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PeerJ  2015 

Horizontal transfer generates genetic variation in an asexual pathogen

DOI: 10.7717/peerj.650

Keywords: Asexual reproduction,Horizontal transfer,Nonhomologous recombination,Verticillium dahliae,Lineage-specific regions,Genetic variation

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Abstract:

There are major gaps in the understanding of how genetic variation is generated in the asexual pathogen Verticillium dahliae. On the one hand, V. dahliae is a haploid organism that reproduces clonally. On the other hand, single-nucleotide polymorphisms and chromosomal rearrangements were found between V. dahliae strains. Lineage-specific (LS) regions comprising about 5% of the genome are highly variable between V. dahliae strains. Nonetheless, it is unknown whether horizontal gene transfer plays a major role in generating genetic variation in V. dahliae. Here, we analyzed a previously sequenced V. dahliae population of nine strains from various geographical locations and hosts. We found highly homologous elements in LS regions of each strain; LS regions of V. dahliae strain JR2 are much richer in highly homologous elements than the core genome. In addition, we discovered, in LS regions of JR2, several structural forms of nonhomologous recombination, and two or three homologous sequence types of each form, with almost each sequence type present in an LS region of another strain. A large section of one of the forms is known to be horizontally transferred between V. dahliae strains. We unexpectedly found that 350 kilobases of dynamic LS regions were much more conserved than the core genome between V. dahliae and a closely related species (V. albo-atrum), suggesting that these LS regions were horizontally transferred recently. Our results support the view that genetic variation in LS regions is generated by horizontal transfer between strains, and by chromosomal reshuffling reported previously.

References

[1]  Amyotte SG, Tan X, Pennerman K, del Mar Jimenez-Gasco M, Klosterman SJ, Ma L-J, Dobinson KF, Veronese P. 2012. Transposable elements in phytopathogenic Verticillium spp.: Insights into genome evolution and inter- and intra-specific diversification. BMC Genomics 12:314
[2]  Atallah ZK, Maruthachalam K, du Toit L, Koike ST, Davis MR, Klosterman SJ, Hayes RJ, Subbarao KV. 2010. Population analyses of the vascular plant pathogen Verticillium dahliae detect recombination and transcontinental gene flow. Fungal Genetics and Biology 47:416-422
[3]  Bolek Y, El-Zik KM, Pepper AE, Bell AA, Magill CW, Thaxton PM, Reddy OUK. 2005. Mapping of Verticillium wilt resistance genes in cotton. Plant Science 168:1581-1590
[4]  Bork P, Hofmann K, Bucher P, Neuwald AF, Altschul SF, Koonin EV. 1997. A superfamily of conserved domains in DNA damage-responsive cell cycle checkpoint proteins. The FASEB Journal 11:68-76
[5]  Burt A. 2000. Perspective: sex, recombination, and the efficacy of selection—was Weismann right? Evolution 54:337-351
[6]  Chuma I, Isobe C, Hotta Y, Ibaragi K, Futamata N, Kusaba M, Yoshida K, Terauchi R, Fujita Y, Nakayashiki H, Valent B, Tosa Y. 2011. Multiple translocation of the AVR-Pita effector gene among chromosomes of the rice blast fungus Magnaporthe oryzae and related species. PLoS Pathogens 7:e1002147
[7]  de Jonge R, Bolton MD, Kombrink A, Van den Berg GCM, Yadeta KA, Thomma BPHJ. 2013. Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen. Genome Research 23:1271-1282
[8]  de Jonge R, Van Esse HP, Maruthachalam K, Bolton MD, Santhanam P, Keykha Saber M, Zhang Z, Usami T, Lievens B, Subbarao KV, Thomma BPHJ. 2012. Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proceedings of the National Academy of Sciences of the United States of America 109:5110-5115
[9]  Felsenstein J. 1974. The evolutionary advantage of recombination. Genetics 78:737-756
[10]  Fradin EF, Thomma BPHJ. 2006. Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum. Molecular Plant Pathology 12:71-86
[11]  Gish W, States DJ. 1993. Identification of protein coding regions by database similarity search. Nature Genetics 3:266-272
[12]  Glass NL, Jacobson DJ, Shiu PK. 2000. The genetics of hyphal fusion and vegetative incompatibility in filamentous ascomycete fungi. Annual Review of Genetics 34:165-186
[13]  Haas BJ, Kamoun S, Zody MC, Jiang RHY, Handsaker RE, Cano LM, Grabherr M, Kodira CD, Raffaele S, Torto-Alalibo T, Bozkurt TO, Ah-Fong AMV, Alvarado L, Anderson VL, Armstrong MR, Avrova A, Baxter L, Beynon J, Boevink PC, Bollmann SR, Bos JIB, Bulone V, Cai G, Cakir C, Carrington JC, Chawner M, Conti L, Costanzo S, Ewan R, Fahlgren N, Fischbach MA, Fugelstad J, Gilroy EM, Gnerre S, Green PJ, Grenville-Briggs LJ, Griffith J, Grunwald NJ, Horn K, Horner NR, Hu C-H, Huitema E, Jeong D-H, Jones AME, Jones JDG, Jones RW, Karlsson EK, Kunjeti SG, Lamour K, Liu Z, Ma L, MacLean D, Chibucos MC, McDonald H, McWalters J, Meijer HJG, Morgan W, Morris PF, Munro CA, ONeill K, Ospina-Giraldo M, Pinzon A, Pritchard L, Ramsahoye B, Ren Q, Restrepo S, Roy S, Sadanandom A, Savidor A, Schornack S, Schwartz DC, Schumann UD, Schwessinger B, Seyer L, Sharpe T, Silvar C, Song J, Studholme DJ, Sykes S, Thines M, Van de Vondervoort PJI, Phuntumart V, Wawra S, Weide R, Win J, Young C, Zhou S, Fry W, Meyers BC, Van West P, Ristaino J, Govers F, Birch PRJ, Whisson SC, Judelson HS, Nusbaum C. 2009. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461:393-398
[14]  Huang X, Adams MD, Zhou H, Kerlavage AR. 1997. A tool for analyzing and annotating genomic sequences. Genomics 46:37-45
[15]  Huang X, Wang J, Aluru S, Yang S-P, Hillier L. 2003. PCAP: a whole-genome assembly program. Genome Research 13:2164-2170
[16]  Huang X, Ye L, Chou H-H, Yang I-H, Chao K-M. 2004. Efficient combination of multiple word models for improved sequence comparison. Bioinformatics 20:2529-2533
[17]  Inderbitzin P, Davis RM, Bostock RM, Subbarao KV. 2011. The ascomycete Verticillium longisporum is a hybrid and a plant pathogen with an expanded host range. PLoS ONE 6:e18260
[18]  Kimura M. 1983. The neutral theory of molecular evolution. Cambridge: Cambridge University Press.
[19]  Klosterman SJ, Subbarao KV, Kang S, Veronese P, Gold SE, Thomma BPHJ, Zehua C, Henrissat B, Lee Y-H, Park J, Garcia-Pedrajas MD, Barbara DJ, Anchieta A, de Jonge R, Santhanam P, Maruthachalam K, Atallah Z, Amyotte SG, Paz Z, Inderbitzin P, Hayes RJ, Heiman DI, Young S, Zeng Q, Engels R, Galagan J, Cuomo CA, Dobinson KF, Ma L-J. 2011. Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens. PLoS Pathogens 7:e1002137
[20]  Langmead B, Salzberg S. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods 9:357-359
[21]  Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup. 2009. The sequence alignment/map (SAM) format and SAMtools. Bioinformatics 25:2078-2079
[22]  Ma L-J, Van der Does HC, Borkovich KA, Coleman JJ, Daboussi M-J, Di Pietro A, Dufresne M, Freitag M, Grabherr M, Henrissat B, Houterman PM, Kang S, Shim W-B, Woloshuk C, Xie X, Xu J-R, Antoniw J, Baker SE, Bluhm BH, Breakspear A, Brown DW, Butchko RAE, Chapman S, Coulson R, Coutinho PM, Danchin EGJ, Diener A, Gale LR, Gardiner DM, Goff S, Hammond-Kosack KE, Hilburn K, Hua-Van A, Jonkers W, Kazan K, Kodira CD, Koehrsen M, Kumar L, Lee Y-H, Li L, Manners JM, Miranda-Saavedra D, Mukherjee M, Park G, Park J, Park S-Y, Proctor RH, Regev A, Ruiz-Roldan MC, Sain D, Sakthikumar S, Sykes S, Schwartz DC, Turgeon BG, Wapinski I, Yoder O, Young S, Zeng Q, Zhou S, Galagan J, Cuomo CA, Kistler HC, Rep M. 2010. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464:367-373
[23]  Masel AM, He C, Poplawski AM, Irwin JAG, Manners JM. 1996. Molecular evidence for chromosome transfer between biotypes of Colletotrichum gloeosporioides. Molecular Plant-Microbe Interactions 9:339-348
[24]  McDonald BA, Linde C. 2002. Pathogen population genetics, evolutionary potential, and durable resistance. Annual Review of Phytopathology 40:349-379
[25]  Michielse CB, Rep M. 2009. Pathogen profile update: Fusarium oxysporum. Molecular Plant Pathology 10:311-324
[26]  Noguchi MT, Yasuda N, Fujita Y. 2006. Evidence of genetic exchange by parasexual recombination and genetic analysis of pathogenicity and mating type of parasexual recombinants in rice blast fungus, Magnaporthe oryzae. Phytopathology 96:746-750
[27]  O‘Garro LW, Clarkson JM. 1992. Variation for pathogenicity on tomato among parasexual recombinants of Verticillium dahliae. Plant Pathology 41:141-147
[28]  Pegg GF, Brady BL. 2002. Verticillium wilts. Wallingford: CABI Publishing.
[29]  Pulhalla JE, Mayfield JE. 1974. The mechanism of heterokaryotic growth in Verticillium dahliae. Genetics 76:411-422
[30]  Usami T, Itoh M, Amemiya Y. 2009a. Asexual fungus Verticillium dahliae is potentially heterothallic. Journal of General Plant Pathology 75:422-427
[31]  Usami T, Itoh M, Amemiya Y. 2009b. Mating type gene MAT1-2-1 is common among Japanese isolates of Verticillium dahliae. Physiological and Molecular Plant Pathology 73:133-137
[32]  Zeigler RS, Scott RP, Leung H, Bordeos AA, Kumar J, Nelson RJ. 1997. Evidence of parasexual exchange of DNA in the rice blast fungus challenges its exclusive clonality. Journal of Phytopathology 87:284-294

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