Phylogeography and virulence structure of the powdery mildew population on its 'new' host triticale

BMC Evolutionary Biology

Geert Haesaert²  Monica Höfte²  Boris Bekaert¹  Kris Audenaert²  Veronique Troch² 

[1]Associated Faculty of Applied Bioscience Engineering, University College Ghent, Valentin Vaerwyckweg 1, B-9000, Ghent, Belgium

[2]Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Coupure links 653, B-9000, Ghent, Belgium

关键词: Nephron-sparing surgery;    Oncologic outcomes;    Robotic partial nephrectomy;    Partial nephrectomy;    Renal cell carcinoma;   

Others  :  1141163
DOI  :  10.1186/1471-2148-12-76

 received in 2011-12-13, accepted in 2012-05-10,  发布年份 2012

【 摘 要 】

Background

Powdery mildew, caused by the obligate biotrophic fungus Blumeria graminis, is a major problem in cereal production as it can reduce quality and yield. B. graminis has evolved eight distinct formae speciales (f.sp.) which display strict host specialization. In the last decade, powdery mildew has emerged on triticale, the artificial intergeneric hybrid between wheat and rye. This emergence is probably triggered by a host range expansion of the wheat powdery mildew B. graminis f.sp. tritici. To gain more precise information about the evolutionary processes that led to this host range expansion, we pursued a combined pathological and genetic approach.

Results

B. graminis isolates were sampled from triticale, wheat and rye from different breeding regions in Europe. Pathogenicity tests showed that isolates collected from triticale are highly pathogenic on most of the tested triticale cultivars. Moreover, these isolates were also able to infect several wheat cultivars (their previous hosts), although a lower aggressiveness was observed compared to isolates collected from wheat. Phylogenetic analysis of nuclear gene regions identified two statistically significant clades, which to a certain extent correlated with pathogenicity. No differences in virulence profiles were found among the sampled regions, but the distribution of genetic variation demonstrated to be geography dependent. A multilocus haplotype network showed that haplotypes pathogenic on triticale are distributed at different sites in the network, but always clustered at or near the tips of the network.

Conclusions

This study reveals a genetic structure in B. graminis with population differentiation according to geography and host specificity. In addition, evidence is brought forward demonstrating that the host range expansion of wheat isolates to the new host triticale occurred recently and multiple times at different locations in Europe.

【 授权许可】

   
2012 Troch et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Salamini F, Ozkan H, Brandolini A, Schafer-Pregl R, Martin W: Genetics and geography of wild cereal domestication in the Near East. Nat Rev Genet 2002, 3:429-441.
• [2]Stukenbrock EH, McDonald BA: The origins of plant pathogens in agro-ecosystems. Annu Rev Phytopathol 2008, 46:75-100.
• [3]Everts K, Leath S, Finney PL: Impact of powdery mildew and leaf rust on milling and baking quality of soft red winter wheat. Plant Dis 2001, 85:423-429.
• [4]Conner RL, Kuzyk AD, Su H: Impact of powdery mildew on the yield of soft white spring wheat cultivars. Can J Plant Sci 2003, 83:725-728.
• [5]Flor HH: The complementary genic systems in flax and flax rust. Adv Genet 1956, 8:29-54.
• [6]Jones JDG, Dangl JL: The plant immune system. Nature 2006, 444:323-329.
• [7]De Wit PJGM, Mehrabi R, Van Den Brug HA, Stergiopoulos I: Fungal effector proteins: past, present and future. Mol Plant Pathol 2009, 10:735-747.
• [8]Ridout CJ, Skamnioti P, Porritt O, Sacristan S, Jones JDG, Brown JKM: Multiple avirulence paralogues in cereal powdery mildew fungi may contribute to parasite fitness and defeat of plant resistance. Plant Cell 2006, 18:2402-2414.
• [9]Nowara D, Gay A, Lacomme C, Shaw J, Ridout C, Douchkov D, Hensel G, Kumlehn J, Schweizer P: HIGS: host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. Plant Cell 2010, 22:3130-3141.
• [10]Sacristan S, Vigouroux M, Pedersen C, Skamnioti P, Thordal-Christensen H, Micali C, Brown JKM, Ridout CJ: Coevolution between a family of parasite virulence effectors and a class of LINE-1 retrotransposons. PLoS One 2009, 4:e7463.
• [11]Marchal E: De la specialisation du paristisme chez l’Erysiphe graminis. Compt Rend Acad Sci Paris 1902, 135:210-212.
• [12]Oku T, Yamashita S, Doi Y, Nishihara N: Host range and forma specialis of cocksfoot powdery mildew fungus (Erysiphe graminis DC) found in Japan. Ann Phytopathol Soc Japan 1985, 51:613-615.
• [13]Olesen KL, Carver TLW, Lyngkjær MF: Fungal suppression of resistance against inappropriate Blumeria graminis formae speciales in barley, oat and wheat. Physiol Mol Plant Pathol 2003, 62:37-50.
• [14]Wyand RA, Brown JKM: Genetic and forma specialis diversity in Blumeria graminis of cereals and its implications for host-pathogen co-evolution. Mol Plant Pathol 2003, 4:187-198.
• [15]Inuma T, Khodaparast SA, Takamatsu S: Multilocus phylogenetic analysis within Blumeria graminis, a powdery mildew fungus of cereals. Mol Phylogenet Evol 2007, 44:741-751.
• [16]Walker AS, Bouguennec A, Confais J, Morgant G, Leroux P: Evidence of host-range expansion from new powdery mildew (Blumeria graminis) infections of triticale (× Triticosecale) in France. Plant Pathol 2011, 60:207-220.
• [17]Takamatsu S, Matsuda S: Estimation of molecular clocks for ITS and 28s rDNA in Erysiphales. Mycoscience 2004, 45:340-344.
• [18]Oberhaensli S, Parlange F, Buchmann JP, Jenny FH, Abbott JC, Burgis TA, Spanu PD, Keller B, Wicker T: Comparative sequence analysis of wheat and barley powdery mildew fungi reveals gene colinearity, dates divergence and indicates host-pathogen co-evolution. Fungal Genet Biol 2011, 48:327-334.
• [19]Ammar K, Mergoum M, Rajaram S: The history and evolution of triticale. In Triticale Improvement and Production. Edited by Mergoum M, Gomez-Macpherson H. FAO, Rome, Italy; 2004:1-9. FAO Plant Production and Protection Paper 179
• [20]Oettler G: The fortune of a botanical curiosity—Triticale: past, present and future. J Agric Sci 2005, 143:329-346.
• [21]FAOSTAT. , ; . [http://faostat.fao.org/site/567/DesktopDefault.aspx?PageID=567 webcite]
• [22]Schulze-Lefert P, Panstruga R: A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends Plant Sci 2011, 16:117-125.
• [23]Spanu PD, Abbott JC, Amselem J, Burgis TA, Soanes DM, Stüber K, Ver Looren van Themaat E, Brown JKM, Butcher SA, Gurr SJ, Lebrun M-H, Ridout CJ, Schulze-Lefert P, Talbot NJ, Ahmadinejad N, Ametz C, Barton GR, Benjdia M, Bidzinski P, Bindschedler LV, Both M, Brewer MT, Cadle-Davidson L, Cadle-Davidson MM, Collemare J, Cramer R, Frenkel O, Godfrey D, Harriman J, Hoede C, King BC, Klages S, Kleemann J, Knoll D, Koti PS, Kreplak J, López-Ruiz FJ, Lu X, Maekawa T, Mahanil S, Micali C, Milgroom MG, Montanna G, Noir S, O’Connell RJ, Oberhaensli S, Parlange F, Pedersen C, Quesneville H, Reinhardt R, Rott M, Sacistán S, Schmidt SM, Schön M, Skamnioti P, Sommer H, Stephens A, Takahara H, Thordal-Christensen H, Vigouroux M, Weßling R, Wicker T, Panstruga R: Genome expansion and gene loss in powdery mildew fungi reveal functional tradeoffs in extreme parasitism. Science 2010, 330:1543-1546.
• [24]Giraud T, Gladieux P, Gavrilets S: Linking the emergence of fungal plant diseases with ecological speciation. Trends Ecol Evol 2010, 25:387-395.
• [25]Couch BC, Kohn LM: A multilocus gene genealogy concordant with host preference indicates segregation of a new species, Magnaporthe oryzae, from M. grisea. Mycologia 2002, 94:683-693.
• [26]Couch BC, Fudal I, Lebrun M-H, Tharreau D, Valent B, van Kim P, Nottéghem J-L, Kohn LM: Origins of host-specific populations of the blast pathogen Magnaporthe oryzae in crop domestication with subsequent expansion of pandemic clones on rice and weeds of rice. Genetics 2005, 170:613-630.
• [27]Mehta YRAB: Variação patogênica entre isolados de Magnaporthe grisea atacando triticale e trigo no estado do Paraná. Summa Phytopathol 1998, 24:119-125.
• [28]Zaffarano PL, McDonald BA, Linde CC: Rapid speciation following recent host shifts in the plant pathogenic fungus Rhynchosporium. Evolution 2008, 62:1418-1436.
• [29]Linde-Laursen I: Reaction of triticale, wheat and rye to the powdery mildew fungi, Eysiphe graminis f.sp. tritici and E. graminis f.sp. secalis. Z Pflanzenzucht 1977, 79:110-121.
• [30]Stukenbrock EH, Banke S, Javan-Nikkhah M, McDonald BA: Origin and domestication of the fungal wheat pathogen Mycosphaerella graminicola via sympatric speciation. Mol Biol Evol 2007, 24:398-411.
• [31]Eshed N, Wahl I: Host ranges and interrelations of Erysiphe graminis hordei, Erysiphe graminis tritici, and Eysiphe graminis avenae. Phytopathology 1970, 60:628-634.
• [32]As N, Leath S: Virulence of Blumeria graminis f.sp. tritici on winter wheat in the eastern United States. Plant Dis 1998, 82:64-68.
• [33]Parks R, Carbone I, Murphy JP, Marshall D, Cowger C: Virulence structure of the eastern U.S. wheat powdery mildew population. Plant Dis 2008, 92:1074-1082.
• [34]Parks R, Carbone I, Murphy JP, Cowger C: Population genetic analysis of an eastern U.S. wheat powdery mildew population reveals geographic subdivision and recent common ancestry with U.K. and Israeli populations. Phytopathology 2009, 99:840-849.
• [35]Brewer MT, Milgroom MG: Phylogeography and population structure of the grape powdery mildew fungus, Erysiphe necator, from diverse Vitis species. BMC Evol Biol 2010, 10:268. BioMed Central Full Text
• [36]Limpert E, Godet F, Müller K: Dispersal of cereal mildews across Europe. Agric Forest Meteorol 1999, 97:293-308.
• [37]Brown JKM, Hovmøller MS: Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 2002, 297:537-541.
• [38]Brown JKM, Wolfe MS: Structure and evolution of a population of Erysiphe graminis f.sp. hordei. Plant Pathol 1990, 39:376-390.
• [39]Hsam SLK, Zeller FJ: Breeding for powdery mildew resistance in common wheat (Triticum aestivum L.). In The Powdery Mildews. A Comprehensive Treatise. Edited by Bélanger RR, Bushnell WR, Dik AJ, Carver TLW. APS Press, St. Paul, Minnesota; 2002:219-238.
• [40]Moseman JG, Macer RCF, Greeley LW: Genetic studies with cultures of Eysiphe graminis f.sp. hordei virulent on Hordeum spontaneum. Trans Br Mycol Soc 1965, 48:479-489.
• [41]Lillemo M, Skinnes H, Brown JKM: Race specific resistance to powdery mildew in Scandinavian wheat cultivars, breeding lines and introduced genotypes with partial resistance. Plant Breed 2010, 129:297-303.
• [42]Peakall R, Smouse PE: GENALEX 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 2006, 6:288-295.
• [43]White TJ, Bruns TD, Lee S, Taylor JW: Amplification and direct sequencing of fungal ribosomal genes for phylogenetics. In PCR Protocols. Edited by Innis MA, Gelfrand DH, Sninsky JJ, White TJ. Academic, San Diego, CA, USA; 1990:315-322.
• [44]Thompson JD, Higgins DG, Gibson TJ: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994, 22:4673-4680.
• [45]Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG: Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
• [46]Hall TA: BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp 1999, Ser 41:95-98.
• [47]Swofford DL: PAUP* 4.0: Phylogenetic Analysis Using Parsimony, 4.0. Illinois Natural History Survey, Champaign; 2002.
• [48]Huelsenbeck JP, Ronquist F: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
• [49]Posada D, Crandall KA: MODELTEST: testing the model of DNA substitution. Bioinformatics 1998, 14:817-818.
• [50]Posada D, Crandall KA: Selecting the best-fit model of nucleotide substitution. Syst Biol 2001, 50:580-601.
• [51]Salzburger W, Ewing GB, Von Haeseler A: The performance of phylogenetic algorithms in estimating haplotype genealogies with migration. Mol Ecol 2011, 20:1952-1963.
• [52]Librado P, Rozas J: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452.