Structural organization of TFL1-like genes in representatives of the tribe Phaseoleae DC.
DOI:
https://doi.org/10.21638/spbu03.2021.201Abstract
The type of stem growth is one of the key features in determining plant architectonics. Stem growth type is an economically important trait. It interconnects with stem length, flowering duration, yield, resistance to lodging, and suitability of mechanized cultivation. Mutations in the TFL1 gene and its homologs have been demonstrated to change meristem indeterminacy across genera. The aim of this work was to characterize and compare the structural organization of TFL1-like genes in representatives of the tribe Phaseoleae (pigeonpea Cajanus cajan, soybean Glycine max, common bean Phaseolus vulgaris, adzuki bean Vigna angularis, mung bean V. radiata, and cowpea V. unguiculata) based on in silico analysis, including analysis of nucleotide sequences, predicted elements in promoter regions, predicted amino acid sequences, putative functional domains and 3D protein structures. We investigated TFL1 (one gene for adzuki bean, four copies for soybean, two copies for other studied species), ATC (two copies for soybean, one gene for other investigated species), and BFT (two copies for soybean, one gene for other studied species) gene family members found in whole-genome sequences databases available for representatives of the tribe Phaseoleae. The presence of duplicated copies for all genes in soybean may be a result of the last genome duplication event during the evolution of this species. Duplication of TFL1 gene to two copies in most of studied species of the tribe Phaseoleae is probably accompanied by the maintenance of the functional state of these genes. The exception is VrTFL1.2 of V. radiata, which likely had lost its functionality. This work broadens the existing data about the number of gene copies, their structural divergence and evolution, and the expected functional differences. This information will be important for understanding the molecular genetic mechanisms underlying the maintenance of indeterminacy in the growth of the shoot apical meristem, as well as in the control of the transition to the reproductive phase of plant development.
Keywords:
ATC, BFT, Cajanus, Glycine, Phaseoleae, Phaseolus, TFL1, Vigna
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References
Ahn, J. H., Miller, D., Winter, V. J., Banfield, M. J., Lee, J. H., Yoo, S. Y., Henz, S. R., Brady, R. L., and Weigel, D. 2006. A divergent external loop confers antagonistic activity on floral regulators FT and TFL1. The EMBO Journal 25:605–614. https://doi.org/10.1038/sj.emboj.7600950
Alvarez, J., Guli, C. L., Yu, X. H., and Smyth, D. R. 1992. Terminal flower: a gene affecting inflorescence development in Arabidopsis thaliana. The Plant Journal 2(1):103–116. https://doi.org/10.1111/j.1365-313X.1992.00103.x
Banfield, M. J. and Brady, R. L. 2000.The structure of Antirrhinum Centroradialis Protein (CEN) suggests a role as a kinase regulator. Journal of Molecular Biology 297(5):1159–1170. https://doi.org/10.1006/jmbi.2000.3619
Benlloch, R., Berbel, A., Serrano-Mislata, A., and Madueno, F. 2007. Floral initiation and inflorescence architecture: a comparative view. Annals of Botany 100(3):659–676. https://doi.org/10.1093/aob/mcm146
Bla´zquez, M. A., Soowal, L. N., Lee, I., and Weigel, D. 1997. LEAFY expression and flower initiation in Arabidopsis. Development 124(19):3835–3844.
Boukar, O., Fatokun, C. A., Roberts, P. A., Abberton, M., Huynh, B. L., Close, T. J., Kyei-Boahen, S., Higgins, T. J. V., and Ehlers J. D. 2015. Cowpea. In: Grain Legumes. Springer: 219–250. https://doi.org/10.1007/978-1-4939-2797-5_7
Burlyaeva, M. O., Gurkina, M. V., Chebukin, P. A., Perchuk, I. N., and Miroshnichenko, E. V. 2019. New varieties of vegetable cowpea (Vigna unguiculata subsp. sesquipedalis (L.) Verdc.) and prospects of their cultivation in southern Russia. Vegetable crops of Russia 5:33–37. https://doi.org/10.18619/2072-9146-2019-5-33-37 (In Russian)
Chow, C. N., Lee, T. Y., Hung, Y. C., Li, G. Z., Tseng, K. C., Liu, Y. H., Kuo, P. L., Zheng, H. Q., and Chang, W. C. 2019. PlantPAN3.0: a new and updated resource for reconstructing transcriptional regulatory networks from ChIP-seq experiments in plants. Nucleic Acids Research 47(D1):D1155–D1163. https://doi.org/10.1093/nar/gky1081
Corpet, F. 1988. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Research 16(22):10881–10890. https://doi.org/10.1093/nar/16.22.10881
Chung, K. S., Yoo, S. Y., Yoo, S. Y., Lee, J. S., and Ahn J. H. 2010. BROTHER OF FT AND TFL1 (BFT), a member of the FT/TFL1 family, shows distinct pattern of expression during the vegetative growth of Arabidopsis. Plant Signaling and Behavior 5(9):1102–1104. https://doi.org/10.4161/psb.5.9.12415
Dhanasekar, P. and Reddy, K. S. 2015. A novel mutation in TFL1 homolog affecting determinacy in cowpea (Vigna unguiculata). Molecular Genetics and Genomics 290(1):55–65. https://doi.org/10.1007/s00438-014-0899-0
FAO Departments and Offices. FAO; 2020 [cited 2020 July]. Available from: http://www.fao.org/faostat/ru/#data/QC
Felsenstein, J. 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
Finn, R. D., Attwood, T. K., Babbitt, P. C., Bateman A., Bork P., Bridge, A. J., Chang, H. Y., Dosztányi, Z., El-Gebali, S., Fraser, M., Gough, J., Haft, D., Holliday, G. L., Huang, H., Huang, X., Letunic, I., Lopez, R., Lu, S., Marchler-Bauer, A., Mi, H., Mistry, J., Natale, D. A., Necci, M., Nuka, G., Orengo, C. A., Park, Y., Pesseat, S., Piovesan, D., Potter, S. C, Rawlings, N. D., Redaschi, N., Richardson, L., Rivoire, C., Sangrador-Vegas, A., Sigrist, C., Sillitoe, I., Smithers, B., Squizzato, S., Sutton, G., Thanki, N., Thomas, P. D., Tosatto, S. C. E., Wu, C. H., Xenarios, I., Yeh, L. S., Young, S. Y., and Mitchell, A. L. 2017. InterPro in 2017-beyond protein family and domain annotations. Nucleic Acids Research 45(D1):D190–D199. https://doi.org/10.1093/nar/gkw1107
Gonzales, M. D., Archuleta, E., Farmer, A., Gajendran, K., Grant, D., Shoemaker, R., Beavis, W. D., and Waugh, M. E. 2005. The Legume Information System (LIS): an integrated information resource for comparative legume biology. Nucleic Acids Research 33(Database issue):D660–D665. https://doi.org/10.1093/nar/gki128
Goodstein, D. M., Shu, S., Howson, R., Neupane, R., Hayes, R. D., Fazo, J., Mitros, T., Dirks, W., Hellsten, U., Putnam, N., and Rokhsar, D. S. 2012. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Research 40(D1):D1178–D1186. https://doi.org/10.1093/nar/gkr944
Goretti, D., Silvestre, M., Collani, S., Langenecker, T., Méndez, C., Madueño, F., and Schmid, M. 2020. TERMINAL FLOWER1 functions as a mobile transcriptional cofactor in the shoot apical meristem. Plant Physiology 182(4):2081–2095. https://doi.org/10.1104/pp.19.00867
Gumber, R. K. and Singh, S. 1997. Genetics of flowering patterns in pigeonpea: further evidence for two gene control. Euphytica 96:233–236. https://doi.org/10.1023/A:1003086519511
Hanzawa, Y., Money, T., and Bradley, D. 2005. A single amino acid converts a repressor to an activator of flowering. Proceedings of the National Academy of Sciences USA 102(21):7748–7753. https://doi.org/10.1073/pnas.0500932102
Higo, K., Ugawa, Y., Iwamoto, M., and Korenaga, T. 1999. Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Research 27(1):297–300. https://doi.org/10.1093/nar/27.1.297
Ho, W. W. H. and Weigel, D. 2014. Structural features determining flower-promoting activity of Arabidopsis FLOWERING LOCUS T. The Plant Cell 26(2):552–564. https://doi.org/10.1105/tpc.113.115220
Huang, N. C., Jane, W. N., Chen, J., and Yu, T. S. 2012. Arabidopsis thaliana CENTRORADIALIS homologue (ATC) acts systemically to inhibit floral initiation in Arabidopsis. The Plant Journal 72(2):175–184. https://doi.org/10.1111/j.1365-313X.2012.05076.x
Jin, S., Nasim, Z., Susila, H., and Ahn, J. H. 2021. Evolution and functional diversification of FLOWERING LOCUS T/TERMINAL FLOWER1 family genes in plants. Seminars in Cell and Developmental Biology 109:20–30. https://doi.org/10.1016/j.semcdb.2020.05.007
Kang, Y. J., Kim, S. K., Kim, M. Y., Lestari, P., Kim, K. H., Ha, B. K., Jun, T. H., Hwang, W. J., Lee, T., Lee, J. Shim, S., Yoon, M. Y., Jang, Y. E., Han, K. S., Taeprayoon, P., Yoon, N., Somta, P., Tanya, P., Kim, K. S., Gwag, J. G., Moon, J. K., Lee, Y. H., Park, B. S., Bombarely, A., Doyle, J. J., Jackson, S. A., Schafleitner, R., Srinives, P., Varshney, R. K., and Lee, S. H. 2014. Genome sequence of mungbean and insights into evolution within Vigna species. Nature Communications 5:5443. https://doi.org/10.1038/ncomms6443
Kang, Y. J., Satyawan, D., Shim, S, Lee, T., Lee, J., Hwang, W. J., Kim, S. K., Lestari, P., Laosatit, K., Kim, K. H., Ha, T. H., Chitikineni, A., Kim, M. Y., Ko, J.-M., Gwag, J.-G., Moon, J.-K., Lee, Y.-Ho, Park, B.-S., Varshney, R. K., and Lee, S. H. 2015. Draft genome sequence of adzuki bean, Vigna angularis. Scientific Reports 5:8069. https://doi.org/10.1038/srep08069
Kersey, P. J., Allen, J. E., Christensen, M., Davis, P., Falin, L. J., Grabmueller, C., Hughes, D. S., Humphrey, J., Kerhornou, A., Khobova, J., Langridge, N., McDowall, M. D., Maheswari, U., Maslen, G., Nuhn, M., Ong, C. K., Paulini, M., Pedro, H., Toneva, I., Tuli, M. A., Walts, B., Williams, G., Wilson, D., Youens-Clark, K., Monaco, M. K., Stein, J., Wei, X., Ware, D., Bolser, D. M., Howe, K. L., Kulesha, E., Lawson, D., and Staines, D. M. 2014. Ensembl Genomes 2013: scaling up access to genome-wide data. Nucleic Acids Research 42(Database issue):D546–552. https://doi.org/10.1093/nar/gkt979
Kushwah, S. N., Ahmad, I., and Ali, S. 2014. Characterization of promoter of Terminal Flower1 (TFL1) gene of Arabidopsis. Research Journal of Biotechnology 9(3):35–40.
Kumar, S., Stecher, G., Li, M., Knyaz, C., and Tamura, K. 2018. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35(6):1547–1549. https://doi.org/10.1093/molbev/msy096
Kwak, M., Velasco, D., and Gepts, P. 2008. Mapping homologous sequences for determinacy and photoperiod sensitivity in common bean (Phaseolus vulgaris). Journal of Heredity 99(3):283–291. https://doi.org/10.1093/jhered/esn005
Kwak, M., Toro, O., Debouck, D. G., and Gepts, P. 2012. Multiple origins of the determinate growth habit in domesticated common bean (Phaseolus vulgaris). Annals of Botany 110(8):1573–1580. https://doi.org/10.1093/aob/mcs207
Li, S., Ding, Y., Zhang, D., Wang, X., Tang, X., Dai, D., Jin, H., Lee, S. H., Cai, C., and Ma, J. 2018. Parallel domestication with a broad mutational spectrum of determinate stem growth habit in leguminous crops. The Plant Journal 96(4):761–771. https://doi.org/10.1111/tpj.14066
Liu, B., Watanabe, S., Uchiyama, T., Kong F., Kanazawa, A., Xia, Z., Nagamatsu, A., Arai, M., Yamada T., Kitamura K., Masuta, C., Harada, K., and Abe, J. 2010. The soybean stem growth habit gene Dt1 is an ortholog of Arabidopsis TERMINAL FLOWER1. Plant Physiology 153(1):198–210. https://doi.org/10.1104/pp.109.150607
Lonardi, S., Munoz-Amatrian, M., Liang, Q., Shu, S, Wanamaker, S. I., Lo, S., Tanskanen, J., Schulman, A. H., Zhu, T., Luo, M. C., Alhakami, H., Ounit, R., Hasan, A. Md., Verdier, J., Roberts, P.A., Santos, J. R. P., Ndeve, A., Dolezel, J., Vrana, J., Hokin, S. A., Farmer, A. D., Cannon, S. B., and Close, T. J. 2019. The genome of cowpea (Vigna unguiculata [L.] Walp.). The Plant Journal 98(5):767–782. https://doi.org/10.1111/tpj.14349
Mimida, N., Sakamoto, W., Murata, M., and Motoyoshi, F. 1999. TERMINAL FLOWER 1-like genes in Brassica species. Plant Science 142(2):155–162. https://doi.org/10.1016/s0168-9452(99)00020-5
Mimida N., Goto K., Kobayashi Y., Araki, T., Ahn, J. H., Weigel, D., Murata, M., Motoyoshi, F., and Sakamoto, W. 2001. Functional divergence of the TFL1-like gene family in Arabidopsis revealed by characterization of a novel homologue. Genes to Cells 6(4):327–336. https://doi.org/10.1046/j.1365-2443.2001.00425.x
Mir, R. R., Kudapa, H., Srikanth, S., Saxena, R. K., Sharma, A., Azam S., Saxena, K., Penmetsa, R. V., and Varshney, R. K. 2014. Candidate gene analysis for determinacy in pigeonpea (Cajanus spp.). Theoretical and Applied Genetics 127:2663–2678. https://doi.org/10.1007/s00122-014-2406-8
Moraes, T. S., Dornelas, M. C., and Martinelli, A. P. 2019. FT/TFL1: calibrating plant architecture. Frontiers in Plant Science 10:1–6. https://doi.org/10.3389/fpls.2019.00097
Munoz-Amatriaın, M., Mirebrahim H., Xu P. Wanamaker, S. I., Luo, M. C., Alhakami, H., Alpert, M., Atokple, I., Batieno, B. J., Boukar, O., Bozdag, S., Cisse, N., Drabo, I., Ehlers, J. D., Farmer, A., Fatokun, C., Gu, Y. Q., Guo, Y. N., Huynh, B. L., Jackson, S. A., Kusi, F., Lawley, C. T., Lucas, M. R., Ma, Y., Timko, M. P., Wu, J., You, F., Barkley, N. A., Roberts, P. A., Lonardi, S., and Close, T. J. 2017. Genome resources for climate-resilient cowpea, an essential crop for food security. The Plant Journal 89(5):1042–1054. https://doi.org/10.1111/tpj.13404
Périlleux, C., Bouché, F., Randoux, M., and Orman-Ligeza, B. 2019.Turning meristems into fortresses. Trends in Plant Science. 24(5):431–442. https://doi.org/10.1016/j.tplants.2019.02.004
Pin, P. A., Benlloch, R., Bonnet, D., Wremerth-Weich, E., Kraft, T., Gielen, J. J., and Nilsson, O. 2010. An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet. Science 330(6009):1397–1400. https://doi.org/10.1126/science.1197004
Ratcliffe, O. J., Amaya, I., Vincent, C. A., Rothstein, S., Carpenter, R., Coen, E. S., and Bradley, D. J. 1998. A common mechanism controls the life cycle and architecture of plants. Development 125(9):1609–1615.
Repinski, S. L., Kwak, M., and Gepts, P. 2012. The common bean growth habit gene PvTFL1y is a functional homolog of Arabidopsis TFL1. Theoretical and Applied Genetics 124(8):1539–1547. https://doi.org/10.1007/s00122-012-1808-8
Ryu, J. Y., Park, C. M., and Seo P. J. 2011. The floral repressor BROTHER OF FT and TFL1 (BFT) modulates flowering initiation under high salinity in Arabidopsis. Molecular Cells 32(3):295–303. https://doi.org/10.1007/s10059-011-0112-9
Ryu, J. Y., Lee, H. J., Seo, P. J., Jung, J. H., Ahn, J. H., and Parka, C. M. 2014. The Arabidopsis floral repressor BFT delays flowering by competing with FT for FD binding under high salinity. Molecular Plant 7(2):377–387. https://doi.org/10.1093/mp/sst114
Saitou, N. and Nei, M. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4(4):406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Sakai, H., Naito, K., Ogiso-Tanaka, E., Takahashi, Y., Iseki, K., Muto, C., Satou, K., Teruya, K., Shiroma, A., Shimoji, M., Hirano, T., Itoh, T., Kaga, A., and Tomooka, N. 2015. The power of single molecule real-time sequencing technology in the de novo assembly of a eukaryotic genome. Scientific Reports 5:16780. https://doi.org/10.1038/srep16780
Sakai, H, Naito, K, Takahashi, Y, Sato, T., Yamamoto, T., Muto, I., Itoh, T., and Tomooka, N. 2016. The Vigna Genome Server, 'VigGS': A genomic knowledge base of the genus Vigna based on high-quality, annotated genome sequence of the azuki bean, Vigna angularis (Willd.) Ohwi & Ohashi. Plant Cell Physiology 57(1):e2. https://doi.org/10.1093/pcp/pcv189
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., and Jackson S. A. 2010. Genome sequence of the palaeopolyploid soybean. Nature 463:178–183. https://doi.org/10.1038/nature08670
Schmutz, J., McClean, P. E., Mamidi, S. G., Wu, A., Cannon, S. B., Grimwood, J., Jenkins, J., Shu, S., Song, Q., Chavarro, C., Torres-Torres, M., Geffroy, V., Moghaddam S. M., Gao, D., Abernathy, B., Barry, K., Blair, M., Brick, M. A., Chovatia, M., Gepts, P., Goodstein, D. M., Gonzales, M., Hellsten U., Hyten, D.L., Jia, G., Kelly, J. D., Kudrna, D., Lee, R., Richard, M. M. S., Miklas, P. N., Osorno, J. N. Rodrigues, J., Thareau, V., Urrea, C. A., Wang, M., Yu, Y., Zhang, M., Wing, R. A., Cregan, P. B., Rokhsar, D. S., and Jackson, S. A. 2014. A reference genome for common bean and genome-wide analysis of dual domestications. Nature Genetics 46:707–713. https://doi.org/10.1038/ng.3008
Tamura, K., Nei, M., and Kumar, S. 2004. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proceedings of the National Academy of Sciences USA 101(30):11030–11035. https://doi.org/10.1073/pnas.0404206101
Tian, Z., Wang, X., Lee, R., Li, Y., Specht, J. E., Nelson, R. L., McClean, P. E., Qiu, L., and Ma, J. 2010. Artificial selection for determinate growth habit in soybean. Proceedings of the National Academy of Sciences USA 107(19):8563–8568. https://doi.org/10.1073/pnas.1000088107
Yoo, S. J., Chung, K. S., Jung, S. H., Yoo, S. Y., Lee, J. S., and Ahn, J. H. 2010. BROTHER OF FT AND TFL1 (BFT) has TFL1-like activity and functions redundantly with TFL1 in inflorescence meristem development in Arabidopsis. The Plant Journal 63(2):241–253. https://doi.org/10.1111/j.1365-313X.2010.04234.x
Varshney, R. K., Chen, W., Li, Y., Bharti, A. K., Saxena, R. K., Schlueter, J. A., Donoghue, M. T., Azam, S., Fan, G. and Whaley, A. M. 2012. Draft genome sequence of pigeonpea (Cajanus cajan), an orphan legume crop of resource-poor farmers. Nature Biotechnology 30:83. https://doi.org/10.1038/nbt.2022
Vasconcelos, E. V., De Andrade Fonseca, A. F., Pedrosa-Harand, A., De Andrade Bortoleti, K. C., Benko-Iseppon, A. M., Da Costa, A. F., and Brasileiro-Vidal, A. C. 2015. Intra- and interchromosomal rearrangements between cowpea [Vigna unguiculata (L.) Walp.] and common bean (Phaseolus vulgaris L.) revealed by BAC-FISH. Chromosome Research 23(2):253–266. https://doi.org/10.1007/s10577-014-9464-2
Vishnyakova, M. A., Aleksandrova, T. G., Buravtseva, T. V., Burlyaeva, M. O., Egorova, G. P., Semenova, E. V., Seferova, I. V., and Suvorova, G. N. 2019. Species diversity of the VIR collection of grain legume genetic resources and its use in domestic breeding. Proceedings on Applied Botany, Genetics and Breeding 180(2):109–123. https://doi.org/10.30901/2227-8834-2019-2-109-123 (In Russian)
Waterhouse, A. Bertoni, M., Bienert, S., Studer, G., Tauriello, G., Gumienny, R., Heer, F. T, de Beer, T. A P, Rempfer, C., Bordoli, L., Lepore, R., and Schwede, T. 2018. SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Research 46(W1):W296–W303. https://doi.org/10.1093/nar/gky427
Wickland, D. P. and Hanzawa, Y. 2015. The FLOWERING LOCUS T / TERMINAL FLOWER 1 gene family: functional evolution and molecular mechanisms. Molecular Plant 8:983–997. https://doi.org/10.1016/j.molp.2015.01.007
Weigel, D., Alvarez, J., Smyth, D. R., Yanofsky, M. F., and Meyerowitz, E. M. 1992. LEAFY controls floral meristem identity in Arabidopsis. Cell 69(5):843–859. https://doi.org/10.1016/0092-8674(92)90295-n
Weigel, D. and Nilsson, O. A. 1995. Developmental switch sufficient for flower initiation in diverse plants. Nature 377:495–500. https://doi.org/10.1038/377495a0
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2021-06-30
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Krylova, E., Strygina, K., & Khlestkina, E. (2021). Structural organization of <em>TFL1</em>-like genes in representatives of the tribe Phaseoleae DC. Biological Communications, 66(2), 85–108. https://doi.org/10.21638/spbu03.2021.201
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