Biologia Plantarum

, Volume 61, Issue 3, pp 473–482 | Cite as

Soybean NAC gene family: sequence analysis and expression under low nitrogen supply

  • X. WangEmail author
  • D. Li
  • J. Jiang
  • Z. Dong
  • Y. Ma
Original paper


NAM, ATAF1/2, and CUC2 (NAC) proteins are plant-specific transcription factors playing essential roles in plant development and various abiotic stress responses. In the present study, we identified 173 full-length NAC genes in soybean, which were phylogenetically clustered into 15 groups (NACa - NACo). The soybean NAC genes (GmNACs) were non-randomly located across the 20 chromosomes, and 128 genes (86.5 %) were preferentially located in duplicated regions of chromosome arms, which implied long segmental duplication and contributed to evolution of the GmNAC gene family. Most GmNACs genes showed a distinct tissue-specific expression pattern and the redundant expression patterns of active duplicate genes suggested that GmNACs have been retained by substantial subfunctionalization during soybean evolution. Furthermore, active GmNACs genes that had undergone strong artificial selection during soybean domestication were identified based on selection analysis. After low nitrogen treatment, enhanced expression of some selected GmNAC genes were noticed in soybean shoot and root, which implied that GmNACs might play an important role in nitrogen metabolism. Here, we summarize the sequence and expression analysis of the NAC gene family in the soybean.

Additional key words

chromosome location evolution Glycine max nitrogen metabolism transcription factors 



ABA responsive element binding protein


Arabidopsis transcription activation factor


cup-shaped cotyledon


milliard year ago


NAM, ATAF1/2 and CUC2


no apical meristem


single nucleotide polymorphism


transcription factor


WRKY DNA-binding protein


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  1. Bu, Q.Y., Jiang, H.L., Li, C.B., Zhai, Q.Z., Zhang, J.Y., Wu, X.Q., Sun, J.Q., Xie, Q., Li, C.Y.: Role of the Arabidopsis thaliana NAC transcription factors ANAC019 and ANAC055 in regulating jasmonic acid-signaled defense responses. — Cell Res. 18: 756–767, 2008.CrossRefPubMedGoogle Scholar
  2. Cannon, E.K., Cannon, S.B.: Chromosome visualization tool: a whole genome viewer. — Int. J. Plant Genomics 2011: 373875, 2011.PubMedPubMedCentralGoogle Scholar
  3. Cenci, A., Guignon, V., Roux, N., Rouard, M.: Genomic analysis of NAC transcription factors in banana (Musa acuminata) and definition of NAC orthologous groups for monocots and dicots. — Plant. mol. Biol. 85: 63–80, 2014.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Chen, Y.J., Perera, V., Christiansen, M.W., Holme, I.B., Gregersen, P.L., Grant, M.R., Collinge, D.B., Lyngkjaer M.F.: The barley HvNAC6 transcription factor affects ABA accumulation and promotes basal resistance against powdery mildew. — Plant mol. Biol. 83: 577–590, 2013.CrossRefPubMedGoogle Scholar
  5. Chuck, G.S., Brown, P.J., Meeley, R., Hake, S.: Maize SBP-box transcription factors unbranched2 and unbranched3 affect yield traits by regulating the rate of lateral primordia initiation. — Proc. nat. Acad. Sci. USA 111: 18775–18780, 2014. DeCrossRefPubMedPubMedCentralGoogle Scholar
  6. Hoon, M.J.L., Imoto, S., Nolan, J., Miyano, S.: Open source clustering software. — Bioinformatics 20: 1453–1454, 2004.CrossRefPubMedGoogle Scholar
  7. Dong, Y., Yang, X., Liu, J., Wang, B.H., Liu, B.L., Wang, Y.Z.: Pod shattering resistance associated with domestication is mediated by a NAC gene in soybean. — Nat. Commun. 5: 3352, 2014.PubMedGoogle Scholar
  8. Dong, Y.P., Fan, G.Q., Zhao, Z.L., Deng, M.J.: Compatible solute, transporter protein, transcription factor, and hormone-related gene expression provides an indicator of drought stress in Paulownia fortunei. — Funct. integr. Genomics 14: 479–491, 2014.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Du, J.C., Tian, Z.X., Sui, Y., Zhao, M.X., Song, Q.J., Cannon, S.B., Cregan, P., Ma, J.X.: Pericentromeric effects shape the patterns of divergence, retention, and expression of duplicated genes in the paleopolyploid soybean. — Plant Cell 24: 21–32, 2015.CrossRefGoogle Scholar
  10. Duval, M., Hsieh, T.F., Kim, S.Y., Thomas, T.L.: Molecular characterization of AtNAM: a member of the Arabidopsis NAC domain superfamily. — Plant mol. Biol. 50: 237–248, 2002.CrossRefPubMedGoogle Scholar
  11. Ernst, H.A., Olsen, A.N., Larsen, S., Lo, Leggio L.: Structure of the conserved domain of ANAC, a member of the NAC family of transcription factors. — EMBO Rep. 5: 297–303, 2004.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Fan, K., Bibi, N., Gan, S., Li, F., Yuan, S., Ni, M., Wang, M., Shen, H., Wang, X.: A novel NAP member GhNAP is involved in leaf senescence in Gossypium hirsutum. — J. exp. Bot. 15: 4669–4682, 2015.CrossRefGoogle Scholar
  13. Fan, K., Wang, M., Miao, Y., Ni, M., Bibi, N., Yuan, S., Li, F., Wang, X.D.: Molecular evolution and expansion analysis of the NAC transcription factor in Zea mays. — PLoS ONE 9: e111837, 2014.CrossRefGoogle Scholar
  14. Fang, Y.J., You, J., Xie, K.B., Xie, W.B., Xiong, L.Z.: Systematic sequence analysis and identification of tissuespecific or stress-responsive genes of NAC transcription factor family in rice. — Mol. Genet. Genomics 280: 547–563, 2008.CrossRefPubMedGoogle Scholar
  15. Gao, F., Xiong, A.S., Peng, R.H., Jin, X.F., Xu, J., Zhu, B., Chen, J.M., Yao, Q.H.: OsNAC52, a rice NAC transcription factor, potentially responds to ABA and confers drought tolerance in transgenic plants. — Plant Cell Tissue Organ Cult. 100: 255–262, 2010.CrossRefGoogle Scholar
  16. Goodstein, D.M., Shu, S.Q., Howson, R., Neupane, R., Hayes, R.D., Fazo, J., Mitros, T., Dirks, W., Hellsten, U., Putnam, N., Rokhsar, D.S.: Phytozome: a comparative platform for green plant genomics. -Nucl. Acids Res. 40: D1178–D1186, 2012.CrossRefPubMedGoogle Scholar
  17. Guo, Y., Qiu, L.J.: Genome-wide analysis of the Dof transcription factor gene family reveals soybean-specific duplicable and functional characteristics. — PloS ONE 8: e76809, 2013.CrossRefGoogle Scholar
  18. Guo, Y.F., Gan, S.S.: AtNAP, a NAC family transcription factor, has an important role in leaf senescence. — Plant J. 46: 601–612, 2006.CrossRefPubMedGoogle Scholar
  19. Han, Q.Q., Zhang, J.H., Li, H.X., Luo, Z.D., Ziaf, K., Ouyang, B., Wang, T.T., Ye Z.B.: Identification and expression pattern of one stress-responsive NAC gene from Solanum lycopersicum. — Mol. Biol. Rep. 39: 1713–1720, 2012.CrossRefPubMedGoogle Scholar
  20. Hao, Y.J., Wei, W., Song, Q.X., Chen, H.W., Zhang, Y.Q., Wang, F., Zou, H.F., Lei, G., Tian, A.G., Zhang, W.K., Ma, B., Zhang, J.S., Chen, S.Y.: Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants. — Plant J. 68: 302–313, 2011.CrossRefPubMedGoogle Scholar
  21. Hendelman, A., Stav, R., Zemach, H., Arazi, T.: The tomato NAC transcription factor SlNAM2 is involved in flowerboundary morphogenesis. — J. exp. Bot. 64: 5497–5507, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Hu, R.B., Qi, G.A., Kong, Y.Z., Kong, D.J., Gao, Q.A., Zhou, G.K.: Comprehensive analysis of NAC domain transcription factor gene family in Populus trichocarpa. — BMC Plant Biol. 10: 145, 2010.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Huang, H., Wang, Y., Wang, S.L., Wu, X., Yang, K., Niu, Y.J., Dai, S.L.: Transcriptome-wide survey and expression analysis of stress-responsive NAC genes in Chrysanthemum lavandulifolium. - Plant Sci. 193: 18–27, 2012.CrossRefPubMedGoogle Scholar
  24. Hurst, L.D.: The Ka/Ks ratio: diagnosing the form of sequence evolution. — Trends Genet. 18: 486–487, 2002.CrossRefPubMedGoogle Scholar
  25. Hyten, D.L., Song, Q.J., Zhu, Y.L., Choi, I.Y., Nelson, R.L., Costa, J.M., Specht, J.E., Shoemaker, R.C., Cregan, P.B.: Impacts of genetic bottlenecks on soybean genome diversity. — Proc. nat. Acad. Sci. USA 103: 16666–16671, 2006.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Jensen, M.K., Hagedorn, P.H., De Torres-Zabala, M., Grant, M.R., Rung, J.H., Collinge, D.B., Lyngkjaer, M.F.: Transcriptional regulation by an NAC (NAM-ATAF1,2-CUC2) transcription factor attenuates ABA signalling for efficient basal defence towards Blumeria graminis f. sp. hordei in Arabidopsis. — Plant J. 56: 867–880, 2008.CrossRefPubMedGoogle Scholar
  27. Joshi, T., Fitzpatrick, M.R., Chen, S.Y., Liu, Y., Zhang, H.X., Endacott, R.Z., Gaudiello, E.C., Stacey, G., Nguyen, H.T., Xu, D.: Soybean knowledge base (SoyKB): a web resource for integration of soybean translational genomics and molecular breeding. — Nucl. Acids Res. 42: D1245–D1252, 2014.CrossRefPubMedGoogle Scholar
  28. Kou, X.H., Watkins, C.B., Gan, S.S.: Arabidopsis AtNAP regulates fruit senescence. — J. exp. Bot. 63: 6139–6147, 2012.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Lam, H.M., Xu, X., Liu, X., Chen, W., Yang, G., Wong, F.L., Li, M.W., He, W., Qin, N., Wang, B., Li, J., Jian, M., Wang, J., Shao, G., Sun, S.S., Zhang, G.: Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. — Natur. Genet. 42: 1053–1059, 2010.CrossRefGoogle Scholar
  30. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J., Higgins, D.G.: Clustal W and Clustal X version 2.0. — Bioinformatics 23: 2947–2948, 2007.CrossRefPubMedGoogle Scholar
  31. Lavin, M., Herendeen, P.S., Wojciechowski, M.F.: Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the tertiary. — Syst. Biol. 54: 575–594, 2005.CrossRefPubMedGoogle Scholar
  32. Le, DT, Nishiyama, R., Watanabe, Y., Mochida, K., Yamaguchi-Shinozaki, K., Shinozaki, K., Tran, L.S.P.: Genome-wide survey and expression analysis of the plantspecific NAC transcription factor family in soybean during development and dehydration stress. — DNA Res. 18: 263–276, 2011.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Lescot, M., Déhais, P., Thijs, G., Marchal, K., Moreau, Y., De Peer, Y.V., Rouzé, P., Rombauts, S.: PlantCARE: a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. — Nucl. Acids Res. 30: 325–327, 2002.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Li, X.L., Yang, X., Hu, Y.X., Yu, X.D., Li, Q.L.: A novel NAC transcription factor from Suaeda liaotungensis K. enhanced transgenic Arabidopsis drought, salt, and cold stress tolerance. — Plant Cell Rep. 33: 767–778, 2014.CrossRefPubMedGoogle Scholar
  35. Li, Y.H., Zhao, S.C., Ma, J.X., Li, D., Yan, L., Li, J., Qi, X.T., Guo, X.S., Zhang, L., He, W.M., Chang, R.Z., Liang, Q.S., Guo, Y., Ye, C., Wang, X.B., Tao, Y., Guan, R.X., Wang, J.Y., Liu, Y.L., Jin, L.G., Zhang, X.Q., Liu, Z.X., Zhang, L.J., Chen, J., Wang, K.J., Nielsen, R., Li, R.Q., Chen, P.Y., Li, W.B., Reif, J.C., Purugganan, M., Wang, J., Zhang, M.C., Wang, J., Qiu, L.J.: Molecular footprints of domestication and improvement in soybean revealed by whole genome re-sequencing. — BMC Genomics 14: 579, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Librado, P., Rozas, J.: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. — Bioinformatics 25: 1451–1452, 2009.CrossRefPubMedGoogle Scholar
  37. Liu, J.F., Zhang, Y., Lei, X.Y., Zhang, Z.M.: Natural selection of protein structural and functional properties: a single nucleotide polymorphism perspective. — Genome Biol. 4: R69, 2008.Google Scholar
  38. Liu, T.K., Song, X.M., Duan, W.K., Huang, Z.N., Liu, G.F., Li, Y., Hou, X.L.: Genome-wide analysis and expression patterns of NAC transcription factor family under different developmental stages and abiotic stresses in chinese cabbage. — Plant mol. Biol. Rep. 32: 1041–1056, 2014.CrossRefGoogle Scholar
  39. Livak, K.J., Schmittgen, T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. — Methods 25: 402–408. 2001.CrossRefPubMedGoogle Scholar
  40. Lopez, S., Stuhl, L., Fichelson, S., Dubart-Kupperschmitt, A., St Arnaud R., Galindo J.R., Murati A., Berda N., Dubreuil P., Gomez S.: NACA is a positive regulator of human erythroid-cell differentiation. — J. cell. Sci. 118: 1595–1605, 2005.CrossRefPubMedGoogle Scholar
  41. Lynch, M., Conery, J.S.: The evolutionary fate and consequences of duplicate genes. — Science 290: 1151–1155, 2000.CrossRefPubMedGoogle Scholar
  42. Mitsuda, N., Ohme-Takagi, M.: NAC transcription factors NST1 and NST3 regulate pod shattering in a partially redundant manner by promoting secondary wall formation after the establishment of tissue identity. — Plant J. 56: 768–778, 2008.CrossRefPubMedGoogle Scholar
  43. Movahedi, A., Zhang, J.X., Gao, P.H., Yang, Y., Wang, L.K., Yin, T.M., Kadkhodaei, S., Ebrahimi, M., Qiang, Z.G.: Expression of the chickpea CarNAC3 gene enhances salinity and drought tolerance in transgenic poplars. — Plant Cell Tissue Organ Cult. 120: 141–154, 2015.CrossRefGoogle Scholar
  44. Nuruzzaman, M., Manimekalai, R., Sharoni, A.M., Satoh, K., Kondoh, H., Ooka, H., Kikuchi, S. Genome-wide analysis of NAC transcription factor family in rice. - Gene 465: 30–44, 2010.CrossRefPubMedGoogle Scholar
  45. Olsen, A.N., Ernst, H.A., Leggio, L.L., Skriver, K.: NAC transcription factors: structurally distinct, functionally diverse. — Trends Plant Sci. 10: 79–87, 2005.CrossRefPubMedGoogle Scholar
  46. Ooka, H., Satoh, K., Doi, K., Nagata, T., Otomo, Y., Murakami, K., Matsubara, K., Osato, N., Kawai, J., Carninci, P., Hayashizaki, Y., Suzuki, K., Kojima, K., Takahara, Y., Yamamoto, K., Kikuchi, S.: Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. — DNA Res. 10: 239–247, 2003.CrossRefPubMedGoogle Scholar
  47. Pinheiro, G.L., Marques, C.S., Costa, M.D.B.L., Reis, P.A.B., Alves, M.S., Carvalho, C.M., Fietto, L.G., Fontes, E.P.B.: Complete inventory of soybean NAC transcription factors: sequence conservation and expression analysis uncover their distinct roles in stress response. — Gene 444: 10–23, 2009.CrossRefPubMedGoogle Scholar
  48. Puranik, S., Sahu, P.P., Mandal, S.N., Venkata Suresh, B., Parida, S.K., Prasad, M.: Comprehensive genome-wide survey, genomic constitution and expression profiling of the NAC transcription factor family in foxtail millet (Setaria italica L.). — PloS ONE 8: e64594, 2013.CrossRefGoogle Scholar
  49. Quevillon, E., Silventoinen, V., Pillai, S., Harte, N., Mulder, N., Apweiler, R., Lopez, R.: InterProScan: protein domains identifier. — Nucl. Acids Res 33: W116–W120, 2005.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Sakuraba, Y., Park, S. Y., Paek, N. C.: The divergent roles of STAYGREEN (SGR) homologs in chlorophyll degradation. — Mol. Cells 38: 390–395, 2015.CrossRefPubMedPubMedCentralGoogle Scholar
  51. Salamov, A.A., Solovyev V.V.: Ab initio gene finding in Drosophila genomic DNA. — Genome Res. 10: 516–522, 2000.CrossRefPubMedPubMedCentralGoogle Scholar
  52. Salvagiotti, F., Cassman, K.G., Specht, J.E., Walters, D.T., Weiss, A., Doberman, A.: Nitrogen uptake, fixation, and response to fertilizer N in soybeans: a review. — Field Crops Res. 108: 1–13, 2008.CrossRefGoogle Scholar
  53. Satheesh, V., Jagannadham, P.T., Chidambaranathan, P., Jain, P.K., Srinivasan, R.: NAC transcription factor genes: genome-wide identification, phylogenetic, motif and cisregulatory element analysis in pigeonpea (Cajanus cajan (L.) Millsp.). — Mol. Biol. Rep. 41: 7763–7773, 2014.CrossRefPubMedGoogle Scholar
  54. Schlueter, J.A., Lin, J.Y., Schlueter, S.D., Vasylenko-Sanders, I.F., Deshpande, S., Yi, J., O'Bleness, M., Roe, B.A., Nelson, R.T., Scheffler, B.E., Jackson, S.A., Shoemaker, R.C.: Gene duplication and paleopolyploidy in soybean and the implications for whole genome sequencing. — BMC Genomics 8: 330, 2007.CrossRefPubMedPubMedCentralGoogle Scholar
  55. Schmutz, J., Cannon, S.B., Schlueter, J., Ma, J., Mitros, T., Nelson, W., Hyten, D.L., Song, Q., Thelen, J.J., Cheng, J., Xu, D., Hellsten, U., May, G.D., Yu, Y., Sakurai, T., Umezawa, T., Bhattacharyya, M.K., Sandhu, D., Valliyodan, B., Lindquist, E., Peto, M., Grant, D., Shu, S., Goodstein, D., Barry, K., Futrell-Griggs, M., Abernathy, B., Du, J., Tian, Z., Zhu, L., Gill, N., Joshi, T., Libault, M., Sethuraman, A., Zhang, X.C., Shinozaki, K., Nguyen, H.T., Wing, R.A., Cregan, P., Specht, J., Grimwood, J., Rokhsar, D., Stacey, G., Shoemaker, R.C., Jackson, S.A.: Genome sequence of the palaeopolyploid soybean. — Nature 463: 178–183, 2010.CrossRefPubMedGoogle Scholar
  56. Shang, H., Li, W., Zou, C., Yuan, Y.: Analyses of the NAC transcription factor gene family in Gossypium raimondii Ulbr.: chromosomal location, structure, phylogeny, and expression patterns. — J. integr. Plant Biol. 55: 663–676, 2013.CrossRefPubMedGoogle Scholar
  57. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S.: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. — Mol. Biol. Evol. 28: 2731–2739, 2011.CrossRefPubMedPubMedCentralGoogle Scholar
  58. Taoka, K., Yanagimoto, Y., Daimon, Y., Hibara, K., Aida, M., Tasaka, M.: The NAC domain mediates functional specificity of Cup-Shaped Cotyledon proteins. — Plant J. 40: 462–473, 2004.CrossRefPubMedGoogle Scholar
  59. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., Higgins, D.G.: The Clustal_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. — Nucl. Acids Res. 25: 4876–4882, 1997.CrossRefPubMedPubMedCentralGoogle Scholar
  60. Tian, Z.X., Wang, X.B., Lee, R., Li, Y.H., Specht, J.E., Nelson, R.L., McClean, P.E., Qiu, L.J., Ma, J.X.: Artificial selection for determinate growth habit in soybean. — Proc. nat. Acad. Sci. USA 107: 8563–8568, 2010.CrossRefPubMedPubMedCentralGoogle Scholar
  61. Tran, L.S., Nakashima, K., Sakuma, Y., Simpson, S.D., Fujita, Y., Maruyama K., Yamaguchi-Shinozaki K.: Isolation and functional analysis of Arabidopsis stress inducible NAC transcription factors that bind to a drought responsive ciselement in the early responsive to dehydration stress 1 promoter. — Plant Cell 16: 2481–2498, 2004.CrossRefPubMedPubMedCentralGoogle Scholar
  62. Tucker, M.L., Whitelaw, C.A., Lyssenko, N.N., Nath, P.: Functional analysis of regulatory elements in the gene promoter for an abscission-specific cellulase from bean and isolation, expression, and binding affinity of three TGAtype basic leucine zipper transcription factors. — Plant Physiol. 130: 1487–1496, 2002.CrossRefPubMedPubMedCentralGoogle Scholar
  63. Udvardi, M.K., Kakar, K., Wandrey, M., Montanari, O., Murray, J., Andriankaja, A., Zhang, J.Y., Benedito, V., Hofer, J.M., Chueng, F., Town, C.D.: Legume transcription factors: global regulators of plant development and response to the environment. — Plant Physiol. 144: 538–549, 2007.CrossRefPubMedPubMedCentralGoogle Scholar
  64. Wang, N., Zheng, Y., Xin, H., Fang, L., Li, S.: Comprehensive analysis of NAC domain transcription factor gene family in Vitis vinifera. — Plant Cell. Rep. 32: 61–75, 2013.CrossRefPubMedGoogle Scholar
  65. Wang, X.B., Zhang, H.W., Sun, G.L., Jin, Y., Qiu, L.J.: Identification of active VQ motif-containing genes and the expression patterns under low nitrogen treatment in soybean. — Gene 543: 237–243, 2014a.CrossRefPubMedGoogle Scholar
  66. Wang, X.B., Zhang, H.W., Gao, Y.L., Sun, G.L., Zhang, W.M., Qiu, L.J.: A comprehensive analysis of the Cupin gene family in soybean (Glycine max). — PloS ONE 9: e110092, 2014b.CrossRefGoogle Scholar
  67. Wang, F., Chen, H.W., Li, Q.T., Wei, W., Li, W., Zhang, W.K., Ma, B., Bi, Y.D., Lai, Y.C., Liu, X.L., Man, W.Q., Zhang, J.S., Chen, S.Y.: GmWRKY27 interacts with GmMYB174 to reduce expression of GmNAC29 for stress tolerance in soybean plants. — Plant J. 83: 224–236, 2015.CrossRefPubMedGoogle Scholar
  68. Wilkins, O., Nahal, H., Foong, J., Provart, N.J., Campbell, M.M.: Expansion and diversification of the Populus R2R3-MYB family of transcription factors. — Plant Physiol. 149: 981–993, 2009.CrossRefPubMedPubMedCentralGoogle Scholar
  69. Wu, Z., Xu, X., Xiong, W., Wu, P., Chen, Y., Li, M., Wu, G., Jiang, H.: Genome-wide analysis of the NAC gene family in physic nut (Jatropha curcas L.). — PloS ONE 10: e0131890, 2015.Google Scholar
  70. Xie, Q., Frugis, G., Colgan, D., Chua, N.H.: Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. — Genes Dev. 14: 3024–3036, 2000.CrossRefPubMedPubMedCentralGoogle Scholar
  71. Xu, G.X., Guo, C.C., Shan, H.Y., Kong, H.Z.: Divergence of duplicate genes in exon-intron structure. — Proc. nat. Acad. Sci. USA 109: 1187–1192, 2012.CrossRefPubMedPubMedCentralGoogle Scholar
  72. Zhou, Z.K., Jiang, Y., Wang, Z., Gou, Z.H., Lyu, J., Li, W.Y., Yu, Y.J., Shu, L.P., Zhao, Y.J., Ma, Y.M., Fang, C., Shen, Y.T., Liu, T.F., Li, C.C., Li, Q., Wu, M., Wang, M., Wu, Y.S., Dong, Y., Wan, W.T., Wang, X., Ding, Z.L., Gao, Y.D., Xiang, H., Zhu, B.G., Lee, S.H., Wang, W., Tian, Z.X.: Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean. — Nat. Biotechnol. 33: 408–414, 2015.CrossRefPubMedGoogle Scholar

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© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  1. 1.Department of Agronomy SciencesAnhui Agricultural UniversityHefeiP.R. China
  2. 2.Key Laboratory of Wheat Biology and Genetic Improvement on South Yellow & Huai River ValleyMinistry of AgricultureHefeiP.R. China

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