Switchgrass Genomic Diversity, Ploidy, and Evolution: Novel Insights from a Network-Based SNP Discovery Protocol

English version České info

Switchgrass (Panicum virgatum L.) is a perennial grass that has been designated as an herbaceous model biofuel crop for the United States of America. To facilitate accelerated breeding programs of switchgrass, we developed both an association panel and linkage populations for genome-wide association study (GWAS) and genomic selection (GS). All of the 840 individuals were then genotyped using genotyping by sequencing (GBS), generating 350 GB of sequence in total. As a highly heterozygous polyploid (tetraploid and octoploid) species lacking a reference genome, switchgrass is highly intractable with earlier methodologies of single nucleotide polymorphism (SNP) discovery. To access the genetic diversity of species like switchgrass, we developed a SNP discovery pipeline based on a network approach called the Universal Network-Enabled Analysis Kit (UNEAK). Complexities that hinder single nucleotide polymorphism discovery, such as repeats, paralogs, and sequencing errors, are easily resolved with UNEAK. Here, 1.2 million putative SNPs were discovered in a diverse collection of primarily upland, northern-adapted switchgrass populations. Further analysis of this data set revealed the fundamentally diploid nature of tetraploid switchgrass. Taking advantage of the high conservation of genome structure between switchgrass and foxtail millet (Setaria italica (L.) P. Beauv.), two parent-specific, synteny-based, ultra high-density linkage maps containing a total of 88,217 SNPs were constructed. Also, our results showed clear patterns of isolation-by-distance and isolation-by-ploidy in natural populations of switchgrass. Phylogenetic analysis supported a general south-to-north migration path of switchgrass. In addition, this analysis suggested that upland tetraploid arose from upland octoploid. All together, this study provides unparalleled insights into the diversity, genomic complexity, population structure, phylogeny, phylogeography, ploidy, and evolutionary dynamics of switchgrass.

Vyšlo v časopise: Switchgrass Genomic Diversity, Ploidy, and Evolution: Novel Insights from a Network-Based SNP Discovery Protocol. PLoS Genet 9(1): e32767. doi:10.1371/journal.pgen.1003215
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003215

Souhrn

Zdroje

1. Martínez-ReynaJM, VogelKP (2002) Incompatibility Systems in Switchgrass. Crop Sci 42: 1800–1805.

2. CostichDE, FriebeB, SheehanMJ, CaslerMD, BucklerES (2010) Genome-size Variation in Switchgrass (Panicum virgatum): Flow Cytometry and Cytology Reveal Rampant Aneuploidy. Plant Gen 3: 130–141.

3. BennettMD, BhandolP, LeitchIJ (2000) Nuclear DNA Amounts in Angiosperms and their Modern Uses—807 New Estimates. Annals of Botany 86: 859–909.

4. ElshireRJ, GlaubitzJC, SunQ, PolandJA, KawamotoK, et al. (2011) A Robust, Simple Genotyping-by-Sequencing (GBS) Approach for High Diversity Species. PLoS ONE 6: e19379 doi:10.1371/journal.pone.0019379.

5. AltshulerD, PollaraVJ, CowlesCR, Van EttenWJ, BaldwinJ, et al. (2000) An SNP map of the human genome generated by reduced representation shotgun sequencing. Nature 407: 513–516.

6. DaveyJW, HohenlohePA, EtterPD, BooneJQ, CatchenJM, et al. (2011) Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Rev Genet 12: 499–510.

7. BairdNA, EtterPD, AtwoodTS, CurreyMC, ShiverAL, et al. (2008) Rapid SNP Discovery and Genetic Mapping Using Sequenced RAD Markers. PLoS ONE 3: e3376 doi:10.1371/journal.pone.0003376.

8. van OrsouwNJ, HogersRCJ, JanssenA, YalcinF, SnoeijersS, et al. (2007) Complexity Reduction of Polymorphic Sequences (CRoPS): A Novel Approach for Large-Scale Polymorphism Discovery in Complex Genomes. PLoS ONE 2: e1172 doi:10.1371/journal.pone.0001172.

9. AndolfattoP, DavisonD, ErezyilmazD, HuTT, MastJ, et al. (2011) Multiplexed shotgun genotyping for rapid and efficient genetic mapping. Genome Research

10. PolandJA, BrownPJ, SorrellsME, JanninkJ-L (2012) Development of High-Density Genetic Maps for Barley and Wheat Using a Novel Two-Enzyme Genotyping-by-Sequencing Approach. PLoS ONE 7: e32253 doi:10.1371/journal.pone.0032253.

11. HanseyCN, VaillancourtB, SekhonRS, de LeonN, KaepplerSM, et al. (2012) Maize (Zea mays L.) Genome Diversity as Revealed by RNA-Sequencing. PLoS ONE 7: e33071 doi:10.1371/journal.pone.0033071.

12. GoreMA, ChiaJ-M, ElshireRJ, SunQ, ErsozES, et al. (2009) A First-Generation Haplotype Map of Maize. Science 326: 1115–1117.

13. Van TassellCP, SmithTPL, MatukumalliLK, TaylorJF, SchnabelRD, et al. (2008) SNP discovery and allele frequency estimation by deep sequencing of reduced representation libraries. Nat Meth 5: 247–252.

14. RamosAM, CrooijmansRPMA, AffaraNA, AmaralAJ, ArchibaldAL, et al. (2009) Design of a High Density SNP Genotyping Assay in the Pig Using SNPs Identified and Characterized by Next Generation Sequencing Technology. PLoS ONE 4: e6524 doi:10.1371/journal.pone.0006524.

15. HohenlohePA, BasshamS, EtterPD, StifflerN, JohnsonEA, et al. (2010) Population Genomics of Parallel Adaptation in Threespine Stickleback using Sequenced RAD Tags. PLoS Genet 6: e1000862 doi:10.1371/journal.pgen.1000862.

16. HytenD, CannonS, SongQ, WeeksN, FickusE, et al. (2010) High-throughput SNP discovery through deep resequencing of a reduced representation library to anchor and orient scaffolds in the soybean whole genome sequence. BMC Genomics 11: 38.

17. WiedmannR, SmithT, NonnemanD (2008) SNP discovery in swine by reduced representation and high throughput pyrosequencing. BMC Genetics 9: 81.

18. SanchezC, SmithT, WiedmannR, VallejoR, SalemM, et al. (2009) Single nucleotide polymorphism discovery in rainbow trout by deep sequencing of a reduced representation library. BMC Genomics 10: 559.

19. HytenD, SongQ, FickusE, QuigleyC, LimJ-S, et al. (2010) High-throughput SNP discovery and assay development in common bean. BMC Genomics 11: 475.

20. YouF, HuoN, DealK, GuY, LuoM-C, et al. (2011) Annotation-based genome-wide SNP discovery in the large and complex Aegilops tauschii genome using next-generation sequencing without a reference genome sequence. BMC Genomics 12: 59.

21. ChutimanitsakunY, NipperR, Cuesta-MarcosA, CistueL, CoreyA, et al. (2011) Construction and application for QTL analysis of a Restriction Site Associated DNA (RAD) linkage map in barley. BMC Genomics 12: 4.

22. McMullenMD, KresovichS, VilledaHS, BradburyP, LiH, et al. (2009) Genetic Properties of the Maize Nested Association Mapping Population. Science 325: 737–740.

23. SchnablePS, WareD, FultonRS, SteinJC, WeiF, et al. (2009) The B73 Maize Genome: Complexity, Diversity, and Dynamics. Science 326: 1112–1115.

24. ChiaJ-M, SongC, BradburyPJ, CostichD, de LeonN, et al. (2012) Maize HapMap2 identifies extant variation from a genome in flux. Nat Genet 44: 803–807.

25. StoneEA, AyrolesJF (2009) Modulated Modularity Clustering as an Exploratory Tool for Functional Genomic Inference. PLoS Genet 5: e1000479 doi:10.1371/journal.pgen.1000479.

26. CheemaJ, DicksJ (2009) Computational approaches and software tools for genetic linkage map estimation in plants. Briefings in Bioinformatics 10: 595–608.

27. GrattapagliaD, SederoffR (1994) Genetic Linkage Maps of Eucalyptus grandis and Eucalyptus urophylla Using a Pseudo-Testcross: Mapping Strategy and RAPD Markers. Genetics 137: 1121–1137.

28. Goldberg DE (1989) Genetics algorithms in search, optimization and machine learning/David E. Goldberg. Reading, Massachusetts: Addison Wesley Longman, Inc.

29. DorigoM, GambardellaLM (1997) Ant colony system: a cooperative learning approach to the traveling salesman problem. IEEE Transactions on Evolutionary Computation 1: 53–66.

30. BennetzenJL, FreelingM (1997) The Unified Grass Genome: Synergy in Synteny. Genome Research 7: 301–306.

31. BrutnellTP, WangL, SwartwoodK, GoldschmidtA, JacksonD, et al. (2010) Setaria viridis: A Model for C4 Photosynthesis. The Plant Cell Online 22: 2537–2544.

32. DoustAN, KelloggEA, DevosKM, BennetzenJL (2009) Foxtail Millet: A Sequence-Driven Grass Model System. Plant Physiology 149: 137–141.

33. BennetzenJL, SchmutzJ, WangH, PercifieldR, HawkinsJ, et al. (2012) Reference genome sequence of the model plant Setaria. Nat Biotech 30: 555–561.

34. BernardoR, YuJ (2007) Prospects for Genomewide Selection for Quantitative Traits in Maize. Crop Sci 47: 1082–1090.

35. Casler MD (2012) Switchgrass Breeding, Genetics, and Genomics. In: Monti A, editor. Switchgrass, Green Energy and Technology: Springer London. pp. 29–53.

36. CaslerMD, BrummerEC (2008) Theoretical Expected Genetic Gains for Among-and-Within-Family Selection Methods in Perennial Forage Crops. Crop Sci 48: 890–902.

37. EmersonKJ, MerzCR, CatchenJM, HohenlohePA, CreskoWA, et al. (2010) Resolving postglacial phylogeography using high-throughput sequencing. Proceedings of the National Academy of Sciences 107: 16196–16200.

38. AmoresA, CatchenJ, FerraraA, FontenotQ, PostlethwaitJH (2011) Genome Evolution and Meiotic Maps by Massively Parallel DNA Sequencing: Spotted Gar, an Outgroup for the Teleost Genome Duplication. Genetics 188: 799–808.

39. PfenderW, SahaM, JohnsonE, SlabaughM (2011) Mapping with RAD (restriction-site associated DNA) markers to rapidly identify QTL for stem rust resistance in Lolium perenne. TAG Theoretical and Applied Genetics 122: 1467–1480.

40. CatchenJM, AmoresA, HohenloheP, CreskoW, PostlethwaitJH (2011) Stacks: Building and Genotyping Loci De Novo From Short-Read Sequences. G3: Genes, Genomes, Genetics 1: 171–182.

41. PatersonAH, BowersJE, ChapmanBA (2004) Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proceedings of the National Academy of Sciences of the United States of America 101: 9903–9908.

42. SchnableJC, SpringerNM, FreelingM (2011) Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss. Proceedings of the National Academy of Sciences 108: 4069–4074.

43. SpringerNM, YingK, FuY, JiT, YehC-T, et al. (2009) Maize Inbreds Exhibit High Levels of Copy Number Variation (CNV) and Presence/Absence Variation (PAV) in Genome Content. PLoS Genet 5: e1000734 doi:10.1371/journal.pgen.1000734.

44. Swanson-WagnerRA, EichtenSR, KumariS, TiffinP, SteinJC, et al. (2010) Pervasive gene content variation and copy number variation in maize and its undomesticated progenitor. Genome Research 20: 1689–1699.

45. BrunnerS, FenglerK, MorganteM, TingeyS, RafalskiA (2005) Evolution of DNA Sequence Nonhomologies among Maize Inbreds. The Plant Cell Online 17: 343–360.

46. FuH, DoonerHK (2002) Intraspecific violation of genetic colinearity and its implications in maize. Proceedings of the National Academy of Sciences 99: 9573–9578.

47. OkadaM, LanzatellaC, SahaMC, BoutonJ, WuR, et al. (2010) Complete Switchgrass Genetic Maps Reveal Subgenome Collinearity, Preferential Pairing and Multilocus Interactions. Genetics 185: 745–760.

48. HuangS, SuX, HaselkornR, GornickiP (2003) Evolution of switchgrass (Panicum virgatum L.) based on sequences of the nuclear gene encoding plastid acetyl-CoA carboxylase. Plant Science 164: 43–49.

49. YoungHA, LanzatellaCL, SarathG, TobiasCM (2011) Chloroplast Genome Variation in Upland and Lowland Switchgrass. PLoS ONE 6: e23980 doi:10.1371/journal.pone.0023980.

50. MorrisGP, GrabowskiPP, BorevitzJO (2011) Genomic diversity in switchgrass (Panicum virgatum): from the continental scale to a dune landscape. Molecular Ecology 20: 4938–4952.

51. ZhangY, ZalapaJ, JakubowskiA, PriceD, AcharyaA, et al. (2011) Post-glacial evolution of Panicum virgatum: centers of diversity and gene pools revealed by SSR markers and cpDNA sequences. Genetica 139: 933–948.

52. ZalapaJ, PriceD, KaepplerS, TobiasC, OkadaM, et al. (2011) Hierarchical classification of switchgrass genotypes using SSR and chloroplast sequences: ecotypes, ploidies, gene pools, and cultivars. TAG Theoretical and Applied Genetics 122: 805–817.

53. CaslerMD, StendalCA, KapichL, VogelKP (2007) Genetic Diversity, Plant Adaptation Regions, and Gene Pools for Switchgrass. Crop Sci 47: 2261–2273.

54. BicknellRA, KoltunowAM (2004) Understanding Apomixis: Recent Advances and Remaining Conundrums. The Plant Cell Online 16: S228–S245.

55. CaslerMD, TobiasCM, KaepplerSM, BuellCR, WangZ-Y, et al. (2011) The Switchgrass Genome: Tools and Strategies. Plant Gen 4: 273–282.

56. AltschulSF, GishW, MillerW, MyersEW, LipmanDJ (1990) Basic local alignment search tool. Journal of Molecular Biology 215: 403–410.

57. BradburyPJ, ZhangZ, KroonDE, CasstevensTM, RamdossY, et al. (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23: 2633–2635.

58. TamuraK, PetersonD, PetersonN, StecherG, NeiM, et al. (2011) MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Molecular Biology and Evolution 28: 2731–2739.