Polyploidy-associated genome modifications during land plant evolution

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 369, Issue 1648, 2014, Pages

  Jiao, Yuannian ^a   Paterson, Andrew H ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

Ancestral gene content; Gene family gain and loss; Genome modification; Polyploidy

Indexed keywords

ANCESTRY; ANGIOSPERM; EVOLUTIONARY BIOLOGY; FUNCTIONAL ROLE; GENETIC VARIATION; GENOME; GENOMICS; POLYPLOIDY; TERRESTRIAL ENVIRONMENT;

EID: 84902959559     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2013.0355     Document Type: Review

References (113)

1. Galitski T, Saldanha AJ, Styles CA, Lander ES, Fink GR. 1999 Ploidy regulation of gene expression. Science 285, 251-254. (doi:10.1126/science.285.5425.251)
2. Hughes T et al. 2000 Widespread aneuploidy revealed by DNA microarray expression profiling. Nat. Genet. 25, 333-337. (doi:10.1038/77116)
3. Arrigo N, Barker MS. 2012 Rarely successful polyploids and their legacy in plant genomes. Curr. Opin. Plant Biol. 15, 140-146. (doi:10.1016/j.pbi.2012.03.010)
4. Ohno S. 1970 Evolution by gene duplication. Berlin, Germany: Springer.
5. Stephens S. 1951 Possible significance of duplications in evolution. Adv. Genet. 4, 247-265. (doi:10.1016/S0065-2660(08)60237-0)
6. Comai L. 2005 The advantages and disadvantages of being polyploid. Nat. Rev. Genet. 6, 836-846. (doi:10.1038/nrg1711)
7. Freeling M, Thomas BC. 2006 Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. Genome Res. 16, 805-814. (doi:10.1101/gr.3681406)
8. Muntzing A. 1936 The evolutionary significance of autopolyploidy. Hereditas 21, 363-378. (doi:10.1111/j.1601-5223.1936.tb03204.x)
9. Love A, Love D. 1949 The geobotanical significance of polyploidy. Portugaliae Acta (Suppl), 273-352.
10. Stebbins GL. 1950 Variation and evolution in plants. New York, NY: Columbia University Press.
11. Grant V. 1971 Plant speciation, 1st edn. New York, NY: Columbia University Press.
12. Stebbins G. 1966 Chromosomal variation and evolution; polyploidy and chromosome size and number shed light on evolutionary processes in higher plants. Science 152, 1463-1469. (doi:10.1126/science.152.3728.1463)
13. Tang H, Bowers JE, Wang X, Ming R, Alam M, Paterson AH. 2008 Synteny and colinearity in plant genomes. Science 320, 486-488. (doi:10.1126/ science.1153917)
14. Paterson AH, Freeling M, Tang H, Wang X. 2010 Insights from the comparison of plant genome sequences. Annu. Rev. Plant Biol. 61, 349-372. (doi:10.1146/annurev-arplant-042809-112235)
15. Gu ZL, Steinmetz LM, Gu X, Scharfe C, Davis RW, Li WH. 2003 Role of duplicate genes in genetic robustness against null mutations. Nature 421, 63-66. (doi:10.1038/nature01198)
16. Christoffels A, Koh EGL, Chia JM, Brenner S, Aparicio S, Venkatesh B. 2004 Fugu genome analysis provides evidence for a whole-genome duplication early during the evolution of ray-finned fishes. Mol. Biol. Evol. 21, 1146-1151. (doi:10.1093/molbev/ msh114)
17. Scannell DR, Byrne KP, Gordon JL, Wong S, Wolfe KH. 2006 Multiple rounds of speciation associated with reciprocal gene loss in polyploid yeasts. Nature 440, 341-345. (doi:10.1038/nature04562)
18. Aury JM et al. 2006 Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 444, 171-178. (doi:10.1038/ nature05230)
19. Lynch M, O'Hely M, Walsh B, Force A. 2001 The probability of preservation of a newly arisen gene duplicate. Genetics 159, 1789-1804.
20. Lynch M. 2006 The origins of eukaryotic gene structure. Mol. Biol. Evol. 23, 450-468. (doi:10.1093/molbev/msj050)
21. Kenrick P, Crane PR. 1997 The origin and early evolution of plants on land. Nature 389, 33-39. (doi:10.1038/37918)
22. Becker B, Marin B. 2009 Streptophyte algae and the origin of embryophytes. Ann. Bot. 103, 999-1004. (doi:10.1093/aob/mcp044)
23. Karol KG, McCourt RM, Cimino MT, Delwiche CF. 2001 The closest living relatives of land plants. Science 294, 2351-2353. (doi:10.1126/science.1065156)
24. Lewis LA, McCourt RM. 2004 Green algae and the origin of land plants. Am. J. Bot. 91, 1535-1556. (doi:10.3732/ajb.91.10.1535)
25. Rensing SA et al. 2008 The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319, 64-69. (doi:10.1126/ science.1150646)
26. Banks JA et al. 2011 The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332, 960-963. (doi:10.1126/science.1203810)
27. Murray B, Leitch I, Bennett M. 2012 Gymnosperm DNA C-values database (release 5.0, Dec. 2012). See http://www.kew.org/cvalues/
28. Nystedt B et al. 2013 The Norway spruce genome sequence and conifer genome evolution. Nature 497, 579-584. (doi:10.1038/nature12211)
29. Arabidopsis Genome Initiative. 2000 Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796-815. (doi:10.1038/35048692)
30. Tuskan GA et al. 2006 The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313, 1596-1604. (doi:10.1126/science.1128691)
31. Jaillon O et al. 2007 The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449, 463-467. (doi:10.1038/nature06148
32. Yu J et al. 2002 A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296, 79-92. (doi:10.1126/science.1068037)
33. Paterson AH et al. 2009 The Sorghum bicolor genome and the diversification of grasses. Nature 457, 551-556. (doi:10.1038/nature07723
34. D'Hont A et al. 2012 The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488, 213-217. (doi:10.1038/ nature11241
35. Li L, Stoeckert Jr CJ, Roos DS. 2003 OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13, 2178-2189. (doi:10.1101/gr.1224503)
36. Chen F, Mackey AJ, Vermunt JK, Roos DS. 2007 Assessing performance of orthology detection strategies applied to eukaryotic genomes. PLoS ONE 2, e383. (doi:10.1371/journal.pone.0000383)
37. Merchant SS et al. 2007 The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318, 245-250. (doi:10.1126/science.1143609)
38. Wang W, Vinocur B, Shoseyov O, Altman A. 2004 Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci. 9, 244-252. (doi:10.1016/j.tplants.2004.03.006)
39. Delevoryas T. 1979 Polyploidy in gymnosperms. Basic Life Sci. 13, 215-218.
40. Morse AM et al. 2009 Evolution of genome size and complexity in Pinus. PLoS ONE 4, e4332. (doi:10.1371/journal.pone.0004332)
41. Kovach A et al. 2010 The Pinus taeda genome is characterized by diverse and highly diverged repetitive sequences. BMC Genomics 11, 420. (doi:10.1186/1471-2164-11-420)
42. Hall SE, Dvorak WS, Johnston JS, Price HJ, Williams CG. 2000 Flow cytometric analysis of DNA content for tropical and temperate New World pines. Ann. Bot. Lond. 86, 1081-1086. (doi:10.1006/anbo.2000.1272)
43. Wakamiya I, Newton RJ, Johnston JS, Price HJ. 1993 Genome size and environmental factors in the genus Pinus. Am. J. Bot. 80, 1235-1241. (doi:10.2307/2445706)
44. Grotkopp E, Rejmanek M, Sanderson MJ, Rost TL. 2004 Evolution of genome size in pines (Pinus) and its life-history correlates: Supertree analyses. Evolution 58, 1705-1729. (doi:10.1111/j.0014-3820.2004.tb00456.x)
45. Burleigh JG, Barbazuk WB, Davis JM, Morse AM, Soltis PS. 2012 Exploring diversification and genome size evolution in extant gymnosperms through phylogenetic synthesis. J. Bot. 2012, 1-6. (doi:10.1155/2012/292857)
46. Klintenas M, Pin PA, Benlloch R, Ingvarsson PK, Nilsson O. 2012 Analysis of conifer Flowering Locus T/Terminal Flower1-like genes provides evidence for dramatic biochemical evolution in the angiosperm FT lineage. New Phytol. 196, 1260-1273. (doi:10.1111/j.1469-8137.2012.04332.x)
47. Karlgren A, Gyllenstrand N, Kallman T, Sundstrom JF, Moore D, Lascoux M, Lagercrantz U. 2011 Evolution of the PEBP gene family in plants: functional diversification in seed plant evolution. Plant Physiol. 156, 1967-1977. (doi:10.1104/pp.111.176206)
48. Ma H, dePamphilis C. 2000 The ABCs of floral evolution. Cell 101, 5-8. (doi:10.1016/S0092-8674(00)80618-2)
49. Sperry JS, Hacke UG, Pittermann J. 2006 Size and function in conifer tracheids and angiosperm vessels. Am. J. Bot. 93, 1490-1500. (doi:10.3732/ ajb.93.10.1490)
50. Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M, Ito J, Mimura T, Fukuda H, Demura T. 2005 Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev. 19, 1855-1860. (doi:10.1101/gad.1331305)
51. Regal PJ. 1977 Ecology and evolution of flowering plant dominance. Science 196, 622-629. (doi:10.1126/science.196.4290.622)
52. Crane PR, Friis EM, Pedersen KR. 1995 The origin and early diversification of angiosperms. Nature 374, 27-33. (doi:10.1038/374027a0)
53. Soltis PS, Soltis DE. 2004 The origin and diversification of angiosperms. Am. J. Bot. 91, 1614-1626. (doi:10.3732/ajb.91.10.1614)
54. Amborella Genome Project. 2013 The Amborella genome and the evolution of flowering plants. Science 342, 1241089. (doi:10.1126/science.1241089)
55. Smith SF, Snell P, Gruetzner F, Bench AJ, Haaf T, Metcalfe JA, Green AR, Elgar G. 2002 Analyses of the extent of shared synteny and conserved gene orders between the genome of Fugu rubripes and human 20q. Genome Res. 12, 776-784. (doi:10.1101/gr.221802)
56. Dehal P, Boore JL. 2005 Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol. 3, e314. (doi:10.1371/journal.pbio.0030314)
57. Bowers JE, Chapman BA, Rong J, Paterson AH. 2003 Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422, 433-438. (doi:10.1038/ nature01521)
58. Tang H, Wang X, Bowers JE, Ming R, Alam M, Paterson AH. 2008 Unraveling ancient hexaploidy through multiply-aligned angiosperm gene maps. Genome Res. 18, 1944-1954. (doi:10.1101/gr.080978.108)
59. Coghlan A, Eichler EE, Oliver SG, Paterson AH, Stein L. 2005 Chromosome evolution in eukaryotes: a multi-kingdom perspective. Trends Genet. 21, 673-682. (doi:10.1016/j.tig.2005.09.009)
60. Chaw SM, Chang CC, Chen HL, Li WH. 2004 Dating the monocot-dicot divergence and the origin of core eudicots using whole chloroplast genomes. J. Mol. Evol. 58, 424-441. (doi:10.1007/s00239-003-2564-9)
61. Wang Y et al. 2012 MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 40, e49. (doi:10.1093/ nar/gkr1293)
62. Vandepoele K, Saeys Y, Simillion C, Raes J, Van de Peer Y. 2002 The automatic detection of homologous regions (ADHoRe) and its application to microcolinearity between Arabidopsis and rice. Genome Res. 12, 1792-1801. (doi:10.1101/ gr.400202)
63. Cannon SB, Kozik A, Chan B, Michelmore R, Young ND. 2003 DiagHunter and GenoPix2D: programs for genomic comparisons, large-scale homology discovery and visualization. Genome Biol. 4, R68. doi:10.1186/gb-2003-4-10)
64. Haas BJ, Delcher AL, Wortman JR, Salzberg SL. 2004 DAGchainer: a tool for mining segmental genome duplications and synteny. Bioinformatics 20, 3643-3646. (doi:10.1093/bioinformatics/bth397)
65. Wang XY, Shi XL, Li Z, Zhu QH, Kong L, Tang W, Ge S, Luo JC. 2006 Statistical inference of chromosomal homology based on gene colinearity and applications to Arabidopsis and rice. BMC Bioinform. 7, 447. (doi:10.1186/1471-2105-7-447)
66. Lyons E et al. 2008 Finding and comparing syntenic regions among Arabidopsis and the outgroups papaya, poplar, and grape: CoGe with rosids. Plant Physiol. 148, 1772-1781. (doi:10.1104/pp.108.124867)
67. Lyons E, Pedersen B, Kane J, Freeling M. 2008 The value of nonmodel genomes and an example using synmap within CoGe to dissect the hexaploidy that predates the rosids. Trop. Plant Biol. 1, 181-190. (doi:10.1007/s12042-008-9017-y)
68. Lyons E, Freeling M, Kustu S, Inwood W. 2011 Using genomic sequencing for classical genetics in E. coli K12. PLoS ONE 6, e16717. (doi:10.1371/journal. pone.0016717)
69. Lee TH, Tang H, Wang X, Paterson AH. 2013 PGDD: a database of gene and genome duplication in plants. Nucleic Acids Res. 41, D1152-D1158. (doi:10.1093/nar/gks1104)
70. Tang H, Bowers JE, Wang X, Paterson AH. 2009 Angiosperm genome comparisons reveal early polyploidy in the monocot lineage. Proc. Natl Acad. Sci. USA 107, 472-477. (doi:10.1073/pnas.0908007107)
71. Ibarra-Laclette E et al. 2013 Architecture and evolution of a minute plant genome. Nature 498, 94-98. (doi:10.1038/nature12132)
72. Lynch M, Force A. 2000 The probability of duplicate gene preservation by subfunctionalization. Genetics 154, 459-473.
73. He XL, Zhang JZ. 2005 Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution. Genetics 169, 1157-1164. (doi:10.1534/genetics.104.037051)
74. Haldane JBS. 1933 The part played by recurrent mutation in evolution. Am. Nat. 67, 5-19. (doi:10.1086/280465)
75. Brunet FG, Crollius HR, Paris M, Aury JM, Gibert P, Jaillon O, Laudet V, Robinson-Rechavi M. 2006 Gene loss and evolutionary rates following whole genome duplication in teleost fishes. Mol. Biol. Evol. 23, 1808-1816. (doi:10.1093/molbev/msl049)
76. Chapman BA, Bowers JE, Feltus FA, Paterson AH. 2006 Buffering crucial functions by paleologous duplicated genes may impart cyclicality to angiosperm genome duplication. Proc. Natl Acad. Sci. USA 103, 2730-2735. (doi:10.1073/pnas.0507782103)
77. Seoighe C, Gehring C. 2004 Genome duplication led to highly selective expansion of the Arabidopsis thaliana proteome. Trends Genet. 20, 461-464. (doi:10.1016/j.tig.2004.07.008)
78. Paterson AH, Chapman BA, Kissinger J, Bowers JE, Feltus FA, Estill J, Marler BS. 2006 Convergent retention or loss of gene/domain families following independent whole-genome duplication events in Arabidopsis, Oryza, Saccharomyces, and Tetraodon. Trends Genet. 22, 597-602. (doi:10.1016/j.tig.2006.09.003)
79. Gao LZ, Innan H. 2004 Very low gene duplication rate in the yeast genome. Science 306, 1367-1370. (doi:10.1126/science.1102033)
80. Wang X, Tang H, Bowers JE, Feltus FA, Paterson AH. 2007 Extensive concerted evolution of rice paralogs and the road to regaining independence. Genetics 177, 1753-1763. (doi:10.1534/genetics.107.073197)
81. Maere S, De Bodt S, Raes J, Casneuf T, Van Montagu M, Kuiper M, Van de Peer Y. 2005 Modeling gene and genome duplications in eukaryotes. Proc. Natl Acad. Sci. USA 102, 5454-5459. (doi:10.1073/pnas.0501102102)
82. Blanc G, Wolfe KH. 2004 Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16, 1679-1691. (doi:10.1105/tpc.021410)
83. Blanc G, Wolfe KH. 2004 Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16, 1667-1678. (doi:10.1105/tpc.021345)
84. Lynch M, Conery JS. 2000 The evolutionary fate and consequences of duplicate genes. Science 290, 1151-1155. (doi:10.1126/science.290.5494.1151)
85. Long M, Betran E, Thornton K, Wang W. 2003 The origin of new genes: glimpses from the young and old. Nat. Rev. Genet. 4, 865-875. (doi:10.1038/ nrg1204)
86. Wang YP, Wang XY, Tang HB, Tan X, Ficklin SP, Feltus FA, Paterson AH. 2011 Modes of gene duplication contribute differently to genetic novelty and redundancy, but show parallels across divergent angiosperms. PLoS ONE 6, e28150. (doi:10.1371/ journal.pone.0028150)
87. Jiao Y et al. 2011 Ancestral polyploidy in seed plants and angiosperms. Nature 473, U97-U113. (doi:10.1038/nature09916)
88. Mathews S, Burleigh JG, Donoghue MJ. 2003 Adaptive evolution in the photosensory domain of phytochrome A in early angiosperms. Mol. Biol. Evol. 20, 1087-1097. (doi:10.1093/molbev/msg123)
89. Prigge MJ, Clark SE. 2006 Evolution of the class III HD-Zip gene family in land plants. Evol. Dev. 8, 350-361. (doi:10.1111/j.1525-142X.2006.00107.x)
90. Paterson AH, Bowers JE, Chapman BA. 2004 Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc. Natl Acad. Sci. USA 101, 9903-9908. (doi:10.1073/pnas.0307901101)
91. Wang X, Gowik U, Tang H, Bowers JE, Westhoff P, Paterson AH. 2009 Comparative genomic analysis of C4 photosynthetic pathway evolution in grasses. Genome Biol. 10, R68. (doi:10.1186/gb-2009-10-6-r68)
92. Vekemans D, Proost S, Vanneste K, Coenen H, Viaene T, Ruelens P, Maere S, Van de Peer Y, Geuten K. 2012 Gamma paleohexaploidy in the stem lineage of core eudicots: significance for MADS-box gene and species diversification. Mol. Biol. Evol. 29, 3793-3806. (doi:10.1093/molbev/mss183)
93. Ming R et al. 2013 Genome of the long-living sacred lotus (Nelumbo nucifera Gaertn.). Genome Biol. 14, R41. (doi:10.1186/gb-2013-14-5-r41)
94. Jiao Y et al. 2012 A genome triplication associated with early diversification of the core eudicots. Genome Biol. 13, R3. (doi:10.1186/gb-2012-13-1-r3)
95. Sato S et al. 2012 The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485, 635-641. (doi:10.1038/nature11119)
96. Yupeng W, Ficklin SP, Wang X, Alex Feltus F, Paterson AH. Submitted. Dispersed duplicated genes and the evolution of genetic complexity.
97. 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. (doi:10.1146/ annurev.arplant.043008.092122)
98. Kassahn KS, Dang VT, Wilkins SJ, Perkins AC, Ragan MA. 2009 Evolution of gene function and regulatory control after whole-genome duplication: comparative analyses in vertebrates. Genome Res. 19, 1404-1418. (doi:10.1101/gr.086827.108)
99. Edger PP, Pires JC. 2009 Gene and genome duplications: the impact of dosage-sensitivity on the fate of nuclear genes. Chromosome Res. 17, 699-717. (doi:10.1007/s10577-009-9055-9)
100. Paterson AH, Chapman BA, Kissinger JC, Bowers JE, Feltus FA, Estill JC. 2006 Many gene and domain families have convergent fates following independent whole-genome duplication events in Arabidopsis, Oryza, Saccharomyces and Tetraodon. Trends Genet. 22, 597-602. (doi:10.1016/j.tig.2006.09.003)
101. Davis JC, Petrov DA. 2004 Preferential duplication of conserved proteins in eukaryotic genomes. PLoS Biol. 2, E55. (doi:10.1371/journal.pbio.0020055)
102. Seoighe C, Wolfe KH. 1999 Yeast genome evolution in the post-genome era. Curr. Opin. Microbiol. 2, 548-554. (doi:10.1016/S1369-5274(99)00015-6)
103. Makino T, McLysaght A. 2012 Positionally biased gene loss after whole genome duplication: evidence from human, yeast, and plant. Genome Res. 22, 2427-2435. (doi:10.1101/gr.131953.111)
104. Woodhouse MR, Schnable JC, Pedersen BS, Lyons E, Lisch D, Subramaniam S, Freeling M. 2010 Following tetraploidy in maize, a short deletion mechanism removed genes preferentially from one of the two homologs. PLoS Biol. 8, e1000409. (doi:10.1371/journal.pbio.1000409)
105. Duarte JM, Wall PK, Edger PP, Landherr LL, Ma H, Pires JC, Leebens-Mack J, dePamphilis CW. 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. (doi:10.1186/1471-2148-10-61)
106. De Smet R, Adams KL, Vandepoele K, van Montagu MCE, Maere S, Van de Peer Y. 2013 Convergent gene loss following gene and genome duplications creates single-copy families in flowering plants. Proc. Natl Acad. Sci. USA 110, 2898-2903. (doi:10.1073/pnas.1300127110)
107. Zhang N, Zeng LP, Shan HY, Ma H. 2012 Highly conserved low-copy nuclear genes as effective markers for phylogenetic analyses in angiosperms. New Phytol. 195, 923-937. (doi:10.1111/j.1469-8137.2012.04212.x)
108. Wu FN, Mueller LA, Crouzillat D, Petiard V, Tanksley SD. 2006 Combining bioinformatics and phylogenetics to identify large sets of single-copy orthologous genes (COSII) for comparative, evolutionary and systematic studies: a test case in the euasterid plant clade. Genetics 174, 1407-1420. (doi:10.1534/genetics.106.062455)
109. Rong J, Feltus FA, Liu L, Lin L, Paterson AH. 2010 Gene copy number evolution during tetraploid cotton radiation. Heredity 105, 463-472. (doi:10.1038/hdy.2009.192)
110. Werth CR, Windham MD. 1991 A model for divergent, allopatric speciation of polyploid pteridophytes resulting from silencing of duplicategene expression. Am. Nat. 137, 515-526. (doi:10.1086/285180)
111. Lynch M, Force AG. 2000 The origin of interspecific genomic incompatibility via gene duplication. Am. Nat. 156, 590-605. (doi:10.1086/316992)
112. Maclean CJ, Greig D. 2011 Reciprocal gene loss following experimental whole-genome duplication causes reproductive isolation in yeast. Evolution 65, 932-945. (doi:10.1111/j.1558-5646.2010.01171.x)
113. Schnable JC, Freeling M, Lyons E. 2012 Genomewide analysis of syntenic gene deletion in the grasses. Genome Biol. Evol. 4, 265-277. (doi:10.1093/gbe/evs009)