Advertisement

Plant Molecular Biology Reporter

, Volume 31, Issue 4, pp 852–861 | Cite as

Patterns of Gene Duplication and Their Contribution to Expansion of Gene Families in Grapevine

  • Nian Wang
  • Yue Xiang
  • Linchuan Fang
  • Yajie Wang
  • Haiping Xin
  • Shaohua Li
Original Paper

Abstract

Grapevine is an important fruit crop that has undergone a long history of evolution. Analysis of the whole genome sequence of grapevine has revealed presence of an early palaeo-hexaploid along with three complements. Thus, gene duplication and genome expansion are common in this genome. In this study, we identified 17,922 duplicated genes in the whole grapevine genome. Among these, 2,039; 628; 1,428; 722; and 2,942 were identified respectively as produced by genome-wide, tandem, proximal, retrotransposed, and DNA-based transposed duplications. Analyses of the evolutionary patterns for different types of duplication using non-synonymous and synonymous substitution rates uncovered a series of underlying rules. Thereafter, all the grapevine genes were classified into families, and the contributions of different types of duplication to the expansion of large families were revealed. No duplication type was solely responsible for the formation of any large gene family, but some families showed enrichment of a special type of duplication. On the basis of this study, we believe that uncovering the underlying rules for gene duplications, expansions of gene families, and their evolutionary styles will contribute significantly to a comprehensive understanding of the features of the grapevine genome.

Keywords

Grapevine Gene duplication Genome expansion Evolution Gene family 

Notes

Acknowledgments

Financial support for this work was provided by the National Natural Science Foundation of China (NSFC accession No.: 31171931) and the National Natural Science Foundation of Hubei Province (No.: 2011CDB409).

Supplementary material

11105_2013_556_MOESM1_ESM.pdf (199 kb)
Supplementary Table 1 Duplication types for all grapevine genes. The names of genes are given according to the 12− V. vinifera genomic sequence (PDF 198 kb)
11105_2013_556_MOESM2_ESM.pdf (38 kb)
Supplementary Table 2 Valid pairs for genome-wide duplicated genes (PDF 37 kb)
11105_2013_556_MOESM3_ESM.pdf (16 kb)
Supplementary Table 3 Valid pairs for tandem duplicated genes (PDF 16 kb)
11105_2013_556_MOESM4_ESM.pdf (29 kb)
Supplementary Table 4 Valid pairs for proximal duplicated genes (PDF 29 kb)
11105_2013_556_MOESM5_ESM.pdf (19 kb)
Supplementary Table 5 Valid pairs for retrotansposed duplicated genes (PDF 18 kb)
11105_2013_556_MOESM6_ESM.pdf (59 kb)
Supplementary Table 6 Valid pairs for DNA-based transposed duplicated genes (PDF 58 kb)
11105_2013_556_MOESM7_ESM.pdf (662 kb)
Supplementary Table 7 Grapevine gene families. The information was summarized from plant gene family database (http://green.dna.affrc.go.jp/PGF-DB/index.html) (PDF 662 kb)
11105_2013_556_MOESM8_ESM.pdf (16 kb)
Supplementary Table 8 Expansion of grapevine gene families (PDF 16 kb)

References

  1. Afoufa-Bastien D, Medici A, Jeauffre J, Coutos-Thevenot P, Lemoine R, Atanassova R, Laloi M (2010) The Vitis vinifera sugar transporter gene family: phylogenetic overview and macroarray expression profiling. BMC Plant Biol 10:245PubMedCrossRefGoogle Scholar
  2. Albalat R, Marfany G, Gonzalez-Duarte R (1994) Analysis of nucleotide substitutions and amino acid conservation in the Drosophila Adh genomic region. Genetica 94:27–36PubMedCrossRefGoogle Scholar
  3. Alturfan AA, Tozan-Beceren A, Sehirli AO, Demiralp E, Sener G, Omurtag GZ (2011) Resveratrol ameliorates oxidative DNA damage and protects against acrylamide-induced oxidative stress in rats. Mol Biol Rep 39:4589–4596PubMedCrossRefGoogle Scholar
  4. Aquea F, Vega A, Timmermann T, Poupin MJ, Arce-Johnson P (2011) Genome-wide analysis of the SET DOMAIN GROUP family in grapevine. Plant Cell Rep 30:1087–1097PubMedCrossRefGoogle Scholar
  5. Brunner S, Fengler K, Morgante M, Tingey S, Rafalski A (2005) Evolution of DNA sequence nonhomologies among maize inbreds. Plant Cell 17:343–360PubMedCrossRefGoogle Scholar
  6. Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10PubMedCrossRefGoogle Scholar
  7. Cheng SH, Willmann MR, Chen HC, Sheen J (2002) Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129:469–485PubMedCrossRefGoogle Scholar
  8. Chi Y, Cheng Y, Vanitha J, Kumar N, Ramamoorthy R, Ramachandran S, Jiang SY (2011) Expansion mechanisms and functional divergence of the glutathione s-transferase family in sorghum and other higher plants. DNA Res 18:1–16PubMedCrossRefGoogle Scholar
  9. Czemmel S, Stracke R, Weisshaar B, Cordon N, Harris NN, Walker AR, Robinson SP, Bogs J (2009) The grapevine R2R3-MYB transcription factor VvMYBF1 regulates flavonol synthesis in developing grape berries. Plant Physiol 151:1513–1530PubMedCrossRefGoogle Scholar
  10. Deluc L, Barrieu F, Marchive C, Lauvergeat V, Decendit A, Richard T, Carde JP, Merillon JM, Hamdi S (2006) Characterization of a grapevine R2R3-MYB transcription factor that regulates the phenylpropanoid pathway. Plant Physiol 140:499–511PubMedCrossRefGoogle Scholar
  11. Deluc L, Bogs J, Walker AR, Ferrier T, Decendit A, Merillon JM, Robinson SP, Barrieu F (2008) The transcription factor VvMYB5b contributes to the regulation of anthocyanin and proanthocyanidin biosynthesis in developing grape berries. Plant Physiol 147:2041–2053PubMedCrossRefGoogle Scholar
  12. Du D, Hao RJ, Cheng TR, Pan HT, Yang WR, Wang J, Zhang QX (2012) Genome-wide analysis of the AP2/ERF gene family in Prunus mume. Plant Mol Biol Rep. doi: 10.1007/s11105-012-0531-6
  13. Falginella L, Castellarin SD, Testolin R, Gambetta GA, Morgante M, Di Gaspero G (2010) Expansion and subfunctionalisation of flavonoid 3′,5′-hydroxylases in the grapevine lineage. BMC Genomics 11:562PubMedCrossRefGoogle Scholar
  14. Flagel LE, Wendel JF (2009) Gene duplication and evolutionary novelty in plants. New Phytol 183:557–564PubMedCrossRefGoogle Scholar
  15. Freeling M (2009) Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Annu Rev Plant Biol 60:433–453PubMedCrossRefGoogle Scholar
  16. Garcia-Fernandez J (2005) The genesis and evolution of homeobox gene clusters. Nat Rev Genet 6:881–892PubMedCrossRefGoogle Scholar
  17. Grimmig B, Gonzalez-Perez MN, Leubner-Metzger G, Vogeli-Lange R, Meins F Jr, Hain R, Penuelas J, Heidenreich B, Langebartels C, Ernst D, Sandermann H Jr (2003) Ozone-induced gene expression occurs via ethylene-dependent and -independent signalling. Plant Mol Biol 51:599–607PubMedCrossRefGoogle Scholar
  18. Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J, Bruyere C, Billault A, Segurens B, Gouyvenoux M, Ugarte E, Cattonaro F, Anthouard V, Vico V, Del Fabbro C, Alaux M, Di Gaspero G, Dumas V, Felice N, Paillard S, Juman I, Moroldo M, Scalabrin S, Canaguier A, Le Clainche I, Malacrida G, Durand E, Pesole G, Laucou V, Chatelet P, Merdinoglu D, Delledonne M, Pezzotti M, Lecharny A, Scarpelli C, Artiguenave F, Pe ME, Valle G, Morgante M, Caboche M, Adam-Blondon AF, Weissenbach J, Quetier F, Wincker P (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467PubMedCrossRefGoogle Scholar
  19. Jiang N, Bao Z, Zhang X, Eddy SR, Wessler SR (2004) Pack-MULE transposable elements mediate gene evolution in plants. Nature 431:569–573PubMedCrossRefGoogle Scholar
  20. Kaessmann H, Vinckenbosch N, Long M (2009) RNA-based gene duplication: mechanistic and evolutionary insights. Nat Rev Genet 10:19–31PubMedCrossRefGoogle Scholar
  21. Kiselev KV, Dubrovina AS, Veselova MV, Bulgakov VP, Fedoreyev SA, Zhuravlev YN (2007) The rolB gene-induced overproduction of resveratrol in Vitis amurensis transformed cells. J Biotechnol 128:681–692PubMedCrossRefGoogle Scholar
  22. Krysan PJ, Jester PJ, Gottwald JR, Sussman MR (2002) An Arabidopsis mitogen-activated protein kinase kinase kinase gene family encodes essential positive regulators of cytokinesis. Plant Cell 14:1109–1120PubMedCrossRefGoogle Scholar
  23. Licausi F, Giorgi FM, Zenoni S, Osti F, Pezzotti M, Perata P (2009) Genomic and transcriptomic analysis of the AP2/ERF superfamily in Vitis vinifera. BMC Genomics 11:719CrossRefGoogle Scholar
  24. Martin DM, Aubourg S, Schouwey MB, Daviet L, Schalk M, Toub O, Lund ST, Bohlmann J (2010) Functional annotation, genome organization and phylogeny of the grapevine (Vitis vinifera) terpene synthase gene family based on genome assembly, FLcDNA cloning, and enzyme assays. BMC Plant Biol 10:226PubMedCrossRefGoogle Scholar
  25. Matus JT, Aquea F, Arce-Johnson P (2008) Analysis of the grape MYB R2R3 subfamily reveals expanded wine quality-related clades and conserved gene structure organization across Vitis and Arabidopsis genomes. BMC Plant Biol 8:83PubMedCrossRefGoogle Scholar
  26. Michelmore RW, Meyers BC (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res 8:1113–1130PubMedGoogle Scholar
  27. O’Connor DJ, Wong RW, Rabie AB (2011) Resveratrol inhibits periodontal pathogens in vitro. Phytother Res 25:1727–1731PubMedCrossRefGoogle Scholar
  28. O’Toole N, Hattori M, Andres C, Iida K, Lurin C, Schmitz-Linneweber C, Sugita M, Small I (2008) On the expansion of the pentatricopeptide repeat gene family in plants. Mol Biol Evol 25:1120–1128PubMedCrossRefGoogle Scholar
  29. Omura T (1999) Forty years of cytochrome P450. Biochem Biophys Res Commun 266:690–698PubMedCrossRefGoogle Scholar
  30. Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Mehboobur R, Ware D, Westhoff P, Mayer KF, Messing J, Rokhsar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556PubMedCrossRefGoogle Scholar
  31. Richter TE, Ronald PC (2000) The evolution of disease resistance genes. Plant Mol Biol 42:195–204PubMedCrossRefGoogle Scholar
  32. Ronald PC (1998) Resistance gene evolution. Curr Opin Plant Biol 1:294–298PubMedCrossRefGoogle Scholar
  33. Rudrabhatla P, Reddy MM, Rajasekharan R (2006) Genome-wide analysis and experimentation of plant serine/threonine/tyrosine-specific protein kinases. Plant Mol Biol 60:293–319PubMedCrossRefGoogle Scholar
  34. Santamaria AR, Antonacci D, Caruso G, Cavaliere C, Gubbiotti R, Lagana A, Valletta A, Pasqua G (2010) Stilbene production in cell cultures of Vitis vinifera L. cvs Red Globe and Michele Palieri elicited by methyl jasmonate. Nat Prod Res 24:1488–1498PubMedCrossRefGoogle Scholar
  35. Schubert R, Fischer R, Hain R, Schreier PH, Bahnweg G, Ernst D, Sandermann H Jr (1997) An ozone-responsive region of the grapevine resveratrol synthase promoter differs from the basal pathogen-responsive sequence. Plant Mol Biol 34:417–426PubMedCrossRefGoogle Scholar
  36. Tassoni A, Fornale S, Franceschetti M, Musiani F, Michael AJ, Perry B, Bagni N (2005) Jasmonates and Na-orthovanadate promote resveratrol production in Vitis vinifera cv. Barbera cell cultures. New Phytol 166:895–905PubMedCrossRefGoogle Scholar
  37. This P, Lacombe T, Thomas MR (2006) Historical origins and genetic diversity of wine grapes. Trends Genet 22:511–519PubMedCrossRefGoogle Scholar
  38. Vannozzi A, Dry IB, Fasoli M, Zenoni S, Lucchin M (2012) Genome-wide analysis of the grapevine stilbene synthase multigenic family: genomic organization and expression profiles upon biotic and abiotic stresses. BMC Plant Biol 12:130PubMedCrossRefGoogle Scholar
  39. Velasco R, Zharkikh A, Troggio M, Cartwright DA, Cestaro A, Pruss D, Pindo M, Fitzgerald LM, Vezzulli S, Reid J, Malacarne G, Iliev D, Coppola G, Wardell B, Micheletti D, Macalma T, Facci M, Mitchell JT, Perazzolli M, Eldredge G, Gatto P, Oyzerski R, Moretto M, Gutin N, Stefanini M, Chen Y, Segala C, Davenport C, Dematte L, Mraz A, Battilana J, Stormo K, Costa F, Tao Q, Si-Ammour A, Harkins T, Lackey A, Perbost C, Taillon B, Stella A, Solovyev V, Fawcett JA, Sterck L, Vandepoele K, Grando SM, Toppo S, Moser C, Lanchbury J, Bogden R, Skolnick M, Sgaramella V, Bhatnagar SK, Fontana P, Gutin A, Van de Peer Y, Salamini F, Viola R (2007) A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS One 2:e1326PubMedCrossRefGoogle Scholar
  40. Wang W, Zheng H, Fan C, Li J, Shi J, Cai Z, Zhang G, Liu D, Zhang J, Vang S, Lu Z, Wong GK, Long M, Wang J (2006) High rate of chimeric gene origination by retroposition in plant genomes. Plant Cell 18:1791–1802PubMedCrossRefGoogle Scholar
  41. Wang Y, Wang X, Tang H, 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:e28150PubMedCrossRefGoogle Scholar
  42. Wang J, Zhang HB, Yang YM, Davies KM (2012a) Isolation and partial characterization of an R2R3MYB transcription factor from the bamboo species Fargesia fungosa. Plant Mol Biol Rep 30:131–138CrossRefGoogle Scholar
  43. Wang Y, Tang H, Debarry JD, Tan X, Li J, Wang X, Lee TH, Jin H, Marler B, Guo H, Kissinger JC, Paterson AH (2012b) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40:e49PubMedCrossRefGoogle Scholar
  44. Wang N, Zheng Y, Xin HP, Fang LC, Li SH (2013) Comprehensive analysis of NAC domain transcription factor gene family in Vitis vinifera. Plant Cell Rep 32:61–75PubMedCrossRefGoogle Scholar
  45. Yamamoto E, Knap HT (2001) Soybean receptor-like protein kinase genes: paralogous divergence of a gene family. Mol Biol Evol 18:1522–1531PubMedCrossRefGoogle Scholar
  46. Yang Y, He M, Zhu Z, Li S, Xu Y, Zhang C, Singer SD, Wang Y (2012) Identification of the dehydrin gene family from grapevine species and analysis of their responsiveness to various forms of abiotic and biotic stress. BMC Plant Biol 12:140PubMedCrossRefGoogle Scholar
  47. Zhang Z, Li J, Zhao XQ, Wang J, Wong GK, Yu J (2006) KaKs_Calculator: calculating Ka and Ks through model selection and model averaging. Genomics Proteomics Bioinforma 4:259–263CrossRefGoogle Scholar
  48. Zhang Z, Xiao J, Wu J, Zhang H, Liu G, Wang X, Dai L (2012) ParaAT: a parallel tool for constructing multiple protein-coding DNA alignments. Biochem Biophys Res Commun 419:779–781PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Key Laboratory of Plant Germplasm Enhancement and Speciality Agriculture, Wuhan Botanical GardenChinese Academy of SciencesWuhanChina
  2. 2.Graduate School of Chinese Academy of SciencesBeijingChina
  3. 3.Key Laboratory for Biological Effects of Nanomaterials and Nanosafety, Institute of High Energy PhysicsChinese Academy of SciencesBeijingChina
  4. 4.Wuhan Botanical GardenChinese Academy of SciencesWuhanChina

Personalised recommendations