留言板

尊敬的读者、作者、审稿人, 关于本刊的投稿、审稿、编辑和出版的任何问题, 您可以本页添加留言。我们将尽快给您答复。谢谢您的支持!

姓名
邮箱
手机号码
标题
留言内容
验证码

Natural variation in the SVP contributes to the pleiotropic adaption of Arabidopsis thaliana across contrasted habitats

Xiang Guo Ruyun Liang Shangling Lou Jing Hou Liyang Chen Xin Liang Xiaoqin Feng Yingjun Yao Jianquan Liu Huanhuan Liu

Xiang Guo, Ruyun Liang, Shangling Lou, Jing Hou, Liyang Chen, Xin Liang, Xiaoqin Feng, Yingjun Yao, Jianquan Liu, Huanhuan Liu. Natural variation in the SVP contributes to the pleiotropic adaption of Arabidopsis thaliana across contrasted habitats[J]. 遗传学报. doi: 10.1016/j.jgg.2023.08.004
引用本文: Xiang Guo, Ruyun Liang, Shangling Lou, Jing Hou, Liyang Chen, Xin Liang, Xiaoqin Feng, Yingjun Yao, Jianquan Liu, Huanhuan Liu. Natural variation in the SVP contributes to the pleiotropic adaption of Arabidopsis thaliana across contrasted habitats[J]. 遗传学报. doi: 10.1016/j.jgg.2023.08.004
Xiang Guo, Ruyun Liang, Shangling Lou, Jing Hou, Liyang Chen, Xin Liang, Xiaoqin Feng, Yingjun Yao, Jianquan Liu, Huanhuan Liu. Natural variation in the SVP contributes to the pleiotropic adaption of Arabidopsis thaliana across contrasted habitats[J]. Journal of Genetics and Genomics. doi: 10.1016/j.jgg.2023.08.004
Citation: Xiang Guo, Ruyun Liang, Shangling Lou, Jing Hou, Liyang Chen, Xin Liang, Xiaoqin Feng, Yingjun Yao, Jianquan Liu, Huanhuan Liu. Natural variation in the SVP contributes to the pleiotropic adaption of Arabidopsis thaliana across contrasted habitats[J]. Journal of Genetics and Genomics. doi: 10.1016/j.jgg.2023.08.004

Natural variation in the SVP contributes to the pleiotropic adaption of Arabidopsis thaliana across contrasted habitats

doi: 10.1016/j.jgg.2023.08.004
基金项目: 

This work was supported by the Natural Science Foundation of China (No. 32030006 and No. 32270302), the Strategic Priority Research Program of the Chinese Academy of Sciences (No. XDB31000000), and the Fundamental Research Funds for the Central Universities (2020SCUNL207 and SCU2022D003).

详细信息
    通讯作者:

    Jianquan Liu,Email addresses:liujq@nwipb.cas.cn

    Huanhuan Liu,Email addresses:liuhuanhuan85@163.com

Natural variation in the SVP contributes to the pleiotropic adaption of Arabidopsis thaliana across contrasted habitats

Funds: 

This work was supported by the Natural Science Foundation of China (No. 32030006 and No. 32270302), the Strategic Priority Research Program of the Chinese Academy of Sciences (No. XDB31000000), and the Fundamental Research Funds for the Central Universities (2020SCUNL207 and SCU2022D003).

  • 摘要:

    Coordinated plant adaptation involves the interplay of multiple traits driven by habitat- specific selection pressures. Pleiotropic effects, wherein genetic variants of a single gene control multiple traits, can expedite such adaptations. Until present, only a limited number of genes have been reported to exhibit pleiotropy. Here, we create a recombinant inbred line (RIL) population derived from two Arabidopsis thaliana (A. thaliana) ecotypes originating from divergent habitats. Using this RIL population, we identify an allelic variation in a MADS-box transcription factor, SHORT VEGETATIVE PHASE (SVP), which exerts a pleiotropic effect on leaf size and drought-versus-humidity tolerance. Further investigation reveals that a natural null variant of the SVP protein disrupts its normal regulatory interactions with target genes, including GRF3, CYP707A1/3, and AtBG1, leading to increased leaf size, enhanced tolerance to humid conditions, and changed in flowering time in humid conditions in A. thaliana. Remarkably, polymorphic variations in this gene have been traced back to early A. thaliana populations, providing a genetic foundation and plasticity for subsequent colonization of diverse habitats by influencing multiple traits. These findings advance our understanding of how plants rapidly adapt to changing environments by virtue of the pleiotropic effects of individual genes on multiple trait alterations.

  • Alvarez, J.P., Furumizu, C., Efroni, I., Eshed, Y., Bowman, J.L., 2016. Active suppression of a leaf meristem orchestrates determinate leaf growth. eLife. 5.
    Atwell, S., Huang, Y.S,, Vilhjalmsson, B.J., Willems, G., Horton, M., Li, Y., Meng, D., Platt, A., Tarone, A.M., Hu, T.T., et al., 2010. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature. 465, 627-631.
    Baird, A.S., Taylor, S.H., Pasquet-Kok, J., Vuong, C., Zhang, Y., Watcharamongkol, T., Scoffoni, C., Edwards, E.J., Christin, P.A., Osborne, C.P., et al., 2021. Developmental and biophysical determinants of grass leaf size worldwide. Nature. 592, 242-247.
    Ballester, P., Navarrete-Gomez, M., Carbonero, P., Onate-Sanchez, L., Ferrandiz, C., 2015. Leaf expansion in Arabidopsis is controlled by a TCP-NGA regulatory module likely conserved in distantly related species. Physiologia plantarum. 155, 21-32.
    Bechtold, U., Penfold, C.A., Jenkins, D.J., Legaie, R., Moore, J.D., Lawson, T., Matthews, J.S., Vialet-Chabrand, S.R., Baxter, L., Subramaniam, S., et al., 2016. Time-Series Transcriptomics Reveals That AGAMOUS-LIKE22 Affects Primary Metabolism and Developmental Processes in Drought-Stressed Arabidopsis. The Plant cell. 28, 345-366.
    Beltramino, M., Ercoli, M.F., Debernardi, J.M., Goldy, C., Rojas, A.M.L., Nota, F., Alvarez, M.E., Vercruyssen, L., Inze, D., Palatnik, J.F., et al., 2018. Robust increase of leaf size by Arabidopsis thaliana GRF3-like transcription factors under different growth conditions. Sci Rep. 8, 13447.
    Bentsink, L., Jowett, J., Hanhart, C.J., Koornneef, M., 2006. Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis. Proc. Natl Acad. Sci. 103, 17042-17047.
    Bowler, C., Benvenuto, G., Laflamme, P., Molino, D., Probst, A.V., Tariq, M., Paszkowski, J., 2004.Chromatin techniques for plant cells. The Plant Journal. 39, 776-789.
    Chen K, Li GJ, Bressan RA, Song CP, Zhu JK, Zhao Y., 2020. Abscisic acid dynamics, signaling, and functions in plants. J Integr Plant Biol. 62, 25-54.
    Chen, X., Zhang, Z., Liu, D., Zhang, K., Li, A., Mao, L., 2010. SQUAMOSA promoter-binding protein-like transcription factors:Star players for plant growth and development. Journal of integrative plant biology. 52, 946-951.
    Cheon, J., Park, S.Y., Schulz, B., Choe, S., 2010 Arabidopsis brassinosteroid biosynthetic mutant dwarf7-1 exhibits slower rates of cell division and shoot induction. BMC plant biology. 10, 270.
    Chiang GC, Barua D, Kramer EM, Amasino RM, Donohue K., 2009. Major flowering time gene, flowering locus C, regulates seed germination in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 106(28), 11661-11666.
    Cho, H.J., Kim, J.J., Lee, J.H., Kim, W., Jung, J.-H., Park, C.-M., Ahn, J.H., 2012. SHORT VEGETATIVE PHASE (SVP) protein negatively regulates miR172 transcription via direct binding to the pri-miR172a promoter in Arabidopsis. FEBS letters. 586, 2332-2337.
    Clauw, P., Coppens, F., Korte, A., Herman, D., Slabbinck, B., Dhondt, S., Van Daele, T., De Milde, L., Vermeersch, M., Maleux, K., et al., 2016. Leaf Growth Response to Mild Drought:Natural Variation in Arabidopsis Sheds Light on Trait Architecture. The Plant Cell. 28, 2417-2434.
    Clough, S.J., Bent, A.F., 1998. Floral dip:a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant journal. 16, 735-743.
    Danecek, P., Auton, A., Abecasis, G., Albers, C.A., Banks, E., DePristo, M.A., Handsaker, R.E., Lunter, G., Marth, G.T., Sherry, S.T., 2011. 1000 Genomes Project Analysis Group. The variant call format and VCFtools. Bioinformatics. 27, 2156-2158.
    Dong, H., Dumenil, J., Lu, F.H., Na, L., Vanhaeren, H., Naumann, C., Klecker, M., Prior, R., Smith, C., McKenzie, N., et al., 2017. Ubiquitylation activates a peptidase that promotes cleavage and destabilization of its activating E3 ligases and diverse growth regulatory proteins to limit cell proliferation in Arabidopsis. Genes & development. 31, 197-208.
    Fisher, R. A., 1930. The Genetical Theory of Natural Selection. Clarendon Press. Oxford.Fusari, C. M. et al., 2017. Genome-wide association mapping reveals that specific and pleiotropic regulatory mechanisms fine-tune central metabolism and growth in Arabidopsis. Plant Cell. 29, 2349-2373.
    Gaut, B., 2012. Arabidopsis thaliana as a model for the genetics of local adaptation. Nature genetics. 44, 115-116.
    Gegas, V.C., Wargent, J.J., Pesquet, E., Granqvist, E., Paul, N.D., Doonan, J.H., 2014.Endopolyploidy as a potential alternative adaptive strategy for Arabidopsis leaf size variation in response to UV-B. Journal of experimental botany. 65, 2757-2766.
    Hanemian, M., Vasseur, F., Marchadier, E., Gilbault, E., Bresson, J., Gy, I., Violle, C., Loudet, O., 2020. Natural variation at FLM splicing has pleiotropic effects modulating ecological strategies in Arabidopsis thaliana. Nature Communications. 11, 4140.
    He, Z., Zeng, J., Ren, Y., Chen, D., Li, W., Gao, F., Cao, Y., Luo, T., Yuan, G., Wu, X., et al., 2017.OsGIF1 Positively Regulates the Sizes of Stems, Leaves, and Grains in Rice. Frontiers in plant science. 8, 1730.
    Hort, A., 1948. Enquiry into Plants, Vol. I, by Theophrastus. Harvard Univ. Press.
    Huo H, Wei S, Bradford KJ., 2016. DELAY OF GERMINATION1 (DOG1) regulates both seed dormancy and flowering time through microRNA pathways. Proc Natl Acad Sci U S A. 113, E2199-206.
    Kushiro, T., Okamoto, M., Nakabayashi, K., Yamagishi, K., Kitamura, S., Asami, T., Hirai, N., Koshiba, T., Kamiya, Y., Nambara, E., 2004. The Arabidopsis cytochrome P450 CYP707A encodes ABA 8'-hydroxylases:key enzymes in ABA catabolism. The EMBO journal. 23, 1647-1656.
    Lantzouni, O., Alkofer, A., Falter-Braun, P., Schwechheimer, C., 2020. GROWTH-REGULATING FACTORS Interact with DELLAs and Regulate Growth in Cold Stress. Plant Cell. 32, 1018-1034.
    Lee, K.H., Piao, H.L., Kim, H.Y., Choi, S.M., Jiang, F., Hartung, W., Hwang, I., Kwak, J.M., Lee, I.J., Hwang, I., 2006. Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell. 126, 1109-1120.
    Li, D., Liu, C., Shen, L., Wu, Y., Chen, H., Robertson, M., Helliwell, C.A., Ito, T., Meyerowitz, E., Yu, H., 2008a. A repressor complex governs the integration of flowering signals in Arabidopsis. Developmental cell. 15, 110-120.
    Li, N., Liu, Z., Wang, Z., Ru, L., Gonzalez, N., Baekelandt, A., Pauwels, L., Goossens, A., Xu, R., Zhu, Z., et al., 2018. STERILE APETALA modulates the stability of a repressor protein complex to control organ size in Arabidopsis thaliana. PLoS genetics. 14, e1007218.
    Li, W., Zhu, Z., Chern, M., Yin, J., Yang, C., Ran, L., Cheng, M., He, M., Wang, K., Wang, J., et al., 2017. A Natural Allele of a Transcription Factor in Rice Confers Broad-Spectrum Blast Resistance. Cell. 170, 114-126.
    Li, Y., Zheng, L., Corke, F., Smith, C., Bevan, M.W., 2008b. Control of final seed and organ size by the DA1 gene family in Arabidopsis thaliana. Genes & development. 22, 1331-1336.
    Liu, X., Sun, Z., Dong, W., Wang, Z., Zhang, L., 2018. Expansion and Functional Divergence of the SHORT VEGETATIVE PHASE (SVP) Genes in Eudicots. Genome biology and evolution. 10, 3026-3037.
    Lou, S., Guo, X., Liu, L., Song, Y., Zhang, L., Jiang, Y., Zhang, L., Sun, P., Liu, B., Tong, S., 2022a.Allelic shift in cis-elements of the transcription factor RAP2. 12 underlies adaptation associated with humidity in Arabidopsis thaliana. Science advances. 8, eabn8281.
    Lou, S., Guo, X., Liu, L., Song, Y., Zhang, L., Jiang, Y., Zhang, L., Sun, P., Liu, B., Tong, S., et al., 2022b. Allelic shift in cis-elements of the transcription factor RAP2.12 underlies adaptation associated with humidity in Arabidopsis thaliana. Science advances. 8, eabn8281.
    Marchadier, E., Hanemian, M., Tisne, S., Bach, L., Bazakos, C., Gilbault, E., Haddadi, P., Virlouvet, L., Loudet, O., 2019. The complex genetic architecture of shoot growth natural variation in Arabidopsis thaliana. PLoS genetics. 15, e1007954.
    Mendez-Vigo, B., Martinez-Zapater, J.M., Alonso-Blanco, C., 2013. The flowering repressor SVP underlies a novel Arabidopsis thaliana QTL interacting with the genetic background. PLoS Genet. 9, e1003289.
    Mitchum, M.G., Yamaguchi, S., Hanada, A., Kuwahara, A., Yoshioka, Y., Kato, T., Tabata, S., Kamiya, Y., Sun, T.P., 2006. Distinct and overlapping roles of two gibberellin 3-oxidases in Arabidopsis development. The Plant journal:for cell and molecular biology. 45, 804-818.
    Novikova, P.Y., Hohmann, N., Nizhynska, V., Tsuchimatsu, T., Ali, J., Muir, G., Guggisberg, A., Paape, T., Schmid, K., Fedorenko, O.M., 2016. Sequencing of the genus Arabidopsis identifies a complex history of nonbifurcating speciation and abundant trans-specific polymorphism. Nature genetics. 48, 1077-1082.
    Ó'Maoiléidigh, D.S., van Driel, A.D., Singh, A., Sang, Q., Le Bec, N., Vincent, C., de Olalla, E.B.G., Vayssières, A., Romera Branchat, M., Severing, E., 2021. Systematic analyses of the MIR172 family members of Arabidopsis define their distinct roles in regulation of APETALA2 during floral transition. PLoS Biology. 19, e3001043.
    Ogura, T., Goeschl, C., Filiault, D., Mirea, M., Slovak, R., Wolhrab, B., Satbhai, S.B., Busch, W., 2019. Root System Depth in Arabidopsis Is Shaped by EXOCYST70A3 via the Dynamic Modulation of Auxin Transport. Cell. 178, 400-412.
    Okamoto, M., Tanaka, Y., Abrams, S.R., Kamiya, Y., Seki, M., Nambara, E., 2009. High humidity induces abscisic acid 8'-hydroxylase in stomata and vasculature to regulate local and systemic abscisic acid responses in Arabidopsis. Plant physiology. 149, 825-834.
    Orr, H.A., 2000. Adaptation and the cost of complexity. Evolution. 54, 13-20.
    Paaby, A.B., Rockman, M.V., 2013. The many faces of pleiotropy. Trends in genetics. 29, 66-73.
    Palatnik, J.F., Allen, E., Wu, X., Schommer, C., Schwab, R., Carrington, J.C., Weigel, D., 2003.Control of leaf morphogenesis by microRNAs. Nature. 425, 257-263.
    Price, M.N., Dehal, P.S., Arkin, A.P., 2009. FastTree:computing large minimum evolution trees with profiles instead of a distance matrix. Molecular biology and evolution. 26, 1641-1650.
    Reich, P.B., 2014. The world-wide ‘fast-slow’plant economics spectrum:a traits manifesto. Journal of ecology. 102, 275-301.
    Saini, K., Markakis, M.N., Zdanio, M., Balcerowicz, D.M., Beeckman, T., De Veylder, L., Prinsen, E., Beemster, G.T.S., Vissenberg, K., 2017. Alteration in Auxin Homeostasis and Signaling by Overexpression Of PINOID Kinase Causes Leaf Growth Defects in Arabidopsis thaliana.Frontiers in plant science. 8, 1009.
    Sartori, K., Vasseur, F., Violle, C., Baron, E., Gerard, M., Rowe, N., Ayala-Garay, O., Christophe, A., Jalón, L.G.d., Masclef, D., 2019. Leaf economics and slow-fast adaptation across the geographic range of Arabidopsis thaliana. Scientific reports. 9, 1-12.
    Shimano, S., Hibara, K.I., Furuya, T., Arimura, S.I., Tsukaya, H., Itoh, J.I., 2018. Conserved functional control, but distinct regulation, of cell proliferation in rice and Arabidopsis leaves revealed by comparative analysis of GRF-INTERACTING FACTOR 1 orthologs.Development. 145.
    Ueguchi-Tanaka, M., Ashikari, M., Nakajima, M., Itoh, H., Katoh, E., Kobayashi, M., Chow, T.Y., Hsing, Y.I., Kitano, H., Yamaguchi, I., et al., 2005. GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature. 437, 693-698.
    Wagner, G.P., Kenney-Hunt, J.P., Pavlicev, M., Peck, J.R., Waxman, D., Cheverud, J.M., 2008.Pleiotropic scaling of gene effects and the ‘cost of complexity’. Nature. 452, 470-472.
    Wang, H., Kong, F., Zhou, C., 2021. From genes to networks:The genetic control of leaf development. J Integr Plant Biol. 63, 1181-1196.
    Wang, Z., Li, N., Jiang, S., Gonzalez, N., Huang, X., Wang, Y., Inze, D., Li, Y., 2016a. SCF(SAP)controls organ size by targeting PPD proteins for degradation in Arabidopsis thaliana.Nature communications. 7, 11192.
    Wang, Z., Liao, B.-Y. & Zhang, J., 2010. Genomic patterns of pleiotropy and the volution of complexity. Proc. Natl Acad. Sci. 107, 18034-18039.
    Wang, Z., Su, G., Li, M., Ke, Q., Kim, S.Y., Li, H., Huang, J., Xu, B., Deng, X.P., Kwak, S.S., 2016b.Overexpressing Arabidopsis ABF3 increases tolerance to multiple abiotic stresses and reduces leaf size in alfalfa. Plant physiology and biochemistry:PPB. 109, 199-208.
    Wang, Z., Wang, F., Hong, Y., Yao, J., Ren, Z., Shi, H., Zhu, J.-K., 2018. The flowering repressor SVP confers drought resistance in Arabidopsis by regulating abscisic acid catabolism.Molecular plant. 11, 1184-1197.
    Wright, I.J., Dong, N., Maire, V., Prentice, I.C., Westoby, M., Diaz, S., Gallagher, R.V., Jacobs, B.F., Kooyman, R., Law, E.A., et al., 2017. Global climatic drivers of leaf size. Science. 357, 917-921.
    Xia, T., Li, N., Dumenil, J., Li, J., Kamenski, A., Bevan, M.W., Gao, F., Li, Y., 2013. The ubiquitin receptor DA1 interacts with the E3 ubiquitin ligase DA2 to regulate seed and organ size in Arabidopsis. The Plant cell. 25, 3347-3359.
    Xu, Z.Y., Lee, K.H., Dong, T., Jeong, J.C., Jin, J.B., Kanno, Y., Kim, D.H., Kim, S.Y., Seo, M., Bressan, R.A., et al., 2012. A vacuolar beta-glucosidase homolog that possesses glucose-conjugated abscisic acid hydrolyzing activity plays an important role in osmotic stress responses in Arabidopsis. The Plant cell. 24, 2184-2199.
    Yu, S., Galvão, V.C., Zhang, Y.-C., Horrer, D., Zhang, T.-Q., Hao, Y.-H., Feng, Y.-Q., Wang, S., Schmid, M., Wang, J.-W., 2012. Gibberellin regulates the Arabidopsis floral transition through miR156-targeted SQUAMOSA PROMOTER BINDING-LIKE transcription factors. The Plant Cell. 24, 3320-3332.
    Zou, Y.P., Hou, X.H., Wu, Q., Chen, J.F., Li, Z.W., Han, T.S., Niu, X.M., Yang, L., Xu, Y.C., Zhang, J., et al., 2017. Adaptation of Arabidopsis thaliana to the Yangtze River basin. Genome biology. 18, 239.
  • 加载中
计量
  • 文章访问数:  112
  • HTML全文浏览量:  52
  • PDF下载量:  19
  • 被引次数: 0
出版历程
  • 收稿日期:  2023-06-09
  • 修回日期:  2023-08-13
  • 网络出版日期:  2023-08-24

目录

    /

    返回文章
    返回