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International Journal of Genomics
Volume 2015, Article ID 536943, 11 pages
http://dx.doi.org/10.1155/2015/536943
Research Article

Divergence of the bZIP Gene Family in Strawberry, Peach, and Apple Suggests Multiple Modes of Gene Evolution after Duplication

College of Horticulture, Nanjing Agricultural University, Nanjing 210095, China

Received 15 September 2015; Revised 10 November 2015; Accepted 11 November 2015

Academic Editor: Yanbin Yin

Copyright © 2015 Xiao-Long Wang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. P. Scott, “Development: the natural history of genes,” Cell, vol. 100, no. 1, pp. 27–40, 2000. View at Publisher · View at Google Scholar · View at Scopus
  2. S. B. Carroll, “Endless forms: the evolution of gene regulation and morphological diversity,” Cell, vol. 101, no. 6, pp. 577–580, 2000. View at Publisher · View at Google Scholar · View at Scopus
  3. P. Pérez-Rodríguez, D. M. Riaño-Pachón, L. G. G. Corrêa, S. A. Rensing, B. Kersten, and B. Mueller-Roeber, “PlnTFDB: updated content and new features of the plant transcription factor database,” Nucleic Acids Research, vol. 38, supplement 1, Article ID gkp805, pp. D822–D827, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. H. C. Hurst, “Transcription factors. 1: bZIP proteins,” Protein Profile, vol. 1, no. 2, pp. 123–168, 1993. View at Google Scholar · View at Scopus
  5. M. Jakoby, B. Weisshaar, W. Dröge-Laser et al., “bZIP transcription factors in Arabidopsis,” Trends in Plant Science, vol. 7, no. 3, pp. 106–111, 2002. View at Publisher · View at Google Scholar · View at Scopus
  6. A. Nijhawan, M. Jain, A. K. Tyagi, and J. P. Khurana, “Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice,” Plant Physiology, vol. 146, no. 2, pp. 333–350, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. S. C. Lee, H. W. Choi, I. S. Hwang, D. S. Choi, and B. K. Hwang, “Functional roles of the pepper pathogen-induced bZIP transcription factor, CAbZIP1, in enhanced resistance to pathogen infection and environmental stresses,” Planta, vol. 224, no. 5, pp. 1209–1225, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. O. Yang, O. V. Popova, U. Süthoff, I. Lüking, K.-J. Dietz, and D. Golldack, “The Arabidopsis basic leucine zipper transcription factor AtbZIP24 regulates complex transcriptional networks involved in abiotic stress resistance,” Gene, vol. 436, no. 1-2, pp. 45–55, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. F. Weltmeier, F. Rahmani, A. Ehlert et al., “Expression patterns within the Arabidopsis C/S1 bZIP transcription factor network: availability of heterodimerization partners controls gene expression during stress response and development,” Plant Molecular Biology, vol. 69, no. 1-2, pp. 107–119, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. Y. Xiang, N. Tang, H. Du, H. Ye, and L. Xiong, “Characterization of OsbZIP23 as a key player of the basic leucine zipper transcription factor family for conferring abscisic acid sensitivity and salinity and drought tolerance in rice,” Plant Physiology, vol. 148, no. 4, pp. 1938–1952, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. G. Lu, C. Gao, X. Zheng, and B. Han, “Identification of OsbZIP72 as a positive regulator of ABA response and drought tolerance in rice,” Planta, vol. 229, no. 3, pp. 605–615, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. H. Shimizu, K. Sato, T. Berberich et al., “LIP19, a basic region leucine zipper protein, is a Fos-like molecular switch in the cold signaling of rice plants,” Plant and Cell Physiology, vol. 46, no. 10, pp. 1623–1634, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Zou, Y. Guan, H. Ren, F. Zhang, and F. Chen, “A bZIP transcription factor, OsABI5, is involved in rice fertility and stress tolerance,” Plant Molecular Biology, vol. 66, no. 6, pp. 675–683, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. M. A. Hossain, J.-I. Cho, M. Han et al., “The ABRE-binding bZIP transcription factor OsABF2 is a positive regulator of abiotic stress and ABA signaling in rice,” Journal of Plant Physiology, vol. 167, no. 17, pp. 1512–1520, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. Z. Jin, W. Xu, and A. Liu, “Genomic surveys and expression analysis of bZIP gene family in castor bean (Ricinus communis L.),” Planta, vol. 239, no. 2, pp. 299–312, 2014. View at Publisher · View at Google Scholar · View at Scopus
  16. K. Wei, J. Chen, Y. Wang et al., “Genome-wide analysis of bZIP-encoding genes in maize,” DNA Research, vol. 19, no. 6, pp. 463–476, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. J. Wang, J. Zhou, B. Zhang, J. Vanitha, S. Ramachandran, and S.-Y. Jiang, “Genome-wide expansion and expression divergence of the basic leucine zipper transcription factors in higher plants with an emphasis on sorghum,” Journal of Integrative Plant Biology, vol. 53, no. 3, pp. 212–231, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. M. C. Baloglu, V. Eldem, M. Hajyzadeh, and T. Unver, “Genome-wide analysis of the bZIP transcription factors in cucumber,” PLoS ONE, vol. 9, no. 4, Article ID e96014, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. J. Liu, N. Chen, F. Chen et al., “Genome-wide analysis and expression profile of the bZIP transcription factor gene family in grapevine (Vitis vinifera),” BMC Genomics, vol. 15, no. 1, article 281, 2014. View at Publisher · View at Google Scholar · View at Scopus
  20. T. Wicker, N. Yahiaoui, and B. Keller, “Illegitimate recombination is a major evolutionary mechanism for initiating size variation in plant resistance genes,” The Plant Journal, vol. 51, no. 4, pp. 631–641, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. E. Dirlewanger, P. Cosson, M. Tavaud et al., “Development of microsatellite markers in peach [Prunus persica (L.) Batsch] and their use in genetic diversity analysis in peach and sweet cherry (Prunus avium L.),” Theoretical and Applied Genetics, vol. 105, no. 1, pp. 127–138, 2002. View at Publisher · View at Google Scholar · View at Scopus
  22. D. Potter, T. Eriksson, R. C. Evans et al., “Phylogeny and classification of Rosaceae,” Plant Systematics and Evolution, vol. 266, no. 1-2, pp. 5–43, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. E. Illa, D. J. Sargent, E. L. Girona et al., “Comparative analysis of rosaceous genomes and the reconstruction of a putative ancestral genome for the family,” BMC Evolutionary Biology, vol. 11, article 9, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. D. R. Morgan, D. E. Soltis, and K. R. Robertson, “Systematic and evolutionary implications of RBCL sequence variation in Rosaceae,” American Journal of Botany, vol. 81, no. 7, pp. 890–903, 1994. View at Publisher · View at Google Scholar · View at Scopus
  25. D. Potter, F. Gao, P. E. Bortiri, S.-H. Oh, and S. Baggett, “Phylogenetic relationships in Rosaceae inferred from chloroplast matK and trnL-trnF nucleotide sequence data,” Plant Systematics and Evolution, vol. 231, no. 1–4, pp. 77–89, 2002. View at Publisher · View at Google Scholar · View at Scopus
  26. V. Shulaev, D. J. Sargent, R. N. Crowhurst et al., “The genome of woodland strawberry (Fragaria vesca),” Nature Genetics, vol. 43, no. 2, pp. 109–116, 2011. View at Publisher · View at Google Scholar
  27. R. Velasco, A. Zharkikh, J. Affourtit et al., “The genome of the domesticated apple (Malus×domestica Borkh.),” Nature Genetics, vol. 42, no. 10, pp. 833–839, 2010. View at Publisher · View at Google Scholar
  28. I. Verde, A. G. Abbott, S. Scalabrin et al., “The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution,” Nature Genetics, vol. 45, no. 5, pp. 487–494, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. D. M. Goodstein, S. Shu, R. Howson et al., “Phytozome: a comparative platform for green plant genomics,” Nucleic Acids Research, vol. 40, no. 1, pp. D1178–D1186, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Punta, P. C. Coggill, R. Y. Eberhardt et al., “The Pfam protein families database,” Nucleic Acids Research, vol. 40, no. 1, pp. D290–D301, 2012. View at Publisher · View at Google Scholar · View at Scopus
  31. S. R. Eddy, “Profile hidden Markov models,” Bioinformatics, vol. 14, no. 9, pp. 755–763, 1998. View at Publisher · View at Google Scholar · View at Scopus
  32. I. Letunic, T. Doerks, and P. Bork, “SMART 7: recent updates to the protein domain annotation resource,” Nucleic Acids Research, vol. 40, no. 1, pp. D302–D305, 2012. View at Publisher · View at Google Scholar · View at Scopus
  33. J. D. Thompson, T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins, “The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools,” Nucleic Acids Research, vol. 25, no. 24, pp. 4876–4882, 1997. View at Publisher · View at Google Scholar · View at Scopus
  34. K. Tamura, J. Dudley, M. Nei, and S. Kumar, “MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0,” Molecular Biology and Evolution, vol. 24, no. 8, pp. 1596–1599, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. N. Saitou and M. Nei, “The neighbor-joining method: a new method for reconstructing phylogenetic trees,” Molecular Biology and Evolution, vol. 4, no. 4, pp. 406–425, 1987. View at Google Scholar · View at Scopus
  36. T.-H. Lee, H. Tang, X. Wang, and A. H. Paterson, “PGDD: a database of gene and genome duplication in plants,” Nucleic Acids Research, vol. 41, no. 1, pp. D1152–D1158, 2013. View at Publisher · View at Google Scholar · View at Scopus
  37. M. A. Larkin, G. Blackshields, N. P. Brown et al., “Clustal W and Clustal X version 2.0,” Bioinformatics, vol. 23, no. 21, pp. 2947–2948, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. K. Tamura, D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar, “MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods,” Molecular Biology and Evolution, vol. 28, no. 10, pp. 2731–2739, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. R. D. Finn, A. Bateman, J. Clements et al., “Pfam: the protein families database,” Nucleic Acids Research, vol. 42, no. 1, pp. D222–D230, 2013. View at Publisher · View at Google Scholar
  40. W. H. Landschulz, P. F. Johnson, and S. L. McKnight, “The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins,” Science, vol. 240, no. 4860, pp. 1759–1764, 1988. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Krzywinski, J. Schein, I. Birol et al., “Circos: an information aesthetic for comparative genomics,” Genome Research, vol. 19, no. 9, pp. 1639–1645, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Jung, A. Cestaro, M. Troggio et al., “Whole genome comparisons of Fragaria, Prunus and Malus reveal different modes of evolution between Rosaceous subfamilies,” BMC Genomics, vol. 13, article 129, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. M. A. Hossain, Y. Lee, J.-I. Cho et al., “The bZIP transcription factor OsABF1 is an ABA responsive element binding factor that enhances abiotic stress signaling in rice,” Plant Molecular Biology, vol. 72, no. 4, pp. 557–566, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. J.-Y. Kang, H.-I. Choi, M.-Y. Im, and Y. K. Soo, “Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling,” The Plant Cell, vol. 14, no. 2, pp. 343–357, 2002. View at Publisher · View at Google Scholar · View at Scopus
  45. S.-J. Oh, I. S. Sang, S. K. Youn et al., “Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth,” Plant Physiology, vol. 138, no. 1, pp. 341–351, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. H. Tak and M. Mhatre, “Cloning and molecular characterization of a putative bZIP transcription factor VvbZIP23 from Vitis vinifera,” Protoplasma, vol. 250, no. 1, pp. 333–345, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. Y. Uno, T. Furihata, H. Abe, R. Yoshida, K. Shinozaki, and K. Yamaguchi-Shinozaki, “Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 21, pp. 11632–11637, 2000. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Yu, S. Tehrim, F. Zhang et al., “Genome-wide comparative analysis of NBS-encoding genes between Brassica species and Arabidopsis thaliana,” BMC Genomics, vol. 15, no. 1, article 3, 2014. View at Publisher · View at Google Scholar · View at Scopus
  49. Y. Jiao, N. J. Wickett, S. Ayyampalayam et al., “Ancestral polyploidy in seed plants and angiosperms,” Nature, vol. 473, no. 7345, pp. 97–100, 2011. View at Publisher · View at Google Scholar · View at Scopus
  50. S. Proost, P. Pattyn, T. Gerats, and Y. Van De Peer, “Journey through the past: 150 million years of plant genome evolution,” Plant Journal, vol. 66, no. 1, pp. 58–65, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. F. Cheng, J. Wu, and X. Wang, “Genome triplication drove the diversification of Brassica plants,” Horticulture Research, vol. 1, Article ID 14024, 2014. View at Publisher · View at Google Scholar
  52. M. Kellis, B. W. Birren, and E. S. Lander, “Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae,” Nature, vol. 428, no. 6983, pp. 617–624, 2004. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Freeling, “The evolutionary position of subfunctionalization, downgraded,” Genome Dynamics, vol. 4, pp. 25–40, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. M. Freeling, “Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition,” Annual Review of Plant Biology, vol. 60, pp. 433–453, 2009. View at Publisher · View at Google Scholar · View at Scopus
  55. J. Yang, Z. L. Wang, X. Q. Zhao et al., “Natural selection and adaptive evolution of leptin in the Ochotona family driven by the cold environmental stress,” PLoS ONE, vol. 3, no. 1, Article ID e1472, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. Z. Yang, R. Nielsen, N. Goldman, and A.-M. K. Pedersen, “Codon-substitution models for heterogeneous selection pressure at amino acid sites,” Genetics, vol. 155, no. 1, pp. 431–449, 2000. View at Google Scholar · View at Scopus
  57. X. Zhao, Q. Yu, L. Huang, Q. Liu, and A. Asakura, “Patterns of positive selection of the myogenic regulatory factor gene family in vertebrates,” PLoS ONE, vol. 9, no. 3, Article ID e92873, 2014. View at Publisher · View at Google Scholar
  58. T. Kusano, T. Berberich, M. Harada, N. Suzuki, and K. Sugawara, “A maize DNA-binding factor with a bZIP motif is induced by low temperature,” Molecular & General Genetics, vol. 248, no. 5, pp. 507–517, 1995. View at Publisher · View at Google Scholar · View at Scopus
  59. J. F. Martinez-García, E. Moyano, M. J. C. Alcocer, and C. Martin, “Two bZIP proteins from Antirrhinum flowers preferentially bind a hybrid C-box/G-box motif and help to define a new sub-family of bZIP transcription factors,” Plant Journal, vol. 13, no. 4, pp. 489–505, 1998. View at Publisher · View at Google Scholar · View at Scopus
  60. A. Strathmann, M. Kuhlmann, T. Heinekamp, and W. Dröge-Laser, “BZI-1 specifically heterodimerises with the tobacco bZIP transcription factors BZI-2, BZI-3/TBZF and BZI-4, and is functionally involved in flower development,” The Plant Journal, vol. 28, no. 4, pp. 397–408, 2001. View at Publisher · View at Google Scholar · View at Scopus
  61. E. Dirlewanger, E. Graziano, T. Joobeur et al., “Comparative mapping and marker-assisted selection in Rosaceae fruit crops,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 26, pp. 9891–9896, 2004. View at Publisher · View at Google Scholar · View at Scopus
  62. S. Vilanova, D. J. Sargent, P. Arús, and A. Monfort, “Synteny conservation between two distantly-related Rosaceae genomes: Prunus (the stone fruits) and Fragaria (the strawberry),” BMC Plant Biology, vol. 8, no. 1, article 67, 2008. View at Publisher · View at Google Scholar · View at Scopus
  63. K. Sax, “The origin of the Pomoideae,” Proceedings of the American Society for Horticultural Science, vol. 30, pp. 147–150, 1933. View at Google Scholar
  64. C. Sterling, “Comparative morphology of the carpel in the Rosaceae. I. Prunoideae: Prunus,” American Journal of Botany, vol. 51, no. 1, pp. 36–44, 1964. View at Publisher · View at Google Scholar