicago truncatula tobacco retrotransposon insertion mutant collection with defects in nodule development and symbiotic nitrogen fixation. Plant Physiol 159:1686–99 [Google Scholar]
  126. Qian D, Allen FL, Stacey G, Gresshoff PM. 126.  1996. Plant genetic study of restricted nodulation in soybean. Crop. Sci. 36:243–49 [Google Scholar]
  127. Radutoiu S, Madsen LH, Madsen EB, Felle HH, Umehara Y. 127.  et al. 2003. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425:585–92 [Google Scholar]
  128. Ranf S, Gisch N, Schäffer M, Illig T, Westphal L. 128.  et al. 2015. A lectin S-domain receptor kinase mediates lipopolysaccharide sensing in Arabidopsis thaliana. Nat. Immunol. 16:426–33 [Google Scholar]
  129. Romer P, Recht S, Lahaye T. 129.  2009. A single plant resistance gene promoter engineered to recognize multiple TAL effectors from disparate pathogens. PNAS 106:20526–31 [Google Scholar]
  130. Roth E, Jeon K, Stacey G. 130.  1988. Homology in endosymbiotic systems: the term ‘symbiosome.’. Molecular Genetics of Plant-Microbe Interactions R Palacios, DP Verma 220–25 St. Paul, MN: Am. Phytopathol. Soc. Press [Google Scholar]
  131. Sadowsky MJ, Cregan PB, Rodriguez-Quinones F, Keyser HH. 131.  1990. Microbial influence on gene-for-gene interactions in legume-Rhizobium symbioses. Plant Soil 129:53–60 [Google Scholar]
  132. Santos R, Hérouart D, Sigaud S, Touati D, Puppo A. 132.  2001. Oxidative burst in alfalfa-Sinorhizobium meliloti symbiotic interaction. Mol. Plant-Microbe Interact. 14:86–89 [Google Scholar]
  133. Sarris PF, Duxbury Z, Huh SU, Ma Y, Segonzac C. 133.  et al. 2015. A plant immune receptor detects pathogen effectors that target WRKY transcription factors. Cell 161:1089–100 [Google Scholar]
  134. Schulze B, Mentzel T, Jehle AK, Mueller K, Beeler S. 134.  et al. 2010. Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1. J. Biol. Chem. 285:9444–51 [Google Scholar]
  135. Sewelam N, Kazan K, Schenk PM. 135.  2016. Global plant stress signaling: reactive oxygen species at the cross-road. Front. Plant Sci. 7:187 [Google Scholar]
  136. Shan L, He P, Li J, Heese A, Peck SC. 136.  et al. 2008. Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 4:17–27 [Google Scholar]
  137. Shao F, Golstein C, Ade J, Stoutemyer M, Dixon JE, Innes RW. 137.  2003. Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301:1230–33 [Google Scholar]
  138. Shimizu T, Nakano T, Takamizawa D, Desaki Y, Ishii-Minami N. 138.  et al. 2010. Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J 64:204–14 [Google Scholar]
  139. Shinya T, Motoyama N, Ikeda A, Wada M, Kamiya K. 139.  et al. 2012. Functional characterization of CEBiP and CERK1 homologs in Arabidopsis and rice reveals the presence of different chitin receptor systems in plants. Plant Cell Physiol 53:1696–706 [Google Scholar]
  140. Sinharoy S, Torres-Jerez I, Bandyopadhyay K, Kereszt A, Pislariu CI. 140.  et al. 2013. The C2H2 transcription factor REGULATOR OF SYMBIOSOME DIFFERENTIATION represses transcription of the secretory pathway gene VAMP721a and promotes symbiosome development in Medicago truncatula. Plant Cell 25:3584–601 [Google Scholar]
  141. Skorpil P, Saad MM, Boukli NM, Kobayashi H, Ares-Orpel F. 141.  et al. 2005. NopP, a phosphorylated effector of Rhizobium sp. strain NGR234, is a major determinant of nodulation of the tropical legumes Flemingia congesta and Tephrosia vogelii. Mol. Microbiol 57:1304–17 [Google Scholar]
  142. Skorupska A, Janczarek M, Marczak M, Mazur A, Król J. 142.  2006. Rhizobial exopolysaccharides: genetic control and symbiotic functions. Microb. Cell Fact. 5:7 [Google Scholar]
  143. Stacey G, McAlvin CB, Kim SY, Olivares J, Soto MJ. 143.  2006. Effects of endogenous salicylic acid on nodulation in the model legumes Lotus japonicus and Medicago truncatula. Plant Physiol. 141:1473–81 [Google Scholar]
  144. Staehelin C, Krishnan HB. 144.  2015. Nodulation outer proteins: double-edged swords of symbiotic rhizobia. Biochem. J. 470:263–74 [Google Scholar]
  145. Stroncek JD, Reichert WM. 145.  2008. Overview of wound healing in different tissue types. Indwelling Neural Implants: Strategies for Contending with the In Vivo Environment WM Reichert 3–38 Boca Raton, FL: CRC [Google Scholar]
  146. Sun J, Miller JB, Granqvist E, Wiley-Kalil A, Gobbato E. 146.  et al. 2013. Activation of symbiosis signaling by arbuscular mycorrhizal fungi in legumes and rice. Plant Cell 27:823–38 [Google Scholar]
  147. Tanaka K, Choi J, Cao Y, Stacey G. 147.  2014. Extracellular ATP acts as a damage-associated molecular pattern (DAMP) signal in plants. Front. Plant Sci. 5:446 [Google Scholar]
  148. Tanaka K, Nguyen CT, Libault M, Cheng J, Stacey G. 148.  2011. Enzymatic activity of the soybean ecto-apyrase GS52 is essential for stimulation of nodulation. Plant Physiol 155:1988–98 [Google Scholar]
  149. Tang F, Yang S, Liu J, Zhu H. 149.  2016. Rj4, a gene controlling nodulation specificity in soybeans, encodes a thaumatin-like protein but not the one previously reported. Plant Physiol 170:26–32 [Google Scholar]
  150. Tasset C, Bernoux M, Jauneau A, Pouzet C, Brière C. 150.  et al. 2010. Autoacetylation of the Ralstonia solanacearum effector PopP2 targets a lysine residue essential for RRS1-R-mediated immunity in Arabidopsis. PLOS Pathog 6:e1001202 [Google Scholar]
  151. Tellström V, Usadel B, Thimm O, Stitt M, Küster H, Niehaus K. 151.  2007. The lipopolysaccharide of Sinorhizobium meliloti suppresses defense-associated gene expression in cell cultures of the host plant Medicago truncatula. Plant Physiol. 143:825–37 [Google Scholar]
  152. Torres MA, Dangl JL, Jones JDG. 152.  2002. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. PNAS 99:517–22 [Google Scholar]
  153. Tóth K, Stacey G. 153.  2015. Does plant immunity play a critical role during initiation of the legume-rhizobium symbiosis?. Front. Plant Sci. 6:401 [Google Scholar]
  154. Trda L, Boutrot F, Claverie J, Brule D, Dorey S, Poinssot B. 154.  2015. Perception of pathogenic or beneficial bacteria and their evasion of host immunity: pattern recognition receptors in the frontline. Front. Plant Sci. 6:219 [Google Scholar]
  155. Uppalapati SR, Ishiga Y, Wangdi T, Kunkel BN, Anand A. 155.  et al. 2007. The phytotoxin coronatine contributes to pathogen fitness and is required for suppression of salicylic acid accumulation in tomato inoculated with Pseudomonassyringae pv. tomato DC3000. Mol. Plant-Microbe Interact. 20:955–65 [Google Scholar]
  156. Van de Velde W, Zehirov G, Szatmari A, Debreczeny M, Ishihara H. 156.  et al. 2010. Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327:1122–26 [Google Scholar]
  157. Van den Ackerveken G, Marois E, Bonas U. 157.  1996. Recognition of the bacterial avirulence protein AvrBs3 occurs inside the host plant cell. Cell 87:1307–16 [Google Scholar]
  158. Vinatzer BA, Monteil CL, Clarke CR. 158.  2014. Harnessing population genomics to understand how bacterial pathogens emerge, adapt to crop hosts, and disseminate. Annu. Rev. Phytopathol. 52:19–43 [Google Scholar]
  159. Wan J, Tanaka K, Zhang XC, Son GH, Brechenmacher L. 159.  et al. 2012. LYK4, a lysin motif receptor-like kinase, is important for chitin signaling and plant innate immunity in Arabidopsis. Plant Physiol. 160:396–406 [Google Scholar]
  160. Wan J, Zhang XC, Neece D, Ramonell KM, Clough S. 160.  et al. 2008. A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20:471–81 [Google Scholar]
  161. Wang C, Yu H, Luo L, Duan L, Cai L. 161.  et al. 2016. NODULESWITH ACTIVATED DEFENSE 1 is required for maintenance of rhizobial endosymbiosis in Medicago truncatula. New Phytol. 212:176–91 [Google Scholar]
  162. Wang D, Griffitts J, Starker C, Fedorova E, Limpens E. 162.  et al. 2010. A nodule-specific protein secretory pathway required for nitrogen-fixing symbiosis. Science 327:1126–29 [Google Scholar]
  163. Wang D, Yang S, Tang F, Zhu H. 163.  2012. Symbiosis specificity in the legume: rhizobial mutualism. Cell. Microbiol. 14:334–42 [Google Scholar]
  164. Wang W, Xie ZP, Staehelin C. 164.  2014. Functional analysis of chimeric lysin motif domain receptors mediating Nod factor-induced defense signaling in Arabidopsis thaliana and chitin-induced nodulation signaling in Lotus japonicus. Plant J. 78:56–69 [Google Scholar]
  165. Willmann R, Lajunen HM, Erbs G, Newman MA, Kolb D. 165.  et al. 2011. Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection. PNAS 108:19824–29 [Google Scholar]
  166. Xiang T, Zong N, Zou Y, Wu Y, Zhang J. 166.  et al. 2008. Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr. Biol. 18:74–80 [Google Scholar]
  167. Xin DW, Liao S, Xie ZP, Hann DR, Steinle L. 167.  et al. 2012. Functional analysis of NopM, a novel E3 ubiquitin ligase (NEL) domain effector of Rhizobium sp. strain NGR234. PLOS Pathog 8:e1002707 [Google Scholar]
  168. Xin XF, He SY. 168.  2013. Pseudomonas syringae pv. tomato DC3000: a model pathogen for probing disease susceptibility and hormone signaling in plants. Annu. Rev. Phytopathol 51:473–98 [Google Scholar]
  169. Yang S, Tang F, Gao M, Krishnan HB, Zhu H. 169.  2010. R gene-controlled host specificity in the legume-rhizobia symbiosis. PNAS 107:18735–40 [Google Scholar]
  170. Yasuda M, Miwa H, Masuda S, Takebayashi Y, Sakakibara H, Okazaki S. 170.  2016. Effector-triggered immunity determines host genotype-specific incompatibility in legume-Rhizobium symbiosis. Plant Cell Physiol 57:1791–800 [Google Scholar]
  171. Zhang B, Ramonell K, Somerville S, Stacey G. 171.  2002. Characterization of early, chitin-induced gene expression in Arabidopsis. Mol. Plant-Microbe Interact. 15:963–70 [Google Scholar]
  172. Zhang J, Li W, Xiang T, Liu Z, Laluk K. 172.  et al. 2010. Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe 7:290–301 [Google Scholar]
  173. Zhang J, Yin Z, White F. 173.  2015. TAL effectors and the executor R genes. Front. Plant Sci. 6:641 [Google Scholar]
  174. Zhang X, Dong W, Sun J, Feng F, Deng Y. 174.  et al. 2015. The receptor kinase CERK1 has dual functions in symbiosis and immunity signalling. Plant J 81:258–67 [Google Scholar]
  175. Zhang XC, Cannon SB, Stacey G. 175.  2009. Evolutionary genomics of LysM genes in land plants. BMC Evol. Biol. 9:183 [Google Scholar]
  176. Zhang XC, Wu X, Findley S, Wan J, Libault M. 176.  et al. 2007. Molecular evolution of lysin motif-type receptor-like kinases in plants. Plant Physiol 144:623–36 [Google Scholar]
  177. Zipfel C.177.  2014. Plant pattern-recognition receptors. Trends Immunol 35:345–51 [Google Scholar]
  178. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JD. 178.  et al. 2006. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749–60 [Google Scholar]
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