The cellulose synthase 3 (CesA3) gene of oomycetes: Structure, phylogeny and influence on sensitivity to carboxylic acid amide (CAA) fungicides

Fungal Biology

Volumn 116, Issue 4, 2012, Pages 529-542

  Blum, Mathias ^a,b   Gamper, Hannes A ^c   Waldner, Maya ^b   Sierotzki, Helge ^b   Gisi, Ulrich ^a,b  

^a UNIVERSITY OF BASEL   (Switzerland)

^b SYNGENTA CROP PROTECTION AG   (Switzerland)

^c ETH ZURICH   (Switzerland)

Author keywords

Amino acid configuration; Cellulose synthesis; Mandipropamid; Phylogenetic analysis; Target site

Indexed keywords

AMIDE; CARBOXYLIC ACID; CELLULOSE SYNTHASE; FUNGAL DNA; FUNGICIDE; GLUCOSYLTRANSFERASE; MANDIPROPAMID; MUTANT PROTEIN;

AMINO ACID; CELLULOSE; CROP YIELD; DISEASE CONTROL; EUKARYOTE; FUNGICIDE; INHIBITION; PESTICIDE RESISTANCE; PHYLOGENETICS; PHYLOGENY; SENSITIVITY ANALYSIS; YIELD RESPONSE;

AMINO ACID SEQUENCE; ANTIFUNGAL RESISTANCE; ARTICLE; CHEMISTRY; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; DRUG EFFECT; ENZYMOLOGY; GENETICS; METABOLISM; MICROBIOLOGICAL EXAMINATION; MISSENSE MUTATION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OOMYCETES; PHYLOGENY; POINT MUTATION; SEQUENCE HOMOLOGY;

AMIDES; AMINO ACID SEQUENCE; CARBOXYLIC ACIDS; CLUSTER ANALYSIS; DNA, FUNGAL; DRUG RESISTANCE, FUNGAL; FUNGICIDES, INDUSTRIAL; GLUCOSYLTRANSFERASES; MICROBIAL SENSITIVITY TESTS; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MUTATION, MISSENSE; OOMYCETES; PHYLOGENY; POINT MUTATION; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID;

LEPTOMITALES; OOMYCETES; PERONOSPORALES; PYTHIALES; RHIPIDIALES; SAPROLEGNIALES;

EID: 84859424257     PISSN: 18786146     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.funbio.2012.02.003     Document Type: Article

References (74)

1. Albert G., Curtze J., Drandarevski C.A. Dimethomorph (CME 151), a novel curative fungicide. Proceedings of the British Crop Protection Conference - Pests and Diseases 1988, Vol. 1. 17-24.
2. Bartnicki-Garcia S. Cell wall chemistry morphogenesis and taxonomy of fungi. Annual Review of Microbiology 1968, 22:87-108.
3. Beakes G.W. Oomycete fungi: their phylogeny and relationship to chromophyte algae. The Chromophyte Algae: Problems and Perspectives 1989, 325-342. Clarendon Press, Oxford. J.P. Green, B.S.C. Leadbeater, W.L. Diver (Eds.).
4. Bakes GW, Glockling SL, Sekimoto S, 2011. The evolutionary phylogeny of the oomycete "fungi". Protoplasma, in press.
5. Beakes G.W., Sekimoto S. The evolutionary phylogeny of Oomycetes-insights gained from studies of holocarpic parasites of algae and invertebrates. Oomycete genetics and Genomics: Diversity, Interactions, and Research Tools 2009, 1-24. Wiley-Blackwell, London. K. Lamour, S. Kamoun (Eds.).
6. Bergsten J. A review of long-branch attraction. Cladistics 2005, 21:163-193.
7. Blanton R.L., Fuller D., Iranfar N., Grimson M.J., Loomis W.F. The cellulose synthase gene of Dictyostelium. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:2391-2396.
8. Blum M., Boehler M., Randall E., Young V., Csukai M., Kraus S., Moulin F., Scalliet G., Avrova A.O., Whisson S.C., Fonne-Pfister R. Mandipropamid targets the cellulose synthase-like PiCesA3 to inhibit cell wall biosynthesis in the oomycete plant pathogen, Phytophthora infestans. Molecular Plant Pathology 2010, 11:227-243.
9. Blum M, Gisi U, Insights into the molecular mechanism of tolerance to carboxylic acid amide (CAA) fungicides in Pythium aphanidermatum. Pest Management Science, . doi:10.1002/ps.3279.
10. Blum M., Waldner M., Gisi U. A single point mutation in the novel PvCesA3 gene confers resistance to the carboxylic acid amide fungicide mandipropamid in Plasmopara viticola. Fungal Genetics and Biology 2010, 47:499-510.
11. Blum M., Waldner M., Olaya G., Cohen Y., Gisi U., Sierotzki H. Resistance mechanism to carboxylic acid amide (CAA) fungicides in the cucurbit downy mildew pathogen Pseudoperonospora cubensis. Pest Management Science 2011, 67:1211-1214.
12. Charnock S.J., Henrissat B., Davies G.J. Three-dimensional structures of UDP-sugar glycosyltransferases illuminate the biosynthesis of plant polysaccharides. Plant Physiology 2001, 125:527-531.
13. Chen L., Wang Q., Lu X., Zhu S., Liu X. Semidominant mutations in cesA3 leading to resistance to CAA fungicides in Phytophthora capsici. Phytopathology 2011, 101(suppl.):S34.
14. Cohen Y., Gisi U. Differential activity of carboxylic acid amide fungicides against various developmental stages of Phytophthora infestans. Phytopathology 2007, 97:1274-1283.
15. Cohen Y., Rubin A., Gotlieb D. Activity of carboxylic acid amide (CAA) fungicides against Bremia lactucae. European Journal of Plant Pathology 2008, 122:169-183.
16. Cooke D.E.L., Drenth A., Duncan J.M., Wagels G., Brasier C.M. A molecular phylogeny of Phytophthora and related oomycetes. Fungal Genetics and Biology 2000, 30:17-32.
17. Desprez T., Juraniec M., Crowell E.F., Jouy H., Pochylova Z., Parcy F., Hofte H., Gonneau M., Vernhettes S. Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsidis thaliana. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:15572-15577.
18. Dick M.W. Straminipilous Fungi: Systematics of the Peronosporomycetes Including Accounts of the Marine Straminipilous Protists, the Plasmodiophorids and Similar Organisms 2001, Kluwer Academic Publishers, Dordrecht.
19. Fink J.L., Hamilton N. DomainDraw: a macromolecular schematic drawing program. In Silico Biology 2007, 7:14.
20. Fugelstad J., Bouzenzana J., Djerbi S., Guerriero G., Ezcurra I., Teeri T.T., Arvestad L., Bulone V. Identification of the cellulose synthase genes from the oomycete Saprolegnia monoica and effect of cellulose synthesis inhibitors on gene expression and enzyme activity. Fungal Genetics and Biology 2009, 46:759-767.
21. Gilijamse E., Raaijmakers J.M., Geerds C.F., Jeger M.J. Influence of environmental factors on the disease cycle of white rust caused by Albugo candida. Advances in Downy Mildew Research 2004, 107-118. Kluwer Academic Publishers, Dordrecht. 2nd edn. P. Spencer-Phillips, M. Jeger (Eds.).
22. Giresse X., Ahmed S., Richard-Cervera S., Delmotte F. Development of new oomycete taxon-specific mitochondrial cytochrome b region primers for use in phylogenetic and phylogeographic studies. Journal of Phytopathology 2010, 158:321-327.
23. Gisi U, Lamberth C, Mehl A, Seitz T, 2012. Carboxylic acid amide (CAA) fungicides. In: Krämer W, Schirmer U, Jeschke P, Witschel M (eds), Modern Crop Protection Compounds, 2nd edn. WILEY-VCH Verlag, Weinheim, "in press".
24. Gisi U., Waldner M., Kraus N., Dubuis P.H., Sierotzki H. Inheritance of resistance to carboxylic acid amide (CAA) fungicides in Plasmopara viticola. Plant Pathology 2007, 56:199-208.
25. Göker M., Voglmayr H., Riethmüller A., Oberwinkler F. How do obligate parasites evolve? A multi-gene phylogenetic analysis of downy mildews. Fungal Genetics and Biology 2007, 44:105-122.
26. Göker M., Voglmayr H., Riethmüller A., Weiss M., Oberwinkler F. Taxonomic aspects of Peronosporaceae inferred from Bayesian molecular phylogenetics. Canadian Journal of Botany 2003, 81:672-683.
27. Grenville-Briggs L.J., Anderson V.L., Fugelstad J., Avrova A.O., Bouzenzana J., Williams A., Wawra S., Whisson S.C., Birch P.R.J., Bulone V., van West P. Cellulose synthesis in Phytophthora infestans is required for normal appressorium formation and successful infection of potato. Plant Cell 2008, 20:720-738.
28. Hakariya M., Hirose D., Tokumasu S. A molecular phylogeny of Haptoglossa species, terrestrial peronosporomycetes (oomycetes) endoparasitic on nematodes. Mycoscience 2007, 48:169-175.
29. Helbert W., Sugiyama J., Ishihara M., Yamanaka S. Characterization of native crystalline cellulose in the cell walls of Oomycota. Journal of Biotechnology 1997, 57:29-37.
30. Hudspeth D.S.S., Nadler S.A., Hudspeth M.E.S. A COX2 molecular phylogeny of the Peronosporomycetes. Mycologia 2000, 92:674-684.
31. Hudspeth D.S.S., Stenger D., Hudspeth M.E.S. A cox2 phylogenetic hypothesis for the downy mildews and white rusts. Fungal Diversity 2003, 13:47-57.
32. Huelsenbeck J.P., Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001, 17:754-755.
33. Kim H.T., Jang H.S., Lee S.M., Kim S.B., Kim J., Knight S., Park K.D., McKenzie D. Baseline sensitivity to mandipropamid among isolates of Phytophthora capsici causing Phytophthora blight on pepper. Plant Pathology Journal 2009, 25:317-321.
34. Kroon L.P.N.M., Bakker F.T., van den Bosch G.B.M., Bonants P.J.M., Flier W.G. Phylogenetic analysis of Phytophthora species based on mitochondrial and nuclear DNA sequences. Fungal Genetics and Biology 2004, 41:766-782.
35. Kuga S., Takagi S., Brown R.M. Native folded-chain cellulose II. Polymer 1993, 34:3293-3297.
36. Kurek I., Kawagoe Y., Jacob-Wilk D., Doblin M., Delmer D. Dimerization of cotton fiber cellulose synthase catalytic subunits occurs via oxidation of the zinc-binding domains. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:11109-11114.
37. Lara E., Belbahri L. SSU rRNA reveals major trends in oomycete evolution. Fungal Diversity 2011, 49:93-100.
38. Levesque C.A., Brouwer H., Cano L., Hamilton J.P., Holt C., Huitema E., Raffaele S., Robideau G.P., Thines M., Win J., Zerillo M.M., Beakes G.W., Boore J.L., Busam D., Dumas B., Ferriera S., Fuerstenberg S.I., Gachon C.M.M., Gaulin E., Govers F., Grenville-Briggs L., Horner N., Hostetler J., Jiang R.H.Y., Johnson J., Krajaejun T., Lin H.N., Meijer H.J.G., Moore B., Morris P., Phuntmart V., Puiu D., Shetty J., Stajich J.E., Tripathy S., Wawra S., van West P., Whitty B.R., Coutinho P.M., Henrissat B., Martin F., Thomas P.D., Tyler B.M., De Vries R.P., Kamoun S., Yandell M., Tisserat N., Buell C.R. Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire. Genome Biology 2010, 11:R73.
39. Levesque C.A., De Cock A.W.A.M. Molecular phylogeny and taxonomy of the genus Pythium. Mycological Research 2004, 108:1363-1383.
40. Lu X.H., Zhu S.S., Bi Y., Liu X.L., Hao J.J.J. Baseline sensitivity and resistance-risk assessment of Phytophthora capsici to iprovalicarb. Phytopathology 2010, 100:1162-1168.
41. Maddison D.R., Maddision W.P. MacClade v4.08 Available from. http://macclade.org/index.html.
42. Marchler-Bauer A., Lu S.N., Anderson J.B., Chitsaz F., Derbyshire M.K., DeWeese-Scott C., Fong J.H., Geer L.Y., Geer R.C., Gonzales N.R., Gwadz M., Hurwitz D.I., Jackson J.D., Ke Z.X., Lanczycki C.J., Lu F., Marchler G.H., Mullokandov M., Omelchenko M.V., Robertson C.L., Song J.S., Thanki N., Yamashita R.A., Zhang D.C., Zhang N.G., Zheng C.J., Bryant S.H. CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Research 2011, 39:D225-D229.
43. Miller M.A., Pfeiffer W., Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE) 2010, 1-8. 14 Nov. 2010, New Orleans, LA.
44. Nylander J.A.A. MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre 2004, Uppsala University.
45. Paredez A.R., Somerville C.R., Ehrhardt D.W. Visualization of cellulose synthase demonstrates functional association with microtubules. Science 2006, 312:1491-1495.
46. Persson S., Paredez A., Carroll A., Palsdottir H., Doblin M., Poindexter P., Khitrov N., Auer M., Somerville C.R. Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsidis. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:15566-15571.
47. Petersen A.B., Rosendahl S. Phylogeny of the Peronosporomycetes (Oomycota) based on partial sequences of the large ribosomal subunit (LSU rDNA). Mycological Research 2000, 104:1295-1303.
48. Phillips A.J., Anderson V.L., Robertson E.J., Secombes C.J., van West P. New insights into animal pathogenic oomycetes. Trends in Microbiology 2008, 16:13-19.
49. Rambaut A., Drummond A.J. Tracer v1.4 Available from. http://beast.bio.ed.ac.uk/Tracer.
50. Richmond T.A., Somerville C.R. The cellulose synthase superfamily. Plant Physiology 2000, 124:495-498.
51. Riethmüller A., Voglmayr H., Göker M., Weiss M., Oberwinkler F. Phylogenetic relationships of the downy mildews (Peronosporales) and related groups based on nuclear large subunit ribosomal DNA sequences. Mycologia 2002, 94:834-849.
52. Roberts E., Roberts A.W. A cellulose synthase (CesA) gene from the red alga Porphyra yezoensis (Rhodophyta). Journal of Phycology 2009, 45:203-212.
53. Robideau G.P., de Cock A.W.A.M., Coffey M.D., Voglmayr H., Brouwer H., Bala K., Chitty D.W., Desaulniers N., Eggertson Q.A., Gachon C.M.M., Hu C.H., Kupper F.C., Rintoul T.L., Sarhan E., Verstappen E.C.P., Zhang Y.H., Bonants P.J.M., Ristaino J.B., Levesque C.A. DNA barcoding of oomycetes with cytochrome c oxidase subunit I and internal transcribed spacer. Molecular Ecology Resources 2011, 11:1002-1011.
54. Rose T.M., Henikoff J.G., Henikoff S. CODEHOP (COnsensus-DEgenerate hybrid oligonucleotide primer) PCR primer design. Nucleic Acids Research 2003, 31:3763-3766.
55. Runge F., Telle S., Ploch S., Savory E., Day B., Sharma R., Thines M. The inclusion of downy mildews in a multi-locus-dataset and its reanalysis reveals a high degree of paraphyly in Phytophthora. IMA Fungus 2011, 2:163-171.
56. Sagane Y., Zech K., Bouquet J.M., Schmid M., Bal U., Thompson E.M. Functional specialization of cellulose synthase genes of prokaryotic origin in chordate larvaceans. Development 2010, 137:1483-1492.
57. Sanderson M.J., Donoghue M.J., Piel W., Eriksson T. TreeBASE: a prototype database of phylogenetic analyses and an interactive tool for browsing the phylogeny of life. American Journal of Botany 1994, 81:183.
58. Sekimoto S., Beakes G.W., Gachon C.M.M., Muller D.G., Kupper F.C., Honda D. The development, ultrastructural cytology, and molecular phylogeny of the basal oomycete Eurychasma dicksonii, infecting the filamentous phaeophyte algae Ectocarpus siliculosus and Pylaiella littoralis. Protist 2008, 159:299-318.
59. Sierotzki H., Blum M., Olaya G., Waldner M., Cohen Y., Gisi U. Sensitivity to CAA fungicides and frequency of mutations in cellulose synthase 3 (CesA3) gene of oomycete pathogen populations. Modern Fungicides and Antifungal Compounds VI 2011, 151-154. DPG-Verlag, Braunschweig. H.W. Dehne, H.B. Deising, U. Gisi, K.H. Kuck, P.E. Russell, H. Lyr (Eds.).
60. Smith L.G., Oppenheimer D.G. Spatial control of cell expansion by the plant cytoskeleton. Annual Review of Cell and Developmental Biology 2005, 21:271-295.
61. Sparrow F.K. The present status of classification in biflagellate fungi. Recent Advances in Aquatic Mycology 1976, 213-222. Elek Science, London. E.B. Gareth-Jones (Ed.).
62. Stenzel K., Pontzen R., Seitz T., Tiemann R., Witzenberger A. SZX 722: a novel systemic oomycete fungicide. Brighton Crop Protection Conference: Pests & Diseases-1998: Volume 2: Proceedings of an International Conference 1998, 335-342. Brighton, UK 16-19.
63. Stöver B.C., Müller K.F. TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinformatics 2010, 11:7.
64. Tamura K., Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 1993, 10:512-526.
65. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 2011, 28:2731-2739.
66. Thines M. Bridging the gulf: Phytophthora and downy mildews are connected by rare grass parasites. Plos One 2009, 4.
67. Thines M., Göker M., Telle S., Ryley M., Mathur K., Narayana Y.D., Spring O., Thakur R.P. Phylogenetic relationships of graminicolous downy mildews based on cox2 sequence data. Mycological Research 2008, 112:345-351.
68. Thines M., Spring O. A revision of Albugo (Chromista, Peronosporomycetes). Mycotaxon 2005, 92:443-458.
69. Thompson J.D., Gibson T.J., Higgins D.G. Multiple sequence alignment using ClustalW and ClustalX. Current Protocols in Bioinformatics 2002, Chapter 2: Unit 2 3.
70. Uzuhashi S., Tojo M., Kakishima M. Phylogeny of the genus Pythium and description of new genera. Mycoscience 2010, 51:337-365.
71. van West P. Saprolegnia parasitica, an oomycete pathogen with a fishy appetite: new challenges for an old problem. Mycologist 2006, 20:99-104.
72. Voglmayr H. Phylogenetic relationships of Peronospora and related genera based on nuclear ribosomal ITS sequences. Mycological Research 2003, 107:1132-1142.
73. Voglmayr H., Riethmüller A. Phylogenetic relationships of Albugo species (white blister rusts) based on LSU rDNA sequence and oospore data. Mycological Research 2006, 110:75-85.
74. Zhu S., Liu P., Liu X., Li J., Yuan S., Si N. Assessing the risk of resistance in Pseudoperonospora cubensis to the fungicide flumorph in vitro. Pest Management Science 2008, 64:255-261.