A secreted Ustilago maydis effector promotes virulence by targeting anthocyanin biosynthesis in maize

eLife

Volumn 2014, Issue 3, 2014, Pages

  Tanaka, Shigeyuki ^a   Brefort, Thomas ^a,d   Neidig, Nina ^a   Djamei, Armin ^a,e   Kahnt, Jörg ^a   Vermerris, Wilfred ^b   Koenig, Stefanie ^c   Feussner, Kirstin ^c   Feussner, Ivo ^c   Kahmann, Regine ^a  

^a MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^b UNIVERSITY OF FLORIDA   (United States)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

^d The Comprehensive Biomarker Center GmbH   (Germany)

^e GREGOR MENDEL INSTITUTE OF MOLECULAR PLANT BIOLOGY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHOCYANIN; FLAVONOID; GLUCOSIDE; PROTEIN; PROTEIN KINASE ZMTTK1; PROTEIN TIN 2; UNCLASSIFIED DRUG;

ARTICLE; BIOINFORMATICS; BIOLOGICAL ACTIVITY; BIOSYNTHESIS; CROP; EXTRACTION; FUNGAL BIOMASS; FUNGAL VIRULENCE; GENE MUTATION; GENOTYPE ENVIRONMENT INTERACTION; INFECTION; MAIZE; MICROARRAY ANALYSIS; MICROSCOPY; NONHUMAN; PHENOTYPE; PLASMID; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; QUANTITATIVE ASSAY; REAL TIME POLYMERASE CHAIN REACTION; USTILAGO MAYDIS;

EID: 84898766977     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.01355.001     Document Type: Article

References (73)

1. Ahmad S, Veyrat N, Gordon-Weeks R, Zhang Y, Martin J, Smart L, Glauser G, Erb M, Flors V, Frey M, Ton J. 2011. Benzoxazinoid metabolites regulate innate immunity against aphids and fungi in maize. Plant Physiology 157:317-327. doi: 10.1104/pp.111.180224.
2. Banuett F, Herskowitz I. 1996. Discrete developmental stages during teliospore formation in the corn smut fungus, Ustilago maydis. Development 122:2965-2976.
3. Barbieri M, Marcel TC, Niks RE. 2011. Host status of false brome grass to the leaf rust fungus Puccinia brachypodii and the stripe rust fungus P. striiformis. Plant Disease 95:1339-1345. doi: 10.1094/PDIS-11-10-0825.
4. Basse CW. 2005. Dissecting defense-related and developmental transcriptional responses of maize during Ustilago maydis infection and subsequent tumor formation. Plant Physiology 138:1774-1784. doi: 10.1104/pp.105.061200.
5. Beggs C, Wellman E. 1985. Analysis of light-controlled anthocyanin formation in coleoptiles of Zea mays L.: The role of UV-B, blue, red and far-red light. Photochemistry and Photobiology 41:481-486. doi: 10.1111/j.1751-1097.1985.tb03515.x.
6. Berndt P, Lanver D, Kahmann R. 2010. The AGC Ser/Thr kinase Aga1 is essential for appressorium formation and maintenance of the actin cytoskeleton in the smut fungus Ustilago maydis. Molecular Microbiology 78:1484-1499. doi: 10.1111/j.1365-2958.2010.07422.x.
7. Besseau S, Hoffmann L, Geoffroy P, Lapierre C, Pollet B, Legrand M. 2007. Flavonoid accumulation in Arabidopsis repressed in lignin synthesis affects auxin transport and plant growth. Plant Cell 19:148-162. doi: 10.1105/tpc.106.044495.
8. Bhargava A, Mansfield SD, Hall HC, Douglas CJ, Ellis BE. 2010. MYB75 functions in regulation of secondary cell wall formation in the Arabidopsis inflorescence stem. Plant Physiology 154:1428-1438. doi: 10.1104/pp.110.162735.
9. Brefort T, Tanaka S, Neidig N, Doehlemann G, Vincon V, Kahmann R. Characterization of the largest effector gene cluster of Ustilago maydis. PLOS Pathogens (in press).
10. Chabbert B, Tollier MT, Monties B. 1994. Biological variability in lignification of maize: expression of the brown midrib bm3 mutation in three maize cultivars. Journal of the Science of Food and Agriculture 64:349-355. doi: 10.1002/jsfa.2740640317.
11. Chen F, Dixon RA. 2007. Lignin modification improves fermentable sugar yields for biofuel production. Nature Biotechnology 25:759-761. doi: 10.1038/nbt1316.
12. Chen W, VanOpdorp N, Fitzl D, Tewari J, Friedemann P, Greene T, Thompson S, Kumpatla S, Zheng P. 2012. Transposon insertion in a cinnamyl alcohol dehydrogenase gene is responsible for a brown midrib1 mutation in maize. Plant Molecular Biology 80:289-297. doi: 10.1007/s11103-012-9948-4.
13. Djamei A, Schipper K, Rabe F, Ghosh A, Vincon V, Kahnt J, Osorio S, Tohge T, Fernie AR, Feussner I, Feussner K, Meinicke P, Stierhof YD, Schwarz H, Macek B, Mann M, Kahmann R. 2011. Metabolic priming by a secreted fungal effector. Nature 478:395-398. doi: 10.1038/nature10454.
14. Djamei A, Kahmann R. 2012. Ustilago maydis: dissecting the molecular interface between pathogen and plant. PLOS Pathogens 8:e1002955. doi: 10.1371/journal.ppat.1002955.
15. Doehlemann G, Wahl R, Horst RJ, Voll LM, Usadel B, Poree F, Stitt M, Pons-Kühnemann J, Sonnewald U, Kahmann R, Kämper J. 2008. Reprogramming a maize plant: transcriptional and metabolic changes induced by the fungal biotroph Ustilago maydis. Plant Journal 56:181-195. doi: 10.1111/j.1365-313X.2008.03590.x.
16. Doehlemann G, van der Linde K, Assmann D, Schwammbach D, Hof A, Mohanty A, Jackson D, Kahmann R. 2009. Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells. PLOS Pathogens 5:e1000290. doi: 10.1371/journal.ppat.1000290.
17. Dooner HK, Robbins TP, Jorgensen RA. 1991. Genetic and developmental control of anthocyanin biosynthesis. Annual Review of Genetics 25:173-199. doi: 10.1146/annurev.ge.25.120191.001133.
18. Dornan D, Shimizu H, Burch L, Smith AJ, Hupp TR. 2003. The proline repeat domain of p53 binds directly to the transcriptional coactivator p300 and allosterically controls DNA-dependent acetylation of p53. Molecular and Cellular Biology 23:8846-8861. doi: 10.1128/MCB.23.23.8846-8861.2003.
19. Eaton CJ, Cox MP, Ambrose B, Becker M, Hesse U, Schardl CL, Scott B. 2010. Disruption of signaling in a fungal-grass symbiosis leads to pathogenesis. Plant Physiology 153:1780-1794. doi: 10.1104/pp.110.158451.
20. Farfsing JD. 2004. Regulation des Mais-induzierten mig2-Genclusters in Ustilago maydis. Ph.D. thesis, Philipps-Universität Marburg.
21. Fornalé S, Shi X, Chai C, Encina A, Irar S, Capellades M, Fuguet E, Torres JL, Rovira P, Puigdomènech P, Rigau J, Grotewold E, Gray J, Caparrós-Ruiz D. 2010. ZmMYB31 directly represses maize lignin genes and redirects the phenylpropanoid metabolic flux. Plant Journal 64:633-644. doi: 10.1111/j.1365-313X.2010.04363.x.
22. Fossen T, Slimestad R, Andersen OM. 2001. Anthocyanins from maize (Zea mays) and reed canarygrass (Phalaris arundinacea). Journal of Agricultural and Food Chemistry 49:2318-2321. doi: 10.1021/jf001399d.
23. Funnell-Harris DL, Pedersen JF, Sattler SE. 2010. Alteration in lignin biosynthesis restricts growth of Fusarium spp. in brown midrib sorghum. Phytopathology 100:671-681. doi: 10.1094/PHYTO-100-7-0671.
24. Glenn AE, Gold SE, Bacon CW. 2002. Fdb1 and Fdb2, Fusarium verticillioides loci necessary for detoxification of preformed antimicrobials from corn. Molecular Plant-Microbe Interactions 15:91-101. doi: 10.1094/MPMI.2002.15.2.91.
25. Goodman CD, Casati P, Walbot V. 2004. A multidrug resistance-associated protein involved in anthocyanin transport in Zea mays. Plant Cell 16:1812-1826. doi: 10.1105/tpc.022574.
26. Grabber JH, Ralph J, Hatfield RD. 2002. Model studies of ferulate-coniferyl alcohol cross-product formation in primary maize walls: implications for lignification in grasses. Journal of Agricultural and Food Chemistry 50:6008-6016. doi: 10.1021/jf0205312.
27. Guillaumie S, Pichon M, Martinant JP, Bosio M, Goffner D, Barrière Y. 2007. Differential expression of phenylpropanoid and related genes in brown-midrib bm1, bm2, bm3, and bm4 young near-isogenic maize plants. Planta 226:235-250. doi: 10.1007/s00425-006-0468-9.
28. Halpin C, Holt K, Chojecki J, Oliver D, Chabbert B, Monties B, Edwards K, Barakate A, Foxon GA. 1998. Brown-midrib maize (bm1)-a mutation affecting the cinnamyl alcohol dehydrogenase gene. Plant Journal 14:545-553. doi: 10.1046/j.1365-313X.1998.00153.x.
29. Hammerschmidt R, Nicholson RL. 1977. Resistance of maize to anthracnose: Effect of light intensity on lesion development. Phytopathology 67:247-250. doi: 10.1094/Phyto-67-247.
30. Hemetsberger C, Herrberger C, Zechmann B, Hillmer M, Doehlemann G. 2012. The Ustilago maydis effector Pep1 suppresses plant immunity by inhibition of host peroxidase activity. PLOS Pathogens 8:e1002684. doi: 10.1371/journal.ppat.1002684.
31. Hipskind J, Wood K, Nicholson RL. 1996. Localized stimulation of anthocyanin accumulation and delineation of pathogen ingress in maize genetically resistant to Bipolaris maydis race O. Physiological and Molecular Plant Pathology 49:247-256. doi: 10.1006/pmpp.1996.0052.
32. Hirota A, Kato T, Fukaki H, Aida M, Tasaka M. 2007. The auxin-regulated AP2/EREBP gene PUCHI is required for morphogenesis in the early lateral root primordium of Arabidopsis. Plant Cell 19:2156-2168. doi: 10.1105/tpc.107.050674.
33. Holton TA, Cornish EC. 1995. Genetics and biochemistry of anthocyanin biosynthesis. Plant Cell 7:1071-1083. doi: 10.1105/tpc.7.7.1071.
34. Horst RJ, Doehlemann G, Wahl R, Hofmann J, Schmiedl A, Kahmann R, Kämper J, Sonnewald U, Voll LM. 2010. Ustilago maydis infection strongly alters organic nitrogen allocation in maize and stimulates productivity of systemic source leaves. Plant Physiology 152:293-308. doi: 10.1104/pp.109.147702.
35. Humphreys JM, Chapple C. 2002. Rewriting the lignin roadmap. Current Opinion in Plant Biology 5:224-229. doi: 10.1016/S1369-5266(02)00257-1.
36. Kämper J, Kahmann R, Bölker M, Ma LJ, Brefort T, Saville BJ, Banuett F, Kronstad JW, Gold SE, Müller O, Perlin MH, Wösten HA, de Vries R, Ruiz-Herrera J, Reynaga-Peña CG, Snetselaar K, McCann M, Pérez-Martín J, Feldbrügge M, Basse CW, Steinberg G, Ibeas JI, Holloman W, Guzman P, Farman M, Stajich JE, Sentandreu R, González-Prieto JM, Kennell JC, Molina L, Schirawski J, Mendoza-Mendoza A, Greilinger D, Münch K, Rössel N, Scherer M, Vranes M, Ladendorf O, Vincon V, Fuchs U, Sandrock B, Meng S, Ho EC, Cahill MJ, Boyce KJ, Klose J, Klosterman SJ, Deelstra HJ, Ortiz-Castellanos L, Li W, Sanchez-Alonso P, Schreier PH, Häuser-Hahn I, Vaupel M, Koopmann E, Friedrich G, Voss H, Schlüter T, Margolis J, Platt D, Swimmer C, Gnirke A, Chen F, Vysotskaia V, Mannhaupt G, Güldener U, Münsterkötter M, Haase D, Oesterheld M, Mewes HW, Mauceli EW, DeCaprio D, Wade CM, Butler J, Young S, Jaffe DB, Calvo S, Nusbaum C, Galagan J, Birren BW. 2006. Insights from the genome of the biotrophic fungal plant pathogen. Ustilago maydis. Nature 444:97-101. doi: 10.1038/nature05248.
37. Kaur H, Shaker K, Heinzel N, Ralph J, Gális I, Baldwin IT. 2012. Environmental stresses of field growth allow cinnamyl alcohol dehydrogenase-deficient Nicotiana attenuata plants to compensate for their structural deficiencies. Plant Physiology 159:1545-1570. doi: 10.1104/pp.112.196717.
38. Kay BK, Williamson MP, Sudol M. 2000. The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains. FASEB Journal 14:231-241.
39. Khang CH, Berruyer R, Giraldo MC, Kankanala P, Park SY, Czymmek K, Czymmek K, Kang S, Valent B. 2010. Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. Plant Cell 22:1388-1403. doi: 10.1105/tpc.109.069666.
40. Koch C, Tria G, Fielding AJ, Brodhun F, Valerius O, Feussner K, Braus GH, Svergun DI, Bennati M, Feussner I. 2013. A structural model of PpoA derived from SAXS-analysis-implications for substrate conversion. Biochimica et Biophysica Acta 1831:1449-1457. doi: 10.1016/j.bbalip.2013.06.003.
41. Lapierre C, Tollier MT, Monties B. 1988. Mise en évidence d'un nouveau type d'unité constitutive dans les lignines d'un mutant de maïs bm3. Comptes rendus de l'Académie des Sciences Paris Ser III 307:723-728.
42. Laurie JD, Ali S, Linning R, Mannhaupt G, Wong P, Güldener U, Münsterkötter M, Moore R, Kahmann R, Bakkeren G, Schirawski J. 2012. Genome comparison of barley and maize smut fungi reveals targeted loss of RNA silencing components and species-specific presence of transposable elements. Plant Cell 24:1733-1745. doi: 10.1105/tpc.112.097261.
43. Lorenc-Kukuła K, Jafra S, Oszmiański J, Szopa J. 2005. Ectopic expression of anthocyanin 5-O-glucosyltransferase in potato tuber causes increased resistance to bacteria. Journal of Agricultural and Food Chemistry 53:272-281. doi: 10.1021/jf048449p.
44. Loubradou G, Brachmann A, Feldbrugge M, Kahmann R. 2001. A homologue of the transcriptional repressor Ssn6p antagonizes cAMP signalling in Ustilago maydis. Molecular Microbiology 40:719-730. doi: 10.1046/j.1365-2958.2001.02424.x.
45. Ludwig SR, Wessler SR. 1990. Maize R gene family: tissue-specific helix-loop-helix proteins. Cell 62:849-851. doi: 10.1016/0092-8674(90)90259-H.
46. Marita JM, Vermerris W, Ralph J, Hatfield RD. 2003. Variations in the cell wall composition of maize brown midrib mutants. Journal of Agricultural and Food Chemistry 51:1313-1321. doi: 10.1021/jf0260592.
47. Mueller AN, Ziemann S, Treitschke S, Assmann D, Doehlemann G. 2013. Compatibility in the Ustilago maydis-maize interaction requires inhibition of host cysteine proteases by the fungal effector Pit2. PLOS Pathogens 9:e1003177. doi: 10.1371/journal.ppat.1003177.
48. Mueller O, Kahmann R, Aguilar G, Trejo-Aguilar B, Wu A, de Vries RP. 2008. The secretome of the maize pathogen Ustilago maydis. Fungal Genetics and Biology 45:S63-S70. doi: 10.1016/j.fgb.2008.03.012.
49. Ravid T, Hochstrasser M. 2008. Diversity of degradation signals in the ubiquitin-proteasome system. Nature Reviews Molecular Cell Biology 9:679-690. doi: 10.1038/nrm2468.
50. Ray H, Yu M, Auser P, Blahut-Beatty L, McKersie B, Bowley S, Westcott N, Coulman B, Lloyd A, Gruber MY. 2003. Expression of anthocyanins and proanthocyanidins after transformation of alfalfa with maize Lc. Plant Physiology 132:1448-1463. doi: 10.1104/pp.103.025361.
51. Ring L, Yeh SY, Hücherig S, Hoffmann T, Blanco-Portales R, Fouche M, Villatoro C, Denoyes B, Monfort A, Caballero JL, Muñoz-Blanco J, Gershenson J, Schwab W. 2013. Metabolic interaction between anthocyanin and lignin biosynthesis is associated with peroxidase FaPRX27 in strawberry fruit. Plant Physiology 163:43-60. doi: 10.1104/pp.113.222778.
52. Saballos A, Sattler SE, Sanchez E, Foster TP, Xin Z, Kang C, Pedersen JF, Vermerris W. 2012. Brown midrib2 (Bmr2) encodes the major 4-coumarate:coenzyme A ligase involved in lignin biosynthesis in sorghum (Sorghum bicolor (L.) Moench). Plant Journal 70:818-830. doi: 10.1111/j.1365-313X.2012.04933.x.
53. Saksela K, Cheng G, Baltimore D. 1995. Proline-rich (PxxP) motifs in HIV-1 Nef bind to SH3 domains of a subset of Src kinases and are required for the enhanced growth of Nef+ viruses but not for down-regulation of CD4. The EMBO Journal 14:484-491.
54. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual. New York: Cold Spring Harbor Laboratory Press.
55. Sheehan H, Hermann K, Kuhlemeier C. 2012. Color and scent: how single genes influence pollinator attraction. Cold Spring Harbor Symposia on Quantitative Biology 77:117-133. doi: 10.1101/sqb.2013.77.014712.
56. Snyder BA, Nicholson RL. 1990. Synthesis of phytoalexins in sorghum as a site-specific response to fungal ingress. Science 248:1637-1639. doi: 10.1126/science.248.4963.1637.
57. Spellig T, Bottin A, Kahmann R. 1996. Green fluorescent protein (GFP) as a new vital marker in the phytopathogenic fungus Ustilago maydis. Molecular & General Genetics 252:503-509. doi: 10.1007/BF02172396.
58. Spoel SH, Mou Z, Tada Y, Spivey NW, Genschik P, Dong X. 2009. Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell 137:860-872. doi: 10.1016/j.cell.2009.03.038.
59. Steyn WJ, Wand SJE, Holcroft DM, Jacobs G. 2002. Anthocyanins in vegetative tissues: a proposed unified function in photoprotection. New Phytologist 155:349-361. doi: 10.1046/j.1469-8137.2002.00482.x.
60. Studer MH, DeMartini JD, Davis MF, Sykes RW, Davison B, Keller M, Tuskan GA, Wyman CE. 2011. Lignin content in natural Populus variants affects sugar release. Proceedings of the National Academy of Sciences of the United States of America 108:6300-6305. doi: 10.1073/pnas.1009252108.
61. van der Linde K, Hemetsberger C, Kastner C, Kaschani F, van der Hoorn RA, Kumlehn J, Doehlemann G. 2012. A maize cystatin suppresses host immunity by inhibiting apoplastic cysteine proteases. Plant Cell 24:1285-1300. doi: 10.1105/tpc.111.093732.
62. Vance CP, Kirk TK, Sherwood RT. 1980. Lignification as a mechanism of disease resistance. Annual Review of Phytopathology 18:259-288. doi: 10.1146/annurev.py.18.090180.001355.
63. Vermerris W, Boon JJ. 2001. Tissue-specific patterns of lignification are disturbed in the brown midrib2 mutant of maize (Zea mays L.). Journal of Agricultural and Food Chemistry 49:721-728. doi: 10.1021/jf000740r.
64. Vermerris W, McIntyre LM. 1999. Time to flowering in brown midrib mutants of maize: an alternative approach to the analysis of developmental traits. Heredity 83:171-178. doi: 10.1046/j.1365-2540.1999.00569.x.
65. Vermerris W, Saballos A, Ejeta G, Mosier NS, Ladisch MR, Carpita NC. 2007. Molecular breeding to enhance ethanol production from corn and sorghum stover. Crop Science 47:S145-S153. doi: 10.2135/cropsci2007.04.0013IPBS.
66. Vermerris W, Sherman DM, McIntyre LM. 2010. Phenotypic plasticity in cell walls of maize brown midrib mutants is limited by lignin composition. Journal of Experimental Botany 61:2479-2490. doi: 10.1093/jxb/erq093.
67. Vignols F, Rigau J, Torres MA, Capellades M, Puigdomènech P. 1995. The brown midrib3 (bm3) mutation in maize occurs in the gene encoding caffeic acid O-methyltransferase. Plant Cell 7:407-416. doi: 10.1105/tpc.7.4.407.
68. Voinnet O, Rivas S, Mestre P, Baulcombe D. 2003. An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant Journal 33:949-956. doi: 10.1046/j.1365-313X.2003.01676.x.
69. Wahl R, Wippel K, Goos S, Kämper J, Sauer N. 2010. A novel high-affinity sucrose transporter is required for virulence of the plant pathogen Ustilago maydis. PLOS Biology 8:e1000303. doi: 10.1371/journal.pbio.1000303.
70. Wang L, Berndt P, Xia X, Kahnt J, Kahmann R. 2011. A seven-WD40 protein related to human RACK1 regulates mating and virulence in Ustilago maydis. Molecular Microbiology 81:1484-1498. doi: 10.1111/j.1365-2958.2011.07783.x.
71. Zhang Y, Butelli E, De Stefano R, Schoonbeek HJ, Magusin A, Pagliarani C, Wellner N, Hill L, Orzaez D, Granell A, Jones JD, Martin C. 2013. Anthocyanins double the shelf life of tomatoes by delaying overripening and reducing susceptibility to gray mold. Current Biology 23:1094-1100. doi: 10.1016/j.cub.2013.04.072.
72. Zhong R, Lee C, McCarthy RL, Reeves CK, Jones EG, Ye ZH. 2011. Transcriptional activation of secondary wall biosynthesis by rice and maize NAC and MYB transcription factors. Plant and Cell Physiology 52:1856-1871. doi: 10.1093/pcp/pcr123.
73. Zuther K, Kahnt J, Utermark J, Imkampe J, Uhse S, Schirawski J. 2012. Host specificity of Sporisorium reilianum is tightly linked to generation of the phytoalexin luteolinidin by Sorghum bicolor. Molecular Plant-Microbe Interactions 25:1230-1237. doi: 10.1094/MPMI-12-11-0314.