Forward genetics approach reveals host genotype-dependent importance of accessory chromosomes in the fungal wheat pathogen Zymoseptoria tritici

mBio

Volumn 8, Issue 6, 2017, Pages

  Habig, Michael ^a   Quade, Jakob ^a   Stukenbrock, Eva Holtgrewe ^a  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY BIOLOGY   (Germany)

Author keywords

Functional dissection; Genome plasticity; Host pathogen interactions; Induced chromosome deletions; Virulence

Indexed keywords

BETA TUBULIN; CARBENDAZIM; BENZIMIDAZOLE DERIVATIVE; CARBAMIC ACID DERIVATIVE; TUBULIN;

ANEUPLOIDY; ARTICLE; CHROMOSOME; CHROMOSOME LOSS; CONTROLLED STUDY; CORRELATIONAL STUDY; FUNGAL GENETICS; FUNGAL STRAIN; FUNGAL VIRULENCE; FUNGUS CULTURE; FUNGUS ISOLATION; FUNGUS MUTANT; GEL ELECTROPHORESIS; GENOTYPE; IN VITRO STUDY; KARYOTYPING; MITOSIS; MOLECULAR INTERACTION; NONHUMAN; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; WHOLE GENOME SEQUENCING; WILD TYPE; ZYMOSEPTORIA TRITICI; ASCOMYCETES; CHROMOSOME DELETION; CLASSIFICATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; PLANT DISEASE; VIRULENCE; WHEAT;

ASCOMYCOTA; BENZIMIDAZOLES; CARBAMATES; CHROMOSOME DELETION; CHROMOSOMES, FUNGAL; GENOTYPE; HOST-PATHOGEN INTERACTIONS; KARYOTYPING; MITOSIS; PLANT DISEASES; TRITICUM; TUBULIN; VIRULENCE;

EID: 85039903797     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01919-17     Document Type: Article

References (41)

1. Goodwin SB, M’barek SB, Dhillon B, Wittenberg AH, Crane CF, Hane JK, Foster AJ, Van der Lee TA, Grimwood J, Aerts A, Antoniw J, Bailey A, Bluhm B, Bowler J, Bristow J, van der Burgt A, Canto-Canche B, Churchill AC, Conde-Ferraez L, Cools HJ, Coutinho PM, Csukai M, Dehal P, De Wit P, Donzelli B, van de Geest HC, van Ham RC, Hammond-Kosack KE, Henrissat B, Kilian A, Kobayashi AK, Koopmann E, Kourmpetis Y, Kuzniar A, Lindquist E, Lombard V, Maliepaard C, Martins N, Mehrabi R, Nap JP. 2011. Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLoS Genet 7:e1002070. https://doi.org/10.1371/journal.pgen.1002070.
2. Marshall R, Kombrink A, Motteram J, Loza-Reyes E, Lucas J, Hammond-Kosack KE, Thomma BPHJ, Rudd JJ. 2011. Analysis of two in planta expressed LysM effector homologs from the fungus Mycosphaerella graminicola reveals novel functional properties and varying contributions to virulence on wheat. Plant Physiol 156:756-769. https://doi.org/10.1104/pp.111.176347.
3. Rudd JJ, Kanyuka K, Hassani-Pak K, Derbyshire M, Andongabo A, Devonshire J, Lysenko A, Saqi M, Desai NM, Powers SJ, Hooper J, Ambroso L, Bharti A, Farmer A, Hammond-Kosack KE, Dietrich RA, Courbot M. 2015. Transcriptome and metabolite profiling of the infection cycle of Zymoseptoria tritici on wheat reveals a biphasic interaction with plant immunity involving differential pathogen chromosomal contributions and a variation on the hemibiotrophic lifestyle definition. Plant Physiol 167: 1158-1185. https://doi.org/10.1104/pp.114.255927.
4. Poppe S, Dorsheimer L, Happel P, Stukenbrock EH. 2015. Rapidly evolving genes are key players in host specialization and virulence of the fungal wheat pathogen Zymoseptoria tritici (Mycosphaerella graminicola). PLoS Pathog 11:e1005055. https://doi.org/10.1371/journal.ppat.1005055.
5. Kema GHJ, Yu DZ, Rijkenberg FHJ, Shaw MW, Baayen RP. 1996. Histology of the pathogenesis of Mycosphaerella graminicola in wheat. Phytopathology 86:777-786. https://doi.org/10.1094/Phyto-86-777.
6. Linde CC, Zhan J, McDonald BA. 2002. Population structure of Mycosphaerella graminicola: from lesions to continents. Phytopathology 92: 946-955. https://doi.org/10.1094/PHYTO.2002.92.9.946.
7. Zhan J, Kema GHJ, Waalwijk C, McDonald BA. 2002. Distribution of mating type alleles in the wheat pathogen Mycosphaerella graminicola over spatial scales from lesions to continents. Fungal Genet Biol 36: 128-136. https://doi.org/10.1016/S1087-1845(02)00013-0.
8. Wittenberg AHJ, van der Lee TAJ, Ben M’Barek S, Ware SB, Goodwin SB, Kilian A, Visser RGF, Kema GHJ, Schouten HJ. 2009. Meiosis drives extraordinary genome plasticity in the haploid fungal plant pathogen Mycosphaerella graminicola. PLoS One 4:e5863. https://doi.org/10.1371/journal.pone.0005863.
9. Jones RN, Viegas W, Houben A. 2008. A century of B chromosomes in plants: so what? Ann Bot 101:767-775. https://doi.org/10.1093/aob/mcm167.
10. Houben A, Banaei-Moghaddam AM, Klemme S, Timmis JN. 2014. Evolution and biology of supernumerary B chromosomes. Cell Mol Life Sci 71:467-478. https://doi.org/10.1007/s00018-013-1437-7.
11. Galazka JM, Freitag M. 2014. Variability of chromosome structure in pathogenic fungi—of “ends and odds”. Curr Opin Microbiol 20:19-26. https://doi.org/10.1016/j.mib.2014.04.002.
12. Coleman JJ, Rounsley SD, Rodriguez-Carres M, Kuo A, Wasmann CC, Grimwood J, Schmutz J, Taga M, White GJ, Zhou S, Schwartz DC, Freitag M, Ma LJ, Danchin EGJ, Henrissat B, Coutinho PM, Nelson DR, Straney D, Napoli CA, Barker BM, Gribskov M, Rep M, Kroken S, Molnar I, Rensing C, Kennell JC, Zamora J, Farman ML, Selker EU, Salamov A, Shapiro H, Pangilinan J, Lindquist E, Lamers C, Grigoriev IV, Geiser DM, Covert SF, Temporini E, Vanetten HD. 2009. The genome of Nectria haematococca: contribution of supernumerary chromosomes to gene expansion. PLoS Genet 5:e1000618. https://doi.org/10.1371/journal.pgen.1000618.
13. Ma LJ, van der Does HC, Borkovich KA, Coleman JJ, Daboussi MJ, Di Pietro A, Dufresne M, Freitag M, Grabherr M, Henrissat B, Houterman PM, Kang S, Shim WB, Woloshuk C, Xie X, Xu JR, 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 YH, 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. https://doi.org/10.1038/nature08850.
14. Miao VP, Covert SF, VanEtten HD. 1991. A fungal gene for antibiotic resistance on a dispensable (“B”) chromosome. Science 254:1773-1776. https://doi.org/10.1126/science.1763326.
15. Kellner R, Bhattacharyya A, Poppe S, Hsu TY, Brem RB, Stukenbrock EH. 2014. Expression profiling of the wheat pathogen Zymoseptoria tritici reveals genomic patterns of transcription and host-specific regulatory programs. Genome Biol Evol 6:1353-1365. https://doi.org/10.1093/gbe/evu101.
16. Schotanus K, Soyer JL, Connolly LR, Grandaubert J, Happel P, Smith KM, Freitag M, Stukenbrock EH. 2015. Histone modifications rather than the novel regional centromeres of Zymoseptoria tritici distinguish core and accessory chromosomes. Epigenetics Chromatin 8:41. https://doi.org/10.1186/s13072-015-0033-5.
17. Croll D, Zala M, McDonald BA. 2013. Breakage-fusion-bridge cycles and large insertions contribute to the rapid evolution of accessory chromosomes in a fungal pathogen. PLoS Genet 9:e1003567. https://doi.org/10.1371/journal.pgen.1003567.
18. Mehrabi R, Taga M, Kema GHJ. 2007. Electrophoretic and cytological karyotyping of the foliar wheat pathogen Mycosphaerella graminicola reveals many chromosomes with a large size range. Mycologia 99: 868-876. https://doi.org/10.3852/mycologia.99.6.868.
19. Plissonneau C, Sturchler A, Croll D. 2016. The evolution of orphan regions in genomes of a fungal pathogen of wheat. mBio 7:e01231-16. https://doi.org/10.1128/mBio.01231-16.
20. Grandaubert J, Bhattacharyya A, Stukenbrock EH. 2015. RNA-seq-based gene annotation and comparative genomics of four fungal grass pathogens in the genus Zymoseptoria identify novel orphan genes and species-specific invasions of transposable elements. G3 5:1323-1333. https://doi.org/10.1534/g3.115.017731.
21. Stukenbrock EH, Banke S, Javan-Nikkhah M, McDonald BA. 2007. Origin and domestication of the fungal wheat pathogen Mycosphaerella graminicola via sympatric speciation. Mol Biol Evol 24:398-411. https://doi.org/10.1093/molbev/msl169.
22. Stukenbrock EH, Bataillon T, Dutheil JY, Hansen TT, Li R, Zala M, McDonald BA, Wang J, Schierup MH. 2011. The making of a new pathogen: insights from comparative population genomics of the domesticated wheat pathogen Mycosphaerella graminicola and its wild sister species. Genome Res 21:2157-2166. https://doi.org/10.1101/gr.118851.110.
23. Stukenbrock EH, Jorgensen FG, Zala M, Hansen TT, McDonald BA, Schierup MH. 2010. Whole-genome and chromosome evolution associated with host adaptation and speciation of the wheat pathogen Mycosphaerella graminicola. PLoS Genet 6:e1001189. https://doi.org/10.1371/journal.pgen.1001189.
24. Croll D, McDonald BA. 2012. The accessory genome as a cradle for adaptive evolution in pathogens. PLoS Pathog 8:e1002608. https://doi.org/10.1371/journal.ppat.1002608.
25. Stewart EL, Croll D, Lendenmann MH, Sanchez-Vallet A, Hartmann FE, Palma-Guerrero J, Ma X, McDonald BA. 2016. Quantitative trait locus mapping reveals complex genetic architecture of quantitative virulence in the wheat pathogen Zymoseptoria tritici. Mol Plant Pathol. https://doi.org/10.1111/mpp.12515.
26. Davidse LC, Flach W. 1977. Differential binding of methyl benzimidazol-2-yl carbamate to fungal tubulin as a mechanism of resistance to this antimitotic agent in mutant strains of Aspergillus nidulans. J Cell Biol 72:174-193. https://doi.org/10.1083/jcb.72.1.174.
27. Ram AFJ, Klis FM. 2006. Identification of fungal cell wall mutants using susceptibility assays based on Calcofluor white and Congo red. Nat Protoc 1:2253-2256. https://doi.org/10.1038/nprot.2006.397.
28. Conover WJ, Iman RL. 1981. Rank transformations as a bridge between parametric and nonparametric statistics. Am Stat 35:124-129. https://doi.org/10.1080/00031305.1981.10479327.
29. Lee WS, Rudd JJ, Hammond-Kosack KE, Kanyuka K. 2014. Mycosphaerella graminicola LysM effector-mediated stealth pathogenesis subverts recognition through both CERK1 and CEBiP homologues in wheat. Mol Plant Microbe Interact 27:236-243. https://doi.org/10.1094/MPMI-07-13-0201-R.
30. Stukenbrock EH, Christiansen FB, Hansen TT, Dutheil JY, Schierup MH. 2012. Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species. Proc Natl Acad Sci U S A 109:10954-10959. https://doi.org/10.1073/pnas.1201403109.
31. Stukenbrock EH, Quaedvlieg W, Javan-Nikhah M, Zala M, Crous PW, McDonald BA. 2012. Zymoseptoria ardabiliae and Z. pseudotritici, two progenitor species of the Septoria tritici leaf blotch fungus Z. tritici (synonym: Mycosphaerella graminicola). Mycologia 104:1397-1407. https://doi.org/10.3852/11-374.
32. Stukenbrock EH, Dutheil JY. 2017. Comparison of fine-scale recombination maps in fungal plant pathogens reveals dynamic recombination landscapes and intragenic hotspots. bioRxiv https://www.biorxiv.org/content/early/2017/07/03/158907.
33. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
34. Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114-2120. https://doi.org/10.1093/bioinformatics/btu170.
35. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357-359. https://doi.org/10.1038/nmeth.1923.
36. 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 format and SAMtools. Bioinformatics 25:2078-2079. https://doi.org/10.1093/bioinformatics/btp352.
37. Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671-675. https://doi.org/10.1038/nmeth.2089.
38. Stewart EL, Hagerty CH, Mikaberidze A, Mundt CC, Zhong Z, McDonald BA. 2016. An improved method for measuring quantitative resistance to the wheat pathogen Zymoseptoria tritici using high-throughput automated image analysis. Phytopathology 106:782-788. https://doi.org/10.1094/PHYTO-01-16-0018-R.
39. R Core Team. 2015. R: a language and environment for statistical computing, R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org.
40. RStudio Team. 2015. RStudio: integrated development environment for R. RStudio, Boston, MA. http://www.rstudio.com/.
41. Tukey JW. 1949. Comparing individual means in the analysis of variance. Biometrics 5:99-114. https://doi.org/10.2307/3001913.