Cytokinin Production by the Rice Blast Fungus Is a Pivotal Requirement for Full Virulence

PLoS Pathogens

Volumn 12, Issue 2, 2016, Pages

  Chanclud, Emilie ^a   Kisiala, Anna ^b,c   Emery, Neil R J ^b   Chalvon, Véronique ^a   Ducasse, Aurélie ^a   Romiti Michel, Corinne ^a   Gravot, Antoine ^d   Kroj, Thomas ^a   Morel, Jean Benoit ^a  

^a CIRAD   (France)

^b TRENT UNIVERSITY   (Canada)

^c UNIVERSITY OF TECHNOLOGY AND LIFE SCIENCES   (Poland)

^d Universite Rennes 1   (France)

Author keywords

[No Author keywords available]

Indexed keywords

6 N (3,3 DIMETHYLALLYL)ADENOSINE; CIS ZEATIN NUCLEOTIDE; CYTOKININ; DIPHENYLIODONIUM SALT; ISOPENTENYLADENINE; ISOPENTENYLADENINE NUCLEOTIDE; ISOPRENOID; REACTIVE OXYGEN METABOLITE; TRANSFER RNA; TRANSFER RNA ISOPENTENYL TRANSFERASE; UNCLASSIFIED DRUG;

AGAR GEL ELECTROPHORESIS; ARTICLE; CKS1 GENE; ELECTROSPRAY MASS SPECTROMETRY; ENVIRONMENTAL STRESS; GENE; GENE DISRUPTION; GENE EXPRESSION; GENE OSRR1; GENE OSRR6; GENE SEQUENCE; GENETIC COMPLEMENTATION; LIQUID CHROMATOGRAPHY; MAGNAPORTHE ORYZAE; NONHUMAN; PLANT GROWTH; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA DEGRADATION; VIRULENCE; BIOSYNTHESIS; FUNGAL GENE; GENE EXPRESSION REGULATION; GENETICS; MAGNAPORTHE; MICROBIOLOGY; ORYZA; PLANT DISEASE; PLANT LEAF;

CYTOKININS; GENE EXPRESSION REGULATION, PLANT; GENES, FUNGAL; MAGNAPORTHE; ORYZA; PLANT DISEASES; PLANT LEAVES; VIRULENCE;

EID: 84959527884     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005457     Document Type: Article

References (100)

1. Kamoun S., (2007) Groovy times: filamentous pathogen effectors revealed. Curr. Opin. Plant Biol. 10, 358–36517611143
2. Macho A.P., Zipfel C., (2015) Targeting of plant pattern recognition receptor- triggered immunity by bacterial type-III secretion system effectors. Curr. Opin. Microbiol. 23, 14–22doi: 10.1016/j.mib.2014.10.00925461568
3. Verdier V., et al. (2012) Transcription activator-like (TAL) effectors targeting OsSWEET genes enhance virulence on diverse rice (Oryza sativa) varieties when expressed individually in a TAL effector-deficient strain of Xanthomonas oryzae. New Phytol. 196, 1197–1207doi: 10.1111/j.1469-8137.2012.04367.x23078195
4. Hogenhout S.A., et al. (2009) Emerging Concepts in Effector Biology of Plant-Associated Organisms. Mol. Plant-Microbe Interact. 22, 115–122doi: 10.1094/MPMI-22-2-011519132864
5. Zipfel C., (2009) Early molecular events in PAMP-triggered immunity. Curr. Opin. Plant Biol. 12, 414–20doi: 10.1016/j.pbi.2009.06.00319608450
6. Mentlak T., et al. (2012) Effector-mediated suppression of chitin-triggered immunity by Magnaporthe oryzae is necessary for rice blast disease. Plant Cell24, 322–35doi: 10.1105/tpc.111.09295722267486
7. Pitzschke A., et al. (2009) MAPK cascade signalling networks in plant defence. Curr. Opin. Plant Biol. 12, 421–426doi: 10.1016/j.pbi.2009.06.00819608449
8. Robert-Seilaniantz A., et al. (2007) Pathological hormone imbalances. Curr. Opin. Plant Biol. 10, 372–917646123
9. Chen Z., et al. (2007) Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology. Proc. Natl. Acad. Sci. U. S. A. 104, 20131–2013618056646
10. Thatcher L.F., et al. (2009) Fusarium oxysporum hijacks COI1-mediated jasmonate signaling to promote disease development in Arabidopsis. Plant J. 58, 927–939doi: 10.1111/j.1365-313X.2009.03831.x19220788
11. Verhage A., et al. (2010) Plant immunity: it’s the hormones talking, but what do they say?Plant Physiol. 154, 536–40doi: 10.1104/pp.110.16157020921180
12. Djamei A., et al. (2011) Metabolic priming by a secreted fungal effector. Nature478, 395–8doi: 10.1038/nature1045421976020
13. Patkar R.N., et al. (2015) A fungal monooxygenase-derived jasmonate attenuates host innate immunity. Nat. Chem. Biol. doi: 10.1038/nchembio.1885
14. Melotto M., et al. (2008) Role of stomata in plant innate immunity and foliar bacterial diseases. Annu. Rev. Phytopathol. 46, 101–122doi: 10.1146/annurev.phyto.121107.10495918422426
15. Uppalapati S.R., et al. (2007) The phytotoxin coronatine contributes to pathogen fitness and is required for suppression of salicylic acid accumulation in tomato inoculated with Pseudomonas syringae pv. tomato DC3000. Mol. Plant. Microbe. Interact. 20, 955–96517722699
16. Greene E.M., (1980) Cytokinin production by microorganismes. Bot. Rev. 46, 25–74
17. Gruen H.E., (1959) Auxins and Fungi. Annu. Rev. Plant Physiol. 10, 405–440
18. Hedden P., et al. (2001) Gibberellin Biosynthesis in Plants and Fungi: A Case of Convergent Evolution?J. Plant Growth Regul. 20, 319–33111986758
19. Kisiala A., et al. (2013) Bioactive cytokinins are selectively secreted by Sinorhizobium meliloti nodulating and nonnodulating strains. Mol. Plant. Microbe. Interact. 26, 1225–31doi: 10.1094/MPMI-02-13-0054-R24001254
20. Özcan B., Topçuoglu S.F., (2001) GA 3, ABA and Cytokinin Production by Lentinus tigrinus and Laetiporus sulphureus Fungi Cultured in the Medium of Olive Oil Mill Waste *. Turk J Biol25, 453–462
21. Strzelczyk E., et al. (1994) Cytokinin-like substances and ethylene production by Azospirillum in media with different carbon sources. Microbiol. Res. 149, 55–60
22. Strzelczyk E., Pokojska-Burdziej A., (1984) Production of auxins and gibberellin-like substances by mycorrhyzal fungi, bacteria and actinomycetes isolated from soil and the mycorrhizosphere. Plant Soil81, 185–194
23. Dihanich M.E., et al. (1987) Isolation and characterization of MOD5, a gene required for isopentenylation of cytoplasmic and mitochondrial tRNAs of Saccharomyces cerevisiae. Mol. Cell. Biol. 7, 177–1843031456
24. Golovko A., et al. (2002) Identification of a tRNA isopentenyltransferase gene from Arabidopsis thaliana. Plant Mol. Biol. 49, 161–16911999372
25. Miyawaki K., et al. (2006) Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. Proc. Natl. Acad. Sci.
26. Riou-Khamlichi C., et al. (1999) Cytokinin Activation of Arabidopsis Cell Division Through a D-Type Cyclin. Science (80-.). 283, 1541–1545
27. Carimi F., et al. (2003) Cytokinins: new apoptotic inducers in plants. Planta216, 413–42112520332
28. Fosket D.E., Torrey J.G., (1969) Hormonal control of cell proliferation and xylem differentiation in cultured tissues of Glycine max var. Biloxi. Plant Physiol. 44, 871–8805816361
29. Peleg Z., et al. (2011) Cytokinin-mediated source/sink modifications improve drought tolerance and increase grain yield in rice under water-stress. Plant Biotechnol. J. 9, 747–758doi: 10.1111/j.1467-7652.2010.00584.x21284800
30. Vescovi M., et al. (2012) Programmed cell death induced by high levels of cytokinin in Arabidopsis cultured cells is mediated by the cytokinin receptor CRE1/AHK4. J. Exp. Bot. 63, 2825–2832doi: 10.1093/jxb/ers00822312114
31. Morrison E.N., et al. (2015) Phytohormone Involvement in the Ustilago maydis–Zea mays Pathosystem: Relationships between Abscisic Acid and Cytokinin Levels and Strain Virulence in Infected Cob Tissue. PLoS One10, e0130945doi: 10.1371/journal.pone.013094526107181
32. Hinsch J., et al. (2015) De novo biosynthesis of cytokinins in the biotrophic fungus Claviceps purpurea. Environ. Microbiol. 17, 2935–2951doi: 10.1111/1462-2920.1283825753486
33. Devos S., et al. (2006) A hormone and proteome approach to picturing the initial metabolic events during Plasmodiophora brassicae infection on Arabidopsis. Mol. Plant. Microbe. Interact. 19, 1431–144317153927
34. Pertry I., et al. (2009) Identification of Rhodococcus fascians cytokinins and their modus operandi to reshape the plant. Proc. Natl. Acad. Sci. U. S. A. 106, 929–34doi: 10.1073/pnas.081168310619129491
35. Wingler A., et al. (1998) Regulation of Leaf Senescence by Cytokinin, Sugars, and Light. Plant Physiol. 116, 329–335
36. Walters D.R., McRoberts N., (2006) Plants and biotrophs: a pivotal role for cytokinins?Trends Plant Sci. 11, 581–58617092762
37. Angra-Sharma R., Sharma D.K., (1999) Cytokinins in pathogenesis and disease resistance of Pyrenophora teres-barley and Dreschslera maydis-maize interactions during early stages of infection. Mycopathologia148, 87–9511189749
38. Behr M., et al. (2012) Remodeling of cytokinin metabolism at infection sites of Colletotrichum graminicola on maize leaves. Mol. Plant. Microbe. Interact. 25, 1073–82doi: 10.1094/MPMI-01-12-0012-R22746825
39. Angra R., Mandahar C.L., (1991) Pathogenesis of barley leaves by Helminthosporium teres I: Green island formation and the possible involvement of cytokinins. Mycopathologia114, 21–27
40. Morrison E.N., et al. (2015) Detection of phytohormones in temperate forest fungi predicts consistent abscisic acid production and a common pathway for cytokinin biosynthesis. Mycologia107, 245–257doi: 10.3852/14-15725572099
41. Murphy A.M., et al. (1997) Comparison of cytokinin production in vitro by Pyrenopeziza brassicae with other plant pathogens. Physiol. Mol. Plant Pathol. 50, 53–65
42. Hu G.G., Rijkenberg E.H.J., (1998) Ultrastructural localization of cytokinins in Puccinia recondita f.sp. tritici-infected wheat leaves. Physiol. Mol. Plant Pathol. 52, 79–94
43. Jiang C.-J., et al. (2013) Cytokinins act synergistically with salicylic acid to activate defense gene expression in rice. Mol. Plant. Microbe. Interact. 26, 287–96doi: 10.1094/MPMI-06-12-0152-R23234404
44. Sakakibara H., (2006) Cytokinins: activity, biosynthesis, and translocation. Annu. Rev. Plant Biol. 57, 431–4916669769
45. Armstrong D.J., et al. (1969) Cytokinins: distribution in species of yeast transfer RNA. Biochemistry63, 504–511
46. Zhang Y., (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics9, 40doi: 10.1186/1471-2105-9-4018215316
47. Golovko A., (2000) Cloning of a human tRNA isopentenyl transferase. Gene258, 85–9311111046
48. Pai D.A., Correction for Pratt-Hyattet al. (2014) et al., Mod5 protein binds to tRNA gene complexes and affects local transcriptional silencing. Proc. Natl. Acad. Sci. 111, 2397–2397
49. Suzuki G., et al. (2012) A yeast prion, Mod5, promotes acquired drug resistance and cell survival under environmental stress. Science336, 355–9doi: 10.1126/science.121949122517861
50. Farrow S.C., Emery R.J.N., (2012) Concurrent profiling of indole-3-acetic acid, abscisic acid, and cytokinins and structurally related purines by high-performance-liquid- chromatography tandem electrospray mass spectrometry Concurrent profiling of indole-3-acetic acid, abscisic acid,. Plant Methods8, 42doi: 10.1186/1746-4811-8-4223061971
51. Brandstatter I., Kieber J.J., (1998) Two Genes with Similarity to Bacterial Response Regulators Are Rapidly and Specifically Induced by Cytokinin in Arabidopsis. Plant Cell10, 1009–10199634588
52. Jain M., et al. (2006) Molecular characterization and differential expression of cytokinin-responsive type-A response regulators in rice (Oryza sativa). BMC Plant Biol. 6, 116472405
53. Pareek A., et al. (2006) Whole-genome analysis of Oryza sativa reveals similar architecture of two-component signaling machinery with Arabidopsis. Plant Physiol. 142, 380–9716891544
54. Chi M.-H., et al. (2009) A novel pathogenicity gene is required in the rice blast fungus to suppress the basal defenses of the host. PLoS Pathog. 5, e1000401doi: 10.1371/journal.ppat.100040119390617
55. Desikan R., et al. (1996) Generation of active oxygen in elicited cells of Arabidopsis thaliana is mediated by a N A D P H oxidase-like enzyme. FEBS Lett. 382, 213–2178612756
56. Nakashita H., et al. (2001) Characterization of PBZ1, a probenazole-inducible gene, in suspension-cultured rice cells. Biosci. Biotechnol. Biochem. 65, 205–20811272832
57. Delteil A., et al. (2012) Building a mutant resource for the study of disease resistance in rice reveals the pivotal role of several genes involved in defence. Mol. Plant Pathol. 13, 72–82doi: 10.1111/j.1364-3703.2011.00731.x21726398
58. Kaku H., et al. (2006) Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc. Natl. Acad. Sci. 103, 11086–1109116829581
59. Kishimoto K., et al. (2010) Perception of the chitin oligosaccharides contributes to disease resistance to blast fungus Magnaporthe oryzae in rice. Plant J. 64, 343–54doi: 10.1111/j.1365-313X.2010.04328.x21070413
60. Otani Y., (1959) Studies on the relation between the principal components of the rice plant and its susceptibility to the blast disease. Annu. Phytopathol. Soc. Japan16, 97–102
61. Ballini E., et al. (2013) Diversity and genetics of nitrogen-induced susceptibility to the blast fungus in rice and wheat. Rice6, 32doi: 10.1186/1939-8433-6-3224280346
62. Parker D., et al. (2009) Metabolomic analysis reveals a common pattern of metabolic re-programming during invasion of three host plant species by Magnaporthe grisea. Plant J. 59, 723–37doi: 10.1111/j.1365-313X.2009.03912.x19453445
63. Kocal N., et al. (2008) Cell wall-bound invertase limits sucrose export and is involved in symptom development and inhibition of photosynthesis during compatible interaction between tomato and Xanthomonas campestris pv vesicatoria. Plant Physiol. 148, 1523–1536doi: 10.1104/pp.108.12797718784281
64. Rivero R.M., et al. (2009) Cytokinin-dependent photorespiration and the protection of photosynthesis during water deficit. Plant Physiol. 150, 1530–40doi: 10.1104/pp.109.13937819411371
65. Persson B.C., et al. (1994) Synthesis and function of isopentenyl adenosine derivatives in tRNA. Biochimie76, 1152–11607748950
66. Vizarova G., (1975) Contribution to the Study of Cytokinin Production by Phytopathogenic Fungi. Biol. Plant. 17, 380–382
67. Ng P.P., et al. (1982) Cytokinin production by ectomycorrhizal fungi. New Phytol. 91, 57–62
68. Laten H.M., Zahareas-doktor S., (1985) Presence and source of free isopentenyladenosine in yeasts. Proc. Natl. Acad. Sci. U. S. A. 82, 1113–11153883351
69. Tsai Y.-C., et al. (2012) Characterization of genes involved in cytokinin signaling and metabolism from rice. Plant Physiol. 158, 1666–84doi: 10.1104/pp.111.19276522383541
70. Chang C., Stewart R.C., (1998) The two-component system. Regulation of diverse signaling pathways in prokaryotes and eukaryotes. Plant Physiol. 117, 723–7319662515
71. Lohrmann J., Harter K., (2002) Plant two-component signaling systems and the role of response regulators. Plant Physiol. 128, 363–36911842140
72. Saito H., et al. (2001) Histidine Phosphorylation and Two-Component Signaling in Eukaryotic Cells. Chem. Rev. 101, 2497–250911749385
73. Stock A.M., et al. (2000) Two-Component Signal Transduction. Annu. Rev. Biochem. 69, 183–21510966457
74. Alex L.A., et al. (1996) Hyphal development in Neurospora crassa: Involvement of a two-component histidine kinase. Proc. Natl. Acad. Sci. U. S. A. 93, 3416–34218622950
75. Motoyama T., et al. (2008) Involvement of putative response regulator genes of the rice blast fungus Magnaporthe oryzae in osmotic stress response, fungicide action, and pathogenicity. Curr. Genet. 54, 185–195doi: 10.1007/s00294-008-0211-018726099
76. Zhang H., et al. (2010) A two-component histidine kinase, MoSLN1, is required for cell wall integrity and pathogenicity of the rice blast fungus, Magnaporthe oryzae. Curr. Genet. 56, 517–528doi: 10.1007/s00294-010-0319-x20848286
77. Li G., et al. (2012) Genetic control of infection-related development in Magnaporthe oryzae. Curr. Opin. Microbiol. 15, 678–84doi: 10.1016/j.mib.2012.09.00423085322
78. Dong Y., et al. (2015) Global Genome and Transcriptome Analyses of Magnaporthe oryzae Epidemic Isolate 98–06 Uncover Novel Effectors and Pathogenicity-Related Genes, Revealing Gene Gain and Lose Dynamics in Genome Evolution. PLOS Pathog. 11, e1004801doi: 10.1371/journal.ppat.100480125837042
79. Morkunas I., Ratajczak L., (2014) The role of sugar signaling in plant defense responses against fungal pathogens. Acta Physiol. Plant. 36, 1607–1619
80. Bolton M.D., (2009) Primary metabolism and plant defense—fuel for the fire. Mol. Plant. Microbe. Interact. 22, 487–497doi: 10.1094/MPMI-22-5-048719348567
81. Sakakibara H., et al. (2006) Interactions between nitrogen and cytokinin in the regulation of metabolism and development. Trends Plant Sci. 11, 440–816899391
82. LeJohn H.B., Stevenson R.M., (1973) Cytokinins and magnesium ions may control the flow of metabolites and calcium ions through fungal cell membranes. Biochim. Biophys. Res. Commun. 54, 1061–1066
83. Durner J., et al. (1997) Salicylic acid and disease resistance in plants. Trends Plant Sci. 2, 266–274
84. León J., Lawton M.A., (1995) Hydrogen Peroxide Stimulates Salicylic Acid Biosynthesis in Tobacco ‘. Plant Physiol. 108, 1673–167812228572
85. Pogány M., et al. (2004) Juvenility of tobacco induced by cytokinin gene introduction decreases susceptibility to Tobacco necrosis virus and confers tolerance to oxidative stress. Physiol. Mol. Plant Pathol. 65, 39–47
86. Akagi A., et al. (2014) WRKY45-dependent priming of diterpenoid phytoalexin biosynthesis in rice and the role of cytokinin in triggering the reaction. Plant Mol. Biol. 86, 171–83doi: 10.1007/s11103-014-0221-x25033935
87. Cheng H., et al. (2015) The WRKY45-2—WRKY13—WRKY42 Transcriptional Regulatory Cascade Is Required for Rice Resistance to Fungal Pathogen. Plant Physiol. 167, 1087–1099doi: 10.1104/pp.114.25601625624395
88. Choi J., et al. (2011) Cytokinins and plant immunity: old foes or new friends?Trends Plant Sci. 16, 388–94doi: 10.1016/j.tplants.2011.03.00321470894
89. Giron D., et al. (2013) Cytokinins as key regulators in plant-microbe-insect interactions: connecting plant growth and defence. Funct. Ecol. 27, 599–609
90. Drüge U., Schonbeck F., (1993) Effect of vesicular-arbuscular mycorrhizal infection on transpiration, photosynthesis and growth of flax (Linum usitatissimum L.) in relation to cytokinin levels. J. Plant Physiol. 141, 40–48
91. Frugier F., et al. (2008) Cytokinin: secret agent of symbiosis. Trends Plant Sci. 13, 115–20doi: 10.1016/j.tplants.2008.01.00318296104
92. Ribot C., et al. (2013) The Magnaporthe oryzae effector AVR1-CO39 is translocated into rice cells independently of a fungal-derived machinery. Plant J. 74, 1–12doi: 10.1111/tpj.1209923279638
93. Böhnert H., et al. (2004) A Putative Polyketide Synthase / Peptide Synthetase from Magnaporthe grisea Signals Pathogen Attack to Resistant Rice. Plant Cell16, 2499–251315319478
94. Kämper J., (2004) A PCR-based system for highly efficient generation of gene replacement mutants in Ustilago maydis. Mol. Genet. Genomics271, 103–1014673645
95. Ou, S.H. (1985) Rice Diseases.
96. Berruyer R., et al. (2003) Identification and fine mapping of Pi33, the rice resistance gene corresponding to the Magnaporthe grisea avirulence gene ACE1. Theor. Appl. Genet. 107, 1139–4712838393
97. Faivre-rampant O., et al. (2008) Characterization of the model system rice—Magnaporthe for the study of nonhost resistance in cereals. New Phytol. 180, 899–910doi: 10.1111/j.1469-8137.2008.02621.x19138233
98. Gravot A., et al. (2010) Diurnal oscillations of metabolite abundances and gene analysis provide new insights into central metabolic processes of the brown alga Ectocarpus siliculosus. New Phytol. 188, 98–11020862781
99. Zhou C., Huang R.H., (2008) Crystallographic snapshots of eukaryotic dimethylallyltransferase acting on tRNA: insight into tRNA recognition and reaction mechanism. Proc. Natl. Acad. Sci. U. S. A. 105, 16142–16147doi: 10.1073/pnas.080568010518852462
100. Dereeper a., et al. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36, 465–469