SPECIAL TOPICS
The Role of Alternative Splicing in Floral Transition
Expand
- 1Plant Genomics and Molecular Improvement of Colored Fiber Laboratory, Zhejiang Sci-Tech University, Hangzhou 310018, China
2Key Laboratory of Horticultural Plant Biology, Ministry of Education, Huazhong Agricultural University, Wuhan 430070, China
Received date: 2021-05-24
Accepted date: 2021-10-12
Online published: 2021-10-12
Abstract
Precise regulation of floral transition, which ensures plants bloom in the suitable environment, is essential for the successful reproduction of plants. The flowering time genes are regulated by a variety of molecular mechanisms, including transcriptional, post-transcriptional and post-translational regulations. Alternative splicing is a universal molecular process at the post-transcriptional level that can generate multiple transcripts from a single gene, thereby enriching the diversity of the transcriptome and proteome. The accumulating evidence indicates that alternative splicing plays an important role in the floral transition. According to developmental and environmental cues, alternative splicing can regulate the levels of functional transcripts and/or proteins of flowering time genes by affecting the stability of mRNA and/or the function of protein isoforms. Therefore, revealing the roles of alternative splicing will further improve our understanding of the functions of flowering time genes and the whole regulatory network of floral transition. In this review, we introduce the research progress of alternative splicing in floral transition, and summarize from the various regulatory pathways, thereby providing a reference for further research on the regulatory mechanisms of alternative splicing and floral transition in plants.
Cite this article
Fangfang Cai, Changsheng Shao, Yuqiang Sun . The Role of Alternative Splicing in Floral Transition[J]. Chinese Bulletin of Botany, 2022 , 57(1) : 69 -79 . DOI: 10.11983/CBB21085
References
| [1] | 马朝峰, 戴思兰 (2019). 光受体介导信号转导调控植物开花研究进展. 植物学报 54, 9-22. |
| [2] | 王翊, 马月萍, 戴思兰 (2010). 观赏植物花期调控途径及其分子机制. 植物学报 45, 641-653. |
| [3] | Ai XY, Zhang JZ, Liu TJ, Hu CG (2016). PtFCA from precocious trifoliate orange is regulated by alternative splicing and affects flowering time and root development in transgenic Arabidopsis. Tree Genet Genom 12, 85. |
| [4] | Airoldi CA, McKay M, Davies B (2015). MAF2 is regulated by temperature-dependent splicing and represses flowering at low temperatures in parallel with FLM. PLoS One 10, e0126516. |
| [5] | Bloomer RH, Dean C (2017). Fine-tuning timing: natural variation informs the mechanistic basis of the switch to flowering in Arabidopsis thaliana. J Exp Bot 68, 5439-5452. |
| [6] | Bouché F, Lobet G, Tocquin P, Périlleux C (2016). FLOR-ID: an interactive database of flowering-time gene networks in Arabidopsis thaliana. Nucleic Acids Res 44, D1167-D1171. |
| [7] | Cai FF, Shao CS, Zhang YP, Bao ZR, Li ZQ, Shi GH, Bao MZ, Zhang JQ (2019). Identification and characterisation of a novel FT orthologous gene in London plane with a distinct expression response to environmental stimuli com- pared to PaFT. Plant Biol 21, 1039-1051. |
| [8] | Cai FF, Shao CS, Zhang YP, Shi GH, Bao ZR, Bao MZ, Zhang JQ (2021). Two FD homologs from London plane (Platanus acerifolia) are associated with floral initiation and flower morphology. Plant Sci 310, 110971. |
| [9] | Capovilla G, Pajoro A, Immink RGH, Schmid M (2015a). Role of alternative pre-mRNA splicing in temperature signaling. Curr Opin Plant Biol 27, 97-103. |
| [10] | Capovilla G, Schmid M, Posé D (2015b). Control of flowering by ambient temperature. J Exp Bot 66, 59-69. |
| [11] | Cheng YL, Tu SL (2018). Alternative splicing and cross-talk with light signaling. Plant Cell Physiol 59, 1104-1110. |
| [12] | Conti L (2017). Hormonal control of the floral transition: can one catch them all? Dev Biol 430, 288-301. |
| [13] | Csorba T, Questa JI, Sun QW, Dean C (2014). Antisense COOLAIR mediates the coordinated switching of chromatin states at FLC during vernalization. Proc Natl Acad Sci USA 111, 16160-16165. |
| [14] | Cui ZB, Tong AZ, Huo YQ, Yan ZQ, Yang WQ, Yang XL, Wang XX (2017). SKIP controls flowering time via the alternative splicing of SEF pre-mRNA in Arabidopsis. BMC Biol 15, 80. |
| [15] | Deng HJ, Cheema J, Zhang H, Woolfenden H, Norris M, Liu ZS, Liu Q, Yang XF, Yang ML, Deng X, Cao XF, Ding YL (2018). Rice in vivo RNA structurome reveals RNA secondary structure conservation and divergence in plants. Mol Plant 11, 607-622. |
| [16] | Fornara F, De Montaigu A, Coupland G (2010). SnapShot: control of flowering in Arabidopsis. Cell 141, 550-550. |
| [17] | Gil KE, Park MJ, Lee HJ, Park YJ, Han SH, Kwon YJ, Seo PJ, Jung JH, Park CM (2017). Alternative splicing provides a proactive mechanism for the diurnal CONSTANS dynamics in Arabidopsis photoperiodic flowering. Plant J 89, 128-140. |
| [18] | Hugouvieux V, Kwak JM, Schroeder JI (2001). An mRNA cap binding protein, ABH1, modulates early abscisic acid signal transduction in Arabidopsis. Cell 106, 477-487. |
| [19] | Jung JH, Domijan M, Klose C, Biswas S, Ezer D, Gao MJ, Khattak AK, Box MS, Charoensawan V, Cortijo S, Kumar M, Grant A, Locke JCW, Schäfer E, Jaeger KE, Wigge PA (2016). Phytochromes function as thermosensors in Arabidopsis. Science 354, 886-889. |
| [20] | Jung JH, Seo PJ, Ahn JH, Park CM (2012). Arabidopsis RNA-binding protein FCA regulates microRNA172 processing in thermosensory flowering. J Biol Chem 287, 16007-16016. |
| [21] | Jung JH, Seo YH, Seo PJ, Reyes JL, Yun J, Chua NH, Park CM (2007). The GIGANTEA-regulated microRNA172 mediates photoperiodic flowering independent of CONSTANS in Arabidopsis. Plant Cell 19, 2736-2748. |
| [22] | Khan MRG, Ai XY, Zhang JZ (2014). Genetic regulation of flowering time in annual and perennial plants. WIREs RNA 5, 347-359. |
| [23] | Kuhn JM, Breton G, Schroeder JI (2007). mRNA metabolism of flowering-time regulators in wild-type Arabidopsis revealed by a nuclear cap binding protein mutant, abh1. Plant J 50, 1049-1062. |
| [24] | Kurokawa K, Kobayashi J, Nemoto K, Nozawa A, Sawasaki T, Nakatsuka T, Yamagishi M (2020). Expression of LhFT1, the flowering inducer of Asiatic hybrid lily, in the bulb scales. Front Plant Sci 11, 570915. |
| [25] | Kwon YJ, Park MJ, Kim SG, Baldwin IT, Park CM (2014). Alternative splicing and nonsense-mediated decay of circadian clock genes under environmental stress conditions in Arabidopsis. BMC Plant Biol 14, 136. |
| [26] | Lazaro A, Valverde F, Piñeiro M, Jarillo JA (2012). The Arabidopsis E3 ubiquitin ligase HOS1 negatively regulates CONSTANS abundance in the photoperiodic control of flowering. Plant Cell 24, 982-999. |
| [27] | Lee JH, Ryu HS, Chung KS, Posé D, Kim S, Schmid M, Ahn JH (2013). Regulation of temperature-responsive flowering by MADS-box transcription factor repressors. Science 342, 628-632. |
| [28] | Lee JH, Yoo SJ, Park SH, Hwang I, Lee JS, Ahn JH (2007). Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. Genes Dev 21, 397-402. |
| [29] | Lempe J, Balasubramanian S, Sureshkumar S, Singh A, Schmid M, Weigel D (2005). Diversity of flowering responses in wild Arabidopsis thaliana strains. PLoS Genet 1, e6. |
| [30] | Li CX, Lin HQ, Dubcovsky J (2015a). Factorial combinations of protein interactions generate a multiplicity of florigen activation complexes in wheat and barley. Plant J 84, 70-82. |
| [31] | Li PJ, Tao Z, Dean C (2015b). Phenotypic evolution through variation in splicing of the noncoding RNA COOLAIR. Genes Dev 29, 696-701. |
| [32] | Li Y, Yang J, Shang XD, Lv WZ, Xia CC, Wang C, Feng JL, Cao Y, He H, Li LG, Ma LG (2019). SKIP regulates environmental fitness and floral transition by forming two distinct complexes in Arabidopsis. New Phytol 224, 321-335. |
| [33] | Lim GH, Zhang X, Chung MS, Lee DJ, Woo YM, Cheong HS, Kim CS (2010). A putative novel transcription factor, AtSKIP, is involved in abscisic acid signaling and confers salt and osmotic tolerance in Arabidopsis. New Phytol 185, 103-113. |
| [34] | Liu FQ, Quesada V, Crevillén P, Bäurle I, Swiezewski S, Dean C (2007). The Arabidopsis RNA-binding protein FCA requires a Lysine-specific demethylase 1 homolog to downregulate FLC. Mol Cell 28, 398-407. |
| [35] | Macknight R, Duroux M, Laurie R, Dijkwel P, Simpson G, Dean C (2002). Functional significance of the alternative transcript processing of the Arabidopsis floral promoter FCA. Plant Cell 14, 877-888. |
| [36] | Mao YC, Sun J, Cao PP, Zhang R, Fu QK, Chen SM, Chen FD, Jiang JF (2016). Functional analysis of alternative splicing of the FLOWERING LOCUS T orthologous gene in Chrysanthemum morifolium. Hort Res 3, 16058. |
| [37] | Marquardt S, Raitskin O, Wu Z, Liu FQ, Sun QW, Dean C (2014). Functional consequences of splicing of the antisense transcript COOLAIR on FLC transcription. Mol Cell 54, 156-165. |
| [38] | Michaels SD, Himelblau E, Kim SY, Schomburg FM, Amasino RM (2005). Integration of flowering signals in winter-annual Arabidopsis. Plant Physiol 137, 149-156. |
| [39] | Oakenfull RJ, Davis SJ (2017). Shining a light on the Arabidopsis circadian clock. Plant Cell Environ 40, 2571-2585. |
| [40] | Posé D, Verhage L, Ott F, Yant L, Mathieu J, Angenent GC, Immink RGH, Schmid M (2013). Temperature-dependent regulation of flowering by antagonistic FLM variants. Nature 503, 414-417. |
| [41] | Qi HD, Lin Y, Ren QP, Wang YY, Xiong F, Wang XL (2019). RNA splicing of FLC modulates the transition to flowering. Front Plant Sci 10, 1625. |
| [42] | Qin ZR, Wu JJ, Geng SF, Feng N, Chen FJ, Kong XC, Song GY, Chen K, Li AL, Mao L, Wu L (2017). Regulation of FT splicing by an endogenous cue in temperate grasses. Nat Commun 8, 14320. |
| [43] | Reddy ASN, Marquez Y, Kalyna M, Barta A (2013). Complexity of the alternative splicing landscape in plants. Plant Cell 25, 3657-3683. |
| [44] | Rosloski SM, Singh A, Jali SS, Balasubramanian S, Weigel D, Grbic V (2013). Functional analysis of splice variant expression of MADS AFFECTING FLOWERING 2 of Arabidopsis thaliana. Plant Mol Biol 81, 57-69. |
| [45] | Scortecci KC, Michaels SD, Amasino RM (2001). Identification of a MADS-box gene, FLOWERING LOCUS M, that represses flowering. Plant J 26, 229-236. |
| [46] | Searle I, He YH, Turck F, Vincent C, Fornara F, Kröber S, Amasino RA, Coupland G (2006). The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes Dev 20, 898-912. |
| [47] | Seaton DD, Smith RW, Song YH, MacGregor DR, Stewart K, Steel G, Foreman J, Penfield S, Imaizumi T, Millar AJ, Halliday KJ (2015). Linked circadian outputs control elongation growth and flowering in response to photoperiod and temperature. Mol Syst Biol 11, 776. |
| [48] | Severing EI, Van Dijk ADJ, Morabito G, Busscher-Lange J, Immink RGH, Van Ham RCHJ (2012). Predicting the impact of alternative splicing on plant MADS domain protein function. PLoS One 7, e30524. |
| [49] | Shikata H, Hanada K, Ushijima T, Nakashima M, Suzuki Y, Matsushita T (2014). Phytochrome controls alternative splicing to mediate light responses in Arabidopsis. Proc Natl Acad Sci USA 111, 18781-18786. |
| [50] | Simpson GG, Dijkwel PP, Quesada V, Henderson I, Dean C (2003). FY is an RNA 3′ end-processing factor that interacts with FCA to control the Arabidopsis floral transition. Cell 113, 777-787. |
| [51] | Song HR, Song JD, Cho JN, Amasino RM, Noh B, Noh YS (2009). The RNA binding protein ELF9 directly reduces SUPPRESSOR OF OVEREXPRESSION OF CO1 transcript levels in Arabidopsis, possibly via nonsense-mediated mRNA decay. Plant Cell 21, 1195-1211. |
| [52] | Song YH, Smith RW, To BJ, Millar AJ, Imaizumi T (2012). FKF1 conveys timing information for CONSTANS stabilization in photoperiodic flowering. Science 336, 1045-1049. |
| [53] | Staiger D, Brown JWS (2013). Alternative splicing at the intersection of biological timing, development, and stress responses. Plant Cell 25, 3640-3656. |
| [54] | Sureshkumar S, Dent C, Seleznev A, Tasset C, Balasubramanian S (2016). Nonsense-mediated mRNA decay modulates FLM-dependent thermosensory flowering response in Arabidopsis. Nat Plants 2, 16055. |
| [55] | Tian YK, Zheng H, Zhang F, Wang SL, Ji XR, Xu C, He YH, Ding Y (2019). PRC2 recruitment and H3K27me3 deposition at FLC require FCA binding of COOLAIR. Sci Adv 5, eaau7246. |
| [56] | Wang XX, Wu FM, Xie QG, Wang HM, Wang Y, Yue YL, Gahura O, Ma SS, Liu L, Cao Y, Jiao YL, Puta F, McClung CR, Xu XD, Ma LG (2012). SKIP is a component of the spliceosome linking alternative splicing and the circadian clock in Arabidopsis. Plant Cell 24, 3278-3295. |
| [57] | Wang YP, Li L, Ye TT, Lu YM, Chen X, Wu Y (2013). The inhibitory effect of ABA on floral transition is mediated by ABI5 in Arabidopsis. J Exp Bot 64, 675-684. |
| [58] | Wang YY, Xiong F, Ren QP, Wang XL (2020). Regulation of flowering transition by alternative splicing: the role of the U2 auxiliary factor. J Exp Bot 71, 751-758. |
| [59] | Werner JD, Borevitz JO, Uhlenhaut NH, Ecker JR, Chory J, Weigel D (2005). FRIGIDA-independent variation in flowering time of natural Arabidopsis thaliana accessions. Genetics 170, 1197-1207. |
| [60] | Wu G, Park MY, Conway SR, Wang JW, Weigel D, Poethig RS (2009). The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138, 750-759. |
| [61] | Wu J, Wei KY, Cheng F, Li SK, Wang Q, Zhao JJ, Bonnema G, Wang XW (2012). A naturally occurring InDel variation in BraA.FLC.b (BrFLC2) associated with flowering time variation in Brassica rapa. BMC Plant Biol 12, 151. |
| [62] | Wu Z, Fang XF, Zhu DL, Dean C (2019). Autonomous pathway: FLOWERING LOCUS C repression through an antisense-mediated chromatin-silencing mechanism. Plant Physiol 182, 27-37. |
| [63] | Xi X, Wei KY, Gao BZ, Liu JH, Liang JL, Cheng F, Wang XW, Wu J (2018). BrFLC5: a weak regulator of flowering time in Brassica rapa. Theor Appl Genet 131, 2107-2116. |
| [64] | Xiong F, Ren JJ, Yu Q, Wang YY, Lu CC, Kong LJ, Otegui MS, Wang XL (2019). AtU2AF65b functions in abscisic acid mediated flowering via regulating the precursor messenger RNA splicing of ABI5 and FLC in Arabidopsis. New Phytol 223, 277-292. |
| [65] | Yang XZ, Zhang HY, Li L (2012). Alternative mRNA processing increases the complexity of microRNA-based gene regulation in Arabidopsis. Plant J 70, 421-431. |
| [66] | Yang ZC, Yang Z, Yang CC, Wang ZY, Chen DY, Xie YG, Wu YJ (2020). Identification and genetic analysis of alternative splicing of long non-coding RNAs in tomato initial flowering stage. Genomics 112, 897-907. |
| [67] | Yu JW, Rubio V, Lee NY, Bai SL, Lee SY, Kim SS, Liu LJ, Zhang YY, Irigoyen ML, Sullivan JA, Zhang Y, Lee I, Xie Q, Paek NC, Deng XW (2008). COP1 and ELF3 control circadian function and photoperiodic flowering by regulating GI stability. Mol Cell 32, 617-630. |
| [68] | Yuan YX, Wu J, Sun RF, Zhang XW, Xu DH, Bonnema G, Wang XW (2009). A naturally occurring splicing site mutation in the Brassica rapa FLC1 gene is associated with variation in flowering time. J Exp Bot 60, 1299-1308. |
| [69] | Zhang J, Liu G, Guo C, He Y, Li Z, Ning G, Shi X, Bao M (2011). The FLOWERING LOCUS T orthologous gene of Platanus acerifolia is expressed as alternatively spliced forms with distinct spatial and temporal patterns. Plant Biol 13, 809-820. |
| [70] | Zhang JZ, Li ZM, Mei L, Yao JL, Hu CG (2009). PtFLC homolog from trifoliate orange (Poncirus trifoliata) is regulated by alternative splicing and experiences seasonal fluctuation in expression level. Planta 229, 847-859. |
| [71] | Zou XX, Suppanz I, Raman H, Hou JN, Wang J, Long Y, Jung C, Meng JL (2012). Comparative analysis of FLC homologues in Brassicaceae provides insight into their role in the evolution of oilseed rape. PLoS One 7, e45751. |