#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Rapidly Evolving Genes Are Key Players in Host Specialization and Virulence of the Fungal Wheat Pathogen ()


Zymoseptoria spp provides a unique model system to study the underlying genetics of host specialization of plant pathogens. Closely related Zymoseptoria species, including the prominent wheat pathogen Z. tritici, have recently specialized to distinct grass hosts. Positively selected substitutions have played a central role in the acquisition of new host specificities. We have identified a small set of genes showing signatures of positive selection. We demonstrate that three of these four candidate genes play an important role during host infection. Two mutants of Z. tritici were impaired in virulence; a third mutant showed a hypervirulent phenotype. New protein specificities not only include changes at the amino acid sequence level but also at the level of the protein structure. We conducted a gene replacement experiment to test if mutant phenotypes in Z. tritici could be complemented by the insertion of orthologous genes from the two closely related species Z. pseudotritici and Z. ardabiliae. For two genes, we confirm that the species-specific protein changes are essential for proper protein functioning in Z. tritici; key traits involved in the evolution of virulence and host specificity of this prominent pathogen can be characterized via a combination of evolutionary predictions and functional analyses.


Vyšlo v časopise: Rapidly Evolving Genes Are Key Players in Host Specialization and Virulence of the Fungal Wheat Pathogen (). PLoS Pathog 11(7): e32767. doi:10.1371/journal.ppat.1005055
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1005055

Souhrn

Zymoseptoria spp provides a unique model system to study the underlying genetics of host specialization of plant pathogens. Closely related Zymoseptoria species, including the prominent wheat pathogen Z. tritici, have recently specialized to distinct grass hosts. Positively selected substitutions have played a central role in the acquisition of new host specificities. We have identified a small set of genes showing signatures of positive selection. We demonstrate that three of these four candidate genes play an important role during host infection. Two mutants of Z. tritici were impaired in virulence; a third mutant showed a hypervirulent phenotype. New protein specificities not only include changes at the amino acid sequence level but also at the level of the protein structure. We conducted a gene replacement experiment to test if mutant phenotypes in Z. tritici could be complemented by the insertion of orthologous genes from the two closely related species Z. pseudotritici and Z. ardabiliae. For two genes, we confirm that the species-specific protein changes are essential for proper protein functioning in Z. tritici; key traits involved in the evolution of virulence and host specificity of this prominent pathogen can be characterized via a combination of evolutionary predictions and functional analyses.


Zdroje

1. Giraud T, Gladieux P, Gavrilets S (2010) Linking the emergence of fungal plant diseases with ecological speciation. Trends Ecol Evol 25: 387–395. doi: 10.1016/j.tree.2010.03.006 20434790

2. Stukenbrock EH (2013) Evolution, selection and isolation: a genomic view of speciation in fungal plant pathogens. New Phytol.

3. Raffaele S, Farrer RA, Cano LM, Studholme DJ, MacLean D, et al. (2010) Genome evolution following host jumps in the Irish potato famine pathogen lineage. Science 330: 1540–1543. doi: 10.1126/science.1193070 21148391

4. Schardl CL, Young CA, Hesse U, Amyotte SG, Andreeva K, et al. (2013) Plant-Symbiotic Fungi as Chemical Engineers: Multi-Genome Analysis of the Clavicipitaceae Reveals Dynamics of Alkaloid Loci. PLoS Genet 9.

5. Stukenbrock EH, McDonald BA (2007) Geographical variation and positive diversifying selection in the host-specific toxin SnToxA. Mol Plant Pathol 8: 321–332. doi: 10.1111/j.1364-3703.2007.00396.x 20507502

6. Brunner PC, Torriani SFF, Croll D, Stukenbrock EH, McDonald BA (2013) Coevolution and life cycle specialization of plant cell wall degrading enzymes in a hemibiotrophic pathogen. Mol Biol Evol 30: 1337–1347. doi: 10.1093/molbev/mst041 23515261

7. Ponomarenko A, Goodwin SB, Kema GHJ (2011) Septoria tritici blotch (STB) of wheat Septoria tritici blotch (STB) of wheat. Plant Heal Instr: 1–7.

8. Stukenbrock EH, Bataillon T, Dutheil JY, Hansen TT, Li R, et al. (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. doi: 10.1101/gr.118851.110 21994252

9. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3: 418–426. 3444411

10. Makde RD, England JR, Yennawar HP, Tan S (2010) Structure of RCC1 chromatin factor bound to the nucleosome core particle. Nature 467: 562–566. doi: 10.1038/nature09321 20739938

11. Williamson MP (1994) The structure and function of proline-rich regions in proteins. Biochem J 297: 249–260. 8297327

12. Stukenbrock EH, McDonald BA (2008) The origins of plant pathogens in agro-ecosystems. Annu Rev Phytopathol 46: 75–100. doi: 10.1146/annurev.phyto.010708.154114 18680424

13. Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586–1591. 17483113

14. Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340: 783–795. 15223320

15. Mikkelsen L, Sarrocco S, Lübeck M, Jensen DF (2003) Expression of the red fluorescent protein DsRed-Express in filamentous ascomycete fungi. FEMS Microbiol Lett 223: 135–139. 12799012

16. Marshall R, Kombrink A, Motteram J, Loza-Reyes E, Lucas J, et al. (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. doi: 10.1104/pp.111.176347 21467214

17. De Jonge R, van Esse HP, Kombrink A, Shinya T, Desaki Y, et al. (2010) Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329: 953–955. doi: 10.1126/science.1190859 20724636

18. Roy A, Kucukural A, Zhang Y (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5: 725–738. doi: 10.1038/nprot.2010.5 20360767

19. Stergiopoulos I, De Kock MJD, Lindhout P, De Wit PJGM (2007) Allelic variation in the effector genes of the tomato pathogen Cladosporium fulvum reveals different modes of adaptive evolution. Mol Plant Microbe Interact 20: 1271–1283. 17918629

20. Dong S, Stam R, Cano LM, Song J, Sklenar J, et al. (2014) Effector specialization in a lineage of the Irish potato famine pathogen. Science 343: 552–555. doi: 10.1126/science.1246300 24482481

21. Aguileta G, Lengelle J, Chiapello H, Giraud T, Viaud M, et al. (2012) Genes under positive selection in a model plant pathogenic fungus, Botrytis. Infect Genet Evol 12: 987–996. doi: 10.1016/j.meegid.2012.02.012 22406010

22. Gummer JPA, Trengove RD, Oliver RP, Solomon PS (2013) Dissecting the role of G-protein signalling in primary metabolism in the wheat pathogen Stagonospora nodorum. Microbiology 159: 1972–1985. doi: 10.1099/mic.0.067009-0 23744904

23. Calvo AM, Wilson RA, Bok JW, Keller NP (2002) Relationship between secondary metabolism and fungal development. Microbiol Mol Biol Rev 66: 447–459, table of contents. 12208999

24. Baldwin TK, Winnenburg R, Urban M, Rawlings C, Koehler J, et al. (2006) The pathogen-host interactions database (PHI-base) provides insights into generic and novel themes of pathogenicity. Mol Plant Microbe Interact 19: 1451–1462. 17153929

25. Degrassi G, Devescovi G, Bigirimana J, Venturi V (2010) Xanthomonas oryzae pv. oryzae XKK.12 contains an AroQgamma chorismate mutase that is involved in rice virulence. Phytopathology 100: 262–270. doi: 10.1094/PHYTO-100-3-0262 20128700

26. Kamper J, Kahmann R, Bolker M, Ma L- JJ, Brefort T, et al. (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444: 97–101. 17080091

27. Meir S, Amsellem Z, Al-Ahmad H, Safran E, Gressel J (2009) Transforming a NEP1 toxin gene into two Fusarium spp. to enhance mycoherbicide activity on Orobanche—failure and success. Pest Manag Sci 65: 588–595. doi: 10.1002/ps.1736 19291699

28. Aebi M, Clark MW, Vijayraghavan U, Abelson J (1990) A yeast mutant, PRP20, altered in mRNA metabolism and maintenance of the nuclear structure, is defective in a gene homologous to the human gene RCC1 which is involved in the control of chromosome condensation. Mol Gen Genet 224: 72–80. http://www.ncbi.nlm.nih.gov/pubmed/2277633. Accessed 13 November 2014. 2277633

29. Kadowaki T, Goldfarb D, Spitz LM, Tartakoff AM, Ohno M (1993) Regulation of RNA processing and transport by a nuclear guanine nucleotide release protein and members of the Ras superfamily. EMBO J 12: 2929–2937. 7687541

30. Clark KL, Sprague GF (1989) Yeast pheromone response pathway: characterization of a suppressor that restores mating to receptorless mutants. Mol Cell Biol 9: 2682–2694. 2548085

31. Sazer S, Nurse P (1994) A fission yeast RCC1-related protein is required for the mitosis to interphase transition. EMBO J 13: 606–615. 8313905

32. Baltrus DA, Nishimura MT, Romanchuk A, Chang JH, Mukhtar MS, et al. (2011) Dynamic evolution of pathogenicity revealed by sequencing and comparative genomics of 19 Pseudomonas syringae isolates. PLoS Pathog 7: e1002132. doi: 10.1371/journal.ppat.1002132 21799664

33. Goodwin SB, Ben M’barek S, Dhillon B, Wittenberg AH, Crane CF, et al. (2011) Finished Genome of the Fungal Wheat Pathogen Mycosphaerella graminicola Reveals Dispensome Structure, Chromosome Plasticity, and Stealth Pathogenesis. PLoS Genet 7: e1002070. doi: 10.1371/journal.pgen.1002070 21695235

34. Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27: 221–224. doi: 10.1093/molbev/msp259 19854763

35. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792–1797. 15034147

36. Yang Z, Nielsen R (1998) Synonymous and nonsynonymous rate variation in nuclear genes of mammals. J Mol Evol 46: 409–418. 9541535

37. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, et al. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59: 307–321. doi: 10.1093/sysbio/syq010 20525638

38. Guex N, Peitsch MC, Schwede T (2009) Automated comparative protein structure modeling with SWISS-MODEL and Swiss-PdbViewer: a historical perspective. Electrophoresis 30 Suppl 1: S162–S173. doi: 10.1002/elps.200900140 19517507

39. Schrödinger, LLC (2010) The {PyMOL} Molecular Graphics System, Version~1.3r1.

40. Kema GH, van Silfhout CH (1997) Genetic Variation for Virulence and Resistance in the Wheat-Mycosphaerella graminicola Pathosystem III. Comparative Seedling and Adult Plant Experiments. Phytopathology 87: 266–272. 18945169

41. Bowler J, Scott E, Tailor R, Scalliet G, Ray J, et al. (2010) Technical advance New capabilities for Mycosphaerella graminicola research. Mol Plant Pathol 11: 691–704. doi: 10.1111/j.1364-3703.2010.00629.x 20696006

42. Shuldiner AR, Tanner K, Scott LA, Moore CA, Roth J (1991) Ligase-free subcloning: a versatile method to subclone polymerase chain reaction (PCR) products in a single day. Anal Biochem 194: 9–15. 1651068

43. Gibson DG, Young L, Chuang R-Y, Venter JC, Hutchison CA, et al. (2009) Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods 6: 343–345. doi: 10.1038/nmeth.1318 19363495

44. Zwiers LH, De Waard MA (2001) Efficient Agrobacterium tumefaciens-mediated gene disruption in the phytopathogen Mycosphaerella graminicola. Curr Genet 39: 388–393. 11525415

45. Sambrook J, Russell DW, Laboratory CSH (2001) Molecular cloning: a laboratory manual. 3rd. ed. Cold Spring Harbor, N. Y: Cold Spring Harbor Laboratory.

46. Southern EM (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98: 503–517. 1195397

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2015 Číslo 7
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#