Whole-Genome and Chromosome Evolution Associated with Host Adaptation and Speciation of the Wheat Pathogen
The fungus Mycosphaerella graminicola has been a pathogen of wheat since host domestication 10,000–12,000 years ago in the Fertile Crescent. The wheat-infecting lineage emerged from closely related Mycosphaerella pathogens infecting wild grasses. We use a comparative genomics approach to assess how the process of host specialization affected the genome structure of M. graminicola since divergence from the closest known progenitor species named M. graminicola S1. The genome of S1 was obtained by Illumina sequencing resulting in a 35 Mb draft genome sequence of 32X. Assembled contigs were aligned to the previously sequenced M. graminicola genome. The alignment covered >90% of the non-repetitive portion of the M. graminicola genome with an average divergence of 7%. The sequenced M. graminicola strain is known to harbor thirteen essential chromosomes plus eight dispensable chromosomes. We found evidence that structural rearrangements significantly affected the dispensable chromosomes while the essential chromosomes were syntenic. At the nucleotide level, the essential and dispensable chromosomes have evolved differently. The average synonymous substitution rate in dispensable chromosomes is considerably lower than in essential chromosomes, whereas the average non-synonymous substitution rate is three times higher. Differences in molecular evolution can be related to different transmission and recombination patterns, as well as to differences in effective population sizes of essential and dispensable chromosomes. In order to identify genes potentially involved in host specialization or speciation, we calculated ratios of synonymous and non-synonymous substitution rates in the >9,500 aligned protein coding genes. The genes are generally under strong purifying selection. We identified 43 candidate genes showing evidence of positive selection, one encoding a potential pathogen effector protein. We conclude that divergence of these pathogens was accompanied by structural rearrangements in the small dispensable chromosomes, while footprints of positive selection were present in only a small number of protein coding genes.
Vyšlo v časopise:
Whole-Genome and Chromosome Evolution Associated with Host Adaptation and Speciation of the Wheat Pathogen. PLoS Genet 6(12): e32767. doi:10.1371/journal.pgen.1001189
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1001189
Souhrn
The fungus Mycosphaerella graminicola has been a pathogen of wheat since host domestication 10,000–12,000 years ago in the Fertile Crescent. The wheat-infecting lineage emerged from closely related Mycosphaerella pathogens infecting wild grasses. We use a comparative genomics approach to assess how the process of host specialization affected the genome structure of M. graminicola since divergence from the closest known progenitor species named M. graminicola S1. The genome of S1 was obtained by Illumina sequencing resulting in a 35 Mb draft genome sequence of 32X. Assembled contigs were aligned to the previously sequenced M. graminicola genome. The alignment covered >90% of the non-repetitive portion of the M. graminicola genome with an average divergence of 7%. The sequenced M. graminicola strain is known to harbor thirteen essential chromosomes plus eight dispensable chromosomes. We found evidence that structural rearrangements significantly affected the dispensable chromosomes while the essential chromosomes were syntenic. At the nucleotide level, the essential and dispensable chromosomes have evolved differently. The average synonymous substitution rate in dispensable chromosomes is considerably lower than in essential chromosomes, whereas the average non-synonymous substitution rate is three times higher. Differences in molecular evolution can be related to different transmission and recombination patterns, as well as to differences in effective population sizes of essential and dispensable chromosomes. In order to identify genes potentially involved in host specialization or speciation, we calculated ratios of synonymous and non-synonymous substitution rates in the >9,500 aligned protein coding genes. The genes are generally under strong purifying selection. We identified 43 candidate genes showing evidence of positive selection, one encoding a potential pathogen effector protein. We conclude that divergence of these pathogens was accompanied by structural rearrangements in the small dispensable chromosomes, while footprints of positive selection were present in only a small number of protein coding genes.
Zdroje
1. KohnLM
2005 Mechanisms of Fungal Speciation. Annual Review of Phytopathology 43 279 308
2. ScannellDR
ByrneKP
GordonJL
WongS
WolfeKH
2006 Multiple rounds of speciation associated with reciprocal gene loss in polyploid yeasts. Nature 440 341 345
3. GalaganJE
CalvoSE
CuomoC
MaL-J
WortmanJR
2005 Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438 1105 1115
4. Banke SMB
2005 Migration patterns among global populations of the pathogenic fungus Mycosphaerella graminicola. Molecular Ecology 14 1881 1896
5. StukenbrockEH
BankeS
Javan-NikkhahM
McDonaldBA
2007 Origin and Domestication of the Fungal Wheat Pathogen Mycosphaerella graminicola via Sympatric Speciation. Mol Biol Evol 24 398 411
6. GoodwinSBBMBS
DhillonB
WittenbergA
CraneCF
submitted Finished Genome of Mycosphaerella graminicola Reveals Stealth Pathogenesis and Extreme Plasticity
7. MehrabiR
TagaM
KemaGHJ
2007 Electrophoretic and cytological karyotyping of the foliar wheat pathogen Mycosphaerella graminicola reveals many chromosomes with a large size range. Mycologia 99 868 876
8. WittenbergAHJ
van der LeeTAJ
Ben M'BarekS
WareSB
GoodwinSB
2009 Meiosis Drives Extraordinary Genome Plasticity in the Haploid Fungal Plant Pathogen Mycosphaerella graminicola. PLoS ONE 4 e5863 doi:10.1371/journal.pone.0005863
9. MiaoV
CovertS
VanEttenH
1991 A fungal gene for antibiotic resistance on a dispensable (“B”) chromosome. Science 254 1773 1776
10. HanY
LiuX
BennyU
KistlerHC
VanEttenHD
2001 Genes determining pathogenicity to pea are clustered on a supernumerary chromosome in the fungal plant pathogen Nectria haematococca. The Plant Journal 25 305 314
11. KabackD
GuacciV
BarberD
MahonJ
1992 Chromosome size-dependent control of meiotic recombination. Science 256 228 232
12. LitiG
CarterDM
MosesAM
WarringerJ
PartsL
2009 Population genomics of domestic and wild yeasts. Nature 458 337 341
13. ButlerG
RasmussenMD
LinMF
SantosMAS
SakthikumarS
2009 Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459 657 662
14. DettmanJR
AndersonJB
KohnLM
2010 Genome-wide investigation of reproductive isolation in experimental lineages and natural species of Neurospora: Identifying candidate regions by microarray-based genotyping and mapping. Evolution 64 694 709
15. ZerbinoDR
BirneyE
2008 Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Research 18 821 829
16. EmanuelssonO
BrunakS
von HeijneG
NielsenH
2007 Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protocols 2 953 971
17. WaalwijkC
MendesO
VerstappenECP
de WaardMA
KemaGHJ
2002 Isolation and Characterization of the Mating-Type Idiomorphs from the Wheat Septoria Leaf Blotch Fungus Mycosphaerella graminicola. Fungal Genetics and Biology 35 277 286
18. McDonaldBA
MartinezJP
1990 Chromosome length polymorphisms in a Septuria tritici population. Cun Genet 19 265 271
19. BurtDW
BruleyC
DunnIC
JonesCT
RamageA
1999 The dynamics of chromosome evolution in birds and mammals. Nature 402 411 413
20. CoghlanA
WolfeKH
2002 Fourfold Faster Rate of Genome Rearrangement in Nematodes Than in Drosophila. Genome Research 12 857 867
21. SharakhovIV
SerazinAC
GrushkoOG
DanaA
LoboN
2002 Inversions and Gene Order Shuffling in Anopheles gambiae and A. funestus. Science 298 182 185
22. PolákováS
BlumeC
ZárateJAI
MentelM
Jarck-RambergD
2009 Formation of new chromosomes as a virulence mechanism in yeast Candida glabrata. Proceedings of the National Academy of Sciences 106 2688 2693
23. CuomoCA
GuldenerU
XuJ-R
TrailF
TurgeonBG
2007 The Fusarium graminearum Genome Reveals a Link Between Localized Polymorphism and Pathogen Specialization. Science 317 1400 1402
24. HeyJ
NielsenR
2004 Multilocus Methods for Estimating Population Sizes, Migration Rates and Divergence Time, With Applications to the Divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167 747 760
25. HeinJ
SchierupMH
WiufC
2005 Gene Genealogies, Variation and Evolution. London/New York/Oxford Oxford University Press
26. LynchM
SungW
MorrisK
CoffeyN
LandryCR
2008 A genome-wide view of the spectrum of spontaneous mutations in yeast. Proceedings of the National Academy of Sciences 105 9272 9277
27. CamachoJPM
SharbelTF
BeukeboomLW
2000 B-chromosome evolution. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences 355 163 178
28. WinzelerEA
Castillo-DavisCI
OshiroG
LiangD
RichardsDR
2003 Genetic Diversity in Yeast Assessed With Whole-Genome Oligonucleotide Arrays. Genetics 163 79 89
29. DujonB
ShermanD
FischerG
DurrensP
CasaregolaS
2004 Genome evolution in yeasts. Nature 430 35 44
30. MenkisA
JacobsonDJ
GustafssonT
JohannessonH
2008 The Mating-Type Chromosome in the Filamentous Ascomycete Neurospora tetrasperma Represents a Model for Early Evolution of Sex Chromosomes. PLoS Genet 4 e1000030 doi:10.1371/journal.pgen.1000030
31. VotintsevaAA
FilatovDA
2009 ‘Evolutionary Strata’ in a Small Mating Type-specific Region of the Smut Fungus Microbotryum violaceum. Genetics 182 1391 1396
32. ArraianoLS
BradingPA
BrownJKM
2001 A detached seedling leaf technique to study resistance to Mycosphaerella graminicola (anamorph Septoria tritici) in wheat. Plant Pathology 50 339 346
33. SchwartzS
KentWJ
SmitA
ZhangZ
BaertschR
2003 Human-Mouse Alignments with BLASTZ. Genome Research 13 103 107
34. BlanchetteM
KentWJ
RiemerC
ElnitskiL
SmitAFA
2004 Aligning Multiple Genomic Sequences With the Threaded Blockset Aligner. Genome Research 14 708 715
35. KemaGHJ
GoodwinSB
HamzaS
VerstappenECP
CavalettoJR
Van der LeeTAJ
Hagenaar-de WeerdtM
BonantsPJM
WaalwijkC
2003 Gene hunting in Mycosphaerella graminicola. Asilomar, California, USA In: Proc 22nd Fungal Genet. Conf. 252
36. SinhaO
1995 Dual culture: Fungi.
RH SinghUS
In Molecular Methods in Plant Pathology Boca Raton, FL, USA CRC Press 289 300
37. PriceAL
JonesNC
PevznerPA
2005 De novo identification of repeat families in large genomes. Bioinformatics 21 351 358
38. NeiM
GojoboriT
1986 Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3 418 426
39. YangZ
NielsenR
2000 Estimating Synonymous and Nonsynonymous Substitution Rates Under Realistic Evolutionary Models. Mol Biol Evol 17 32 43
40. YangZ
2007 PAML 4: Phylogenetic Analysis by Maximum Likelihood. Mol Biol Evol 24 1586 1591
41. MenneKML
HermjakobH
ApweilerR
2000 A comparison of signal sequence prediction methods using a test set of signal peptides. Bioinformatics 16 741 742
42. RozasJ
Sanchez-DelBarrioJC
MesseguerX
RozasR
2003 DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19 2496 2497
43. ZhanJ
KemaGHJ
WaalwijkC
McDonaldBA
2002 Distribution of mating type alleles in the wheat pathogen Mycosphaerella graminicola over spatial scales from lesions to continents. Fungal Genetics and Biology 36 128 136
44. BankeS
PeschonA
McDonaldBA
2004 Phylogenetic analysis of globally distributed Mycosphaerella graminicola populations based on three DNA sequence loci. Fungal Genetics and Biology 41 226 238
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2010 Číslo 12
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
Najčítanejšie v tomto čísle
- Functional Comparison of Innate Immune Signaling Pathways in Primates
- Expression of Linear and Novel Circular Forms of an -Associated Non-Coding RNA Correlates with Atherosclerosis Risk
- Genome-Wide Interrogation of Mammalian Stem Cell Fate Determinants by Nested Chromosome Deletions
- Histone H2A C-Terminus Regulates Chromatin Dynamics, Remodeling, and Histone H1 Binding