Evolutionary Histories of Gene Families in Angiosperm Trees

  • S. G. Hussey
  • Jill L. Wegrzyn
  • H. A. Vasquez-Gross
Part of the Plant Genetics and Genomics: Crops and Models book series (PGG, volume 21)


Genes can be grouped into families based on either the presence of conserved domains or by parameter-based clustering of pairwise alignments of the proteins they encode. The vast majority of gene families found in angiosperm trees have existed before the origin of seed plants, while the lineage-specific adaptations of trees have depended on highly dynamic but selective patterns of gene family gain and loss. The mechanisms governing the diversification of gene families, among them various types of gene duplication, horizontal gene transfer, protein domain re-arrangement and de novo evolution, each play distinct roles in expanding the functional repertoire of the core proteome of land plants. In this chapter we reconstructed a parsimonious evolutionary history of gene family gain and loss in angiosperm tree lineages relative to close herbaceous relatives, gymnosperms and nonvascular plants, revealing considerable variation in the frequency and functional enrichment of gain and loss events across lineages. Throughout the chapter, we highlight general and tree-specific examples of gene family adaptations that have contributed to the remarkable success of these organisms.


Gene family Evolution Protein domain Functional enrichment Genomics Angiosperm 


  1. Al-Dous EK, George B, Al-Mahmoud ME, Al-Jaber MY, Wang H, et al. De novo genome sequencing and comparative genomics of date palm (Phoenix dactylifera). Nat Biotechnol. 2011;29:521–7.PubMedCrossRefGoogle Scholar
  2. Allario T, Brumos J, Colmenero-Flores JM, Tadeo F, Froelicher Y, et al. Large changes in anatomy and physiology between diploid Rangpur lime (Citrus limonia) and its autotetraploid are not associated with large changes in leaf gene expression. J Exp Bot. 2011;62:2507–19.PubMedCrossRefGoogle Scholar
  3. Al-Mssallem IS, Hu S, Zhang X, Lin Q, Liu W, et al. Genome sequence of the date palm Phoenix dactylifera L. Nat Commun. 2013;4:2274.PubMedPubMedCentralCrossRefGoogle Scholar
  4. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389–402.PubMedPubMedCentralCrossRefGoogle Scholar
  5. Arendsee ZW, Li L, Wurtele ES. Coming of age: orphan genes in plants. Trends Plant Sci. 2014;19:698–708.PubMedCrossRefGoogle Scholar
  6. Argout X, Salse J, Aury J-M, Guiltinan MJ, Droc G, et al. The genome of Theobroma cacao. Nat Genet. 2011;43:101–8.PubMedCrossRefGoogle Scholar
  7. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. Gene Ontology: tool for the unification of biology. Nat Genet. 2000;25:25–9.PubMedPubMedCentralCrossRefGoogle Scholar
  8. Banks JA, Nishiyama T, Hasebe M, Bowman JL, Gribskov M, et al. The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science. 2011;332:960–3.PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bergthorsson U, Richardson AO, Young GJ, Goertzen LR, Palmer JD. Massive horizontal transfer of mitochondrial genes from diverse land plant donors to the basal angiosperm Amborella. Proc Natl Acad Sci U S A. 2004;101:17747–52.PubMedPubMedCentralCrossRefGoogle Scholar
  10. Biezen EAVD, Jones JDG. The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals. Curr Biol. 1998;8:R226–8.PubMedCrossRefGoogle Scholar
  11. Birchler JA, Veitia RA. The Gene Balance Hypothesis: from classical genetics to modern genomics. Plant Cell. 2007;19:395–402.PubMedPubMedCentralCrossRefGoogle Scholar
  12. Birchler JA, Riddle NC, Auger DL, Veitia RA. Dosage balance in gene regulation: biological implications. Trends Genet. 2005;21:219–26.PubMedCrossRefGoogle Scholar
  13. Birol I, Raymond A, Jackman SD, Pleasance S, Coope R, et al. Assembling the 20 Gb white spruce (Picea glauca) genome from whole-genome shotgun sequencing data. Bioinformatics. 2013;29:1492–7.PubMedPubMedCentralCrossRefGoogle Scholar
  14. Bock R. The give-and-take of DNA: horizontal gene transfer in plants. Trends Plant Sci. 2009;15:11–22.PubMedCrossRefGoogle Scholar
  15. Bornberg-Bauer E, Albà MM. Dynamics and adaptive benefits of modular protein evolution. Curr Opin Struct Biol. 2013;23:459–66.PubMedCrossRefGoogle Scholar
  16. Cannon, S. B., A. Mitra, A. Baumgarten, N. D. Young and G. 2004 The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4: 10.Google Scholar
  17. Casneuf T, De Bodt S, Raes J, Maere S, van de Peer Y. Nonrandom divergence of gene expression following gene and genome duplications in the flowering plant Arabidopsis thaliana. Genome Biol. 2006;7:R13.PubMedPubMedCentralCrossRefGoogle Scholar
  18. Chaw S-M, Chang C-C, Chen H-L, Li W-H. Dating the monocot–dicot divergence and the origin of core eudicots using whole chloroplast genomes. J Mol Evol. 2004;58:424–41.PubMedCrossRefGoogle Scholar
  19. D’Hont A, Denoeud F, Aury J-M, Baurens F-C, Carreel F, et al. The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature. 2012;488:213–7.PubMedCrossRefGoogle Scholar
  20. Dayhoff MO. The origin and evolution of protein superfamilies. Fed Proc. 1976;35:2132–8.PubMedGoogle Scholar
  21. De Smet R, Adams KL, Vandepoele K, Van Montagu MCE, Maere S, et al. Convergent gene loss following gene and genome duplications creates single-copy families in flowering plants. Proc Natl Acad Sci U S A. 2013;110:2898–903.PubMedPubMedCentralCrossRefGoogle Scholar
  22. Demuth JP, Hahn MW. The life and death of gene families. Bioessays. 2009;31:29–39.PubMedCrossRefGoogle Scholar
  23. Donoghue MT, Keshavaiah C, Swamidatta SH, Spillane C. Evolutionary origins of Brassicaceae specific genes in Arabidopsis thaliana. BMC Evol Biol. 2011;11:47.PubMedPubMedCentralCrossRefGoogle Scholar
  24. Droc G, Larivière D, Guignon V, Yahiaoui N, This D, et al. The banana genome hub. Database. 2013;2013:bac035.CrossRefGoogle Scholar
  25. Emiliani G, Fondi M, Fani R, Gribaldo S. A horizontal gene transfer at the origin of phenylpropanoid metabolism: a key adaptation of plants to land. Biol Direct. 2009;4:7.PubMedPubMedCentralCrossRefGoogle Scholar
  26. Enright AJ, Van Dongen S, Ouzounis CA. An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res. 2002;30:1575–84.PubMedPubMedCentralCrossRefGoogle Scholar
  27. Fawcett JA, Maere S, Peer YVD. Plants with double genomes might have had a better chance to survive the Cretaceous–Tertiary extinction event. Proc Natl Acad Sci U S A. 2010;106:5737–42.CrossRefGoogle Scholar
  28. Felsenstein J. PHYLIP―phylogeny inference package (version 3.2). Cladistics. 1989;5:163–6.CrossRefGoogle Scholar
  29. Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, et al. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res. 2016;44:D279–85.PubMedCrossRefGoogle Scholar
  30. Flagel LE, Wendel JF. Gene duplication and evolutionary novelty in plants. New Phytol. 2009;183:557–64.PubMedCrossRefGoogle Scholar
  31. Freeling M. Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Annu Rev Plant Biol. 2009;60:433–53.PubMedCrossRefGoogle Scholar
  32. Fuentes I, Stegemann S, Golczyk H, Karcher D, Bock R. Horizontal genome transfer as an asexual path to the formation of new species. Nature. 2014;511:232–5.PubMedCrossRefGoogle Scholar
  33. Ganko EW, Meyers BC, Vision TJ. Divergence in expression between duplicated genes in Arabidopsis. Mol Biol Evol. 2007;24:2298–309.PubMedCrossRefGoogle Scholar
  34. Gough J, Karplus K, Hughey R, Chothia C. Assignment of homology to genome sequences using a library of hidden Markov models that represent all proteins of known structure. J Mol Biol. 2001;313:903–19.PubMedCrossRefGoogle Scholar
  35. Groover AT. What genes make a tree a tree? Trends Plant Sci. 2005;10:210–4.PubMedCrossRefGoogle Scholar
  36. Guo Y-L. Gene family evolution in green plants with emphasis on the origination and evolution of Arabidopsis thaliana genes. Plant J. 2013;73:941–51.PubMedCrossRefGoogle Scholar
  37. Haft DH, Selengut JD, White O. The TIGRFAMs database of protein families. Nucleic Acids Res. 2003;31:371–3.PubMedPubMedCentralCrossRefGoogle Scholar
  38. He X, Zhang J. Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution. Genetics. 2005;169:1157–64.PubMedPubMedCentralCrossRefGoogle Scholar
  39. Hefer C, Mizrachi E, Joubert F, Myburg A. The Eucalyptus genome integrative explorer (EucGenIE): a resource for Eucalyptus genomics and transcriptomics. BMC Proc. 2011;5:O49.PubMedCentralCrossRefGoogle Scholar
  40. Hefer CA, Mizrachi E, Myburg AA, Douglas CJ, Mansfield SD. Comparative interrogation of the developing xylem transcriptomes of two wood-forming species: Populus trichocarpa and Eucalyptus grandis. New Phytol. 2015;206:1391–405.PubMedCrossRefGoogle Scholar
  41. Huntley RP, Sawford T, Martin MJ, O’Donovan C. Understanding how and why the Gene Ontology and its annotations evolve: the GO within UniProt. Giga Sci. 2014;3:4.CrossRefGoogle Scholar
  42. Janssen T, Bremer K. The age of major monocot groups inferred from 800+ rbcL sequences. Bot J Linn Soc. 2004;146:385–98.CrossRefGoogle Scholar
  43. Jiao Y, Paterson AH. Polyploidy-associated genome modifications during land plant evolution. Philos Trans R Soc Lon B. 2014;369:20130355.CrossRefGoogle Scholar
  44. Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, et al. Ancestral polyploidy in seed plants and angiosperms. Nature. 2011;473:97–100.PubMedCrossRefGoogle Scholar
  45. Jiao Y, Leebens-Mack J, Ayyampalayam S, Bowers JE, McKain MR, et al. A genome triplication associated with early diversification of the core eudicots. Genome Biol. 2012;13:R3.PubMedPubMedCentralCrossRefGoogle Scholar
  46. Jones JDG, Dangl JL. The plant immune system. Nat Rev. 2006;444:323–9.Google Scholar
  47. Katju V. In with the old, in with the new: the promiscuity of the duplication process engenders diverse pathways for novel gene creation. Int J Evol Biol. 2012;2012:341932.PubMedPubMedCentralCrossRefGoogle Scholar
  48. Kempe A, Lautenschläger T, Lange A, Neinhuis C. How to become a tree without wood – biomechanical analysis of the stem of Carica papaya L. Plant Biol. 2014;16:264–71.PubMedCrossRefGoogle Scholar
  49. Kersting AR, Bornberg-Bauer E, Moore AD, Grath S. Dynamics and adaptive benefits of protein domain emergence and arrangements during plant genome evolution. Genome Biol Evol. 2012;4:316–29.PubMedPubMedCentralCrossRefGoogle Scholar
  50. Kersting AR, Mizrachi E, Bornberg-Bauer E, Myburg AA. Protein domain evolution is associated with reproductive diversification and adaptive radiation in the genus Eucalyptus. New Phytol. 2015;206:1328–36.PubMedCrossRefGoogle Scholar
  51. Kyndt T, Quispe D, Zhai H, Jarret R, Ghislain M, et al. The genome of cultivated sweet potato contains Agrobacterium T-DNAs with expressed genes: an example of a naturally transgenic food crop. Proc Natl Acad Sci U S A. 2015;112:5844–9.PubMedPubMedCentralCrossRefGoogle Scholar
  52. Li L, Wurtele ES. The QQS orphan gene of Arabidopsis modulates carbon and nitrogen allocation in soybean. Plant Biotechnol J. 2015;13:177–87.PubMedCrossRefGoogle Scholar
  53. Li L, Foster CM, Gan Q, Nettleton D, James MG, et al. Identification of the novel protein QQS as a component of the starch metabolic network in Arabidopsis leaves. Plant J. 2009a;58:485–98.PubMedCrossRefGoogle Scholar
  54. Li Z, Zhang H, Ge S, Gu X, Gao G, et al. Expression pattern divergence of duplicated genes in rice. BMC Bioinf. 2009b;10:S8.CrossRefGoogle Scholar
  55. Li F-W, Villarreal JC, Kelly S, Rothfels CJ, Melkonian M, et al. Horizontal transfer of an adaptive chimeric photoreceptor from bryophytes to ferns. Proc Natl Acad Sci U S A. 2014a;111:6672–7.PubMedPubMedCentralCrossRefGoogle Scholar
  56. Li F, Fan G, Wang K, Sun F, Yuan Y, et al. Genome sequence of the cultivated cotton Gossypium arboreum. Nat Genet. 2014b;46:567–72.PubMedCrossRefGoogle Scholar
  57. Li L, Zheng W, Zhu Y, Ye H, Tang B, et al. QQS orphan gene regulates carbon and nitrogen partitioning across species via NF-YC interactions. Proc Natl Acad Sci U S A. 2015a;112:14734–9.PubMedPubMedCentralCrossRefGoogle Scholar
  58. Li Z, Baniaga AE, Sessa EB, Scascitelli M, Graham SW, et al. Early genome duplications in conifers and other seed plants. Sci Adv. 2015b;1:e1501084.PubMedPubMedCentralCrossRefGoogle Scholar
  59. Li Z, Defoort J, Tasdighian S, Maere S, Peer YVD, et al. Gene duplicability of core genes is highly consistent across all angiosperms. Plant Cell. 2016;28:326–44.PubMedPubMedCentralCrossRefGoogle Scholar
  60. Lu P, Jernstedt JA. Rhizophore and root development in Selaginella martensii: meristem transitions and identity. Int J Plant Sci. 1996;157:180–94.CrossRefGoogle Scholar
  61. Maere S, Bodt SD, Raes J, Casneuf T, Montagu MV, et al. Modeling gene and genome duplications in eukaryotes. Proc Natl Acad Sci U S A. 2005;102:5454–9.PubMedPubMedCentralCrossRefGoogle Scholar
  62. Magallón S, Hilu KW, Quandt D. Land plant evolutionary timeline: Gene effects are secondary to fossil constraints in relaxed clock estimation of age and substitution rates. Am J Bot. 2013;100:556–73.PubMedCrossRefGoogle Scholar
  63. Ming R, Hou S, Feng Y, Yu Q, Dionne-Laporte A, et al. The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature. 2008;452:991–6.PubMedPubMedCentralCrossRefGoogle Scholar
  64. Moreira D, Philippe H. Smr: a bacterial and eukaryotic homologue of the C-terminal region of the MutS2 family. Trends Biochem Sci. 1999;24:298–300.PubMedCrossRefGoogle Scholar
  65. Motamayor JC, Mockaitis K, Schmutz J, Haiminen N, Livingstone D, et al. The genome sequence of the most widely cultivated cacao type and its use to identify candidate genes regulating pod color. Genome Biol. 2013;14:r53.PubMedPubMedCentralCrossRefGoogle Scholar
  66. Mower JP, Stefanović S, Hao W, Gummow JS, Jain K, et al. Horizontal acquisition of multiple mitochondrial genes from a parasitic plant followed by gene conversion with host mitochondrial genes. BMC Biol. 2010;8:150.PubMedPubMedCentralCrossRefGoogle Scholar
  67. Myburg AA, Grattapaglia D, Tuskan GA, Hellsten U, Hayes RD, et al. The genome of Eucalyptus grandis – a global tree for fiber and energy. Nature. 2014;510:356–62.PubMedGoogle Scholar
  68. Neale D, Wegrzyn J, Stevens K, Zimin A, Puiu D, et al. Decoding the massive genome of loblolly pine using haploid DNA and novel assembly strategies. Genome Biol. 2014;15:R59.PubMedPubMedCentralCrossRefGoogle Scholar
  69. Neme R, Tautz D. Phylogenetic patterns of emergence of new genes support a model of frequent de novo evolution. BMC Genomics. 2013;14:117.PubMedPubMedCentralCrossRefGoogle Scholar
  70. Nikolaidis N, Doran N, Cosgrove DJ. Plant expansins in bacteria and fungi: evolution by horizontal gene transfer and independent domain fusion. Mol Biol Evol. 2013;31:376–86.PubMedCrossRefGoogle Scholar
  71. Nystedt B, Street NR, Wetterbom A, Zuccolo A, Lin Y-C, et al. The Norway spruce genome sequence and conifer genome evolution. Nature. 2013;497:579–84.PubMedCrossRefGoogle Scholar
  72. Philipson WR, Ward JM. The ontogeny of the vascular cambium in the stem of seed plants. Biol Rev. 1965;40:534–79.CrossRefGoogle Scholar
  73. Proost S, Bel MV, Vaneechoutte D, Peer YVD, Inzé D, et al. PLAZA 3.0: an access point for plant comparative genomics. Nucleic Acids Res. 2014;43:D974–81.PubMedPubMedCentralCrossRefGoogle Scholar
  74. Punta M, Coggill PC, Eberhardt RY, Tate JMJ, Boursnell C, et al. The Pfam protein families database. Nucleic Acids Res. 2012;40:D290–301.PubMedCrossRefGoogle Scholar
  75. Qian W, Zhang J. Genomic evidence for adaptation by gene duplication. Genome Res. 2014;24:1356–62.PubMedPubMedCentralCrossRefGoogle Scholar
  76. Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, et al. InterProScan: protein domains identifier. Nucleic Acids Res. 2005;33:W116–20.PubMedPubMedCentralCrossRefGoogle Scholar
  77. Ratke C, Pawar PM-A, Balasubramanian VK, Naumann M, Duncranz ML, et al. Populus GT43 family members group into distinct sets required for primary and secondary wall xylan biosynthesis and include useful promoters for wood modification. Plant Biotechnol J. 2015;13:26–37.PubMedCrossRefGoogle Scholar
  78. Rensing SA. Gene duplication as a driver of plant morphogenetic evolution. Curr Opin Plant Biol. 2014;17:43–8.PubMedCrossRefGoogle Scholar
  79. Rensing SA, Ick J, Fawcett JA, Lang D, Zimmer A, et al. An ancient genome duplication contributed to the abundance of metabolic genes in the moss Physcomitrella patens. BMC Evol Biol. 2007;7:130.PubMedPubMedCentralCrossRefGoogle Scholar
  80. Rice DW, Alverson AJ, Richardson AO, Young GJ, Sanchez-Puerta MV, et al. Horizontal transfer of entire genomes via mitochondrial fusion in the angiosperm Amborella. Science. 2013;342:1468–73.PubMedCrossRefGoogle Scholar
  81. Rodgers-Melnick E, Mane SP, Dharmawardhana P, Slavov GT, Crasta OR, et al. Contrasting patterns of evolution following whole genome versus tandem duplication events in Populus. Genome Res. 2012;22:95–105.PubMedPubMedCentralCrossRefGoogle Scholar
  82. Rudall P. Lateral meristems and secondary thickening growth in monocotyledons. Bot Rev. 1991;57:150–63.CrossRefGoogle Scholar
  83. Rutter MT, Cross KV, Woert PAV. Birth, death and subfunctionalization in the Arabidopsis genome. Trends Plant Sci. 2012;17:204–12.PubMedCrossRefGoogle Scholar
  84. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, et al. Genome sequence of the palaeopolyploid soybean. Nature. 2010;463:178–83.PubMedCrossRefGoogle Scholar
  85. Spicer R, Groover A. Evolution of development of vascular cambia and secondary growth. New Phytol. 2010;186:577–92.PubMedCrossRefGoogle Scholar
  86. Takata N, Taniguchi T. Expression divergence of cellulose synthase (CesA) genes after a recent whole genome duplication event in Populus. Planta. 2015;241:29–42.PubMedCrossRefGoogle Scholar
  87. Tautz D, Domatez-Lošo T. The evolutionary origin of orphan genes. Nat Rev Genet. 2011;12:692–702.PubMedCrossRefGoogle Scholar
  88. Taylor ZN, Rice DW, Palmer JD. The complete moss mitochondrial genome in the angiosperm Amborella is a chimera derived from two moss whole-genome transfers. PLoS One. 2014;10:e0137532.CrossRefGoogle Scholar
  89. Timell TE. Recent progress in the chemistry of wood hemicelluloses. Wood Sci Technol. 1967;1:45–70.CrossRefGoogle Scholar
  90. Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, et al. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science. 2006;313:1596–604.PubMedCrossRefGoogle Scholar
  91. Van de Peer Y, Fawcett JA, Proost S, Sterck L, Vandepoele K. The flowering world: a tale of duplications. Trends Plant Sci. 2009;14:680–8.PubMedCrossRefGoogle Scholar
  92. Vanneste K, Maere S, Peer YVD. Tangled up in two: a burst of genome duplications at the end of the Cretaceous and the consequences for plant evolution. Philos Trans R Soc Lon B. 2014;369:20130353.CrossRefGoogle Scholar
  93. Vanneste K, Sterck L, Myburg AA, Peer YVD, Mizrachi E. Horsetails are ancient polyploids: evidence from Equisetum giganteum. Plant Cell. 2015;27:1567–78.PubMedPubMedCentralCrossRefGoogle Scholar
  94. Vekemans D, Proost S, Vanneste K, Coenen H, Viaene T, et al. Gamma paleohexaploidy in the stem lineage of core eudicots: significance for MADS-box gene and species diversification. Mol Biol Evol. 2012;29:3793–806.PubMedCrossRefGoogle Scholar
  95. Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, et al. The genome of the domesticated apple (Malus × domestica Borkh.). Nat Genet. 2010;42:833–9.PubMedCrossRefGoogle Scholar
  96. Verde I, Abbott AG, Scalabrin S, Jung S, Shu S, et al. The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet. 2013;45:487–94.PubMedCrossRefGoogle Scholar
  97. Wang Y, Wang X, Paterson AH. Genome and gene duplications and gene expression divergence: a view from plants. Ann N Y Acad Sci. 2012;1256:1–14.PubMedCrossRefGoogle Scholar
  98. Wang Q, Sun H, Huang J. The evolution of land plants: a perspective from horizontal gene transfer. Acta Soc Bot Pol. 2014;83:363–8.CrossRefGoogle Scholar
  99. Wang B, Climent J, Wang X-R. Horizontal gene transfer from a flowering plant to the insular pine Pinus canariensis (Chr. Sm. Ex DC in Buch). Heredity. 2015;114:413–8.PubMedPubMedCentralCrossRefGoogle Scholar
  100. Warren RL, Keeling CI, Yuen MMS, Raymond A, Taylor GA, et al. Improved white spruce (Picea glauca) genome assemblies and annotation of large gene families of conifer terpenoid and phenolic defense metabolism. Plant J. 2015;83:189–212.PubMedCrossRefGoogle Scholar
  101. Wegrzyn JL, Liechty JD, Stevens KA, Wu L-S, Loopstra CA, et al. Unique features of the Loblolly Pine (Pinus taeda L.) megagenome revealed through sequence annotation. Genetics. 2014;196:891–909.PubMedPubMedCentralCrossRefGoogle Scholar
  102. Wikström N, Savolainen V, Chase MW. Evolution of the angiosperms: calibrating the family tree. Proc R Soc B. 2001;268:2211–20.PubMedPubMedCentralCrossRefGoogle Scholar
  103. Willyard A, Syring J, Gernandt DS, Liston A, Cronn R. Fossil calibration of molecular divergence infers a moderate mutation rate and recent radiations for Pinus. Mol Biol Evol. 2007;24:90–101.PubMedCrossRefGoogle Scholar
  104. Wu GA, Prochnik S, Jenkins J, Salse J, Hellsten U, et al. Sequencing of diverse mandarin, pummelo and orange genomes reveals complex history of admixture during citrus domestication. Nat Biotechnol. 2014;32:656–62.PubMedPubMedCentralCrossRefGoogle Scholar
  105. Xi Z, Wang Y, Bradley RK, Sugumaran M, Marx CJ, et al. Massive mitochondrial gene transfer in a parasitic flowering plant clade. PLoS Genet. 2013;9:e1003265.PubMedPubMedCentralCrossRefGoogle Scholar
  106. Xu Q, Chen L-L, Ruan X, Chen D, Zhu A, et al. The draft genome of sweet orange (Citrus sinensis). Nat Genet. 2013;45:59–66.PubMedCrossRefGoogle Scholar
  107. Xu B, Ohtani M, Yamaguchi M, Toyooka K, Wakazaki M, et al. Contribution of NAC transcription factors to plant adaptation to land. Science. 2014;343:1505–8.PubMedCrossRefGoogle Scholar
  108. Yamasaki K, Kigawa T, Seki M, Shinozaki K, Yokoyama S. DNA-binding domains of plant-specific transcription factors: structure, function, and evolution. Trends Plant Sci. 2013;18:267–76.PubMedCrossRefGoogle Scholar
  109. Yang Z, Zhou Y, Huang J, Hu Y, Zhang E, et al. Ancient horizontal transfer of transaldolase-like protein gene and its role in plant vascular development. New Phytol. 2015;206:807–16.PubMedCrossRefGoogle Scholar
  110. Yoshida S, Maruyama S, Nozaki H, Shirasu K. Horizontal gene transfer by the parasitic plant Striga hermonthica. Science. 2010;328:1128.PubMedCrossRefGoogle Scholar
  111. Yue J-X, Meyers BC, Chen J-Q, Tian D, Yang S. Tracing the origin and evolutionary history of plant nucleotide-binding site–leucine-rich repeat (NBS-LRR) genes. New Phytol. 2011;193:1049–63.PubMedCrossRefGoogle Scholar
  112. Zhang J. Evolution by gene duplication: an update. Trends Ecol Evol. 2003;18:292–8.CrossRefGoogle Scholar
  113. Zimin A, Stevens KA, Crepeau MW, Holtz-Morris A, Koriabine M, et al. Sequencing and assembly of the 22-Gb loblolly pine genome. Genetics. 2014;196:875–90.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2016

Authors and Affiliations

  • S. G. Hussey
    • 1
  • Jill L. Wegrzyn
    • 2
  • H. A. Vasquez-Gross
    • 2
  1. 1.Department of GeneticsForestry and Agricultural Biotechnology Institute (FABI), Genomics Research Institute (GRI), University of PretoriaPretoriaSouth Africa
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of ConnecticutStorrsUSA

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