A phylogenomic assessment of ancient polyploidy and genome evolution across the poales

Genome Biology and Evolution

Volumn 8, Issue 4, 2016, Pages 1150-1164

  McKain, Michael R ^a,b   Tang, Haibao ^c,d   McNeal, Joel R ^b,e   Ayyampalayam, Saravanaraj ^b   Davis, Jerrold I ^f   Depamphilis, Claude W ^g   Givnish, Thomas J ^h   Chris Pires, J ⁱ   Stevenson, Dennis W ^j   Leebens Mack, James H ^b  

^a DONALD DANFORTH PLANT SCIENCE CENTER   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

^c FUJIAN AGRICULTURE AND FORESTRY UNIVERSITY   (China)

^d UNIVERSITY OF ARIZONA   (United States)

^e KENNESAW STATE UNIVERSITY   (United States)

^f Department of Obstetrics Gynecology   (United States)

^g PENNSYLVANIA STATE UNIVERSITY   (United States)

^h UNIVERSITY OF WISCONSIN MADISON   (United States)

ⁱ UNIVERSITY OF MISSOURI   (United States)

^j NEW YORK BOTANICAL GARDEN   (United States)

more..

Author keywords

GC content; Grasses; Monocots; Whole genome duplication

Indexed keywords

PLANT RNA; TRANSCRIPTOME;

ANGIOSPERM; GENE DUPLICATION; GENETICS; MOLECULAR EVOLUTION; ORYZA; PHYLOGENY; PLANT GENOME; POACEAE; POLYPLOIDY; SORGHUM;

ANGIOSPERMS; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENOME, PLANT; ORYZA; PHYLOGENY; POACEAE; POLYPLOIDY; RNA, PLANT; SORGHUM; TRANSCRIPTOME;

EID: 85015353177     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evw060     Document Type: Article

References (103)

1. Amborella Genome Project. 2013. The Amborella genome and the evolution of flowering plants. Science 342:9–1.
2. Andrews S. 2010. FastQC. Available from: http://www.bioinformatics.babraham.ac.uk/projects/fastqc/.
3. Barker MS, et al. 2016. On the relative abundance of autopolyploids and allopolyploids. New Phytol. 210(2):391–398.
4. Barrett CF, et al. 2016. Plastid genomes reveal support for deep phylogenetic relationships and extensive rate variation among palms and other commelinid monocots. New Phytol. 209(2):855–870.
5. Beckles DM, Smith AM, ap Rees T. 2001. A cytosolic ADP-glucose pyro-phosphorylase is a feature of graminaceous endosperms, but not of other starch-storing organs. Plant Physiol. 125:818–827.
6. Birney E, Clamp M, Durbin R. 2004. GeneWise and genomewise. Genome Res. 14:988–995.
7. Blanc G, Wolfe KH. 2004. Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16:1667–1678.
8. Bowers JE, Chapman BA, Rong J, Paterson AH. 2003. Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422:433–438.
9. Cai J, et al. 2014. The genome sequence of the orchid Phalaenopsis equestris. Nat Genet. 47:65–72.
10. Cannon SB, et al. 2015. Multiple polyploidy events in the early radiation of nodulating and nonnodulating legumes. Mol Biol Evol. 32:193–210.
11. Carels N, Bernardi G. 2000. Two classes of genes in plants. Genetics 154:1819–1825.
12. Carels N, Hatey P, Jabbari K, Bernardi G. 1998. Compositional properties of homologous coding sequences from plants. J Mol Evol. 46:45–53.
13. Chevreux B, et al. 2004. Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Res. 14:1147–1159.
14. Clément Y, Fustier M-A, Nabholz B, Glémin S. 2015. The bimodal distribution of genic GC content is ancestral to monocot species. Genome Biol Evol. 7:336–348.
15. Comparot-Moss S, Denyer K. 2009. The evolution of the starch biosynthetic pathway in cereals and other grasses. J Exp Bot. 60:2481–2492.
16. Cui L, et al. 2006. Widespread genome duplications throughout the history of flowering plants. Genome Res. 16:738–749.
17. D’Hont A, et al. 2012. The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488:213–217.
18. De Smet R, Van de Peer Y. 2012. Redundancy and rewiring of genetic networks following genome-wide duplication events. Curr Opin Plant Biol. 15:168–176.
19. Doyle JJ, et al. 2008. Evolutionary genetics of genome merger and doubling in plants. Annu Rev Genet. 42:443–461.
20. Duarte JM, et al. 2010. Identification of shared single copy nuclear genes in Arabidopsis, Populus, Vitis and Oryza and their phylogenetic utility across various taxonomic levels. BMC Evol Biol. 10:61.
21. Duret L, Galtier N. 2009. Biased gene conversion and the evolution of mammalian genomic landscapes. Annu Rev Genomics Hum Genet. 10:285–311.
22. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792–1797.
23. Edger PP, et al. 2015. The butterfly plant arms-race escalated by gene and genome duplications. Proc Natl Acad Sci U S A. 112:8362–8366.
24. Escobar JS, Glémin S, Galtier N. 2011. GC-biased gene conversion impacts ribosomal DNA evolution in vertebrates, angiosperms, and other eu-karyotes. Mol Biol Evol. 28:2561–2575.
25. Estep MC, et al. 2014. Allopolyploidy, diversification, and the Miocene grassland expansion. Proc Natl Acad Sci U S A. 111:15149–15154.
26. Eyre-Walker A, Hurst LD. 2001. The evolution of isochores. Nat Rev Genet. 2:549–555.
27. Fraley C, Raftery AE. 2002. Model-based clustering, discriminant analysis, and density estimation. J Am Stat Assoc. 97:611–631.
28. Fraley C, Raftery AE, Murphy TB, Scrucca L. 2012. mclust Version 4 for R: normal mixture modeling for model-based clustering, classification, and density estimation.
29. Freeling M. 2009. Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Annu Rev Plant Biol. 60:433–453.
30. Givnish TJ, et al. 2010. Assembling the tree of the monocotyledons: plastome sequence phylogeny and evolution of poales. Ann Missouri Bot Gard. 97:584–616.
31. Givnish TJ, et al. 2011. Phylogeny, adaptive radiation, and historical bio-geography in Bromeliaceae: insights from an eight-locus plastid phylogeny. Am J Bot. 98:872–895.
32. Glémin S, Clément Y, David J, Ressayre A. 2014. GC content evolution in coding regions of angiosperm genomes: a unifying hypothesis. Trends Genet. 30:263–270.
33. Grabherr MG, et al. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 29:644–652.
34. Grass Phylogeny Working Group. 2001. Phylogeny and subfamilial classification of the grasses (Poaceae). Ann Missouri Bot Gard. 88:373–457.
35. Grass Phylogeny Working Group II. 2012. New grass phylogeny resolves deep evolutionary relationships and discovers C4 origins. New Phytol. 193:304–312.
36. Jiao Y, et al. 2011. Ancestral polyploidy in seed plants and angiosperms. Nature 473:97–100.
37. Jiao Y, et al. 2012. A genome triplication associated with early diversification of the core eudicots. Genome Biol. 13:R3.
38. Jiao Y, Li J, Tang H, Paterson AH. 2014. Integrated syntenic and phylogenomic analyses reveal an ancient genome duplication in monocots. Plant Cell 26:2792–2802.
39. Kuhl JC, et al. 2004. A unique set of 11,008 onion expressed sequence tags reveals expressed sequence and genomic differences between the monocot orders Asparagales and Poales. Plant Cell 16:114–125.
40. Kuhl JC, et al. 2005. Comparative genomic analyses in Asparagus. Genome 48:1052–1060.
41. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10:R25.
42. Leebens-Mack J, et al. 2005. Identifying the basal angiosperm node in chloroplast genome phylogenies: sampling one’s way out of the Felsenstein zone. Mol Biol Evol. 22:1948–1963.
43. Levin DA. 1983. Polyploidy and novelty in flowering plants. Am Nat. 122:1–25.
44. Levin DA. 2002. The role of chromosomal change in plant evolution. New York: Oxford University Press.
45. Li B, Dewey CN. 2011. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12:323.
46. Li C, Li Q-G, Dunwell JM, Zhang Y-M. 2012. Divergent evolutionary pattern of starch biosynthetic pathway genes in grasses and dicots. Mol Biol Evol. 29:3227–3236.
47. Li L, Stoeckert CJ, Roos DS. 2003. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13:2178–2189.
48. Linder HP, Rudall PJ. 2005. Evolutionary history of Poales. Annu Rev Ecol Evol Syst. 36:107–124.
49. Litt A, Irish VF. 2003. Duplication and diversification in the APETALA1/FRUITFULL floral homeotic gene lineage: implications for the evolution of floral development. Genetics 165:821–833.
50. Lynch M, Conery JS. 2003. The evolutionary demography of duplicate genes. J Struct Funct Genomics. 3:35–44.
51. Maddison WP. 1997. Gene trees in species trees. Syst Biol. 46:523–536.
52. Maere S, et al. 2005. Modeling gene and genome duplications in eukary-otes. Proc Natl Acad Sci U S A. 102:5454–5459.
53. Magallón S, Castillo A. 2009. Angiosperm diversification through time. Am J Bot. 96:349–365.
54. Magallón S, Gómez-Acevedo S, Sánchez-Reyes LL, Hernández-Hernández T. 2015. A metacalibrated time-tree documents the early rise of flowering plant phylogenetic diversity. New Phytol. 207:437–453.
55. Mallet J. 2007. Hybrid speciation. Nature 446:279–283.
56. Martin M. 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17:10–12.
57. Mayrose I, et al. 2011. Recently formed polyploid plants diversify at lower rates. Science 333:1257.
58. McKain MR, et al. 2012. Phylogenomic analysis of transcriptome data elucidates co-occurrence of a paleopolyploid event and the origin of bimodal karyotypes in Agavoideae (Asparagaceae). Am J Bot. 99:397–406.
59. Ming R, et al. 2015. The pineapple genome and the evolution of CAM photosynthesis. Nat Genet. 47:1435–1442
60. Mirarab S, et al. 2014. ASTRAL: genome-scale coalescent-based species tree estimation. Bioinformatics 30:i541–i548.
61. Muyle A, Serres-Giardi L, Ressayre A, Escobar J, Glémin S. 2011. GC-biased gene conversion and selection affect GC content in the Oryza genus (rice). Mol Biol Evol. 28:2695–2706.
62. Ohno S. 1970. Evolution by gene duplication. New York: Springer-Verlag.
63. Paterson AH, Bowers JE, Chapman BA. 2004. Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc Natl Acad Sci U S A. 101:9903–9908.
64. Paterson AH, et al. 2009. The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556.
65. Paterson AH, et al. 2012. Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres. Nature 492:423–427.
66. Paterson AH, Freeling M, Tang H, Wang X. 2010. Insights from the comparison of plant genome sequences. Annu Rev Plant Biol. 61:349–372.
67. Preston JC, Christensen A, Malcomber ST, Kellogg EA. 2009. MADS-box gene expression and implications for developmental origins of the grass spikelet. Am J Bot. 96:1419–1429.
68. Preston JC, Kellogg EA. 2006. Reconstructing the evolutionary history of paralogous APETALA1/FRUITFULL-like genes in grasses (Poaceae). Genetics 174:421–437.
69. Ramsey J, Schemske DW. 1998. Pathyways, mechanisms, and rates of polyploid formation in flowering plants. Annu Rev Ecol Syst. 29:467–501.
70. Rudall P, Stuppy W. 2005. Evolution of reproductive structures in grasses (Poaceae) inferred by sister-group comparison with their putative closest living relatives, Ecdeiocoleaceae. Am J Bot. 92:1432–1443.
71. Reproductive morphology of the early-divergent grass Streptochaeta and its bearing on the homologies of the grass spikelet. Plant Syst Evol. 275:245–255.
72. Sajo MG, Rudall PJ. 2012. Morphological evolution in the graminid clade: comparative floral anatomy of the grass relatives Flagellariaceae and Joinvilleaceae. Bot J Linn Soc. 170:393–404.
73. Sajo M, Longhi-Wagner H, Rudall P. 2008. Reproductive morphology of the early-divergent grass Streptochaeta and its bearing on the homologies of the grass spikelet. Plant Syst Evol. 275:245–255.
74. Schlueter JA, et al. 2004. Mining EST databases to resolve evolutionary events in major crop species. Genome 47:868–876.
75. Serres-Giardi L, Belkhir K, David J, Glemin S. 2012. Patterns and evolution of nucleotide landscapes in seed plants. Plant Cell 24:1379–1397.
76. Shi X, et al. 2006. Nucleotide substitution pattern in rice paralogues: implication for negative correlation between the synonymous substitution rate and codon usage bias. Gene 376:199–206.
77. Smarda P, et al. 2014. Ecological and evolutionary significance of genomic GC content diversity in monocots. Proc Natl Acad Sci U S A. 111:E4096–E4102.
78. Soltis DE, et al. 2009. Polyploidy and angiosperm diversification. Am J Bot. 96:336–348.
79. Soltis DE, et al. 2014. Are polyploids really evolutionary dead-ends (again)? A critical reappraisal of Mayrose et al. (2011). New Phytol. 202:1105–1117.
80. Soreng RJ, et al. 2015. A worldwide phylogenetic classification of the Poaceae (Gramineae). J Syst Evol. 53:117–137.
81. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Nucleic Acids Res. 22:2688–2690.
82. Suyama M, Torrents D, Bork P. 2006. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 34:W609–W612.
83. Tang H, Bowers JE, Wang X, Paterson AH. 2010. Angiosperm genome comparisons reveal early polyploidy in the monocot lineage. Proc Natl Acad Sci U S A. 107:472–477.
84. Tang H, et al. 2007. Synteny and collinearity in plant genomes. Science 320:486–488.
85. Tang H, et al. 2012. Altered patterns of fractionation and exon deletions in Brassica rapa support a two-step model of paleohexaploidy. Genetics 190:1563–1574.
86. Tatarinova TV, Alexandrov NN, Bouck JB, Feldmann KA. 2010. GC3 biology in corn, rice, sorghum and other grasses. BMC Genomics 11:308.
87. Tatarinova T, Elhaik E, Pellegrini M. 2013. Cross-species analysis of genic GC3 content and DNA methylation patterns. Genome Biol Evol. 5:1443–1456.
88. Taylor JS, Raes J. 2004. Duplication and divergence: the evolution of new genes and old ideas. Annu Rev Genet. 38:615–643.
89. Tuskan Ga, et al. 2006. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604.
90. Van de Peer Y, Fawcett JA, Proost S, Sterck L, Vandepoele K. 2009. The flowering world: a tale of duplications. Trends Plant Sci. 14:680–688.
91. Vanneste K, Baele G, Maere S, Van De Peer Y. 2014. Analysis of 41 plant genomes supports a wave of successful genome duplications in association with the Cretaceous-Paleogene boundary. Genome Res. 24:1334–1347.
92. Vanneste K, Van de Peer Y, Maere S. 2012. Inference of genome duplications from age distributions revisited. Mol Biol Evol. 30:177–190.
93. Wall PK, et al. 2008. PlantTribes: a gene and gene family resource for comparative genomics in plants. Nucleic Acids Res. 36:D970–D976.
94. Wang H, Singer GaC, Hickey DA. 2004. Mutational bias affects protein evolution in flowering plants. Mol Biol Evol. 21:90–96.
95. Wang X, Shi X, Hao B, Ge S, Luo J. 2005. Duplication and DNA segmental loss in the rice genome: implications for diploidization. New Phytol. 165:937–946.
96. Wong GK-S, et al. 2002. Compositional gradients in Gramineae genes. Genome Res. 12:851–856.
97. Wu Y, Zhu Z, Ma L, Chen M. 2008. The preferential retention of starch synthesis genes reveals the impact of whole-genome duplication on grass evolution. Mol Biol Evol. 25:1003–1006.
98. Yang Y, Moore MJ, Brockington SF, Soltis DE, Wong GK. 2015. Dissecting molecular evolution in the highly diverse plant clade Caryophyllales using transcriptome sequencing. Mol Biol Evol. 32:2001–2014.
99. Yang Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 24:1586–1591.
100. Yoo M-J, Liu X, Pires JC, Soltis PS, Soltis DE. 2014. Nonadditive gene expression in polyploids. Annu Rev Genet. 48:485–517.
101. Yoo M-J, Szadkowski E, Wendel JF. 2013. Homoeolog expression bias and expression level dominance in allopolyploid cotton. Heredity 110:171–180.
102. Yu J, et al. 2005. The genomes of Oryza sativa: a history of duplications. PLoS Biol. 3:1003–1006.
103. Zwickl DJ, Hillis DM. 2002. Increased taxon sampling greatly reduces phylogenetic error. Syst Biol. 51:588–598.