Abstract
Determining how function evolves following gene duplication is necessary for understanding gene expansion. Transcription factors (TFs) are a class of proteins that regulate gene expression by binding to specific cis-acting elements in the promoters of target genes, subsequently activating or repressing their transcription. In the present study, we systematically examined the functional diversification of the NAC transcription factor (NAC-TFs) family by analyzing their chromosomal location, structure, phylogeny, and expression pattern in Gossypium raimondii (Gr) and G. arboreum (Ga). The 145 and 141 NAC genes identified in the Gr and Ga genomes, respectively, were annotated and divided into 18 subfamilies, which showed distinct divergence in gene structure and expression patterns during fiber development. In addition, when the functional parameters were examined, clear divergence was observed within tandem clusters, which suggested that subfunctionalization had occurred among duplicate genes. The expression patterns of homologous gene pairs also changed, suggestive of the diversification of gene function during the evolution of diploid cotton. These findings provide insights into the mechanisms underlying the functional differentiation of duplicated NAC-TFs genes in two diploid cotton species.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Cao, X. (2015). Whole genome sequencing of cotton-a new chapter in cotton genomics. Sci China Life Sci 58, 515–516.
Cenci, A., Guignon, V., Roux, N., and Rouard, M. (2014). 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.
Dong, Z., and Chen, Y. (2013). Transcriptomics: advances and approaches. Sci China Life Sci 56, 960–967.
Fan, K., Wang, M., Miao, Y., Ni, M., Bibi, N., Yuan, S., Li, F., and Wang, X. (2014). Molecular evolution and expansion analysis of the NAC transcription factor in Zea mays. PLoS One 9, e111837.
Fang, Y., You, J., Xie, K., Xie, W., and Xiong, L. (2008). Systematic sequence analysis and identification of tissue-specific or stress-responsive genes of NAC transcription factor family in rice. Mol Genet Genomics 280, 547–563.
Finn, R.D, Clements, J., and Eddy, S.R. (2011). HMMER web server: interactive sequence similarity searching. Nucleic Acids Re 39, W29–W37.
Hu, R., Qi, G., Kong, Y., Kong, D., Gao, Q., and Zhou, G. (2010). Comprehensive analysis of NAC domain transcription factor gene family in Populus trichocarpa. BMC Plant Biol 10, 145.
Hui, S., Yin, Y.B., Chen, F., Xu,Y., Richard, A,. and Dixon R.A. (2009). A bioinformatic analysis of NAC genes for plant cell wall development in relation to lignocellulosic bioenergy production. Bioenerg Res 2, 217–232.
Hussey, S.G., Saϊdi, M.N., Hefer, C.A., Myburg, A.A., and Grima-Pettenati, J. (2015). Structural, evolutionary and functional analysis of the NAC domain protein family in Eucalyptus. New Phytol 206, 1337–1350.
Ji, S., Lu, Y., Feng, J., Wei, G., Li, J., Shi, Y., Fu, Q., Liu, D., Luo, J., and Zhu, Y. (2003). Isolation and analyses of genes preferentially expressed during early cotton fiber development by subtractive PCR and cDNA array. Nucleic Acids Res 31, 2534–2543.
Le, D.T., Nishiyama, R., Watanabe, Y., Mochida, K., Yamaguchi- Shinozaki, K., Shinozaki, K., and Tran, L.S. (2011). Genome-wide survey and expression analysis of the plant-specific NAC Transcription factor family in soybean during development and dehydration stress. DNA Res 18, 263–276.
Lee, S., Seo, P.J., Lee, H.J., and Park, C.M. (2012). A NAC transcription factor NTL4 promotes reactive oxygen species production during drought-induced leaf senescence in Arabidopsis. Plant 70, 831–844.
Li, F., Fan, G., Wang, K., Sun, F., Yuan, Y., Song, G., Qin, L., Ma, Z., Lu, C., Zou, C., Chen, W., Liang, X., Shang, H., Liu, W., Shi, C., Xiao, G., Gou, C., Ye, W., Xu, X., Zhang, X., Wei, H., Li, Z., Zhang, G., Wang, J., Liu, K., Kohel, R.J., Percy, R.G., Yu, J., Zhu, Y., and Yu, S. (2014). Genome sequence of the cultivated cotton Gossypium arboreum. Nat Genet 46, 567–572.
Li, Q., Lin, Y., Sun, Y., Song, J., Chen, H., Zhang, X., Sederoff, R.R., and Chiang, V.L. (2012). Splice variant of the SND1 transcription factor is a dominant negative of SND1 members and their regulation in Populus trichocarpa. Proc Natl Acad Sci USA 109, 14699–14704.
Li, W., Huang, G., Zhou, W., Xia, X., Li, D., and Li, X. (2014). A cotton (Gossypium hirsutum) gene encoding a NAC transcription factor is involved in negative regulation of plant xylem development. Plant Physiol Biochem 83, 134–141.
Lynch, M., and Conery, J.S. (2000). The evolutionary fate and consequences of duplicate genes. Science 290, 1151–1155.
Mitsuda, N., Iwase, A., Yamamoto, H., Yoshida, M., Seki, M., Shinozaki, K., and Ohme-Takagi, M. (2007). NAC transcription factors, NST1 and NST3, are key regulators of the formation of secondary walls in woody tissues of Arabidopsis. Plant Cell 19, 270–280.
Mitsuda, N., Seki, M., Shinozaki, K., and Ohme-Takagi, M. (2005). The NAC transcription factors NST1 and NST2 of Arabidopsis regulate secondary wall thickenings and are required for anther dehiscence. Plant Cell 17, 2993–3006.
Nuruzzaman, M., Manimekalai, R., Sharoni, A.M., Satoh, K,, Kondoh, H., Ooka, H., and Kikuchi, S. (2010). Genome wide analysis of NAC transcription factor family in rice. Gene 465, 30–44.
Ohashi-Ito, K., Oda, Y., and Fukuda, H. (2010). Arabidopsis VASCULAR-RELATED NAC-DOMAIN6 directly regulates the genes that govern programmed cell death and secondary wall formation during xylem differentiation. Plant Cell 22, 3461–3473.
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., and Kikuchi, S. (2003). Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res 10, 239–247.
Pei, Y. (2015). The homeodomain-containing transcription factor, GhHOX3, is a key regulator of cotton fiber elongation. Sci China Life Sci 58, 309–310.
Pinheiro, G.L., Marques, C.S., Costa, M.D., Reis, P.A., Alves, M,S., Carvalho, C.M., Fietto, L.G., and Fontes, E.P. (2009). Complete inventory of soybean NAC transcription factors: sequence conservation and expression analysis uncover their distinct roles in stress response. Gene 444, 10–23.
Puranik, S., Sahu, P.P., Mandal, S.N., B, V.S., Parida, S.K., and Prasad, M. (2013). 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.
Qin, Y., and Zhu, Y. (2011). How cotton fibers elongate: a tale of linear cell growth mode. Curr Opin Plant Biol 14, 106–111.
Rushton, P.J., Bokowiec, M.T., Han, S., Zhang, H., Brannock, J.F., Chen, X., Laudeman, T.W., and Timko, M.P. (2008). Tobacco transcription factors: novel insights into transcriptional regulation in the Solanaceae, Plant Physiol 47, 280–295.
Saeed, A.I., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N., Braist ed, J., Klapa, M., Currier, T., Thiagarajan, M., Sturn, A., Snuffin, M., Rezantsev, A., Popov, D., Ryltsov, A., Kostukovich, E., Borisovsky, I., Liu, Z., Vinsavich, A., Trush, V., and Quackenbush, J. (2003). TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34, 374–378.
Shah, S.T., Pang, C., Fan, S., Song, M., Arain, S., and Yu, S. (2013). Isolation and expression profiling of GhNAC transcription factor genes in cotton (Gossypium hirsutum L.) during leaf senescence and in response to stresses. Gene 531, 220–234.
Shang, H., Li, W., Zou, C., and Yuan, Y. (2013). 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.
Singh, A.K., Sharma, V., Pal, A.K., Acharya, V., and Ahuja, P.S. (2013). Genome-wide organization and expression profiling of the NAC transcription factor family in potato (Solanum tuberosum L.) DNA Res 20, 403–423.
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28, 2731–2739.
Wang, H., Zhao, Q., Chen, F., Wang, M., and Dixon, R.A. (2011). NAC domain function and transcriptional control of a secondary cell wall master switch. Plant J 68, 1104–1114.
Wang, K., Wang, Z., Li, F., Ye, W., Wang, J., Song, G., Yue, Z., Cong, L., Shang, H., Zhu, S., Zou, C., Li, Q., Yuan, Y., Lu, C., Wei, H., Gou, C., Zheng, Z., Yin, Y., Zhang, X., Liu, K., Wang, B., Song, C., Shi, N., Kohel, R., Percy, R.G., John, Z., Yu, J., Zhu, Y., Wang, J., and Yu, S. (2012). The draft genome of a diploid cotton Gossypium raimondii. Nat Genet 44, 1098–1103.
Wang, N., Zheng, Y., Xin, H., Fang, L., and Li, S. (2013). Comprehensive analysis of NAC domain transcription factor gene family in Vitis vinifera. Plant Cell Rep 32, 61–75.
Yamaguchi, M., Mitsuda, N., Ohtani, M., Ohme-Takagi, M., Kato, K., and Demura, T. (2011). VASCULAR-RELATED NAC-DOMAIN7 directly regulates the expression of a broad range of genes for xylem vessel formation. Plant J 66, 579–590.
Yamaguchi, M., Ohtani, M., Mitsuda, N., Kubo, M., Ohme-Takagi, M., Fukuda, H., and Demura, T. (2010). VND-INTERACTING2, a NAC domain transcription factor, negatively regulates xylem vessel formation in Arabidopsis. Plant Cell 22, 1249–1263.
Yao, D., Wei, Q., Xu,W., Syrenne, R.D., Yuan, J., and Su, Z. (2012). Comparative genomic analysis of NAC transcriptional factors to dissect the regulatory mechanisms for cell wall biosynthesis. BMC Bioinformatics 15, S10.
You, J., Zhang, L., Song B., Qi X., and Chan Z. (2015). Systematic analysis and identification of stress-responsive genes of the NAC gene family in Brachypodium distachyon. PLoS One 10, e0122027.
Zhang, G., Chen, M., Chen, X., Xu, Z., Guan, S., Li, L.C., Li, A., Guo, J., Mao, L., and Ma, Y. (2008). Phylogeny, gene structures, and expression patterns of the ERF gene family in soybean (Glycine max L.), J Exp Bot 59, 4095–4107.
Zhong, R., Demura, T., and Ye, Z. (2006). SND, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. Plant Cell 18, 3158–3170.
Zhong, R., Richardson, E.A., and Ye, Z. (2007). Two NAC domain transcription factors, SND1 and NST, function redundantly in regulation of secondary wall synthesis in fibers of Arabidopsis. Planta 225, 1603–1611.
Zhu, T., Nevo, E., Sun, D., and Peng, J. (2012). Phylogenetic analyses unravel the evolutionary history of NAC proteins in plants. Evolution 66, 1833–1848.
Zhu, Y., and Li, F. (2013). The Gossypium raimondii genome, a huge leap forward in cotton genomics. J Integr Plant Biol 55, 570–571.
Author information
Authors and Affiliations
Corresponding author
Additional information
This article is published with open access at link.springer.com
Electronic supplementary material
Rights and permissions
Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0), which permits use, duplication, adaptation, distribution, and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
About this article
Cite this article
Shang, H., Wang, Z., Zou, C. et al. Comprehensive analysis of NAC transcription factors in diploid Gossypium: sequence conservation and expression analysis uncover their roles during fiber development. Sci. China Life Sci. 59, 142–153 (2016). https://doi.org/10.1007/s11427-016-5001-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11427-016-5001-1