Plant Molecular Biology Reporter

, Volume 32, Issue 6, pp 1129–1145 | Cite as

Genome-wide Comparative Analysis of the GRAS Gene Family in Populus, Arabidopsis and Rice

Original Paper

Abstract

GRAS genes belong to a gene family of transcription regulators that function in the regulation of plant growth and development. Our knowledge about the expansion and diversification of this gene family in flowering plants is presently limited to the herbaceous species Arabidopsis and rice. Numerous aspects, including the phylogenetic history, expansion, functional divergence and adaptive evolution await further study, especially in woody tree species. Based on the latest genome assemblies, we found 106, 34 and 60 putative GRAS genes in Populus, Arabidopsis and rice, respectively. Phylogenetic analysis revealed that GRAS proteins could be divided into at least 13 subfamilies. Tandem and segmental duplications are the most common expansion mechanisms of this gene family, and their frequent joint action may explain the rapid expansion in Populus. Site-specific shifts in evolutionary rates might be the main force driving subfamily-specific functional diversification. Adaptive evolution analysis revealed that GRAS genes have evolved mainly under purifying selection after duplication, suggesting that strong functional constraints have a bearing on the evolution of GRAS genes. Both expressed sequence tags (EST) and microarray data revealed that GRAS genes in Populus have broad expression patterns across a variety of organs/tissues. Expression divergence analyses between paralogous pairs of GRAS genes suggested that the retention of GRAS genes after duplication could be mainly attributed to substantial functional novelty such as neo-functionalization or sub-functionalization. Our study highlights the expansion and diversification of the GRAS gene family in Populus and provides the first comprehensive analysis of this gene family in the Populus genome.

Keywords

Adaptive evolution Expansion Expression The GRAS gene family Phylogeny Populus 

Supplementary material

11105_2014_721_MOESM1_ESM.pdf (576 kb)
Fig. S1Multiple sequence alignment of 176 GRAS domain sequences from Populus, Arabidopsis and rice. Conserved residues are shaded. The five conserved motifs within the domain (LHR I, VHIID, LHRII, PFYRE and SAM) are indicated above the sequence alignment following the study of Pysh et al. (1999) (PDF 575 kb)
11105_2014_721_MOESM2_ESM.pdf (870 kb)
Fig. S2The maximum likelihood tree and Bayesian inference tree based on 176 GRAS proteins from Populus, Arabidopsis and rice. a The ML tree was generated using the PhyML 3.0 program (Guindon et al. 2010; Guindon and Gascuel 2003) with 100 bootstrap replicates, using BIONJ distance-based starting tree and under the JTT + I + G + F model as inferred by the program ProtTest 2.4 (Abascal et al. 2005). b Under the same model of evolution, MrBayes 3.2.1 program (Ronquist and Huelsenbeck 2003) was used to construct the Bayesian inference (BI) tree. Three independent runs were performed with four Markov chains starting from random trees, each consisting of 2 million generations with trees sampled every 1,000 generations (PDF 870 kb)
11105_2014_721_MOESM3_ESM.pdf (489 kb)
Fig. S3Neighbor joining tree based on 176 full-length protein sequences of GRAS genes from Populus, Arabidopsis and rice (PDF 488 kb)
11105_2014_721_MOESM4_ESM.pdf (281 kb)
Fig. S4Frequency and distribution of critical amino acid sites responsible for type I functional divergence between subfamilies along the GRAS domain. The five conserved motifs within the domain are indicated with colored boxes (PDF 281 kb)
11105_2014_721_MOESM5_ESM.pdf (674 kb)
Fig. S5In silico expressed sequence tag (EST) analysis of Populus GRAS genes. EST frequency for each of the 39 Populus GRAS genes was counted by searching NCBI EST datasets from various libraries across a set of 18 organ/tissue types (PDF 673 kb)
11105_2014_721_MOESM6_ESM.xls (130 kb)
Table S1The GRAS genes identified in Arabidopsis, rice, Populus and other species. “ψ” prior to gene symbols indicates pseudogene fragments (XLS 129 kb)
11105_2014_721_MOESM7_ESM.xls (54 kb)
Table S2Tandem and segmental duplications of GRAS genes in Arabidopsis and rice. Genes in tandem clusters are indicated in red (XLS 53 kb)
11105_2014_721_MOESM8_ESM.xls (36 kb)
Table S3Type I functional divergence between subfamilies of GRAS genes (XLS 35 kb)
11105_2014_721_MOESM9_ESM.xls (43 kb)
Table S4Critical amino acid sites responsible for the type I functional divergence between subfamilies (XLS 43 kb)
11105_2014_721_MOESM10_ESM.xls (111 kb)
Table S5Sequence similarities, dN/dS ratios, and Pearson’s correlation coefficient of expression between paralogous genes in Arabidopsis, rice and Populus (XLS 111 kb)
11105_2014_721_MOESM11_ESM.xls (32 kb)
Table S6Likelihood ratio tests and parameter estimations for the six site models based on the coding sequences of 176 GRAS genes from Populus, Arabidopsis and rice (XLS 31 kb)
11105_2014_721_MOESM12_ESM.xls (40 kb)
Table S7Corresponding probe sets of Populus GRAS genes in Affymetrix microarray analysis (XLS 40 kb)

References

  1. Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104–2105PubMedCrossRefGoogle Scholar
  2. Aubourg S, Kreis M, Lecharny A (1999) The DEAD box RNA helicase family in Arabidopsis thaliana. Nucleic Acids Res 27:628–636PubMedCrossRefPubMedCentralGoogle Scholar
  3. Blanc G, Wolfe KH (2004) Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16:1679–1691PubMedCrossRefPubMedCentralGoogle Scholar
  4. Bolle C (2004) The role of GRAS proteins in plant signal transduction and development. Planta 218:683–692PubMedCrossRefGoogle Scholar
  5. Bolle C, Koncz C, Chua N-H (2000) PAT1, a new member of the GRAS family, is involved in phytochrome A signal transduction. Genes Dev 14:1269–1278PubMedPubMedCentralGoogle 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 4:10PubMedCrossRefPubMedCentralGoogle Scholar
  7. Cao J, Huang J, Yang Y, Hu X (2011) Analyses of the oligopeptide transporter gene family in poplar and grape. BMC Genomics 12:465PubMedCrossRefPubMedCentralGoogle Scholar
  8. Chaffey N (1999) Wood formation in forest trees: from Arabidopsis to Zinnia. Trends Plant Sci 4:203–204PubMedCrossRefGoogle Scholar
  9. Chai G, Hu R, Zhang D, Qi G, Zuo R, Cao Y, Chen P, Kong Y, Zhou G (2012) Comprehensive analysis of CCCH zinc finger family in poplar (Populus trichocarpa). BMC Genomics 13:253PubMedCrossRefPubMedCentralGoogle Scholar
  10. 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 18:1–16PubMedCrossRefPubMedCentralGoogle Scholar
  11. Dean EJ, Davis JC, Davis RW, Petrov DA (2008) Pervasive and persistent redundancy among duplicated genes in yeast. PLoS Genet 4:e1000113PubMedCrossRefPubMedCentralGoogle Scholar
  12. Demuth JP, Hahn MW (2009) The life and death of gene families. Bioessays 31:29–39PubMedCrossRefGoogle Scholar
  13. Di Laurenzio L, Wysocka-Diller J, Malamy JE, Pysh L, Helariutta Y, Freshour G, Hahn MG, Feldmann KA, Benfey PN (1996) The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86:423–433PubMedCrossRefGoogle Scholar
  14. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797PubMedCrossRefPubMedCentralGoogle Scholar
  15. Engstrom EM (2011) Phylogenetic analysis of GRAS proteins from moss, lycophyte and vascular plant lineages reveals that GRAS genes arose and underwent substantial diversification in the ancestral lineage common to bryophytes and vascular plants. Plant Signal Behav 6:850PubMedCrossRefPubMedCentralGoogle Scholar
  16. 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
  17. Fujita M, Horiuchi Y, Ueda Y, Mizuta Y, Kubo T, Yano K, Yamaki S, Tsuda K, Nagata T, Niihama M (2010) Rice expression atlas in reproductive development. Plant Cell Physiol 51:2060–2081PubMedCrossRefGoogle Scholar
  18. Gautier L, Cope L, Bolstad BM, Irizarry RA (2004) affy—analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20:307–315PubMedCrossRefGoogle Scholar
  19. Georgelis N, Braun EL, Hannah LC (2008) Duplications and functional divergence of ADP-glucose pyrophosphorylase genes in plants. BMC Evol Biol 8:232PubMedCrossRefPubMedCentralGoogle Scholar
  20. Greb T, Clarenz O, Schafer E, Muller D, Herrero R, Schmitz G, Theres K (2003) Molecular analysis of the LATERAL SUPPRESSOR gene in Arabidopsis reveals a conserved control mechanism for axillary meristem formation. Genes Dev 17:1175–1187PubMedCrossRefPubMedCentralGoogle Scholar
  21. Gu J, Wang Y, Gu X (2002) Evolutionary analysis for functional divergence of Jak protein kinase domains and tissue-specific genes. J Mol Evol 54:725–733PubMedCrossRefGoogle Scholar
  22. Gu X (1999) Statistical methods for testing functional divergence after gene duplication. Mol Biol Evol 16:1664–1674PubMedCrossRefGoogle Scholar
  23. Gu X (2001) Maximum-likelihood approach for gene family evolution under functional divergence. Mol Biol Evol 18:453–464PubMedCrossRefGoogle Scholar
  24. Gu X (2006) A simple statistical method for estimating type-II (cluster-specific) functional divergence of protein sequences. Mol Biol Evol 23:1937–1945PubMedCrossRefGoogle Scholar
  25. Gu X, Vander Velden K (2002) DIVERGE: phylogeny-based analysis for functional–structural divergence of a protein family. Bioinformatics 18:500–501PubMedCrossRefGoogle Scholar
  26. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321PubMedCrossRefGoogle Scholar
  27. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704PubMedCrossRefGoogle Scholar
  28. Hanada K, Zou C, Lehti-Shiu MD, Shinozaki K, Shiu SH (2008) Importance of lineage-specific expansion of plant tandem duplicates in the adaptive response to environmental stimuli. Plant Physiol 148:993–1003PubMedCrossRefPubMedCentralGoogle Scholar
  29. Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, Sena G, Hauser M-T, Benfey PN (2000) The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101:555–567PubMedCrossRefGoogle Scholar
  30. Heo JO, Chang KS, Kim IA, Lee MH, Lee SA, Song SK, Lee MM, Lim J (2011) Funneling of gibberellin signaling by the GRAS transcription regulator SCARECROW-LIKE 3 in the Arabidopsis root. Proc Natl Acad Sci 108:2166–2171PubMedCrossRefPubMedCentralGoogle Scholar
  31. Hu R, Chi X, Chai G, Kong Y, He G, Wang X, Shi D, Zhang D, Zhou G (2012) Genome-wide identification, evolutionary expansion, and expression profile of homeodomain-leucine zipper gene family in poplar (Populus trichocarpa). PLoS One 7:e31149PubMedCrossRefPubMedCentralGoogle Scholar
  32. Jaillon O, Aury J-M, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467PubMedCrossRefGoogle Scholar
  33. Jain M, Khurana P, Tyagi AK, Khurana JP (2008) Genome-wide analysis of intronless genes in rice and Arabidopsis. Funct Integr Genomics 8:69–78PubMedCrossRefGoogle Scholar
  34. Jain M, Nijhawan A, Arora R, Agarwal P, Ray S, Sharma P, Kapoor S, Tyagi AK, Khurana JP (2007) F-box proteins in rice. Genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress. Plant Physiol 143:1467–1483PubMedCrossRefPubMedCentralGoogle Scholar
  35. Jain M, Tyagi AK, Khurana JP (2006) Genome-wide analysis, evolutionary expansion, and expression of early auxin-responsive SAUR gene family in rice Oryza sativa. Genomics 88:360–371PubMedCrossRefGoogle Scholar
  36. Jansson S, Douglas CJ (2007) Populus: a model system for plant biology. Annu Rev Plant Biol 58:435–458PubMedCrossRefGoogle Scholar
  37. Jiang SY, Ma Z, Ramachandran S (2010) Evolutionary history and stress regulation of the lectin superfamily in higher plants. BMC Evol Biol 10:79PubMedCrossRefPubMedCentralGoogle Scholar
  38. Krzywinski M, Schein J, Birol İ, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645PubMedCrossRefPubMedCentralGoogle Scholar
  39. Kullan AR, van Dyk MM, Hefer CA, Jones N, Kanzler A, Myburg AA (2012) Genetic dissection of growth, wood basic density and gene expression in interspecific backcrosses of Eucalyptus grandis and E. urophylla. BMC Genet 13:60PubMedCrossRefPubMedCentralGoogle Scholar
  40. Kulmuni J, Wurm Y, Pamilo P (2013) Comparative genomics of chemosensory protein genes reveals rapid evolution and positive selection in ant-specific duplicates. Heredity (Edinb) 110:538–547CrossRefGoogle Scholar
  41. Lan T, Yang ZL, Yang X, Liu YJ, Wang XR, Zeng QY (2009) Extensive functional diversification of the Populus glutathione S-transferase supergene family. Plant Cell 21:3749–3766PubMedCrossRefPubMedCentralGoogle Scholar
  42. Lehti-Shiu MD, Zou C, Hanada K, Shiu SH (2009) Evolutionary history and stress regulation of plant receptor-like kinase/pelle genes. Plant Physiol 150:12–26PubMedCrossRefPubMedCentralGoogle Scholar
  43. Lei L, Zhou SL, Ma H, Zhang LS (2012) Expansion and diversification of the SET domain gene family following whole-genome duplications in Populus trichocarpa. BMC Evol Biol 12:51PubMedCrossRefPubMedCentralGoogle Scholar
  44. Li W, Liu B, Yu L, Feng D, Wang H, Wang J (2009) Phylogenetic analysis, structural evolution and functional divergence of the 12-oxo-phytodienoate acid reductase gene family in plants. BMC Evol Biol 9:90PubMedCrossRefPubMedCentralGoogle Scholar
  45. Liu Q, Wang H, Zhang Z, Wu J, Feng Y, Zhu Z (2009) Divergence in function and expression of the NOD26-like intrinsic proteins in plants. BMC Genomics 10:313PubMedCrossRefPubMedCentralGoogle Scholar
  46. Liu Q, Zhang C, Yang Y, Hu X (2010) Genome-wide and molecular evolution analyses of the phospholipase D gene family in Poplar and Grape. BMC Plant Biol 10:117PubMedCrossRefPubMedCentralGoogle Scholar
  47. Lurin C, Andrés C, Aubourg S, Bellaoui M, Bitton F, Bruyère C, Caboche M, Debast C, Gualberto J, Hoffmann B (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16:2089–2103PubMedCrossRefPubMedCentralGoogle Scholar
  48. Lynch M, Conery J (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155PubMedCrossRefGoogle Scholar
  49. Ma HS, Liang D, Shuai P, Xia XL, Yin WL (2010) The salt- and drought-inducible poplar GRAS protein SCL7 confers salt and drought tolerance in Arabidopsis thaliana. J Exp Bot 61:4011–4019PubMedCrossRefPubMedCentralGoogle Scholar
  50. Morohashi K, Minami M, Takase H, Hotta Y, Hiratsuka K (2003) Isolation and characterization of a novel GRAS gene that regulates meiosis-associated gene expression. J Biol Chem 278:20865–20873PubMedCrossRefGoogle Scholar
  51. Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M, Childs K, Thibaud-Nissen F, Malek RL, Lee Y, Zheng L (2007) The TIGR rice genome annotation resource: improvements and new features. Nucleic Acids Res 35:D883–D887PubMedCrossRefPubMedCentralGoogle Scholar
  52. Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556PubMedCrossRefGoogle Scholar
  53. Peng J, Carol P, Richards DE, King KE, Cowling RJ, Murphy GP, Harberd NP (1997) The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Gene Dev 11:3194–3205PubMedCrossRefPubMedCentralGoogle Scholar
  54. Petre B, Major I, Rouhier N, Duplessis S (2011) Genome-wide analysis of eukaryote thaumatin-like proteins (TLPs) with an emphasis on poplar. BMC Plant Biol 11:33PubMedCrossRefPubMedCentralGoogle Scholar
  55. Plomion C, Leprovost G, Stokes A (2001) Wood formation in trees. Plant Physiol 127:1513–1523PubMedCrossRefPubMedCentralGoogle Scholar
  56. Pysh LD, Wysocka-Diller JW, Camilleri C, Bouchez D, Benfey PN (1999) The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J 18:111–119PubMedCrossRefGoogle Scholar
  57. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  58. Saeed A, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34:374PubMedGoogle Scholar
  59. Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Schölkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37:501–506PubMedCrossRefGoogle Scholar
  60. Schumacher K, Schmitt T, Rossberg M, Schmitz G, Theres K (1999) The Lateral suppressor (Ls) gene of tomato encodes a new member of the VHIID protein family. Proc Natl Acad Sci 96:290–295PubMedCrossRefPubMedCentralGoogle Scholar
  61. Stuurman J, Jäggi F, Kuhlemeier C (2002) Shoot meristem maintenance is controlled by a GRAS-gene mediated signal from differentiating cells. Genes Dev 16:2213–2218PubMedCrossRefPubMedCentralGoogle Scholar
  62. Sun X, Jones WT, Rikkerink EH (2012) GRAS proteins: the versatile roles of intrinsically disordered proteins in plant signalling. Biochem J 442:1–12PubMedCrossRefGoogle Scholar
  63. Sun X, Xue B, Jones WT, Rikkerink E, Dunker AK, Uversky VN (2011) A functionally required unfoldome from the plant kingdom: intrinsically disordered N-terminal domains of GRAS proteins are involved in molecular recognition during plant development. Plant Mol Biol 77:205–223PubMedCrossRefGoogle Scholar
  64. Suyama M, Torrents D, Bork P (2006) PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 34:W609–W612PubMedCrossRefPubMedCentralGoogle Scholar
  65. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCrossRefPubMedCentralGoogle Scholar
  66. Tang H, Bowers JE, Wang X, Ming R, Alam M, Paterson AH (2008) Synteny and collinearity in plant genomes. Science 320:486–488PubMedCrossRefGoogle Scholar
  67. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882PubMedCrossRefPubMedCentralGoogle Scholar
  68. Tian C, Wan P, Sun S, Li J, Chen M (2004) Genome-wide analysis of the GRAS gene family in rice and Arabidopsis. Plant Mol Biol 54:519–532PubMedCrossRefGoogle Scholar
  69. Tong H, Jin Y, Liu W, Li F, Fang J, Yin Y, Qian Q, Zhu L, Chu C (2009) DWARF AND LOW‐TILLERING, a new member of the GRAS family, plays positive roles in brassinosteroid signaling in rice. Plant J 58:803–816PubMedCrossRefGoogle Scholar
  70. Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604PubMedCrossRefGoogle Scholar
  71. Verde I, Abbott AG, Scalabrin S, Jung S, Shu S, Marroni F, Zhebentyayeva T, Dettori MT, Grimwood J, Cattonaro F (2013) The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet 45:487–494PubMedCrossRefGoogle Scholar
  72. Viiri KM, Heinonen TY, Maki M, Lohi O (2009) Phylogenetic analysis of the SAP30 family of transcriptional regulators reveals functional divergence in the domain that binds the nuclear matrix. BMC Evol Biol 9:149PubMedCrossRefPubMedCentralGoogle Scholar
  73. Wang J, Andersson-Gunneras S, Gaboreanu I, Hertzberg M, Tucker MR, Zheng B, Lesniewska J, Mellerowicz EJ, Laux T, Sandberg G et al (2011a) Reduced expression of the SHORT-ROOT gene increases the rates of growth and development in hybrid poplar and Arabidopsis. PLoS One 6:e28878PubMedCrossRefPubMedCentralGoogle Scholar
  74. Wang J, Zhou J, Zhang B, Vanitha J, Ramachandran S, Jiang SY (2011b) Genome-wide expansion and expression divergence of the basic leucine zipper transcription factors in higher plants with an emphasis on sorghum. J Integr Plant Biol 53:212–231PubMedCrossRefGoogle Scholar
  75. Wang Y, Gu X (2001) Functional divergence in the caspase gene family and altered functional constraints: statistical analysis and prediction. Genetics 158:1311–1320PubMedPubMedCentralGoogle Scholar
  76. Wilkins O, Nahal H, Foong J, Provart NJ, Campbell MM (2009) Expansion and diversification of the Populus R2R3-MYB family of transcription factors. Plant Physiol 149:981–993PubMedCrossRefPubMedCentralGoogle Scholar
  77. Xu Q, Chen L-L, Ruan X, Chen D, Zhu A, Chen C, Bertrand D, Jiao W-B, Hao B-H, Lyon MP (2012) The draft genome of sweet orange (Citrus sinensis). Nat Genet 45:59–66PubMedCrossRefGoogle Scholar
  78. Yang X, Kalluri UC, DiFazio SP, Wullschleger SD, Tschaplinski TJ, Cheng MZ-M, Tuskan GA (2009) Poplar genomics: state of the science. Crit Rev Plant Sci 28:285–308CrossRefGoogle Scholar
  79. Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591PubMedCrossRefGoogle Scholar
  80. Yang Z, Nielsen R, Goldman N, Pedersen AMK (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431–449PubMedPubMedCentralGoogle Scholar
  81. Yang Z, Wang X, Gu S, Hu Z, Xu H, Xu C (2008) Comparative study of SBP-box gene family in Arabidopsis and rice. Gene 407:1–11PubMedCrossRefGoogle Scholar
  82. Yang Z, Wong WS, Nielsen R (2005) Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22:1107–1118PubMedCrossRefGoogle Scholar
  83. Young ND, Debellé F, Oldroyd GE, Geurts R, Cannon SB, Udvardi MK, Benedito VA, Mayer KF, Gouzy J, Schoof H (2011) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480:520–524PubMedCrossRefPubMedCentralGoogle Scholar
  84. Zhang D, Iyer LM, Aravind L (2012) Bacterial GRAS domain proteins throw new light on gibberellic acid response mechanisms. Bioinformatics 28:2407–2411PubMedCrossRefPubMedCentralGoogle Scholar
  85. Zou M, Guo B, He S (2011) The roles and evolutionary patterns of intronless genes in deuterostomes. Comp Funct Genomics 2011:1–8CrossRefGoogle Scholar
  86. Zouine M, Latché A, Rousseau C, Regad F, Pech J-C, Philippot M, Bouzayen M, Delalande C, Frasse P, Schiex T (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.ETH Zürich, Institute of Integrative BiologyZurichSwitzerland

Personalised recommendations