Building the interaction interfaces: Host responses upon infection with microorganisms

Current Opinion in Plant Biology

Volumn 23, Issue , 2015, Pages 132-139

  Yamazaki, Akihiro ^a   Hayashi, Makoto ^a  

^a Elements Chemistry Laboratory   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM; CELL CYCLE; CELL MEMBRANE; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT; PLANT IMMUNITY;

BACTERIA; CELL CYCLE; CELL MEMBRANE; HOST-PATHOGEN INTERACTIONS; PLANT IMMUNITY; PLANTS;

EID: 84925111222     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2014.12.003     Document Type: Review

References (75)

1. Oldroyd G.E., Murray J.D., Poole P.S., Downie J.A. The rules of engagement in the legume-rhizobial symbiosis. Annu Rev Genet 2011, 45:119-144.
2. Parniske M. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 2008, 6:763-775.
3. Yi M., Valent B. Communication between filamentous pathogens and plants at the biotrophic interface. Annu Rev Phytopathol 2013, 51:587-611.
4. Xin X.F., He S.Y. Pseudomonas syringae pv. tomato DC3000: a model pathogen for probing disease susceptibility and hormone signaling in plants. Annu Rev Phytopathol 2013, 51:473-498.
5. Glazebrook J. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 2005, 43:205-227.
6. Oldroyd G.E. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 2013, 11:252-263.
7. Koltai H. Strigolactones are regulators of root development. New Phytol 2011, 190:545-549.
8. Liang Y., Cao Y., Tanaka K., Thibivilliers S., Wan J., Choi J., Kang Ch., Qiu J., Stacey G. Nonlegumes respond to rhizobial Nod factors by suppressing the innate immune response. Science 2013, 341:1384-1387.
9. Palmer A.G., Senechal A.C., Mukherjee A., Ané J.M., Blackwell H.E. Plant responses to bacterial N-acyl l-homoserine lactones are dependent on enzymatic degradation to l-homoserine. ACS Chem Biol 2015, 9:1834-1845.
10. Schenk S.T., Hernández-Reyes C., Samans B., Stein E., Neumann C., Schikora M., Reichelt M., Mithöfer A., Becker A., Kogel K.H., Schikora A. N-acyl-homoserine lactone primes plants for cell wall reinforcement and induces resistance to bacterial pathogens via the salicylic acid/oxylipin pathway. Plant Cell 2014, 26:2708-2723.
11. Liu W., Zhou X., Li G., Li L., Kong L., Wang C., Zhang H., Xu J.R. Multiple plant surface signals are sensed by different mechanisms in the rice blast fungus for appressorium formation. PLoS Pathog 2011, 7:e1001261.
12. Gobbato E., Marsh J.F., Vernié T., Wang E., Maillet F., Kim J., Miller J.B., Sun J., Bano S.A., Ratet P., Mysore K.S., Dénarié J., Schultze M., Oldroyd G.E. A GRAS-type transcription factor with a specific function in mycorrhizal signaling. Curr Biol 2012, 22:2236-2241.
13. Wang E., Schornack S., Marsh J.F., Gobbato E., Schwessinger B., Eastmond P., Schultze M., Kamoun S., Oldroyd G.E. A common signaling process that promotes mycorrhizal and oomycete colonization of plants. Curr Biol 2012, 22:2242-2246.
14. Gobbato E., Wang E., Higgins G., Bano S.A., Henry C., Schultze M., Oldroyd G.E. RAM1 and RAM2 function and expression during arbuscular mycorrhizal symbiosis and Aphanomyces euteiches colonization. Plant Signal Behav 2013, 8:e26049.
15. Gilbert R.D., Johnson A.M., Dean R.A. Chemical signals responsible for appressorium formation in the rice blast fungus Magnaporthe grisea. Physiol Mol Plant Pathol 1996, 48:335-346.
16. Skamnioti P., Gurr S.J. Magnaporthe grisea cutinase2 mediates appressorium differentiation and host penetration and is required for full virulence. Plant Cell 2007, 19:2674-2689.
17. Lanver D., Berndt P., Tollot M., Naik V., Vranes M., Warmann T., Münch K., Rössel N., Kahmann R. Plant surface cues prime Ustilago maydis for biotrophic development. PLoS Pathog 2014, 10:e1004272.
18. Bogino P.C., Oliva M.de.L., Sorroche F.G., Giordano W. The role of bacterial biofilms and surface components in plant-bacterial associations. Int J Mol Sci 2013, 14:15838-15859.
19. Pérez-Giménez J., Mongiardini E.J., Althabegoiti M.J., Covelli J., Quelas J.I., López-García S.L., Lodeiro A.R. Soybean lectin enhances biofilm formation by Bradyrhizobium japonicum in the absence of plants. Int J Molbiol 2009, 2009:719367.
20. van Workum W.A.T., van Slageren S., van Brussel A.A.N., Kijne J.W. Role of exopolysaccharides of Rhizobium leguminosarum bv. viciae as host plant-specific molecules required for infection thread formation during nodulation of Vicia sativa. Mol Plant Microbe Interact 1998, 11:1233-1241.
21. Wang P., Zhong Z., Zhou J., Cai T., Zhu J. Exopolysaccharide biosynthesis is important for Mesorhizobium tianshanense: plant host interaction. Arch Microbiol 2008, 189:525-530.
22. Heindl J.E., Wang Y., Heckel B.C., Mohari B., Feirer N., Fuqua C. Mechanisms and regulation of surface interactions and biofilm formation in Agrobacterium. Front Plant Sci 2014, 5:176.
23. Bauer W.D., Mathesius U. Plant responses to bacterial quorum sensing signals. Curr Opin Plant Biol 2004, 7:429-433.
24. Muthamilarasan M., Prasad M. Plant innate immunity: an updated insight into defense mechanism. J Biosci 2013, 38:433-449.
25. Plett J.M., Kemppainen M., Kale S.D., Kohler A., Legué V., Brun A., Tyler B.M., Pardo A.G., Martin F. A secreted effector protein of Laccaria bicolor is required for symbiosis development. Curr Biol 2011, 21:1197-1203.
26. Plett J.M., Daguerre Y., Wittulsky S., Vayssières A., Deveau A., Melton S.J., Kohler A., Morrell-Falvey J.L., Brun A., Veneault-Fourrey C., Martin F. Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes. Proc Natl Acad Sci U S A 2014, 111:8229-8304.
27. Park C.H., Chen S., Shirsekar G., Zhou B., Khang C.H., Songkumarn P., Afzal A.J., Ning Y., Wang R., Bellizzi M., Valent B., Wang G.L. The Magnaporthe oryzae effector AvrPiz-t targets the RING E3 ubiquitin ligase APIP6 to suppress pathogen-associated molecular pattern-triggered immunity in rice. Plant Cell 2012, 24:4748-4762.
28. Mentlak T.A., Kombrink A., Shinya T., Ryder L.S., Otomo I., Saitoh H., Terauchi R., Nishizawa Y., Shibuya N., Thomma B.P., Talbot N.J. Effector-mediated suppression of chitin-triggered immunity by Magnaporthe oryzae is necessary for rice blast disease. Plant Cell 2012, 24:322-335.
29. de Jonge R., van Esse H.P., Kombrink A., Shinya T., Desaki Y., Bours R., van der Krol S., Shibuya N., Joosten M.H., Thomma B.P. Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 2010, 329:953-955.
30. Göhre V., Spallek T., Häweker H., Mersmann S., Mentzel T., Boller T., de Torres M., Mansfield J.W., Robatzek S. Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr Biol 2008, 18:1824-1832.
31. Xiang T., Zong N., Zou Y., Wu Y., Zhang J., Xing W., Li Y., Tang X., Zhu L., Chai J., Zhou J.M. Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr Biol 2008, 18:74-80.
32. Zhang J., Li W., Xiang T., Liu Z., Laluk K., Ding X., Zou Y., Gao M., Zhang X., Chen S., Mengiste T., Zhang Y., Zhou J.M. Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe 2010, 7:290-301.
33. Zhang J., Shao F., Li Y., Cui H., Chen L., Li H., Zou Y., Long C., Lan L., Chai J., Chen S., Tang X., Zhou J.M. A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe 2007, 1:175-185.
34. Wang Y., Li J., Hou S., Wang X., Li Y., Ren D., Chen S., Tang X., Zhou J.M. A Pseudomonas syringae ADP-ribosyltransferase inhibits Arabidopsis mitogen-activated protein kinase kinases. Plant Cell 2010, 22:2033-2044.
35. Tanaka K., Gilroy S., Jones A.M., Stacey G. Extracellular ATP signaling in plants. Trends Cell Biol 2010, 2:601-608.
36. Etzler M.E., Kalsi G., Ewing N.N., Roberts N.J., Day R.B., Murphy J.B. A nod factor binding lectin with apyrase activity from legume roots. Proc Natl Acad Sci U S A 1999, 96:5856-5861.
37. Roberts N.J., Morieri G., Kalsi G., Rose A., Stiller J., Edwards A., Xie F., Gresshoff P.M., Oldroyd G.E., Downie J.A., Etzler M.E. Rhizobial and mycorrhizal symbioses in Lotus japonicus require lectin nucleotide phosphohydrolase, which acts upstream of calcium signaling. Plant Physiol 2013, 161:556-567.
38. Day R.B., McAlvin C.B., Loh J.T., Denny R.L., Wood T.C., Young N.D., Stacey G. Differential expression of two soybean apyrases, one of which is an early nodulin. Mol Plant Microbe Interact 2000, 13:1053-1070.
39. Cannon S.B., McCombie W.R., Sato S., Tabata S., Denny R., Palmer L., Katari M., Young N.D., Stacey G. Evolution and microsynteny of the apyrase gene family in three legume genomes. Mol Genet Genomics 2003, 270:347-361.
40. Govindarajulu M., Kim S.Y., Libault M., Berg R.H., Tanaka K., Stacey G., Taylor C.G. GS52 ecto-apyrase plays a critical role during soybean nodulation. Plant Physiol 2009, 149:994-1004.
41. Tanaka K., Nguyen T.H., Stacey G. Enzymatic role for soybean ecto-apyrase in nodulation. Plant Signal Behav 2011, 6:1034-1036.
42. Genre A., Chabaud M., Timmers T., Bonfante P., Barker D.G. Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 2005, 17:3489-3499.
43. Genre A., Ivanov S., Fendrych M., Faccio A., Zársky V., Bisseling T., Bonfante P. Multiple exocytotic markers accumulate at the sites of perifungal membrane biogenesis in arbuscular mycorrhizas. Plant Cell 2012, 53:244-255.
44. Cárdenas L., Vidali L., Domnguez J., Prez H., Snchez F., Hepler P.K., Quinto C. Rearrangement of actin microfilaments in plant root hairs responding to Rhizobium etli nodulation signals. Plant Physiol 1998, 116:871-877.
45. Perrine-Walker F.M., Kouchi H., Ridge R.W. Endoplasmic reticulum-targeted GFP reveals ER remodeling in Mesorhizobium-treated Lotus japonicus root hairs during root hair curling and infection thread formation. Protoplasma 2014, 251:817-826.
46. Perrine-Walker F.M., Lartaud M., Kouchi H., Ridge R.W. Microtubule array formation during root hair infection thread initiation and elongation in the Mesorhizobium-Lotus symbiosis. Protoplasma 2014, 251:1099-1111.
47. Hoefle C., Huesmann C., Schultheiss H., Börnke F., Hensel G., Kumlehn J., Hückelhoven R. A barley ROP GTPase ACTIVATING PROTEIN associates with microtubules and regulates entry of the barley powdery mildew fungus into leaf epidermal cells. Plant Cell 2011, 23:2422-2439.
48. Hermanns M., Slusarenko A.J., Schlaich N.L. The early organelle migration response of Arabidopsis to Hyaloperonospora arabidopsidis is independent of RAR1, SGT1b, PAD4 and NPR1. Physiol Mol Plant Pathol 2008, 72:96-101.
49. Takemoto D., Jones D.A., Hardham A.R. GFP-tagging of cell components reveals the dynamics of subcellular re-organization in response to infection of Arabidopsis by oomycete pathogens. Plant J 2003, 33:775-792.
50. Croxen M.A., Law R.J., Scholz R., Keeney K.M., Wlodarska M., Finlay B.B. Recent advances in understanding enteric pathogenic Escherichia coli. Clin Microbiol Rev 2013, 26:822-880.
51. Parniske M. Intracellular accommodation of microbes by plants: a common developmental program for symbiosis and disease?. Curr Opin Plant Biol 2000, 3:320-328.
52. Ivanov S., Fedorova E.E., Limpens E., De Mita S., Genre A., Bonfante P., Bisseling T. Rhizobium-legume symbiosis shares an exocytotic pathway required for arbuscule formation. Proc Natl Acad Sci U S A 2012, 109:8316-8321.
53. Dörmann P., Kim H., Ott T., Schulze-Lefert P., Trujillo M., Wewer V., Hückelhoven R. Cell-autonomous defense, re-organization and trafficking of membranes in plant-microbe interactions. New Phytol 2015, 204:815-822.
54. Wang W., Zhang Y., Wen Y., Berkey R., Ma X., Pan Z., Bendigeri D., King H., Zhang Q., Xiao S. A comprehensive mutational analysis of the Arabidopsis resistance protein RPW8.2 reveals key amino acids for defense activation and protein targeting. Plant Cell 2013, 25:4242-4261.
55. Kim H., O'Connell R., Maekawa-Yoshikawa M., Uemura T., Neumann U., Schulze-Lefert P. The powdery mildew resistance protein RPW8.2 is carried on VAMP721/722 vesicles to the extrahaustorial membrane of haustorial complexes. Plant J 2014, 79:835-847.
56. Jones K.M., Kobayashi H., Davies B.W., Taga M.E., Walker G.C. How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nat Rev Microbiol 2007, 5:619-633.
57. Leborgne-Castel N., Adam T., Bouhidel K. Endocytosis in plant-microbe interactions. Protoplasma 2010, 247:177-193.
58. Rafiqi M., Gan P.H., Ravensdale M., Lawrence G.J., Ellis J.G., Jones D.A., Hardham A.R., Dodds P.N. Internalization of flax rust avirulence proteins into flax and tobacco cells can occur in the absence of the pathogen. Plant Cell 2010, 22:2017-2032.
59. Gan P.H., Rafiqi M., Ellis J.G., Jones D.A., Hardham A.R., Dodds P.N. Lipid binding activities of flax rust AvrM and AvrL567 effectors. Plant Signal Behav 2010, 5:1272-1275.
60. An Q., Hückelhoven R., Kogel K.H., van Bel A.J.E. Multivesicular bodies participate in a cell wall-associated defence response in barley leaves attacked by the pathogenic powdery mildew fungus. Cell Microbiol 2006, 8:1009-1019.
61. Tahiri-Alaoui A., Lingua G., Avrova A., Sampò S., Fusconi A., Antoniw J., Berta G. A cullin gene is induced in tomato roots forming arbuscular mycorrhizae. Can J Botany 2002, 80:607-616.
62. Fusconi A., Lingua G., Trotta A., Berta G. Effects of arbuscular mycorrhizal colonization and phosphorus application on nuclear ploidy in Allium porrum plants. Mycorrhiza 2005, 15:313-321.
63. Bainard L.D., Bainard J.D., Newmaster S.G., Klironomos J.N. Mycorrhizal symbiosis stimulates endoreduplication in angiosperms. Plant Cell Environ 2011, 34:1577-1585.
64. Suzaki T., Ito M., Yoro E., Sato S., Hirakawa H., Takeda N., Kawaguchi M. Endoreduplication-mediated initiation of symbiotic organ development in Lotus japonicus. Development 2014, 141:2441-2445.
65. Yoon H.J., Hossain M.S., Held M., Hou H., Kehl M., Tromas A., Sato S., Tabata S., Andersen S.U., Stougaard J., Ross L., Szczyglowski K. Lotus japonicus SUNERGOS1 encodes a predicted subunit A of a DNA topoisomerase VI that is required for nodule differentiation and accommodation of rhizobial infection. Plant J 2014, 78:811-821.
66. Chandran D., Inada N., Hather G., Kleindt C.K., Wildermuth M.C. Laser microdissection of Arabidopsis cells at the powdery mildew infection site reveals site-specific processes and regulators. Proc Natl Acad Sci U S A 2010, 107:460-465.
67. Chagnon P.L., Bradley R.L., Maherali H., Klironomos J.N. A trait-based framework to understand life history of mycorrhizal fungi. Trends Plant Sci 2013, 18:484-491.
68. Mangan S.A., Schnitzer S.A., Herre E.A., Mack K.M., Valencia M.C., Sanchez E.I., Bever J.D. Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest. Nature 2010, 566:752-755.
69. Bever J.D. Negative feedback within a mutualism: host-specific growth of mycorrhizal fungi reduces plant benefit. Proc Biol Sci 2002, 269:2595-2601.
70. Wenke K., Kai M., Piechulla B. Belowground volatiles facilitate interactions between plant roots and soil organisms. Planta 2010, 231:499-506.
71. Kost B., Mathur J., Chua N.H. Cytoskeleton in plant development. Curr Opin Plant Biol 1999, 2:462-470.
72. Lu Y.J., Schornack S., Spallek T., Geldner N., Chory J., Schellmann S., Karin S., Kamoun S., Robatzek S. Patterns of plant subcellular responses to successful oomycete infections reveal differences in host cell reprogramming and endocytic trafficking. Cell Microbiol 2012, 14:682-697.
73. Qin Y., Yang Z. Rapid tip growth: insights from pollen tubes. Semin Cell Dev Biol 2011, 22:816-824.
74. Wildermuth M.C. Modulation of host nuclear ploidy: a common plant biotroph mechanism. Curr Opin Plant Biol 2010, 13:449-458.
75. Inzé D., De Veylder L. Cell cycle regulation in plant development. Annu Rev Genet 2006, 40:77-105.