OsFD4 promotes the rice floral transition via florigen activation complex formation in the shoot apical meristem.
bZIP
florigen activation complex
photoperiodic flowering
rice
shoot apical meristem
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
01 2021
01 2021
Historique:
received:
22
02
2020
accepted:
15
07
2020
pubmed:
2
8
2020
medline:
15
5
2021
entrez:
2
8
2020
Statut:
ppublish
Résumé
In rice, the florigens Heading Date 3a (Hd3a) and Rice Flowering Locus T 1 (RFT1), OsFD-like basic leucine zipper (bZIP) transcription factors, and Gf14 proteins assemble into florigen activation/repressor complexes (FACs/FRCs), which regulate transition to flowering in leaves and apical meristem. Only OsFD1 has been described as part of complexes promoting flowering at the meristem, and little is known about the role of other bZIP transcription factors, the combinatorial complexity of FAC formation, and their DNA-binding properties. Here, we used mutant analysis, protein-protein interaction assays and DNA affinity purification (DAP) sequencing coupled to in silico prediction of binding syntaxes to study several bZIP proteins that assemble into FACs or FRCs. We identified OsFD4 as a component of a FAC promoting flowering at the shoot apical meristem, downstream of OsFD1. The osfd4 mutants are late flowering and delay expression of genes promoting inflorescence development. Protein-protein interactions indicate an extensive network of contacts between several bZIPs and Gf14 proteins. Finally, we identified genomic regions bound by bZIPs with promotive and repressive effects on flowering. We conclude that distinct bZIPs orchestrate floral induction at the meristem and that FAC formation is largely combinatorial. While binding to the same consensus motif, their DNA-binding syntax is different, suggesting discriminatory functions.
Substances chimiques
Florigen
0
Plant Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
429-443Informations de copyright
© 2020 The Authors New Phytologist © 2020 New Phytologist Trust.
Références
Abe M, Kobayashi Y, Yamamoto S, Daimon Y, Yamaguchi A, Ikeda Y, Ichinoki H, Notaguchi M, Goto K, Araki T. 2005. FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309: 1052-1056.
Andrés F, Coupland G. 2012. The genetic basis of flowering responses to seasonal cues. Nature Reviews. Genetics 13: 627-639.
Bartlett A, Malley RCO, Huang SC, Galli M, Nery JR, Gallavotti A, Ecker JR. 2017. Mapping genome-wide transcription-factor binding sites using DAP-seq. Nature Protocols 12: 1659-1672.
Benlloch R, Kim MC, Sayou C, Thévenon E, Parcy F, Nilsson O. 2011. Integrating long-day flowering signals: a LEAFY binding site is essential for proper photoperiodic activation of APETALA1. The Plant Journal 67: 1094-1102.
Bolger AM, Lohse M, Usadel B. 2014. Genome analysis Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114-2120.
Brambilla V, Martignago D, Goretti D, Cerise M, Somssich M, de Rosa M, Galbiati F, Shrestha R, Lazzaro F, Simon R et al. 2017. Antagonistic transcription factor complexes modulate the floral transition in rice. The Plant Cell 29: 2801-2816.
Cho L-H, Yoon J, Pasriga R, An G. 2016. Homodimerization of Ehd1 is required to induce flowering in rice. Plant Physiology 170: 2159-2171.
Collani S, Neumann M, Yant L, Schmid M. 2019. FT modulates genome-wide DNA-binding of the bZIP transcription factor FD. Plant Physiology 180: 367-380.
Doi K, Izawa T, Fuse T, Yamanouchi U, Kubo T, Shimatani Z, Yano M, Yoshimura A. 2004. Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Genes & Development 18: 926-936.
Dröge-Laser W, Snoek BL, Snel B, Weiste C. 2018. The Arabidopsis bZIP transcription factor family - an update. Current Opinion in Plant Biology 45: 36-49.
Du A, Tian W, Wei M, Yan W, He H, Zhou D, Huang X, Li S, Ouyang X. 2017. The DTH8-Hd1 module mediates day-length-dependent regulation of rice flowering. Molecular Plant 10: 948-961.
Furutani I, Sukegawa S, Kyozuka J. 2006. Genome-wide analysis of spatial and temporal gene expression in rice panicle development. The Plant Journal 46: 503-511.
Galbiati F, Chiozzotto R, Locatelli F, Spada A, Genga A, Fornara F. 2016. Hd3a, RFT1 and Ehd1 integrate photoperiodic and drought stress signals to delay the floral transition in rice. Plant, Cell & Environment 39: 1982-1993.
Galli M, Khakhar A, Lu Z, Chen Z, Sen S, Joshi T, Nemhauser JL, Schmitz RJ, Gallavotti A. 2018. The DNA binding landscape of the maize AUXIN RESPONSE FACTOR family. Nature Communications 9: 4526.
Gómez-Ariza J, Brambilla V, Vicentini G, Landini M, Cerise M, Carrera E, Shrestha R, Chiozzotto R, Galbiati F, Caporali E et al. 2019. A transcription factor coordinating internode elongation and photoperiodic signals in rice. Nature Plants 5: 358-362.
Goretti D, Martignago D, Landini M, Brambilla V, Gómez-Ariza J, Gnesutta N, Galbiati F, Collani S, Takagi H, Terauchi R et al. 2017. Transcriptional and post-transcriptional mechanisms limit heading date 1 (Hd1) function to adapt rice to high latitudes. PLoS Genetics 13: e1006530.
Guo Y, Mahony S, Gifford DK. 2012. High resolution genome wide binding event finding and motif discovery reveals transcription factor spatial binding constraints. PLoS Computational Biology 8: e1002638.
Hayama R, Yokoi S, Tamaki S, Yano M, Shimamoto K. 2003. Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422: 719-722.
Huang W, Loganantharaj R, Schroeder B, Fargo D, Li L. 2013. PAVIS: a tool for peak annotation and visualization. Bioinformatics 29: 3097-3099.
Itoh H, Nonoue Y, Yano M, Izawa T. 2010. A pair of floral regulators sets critical day length for Hd3a florigen expression in rice. Nature Genetics 42: 635-638.
Izawa T, Foster R, Chua NH. 1993. Plant bZIP protein DNA binding specificity. Journal of Molecular Biology 230: 1131-1144.
Jaeger KE, Pullen N, Lamzin S, Morris RJ, Wigge PA. 2013. Interlocking feedback loops govern the dynamic behavior of the floral transition in Arabidopsis. The Plant Cell 25: 820-833.
Jang S, Li H-Y, Kuo M-L. 2017. Ectopic expression of Arabidopsis FD and FD PARALOGUE in rice results in dwarfism with size reduction of spikelets. Scientific Reports 7: 44477.
Jung J-H, Lee H-J, Ryu JY, Park C-M. 2016. SPL3/4/5 integrate developmental aging and photoperiodic signals into the FT-FD module in Arabidopsis flowering. Molecular Plant 9: 1647-1659.
Kaneko-Suzuki M, Kurihara-Ishikawa R, Okushita-Terakawa C, Kojima C, Nagano-Fujiwara M, Ohki I, Tsuji H, Shimamoto K, Taoka KI. 2018. TFL1-like proteins in rice antagonize rice FT-like protein in inflorescence development by competition for complex formation with 14-3-3 and FD. Plant and Cell Physiology 59: 458-468.
Kawamoto N, Sasabe M, Endo M, Machida Y, Araki T. 2015. Calcium-dependent protein kinases responsible for the phosphorylation of a bZIP transcription factor FD crucial for the florigen complex formation. Scientific Reports 5: 8341.
Kim S-K, Park H-Y, Jang YH, Lee KC, Chung YS, Lee JH, Kim J-K. 2016. OsNF-YC2 and OsNF-YC4 proteins inhibit flowering under long-day conditions in rice. Planta 243: 563-576.
Kobayashi K, Maekawa M, Miyao A, Hirochika H, Kyozuka J. 2010. PANICLE PHYTOMER2 (PAP2), encoding a SEPALLATA subfamily MADS-box protein, positively controls spikelet meristem identity in rice. Plant and Cell Physiology 51: 47-57.
Kobayashi K, Yasuno N, Sato Y, Yoda M, Yamazaki R, Kimizu M, Yoshida H, Nagamura Y, Kyozuka J. 2012. Inflorescence meristem identity in rice is specified by overlapping functions of three AP1/FUL-like MADS box genes and PAP2, a SEPALLATA MADS box gene. The Plant Cell 24: 1848-1859.
Kojima S, Takahashi Y, Kobayashi Y, Monna L, Sasaki T, Araki T, Yano M. 2002. Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant & Cell Physiology 43: 1096-1105.
Komiya R, Ikegami A, Tamaki S, Yokoi S, Shimamoto K. 2008. Hd3a and RFT1 are essential for flowering in rice. Development 135: 767-774.
Komiya R, Yokoi S, Shimamoto K. 2009. A gene network for long-day flowering activates RFT1 encoding a mobile flowering signal in rice. Development 136: 3443-3450.
Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods 9: 357-359.
Li C, Lin H, Dubcovsky J. 2015. Factorial combinations of protein interactions generate a multiplicity of florigen activation complexes in wheat and barley. The Plant Journal 84: 70-82.
Li D, Zhang H, Mou M, Chen Y, Xiang S, Chen L, Yu D. 2019. Arabidopsis class II TCP transcription factors integrate with the FT-FD module to control flowering. Plant Physiology 181: 97-111.
Liu B, Liu Y, Wang B, Luo Q, Shi J, Gan J, Shen WH, Yu Y, Dong A. 2019. The transcription factor OsSUF4 interacts with SDG725 in promoting H3K36me3 establishment. Nature Communications 10: 1-14.
Liu Y, Cui S, Wu F, Yan S, Lin X, Du X, Chong K, Schilling S, Theißen G, Meng Z. 2013. Functional conservation of MIKC*-type MADS box genes in Arabidopsis and rice pollen maturation. The Plant Cell 25: 1288-1303.
Miao J, Guo D, Zhang J, Huang Q, Qin G, Zhang X, Wan J, Gu H, Qu L-J. 2013. Targeted mutagenesis in rice using CRISPR-Cas system. Cell Research 23: 1233-1236.
Nemoto Y, Nonoue Y, Yano M, Izawa T. 2016. Hd1, a CONSTANS ortholog in rice, functions as an Ehd1 repressor through interaction with monocot-specific CCT-domain protein Ghd7. The Plant Journal 86: 221-233.
O’Malley RC, Huang S-sC, Song L, Lewsey MG, Bartlett A, Nery JR, Galli M, Gallavotti A, Ecker JR. 2016. Cistrome and epicistrome features shape the regulatory DNA landscape. Cell 166: 1598.
Oliveros J. 2007. Venny. An interactive tool for comparing lists with Venn’s diagrams. [WWW document] URL http://bioinfogp.cnb.csic.es/tools/venny/index.html.
Park SJ, Jiang K, Tal L, Yichie Y, Gar O, Zamir D, Eshed Y, Lippman ZB. 2014. Optimization of crop productivity in tomato using induced mutations in the florigen pathway. Nature Genetics 46: 1337-1342.
Purwestri YA, Ogaki Y, Tamaki S, Tsuji H, Shimamoto K. 2009. The 14-3-3 protein GF14c acts as a negative regulator of flowering in rice by interacting with the florigen Hd3a. Plant and Cell Physiology 50: 429-438.
Sahoo KK, Tripathi AK, Pareek A, Sopory SK, Singla-Pareek SL. 2011. An improved protocol for efficient transformation and regeneration of diverse indica rice cultivars. Plant Methods 7: 49.
Stigliani A, Martin-Arevalillo R, Lucas J, Bessy A, Vinos-Poyo T, Mironova V, Vernoux T, Dumas R, Parcy F. 2019. Capturing auxin response factors syntax using DNA binding models. Molecular Plant 12: 822-832.
Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K. 2007. Hd3a protein is a mobile flowering signal in rice. Science 316: 1033-1036.
Tamaki S, Tsuji H, Matsumoto A, Fujita A, Shimatani Z, Terada R, Sakamoto T, Kurata T, Shimamoto K. 2015. FT-like proteins induce transposon silencing in the shoot apex during floral induction in rice. Proceedings of the National Academy of Sciences, USA 112: E901-E910.
Taoka K, Ohki I, Tsuji H, Furuita K, Hayashi K, Yanase T, Yamaguchi M, Nakashima C, Purwestri YA, Tamaki S et al. 2011. 14-3-3 proteins act as intracellular receptors for rice Hd3a florigen. Nature 476: 332-335.
Teo C-J, Takahashi K, Shimizu K, Shimamoto K, Taoka K. 2017. Potato tuber induction is regulated by interactions between components of a Tuberigen complex. Plant and Cell Physiology 58: 365-374.
Tsuji H, Nakamura H, Taoka K, Shimamoto K. 2013. Functional diversification of FD transcription factors in rice, components of florigen activation complexes. Plant & Cell Physiology 54: 385-397.
Tylewicz S, Tsuji H, Miskolczi P, Petterle A, Azeez A, Jonsson K, Shimamoto K, Bhalerao RP. 2015. Dual role of tree florigen activation complex component FD in photoperiodic growth control and adaptive response pathways. Proceedings of the National Academy of Sciences, USA 112: 3140-5.
Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D. 2005. Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309: 1056-1059.
Wu F, Shi X, Lin X, Liu Y, Chong K, Theißen G, Meng Z. 2017. The ABCs of flower development: mutational analysis of AP1/FUL-like genes in rice provides evidence for a homeotic (A)-function in grasses. The Plant Journal 89: 310-324.
Xue W, Xing Y, Weng X, Zhao Y, Tang W, Wang L, Zhou H, Yu S, Xu C, Li X et al. 2008. Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nature Genetics 40: 761-767.
Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L, Fuse T, Baba T, Yamamoto K, Umehara Y, Nagamura Y et al. 2000. Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. The Plant Cell 12: 2473-2484.
Zhang S, Wang S, Xu Y, Yu C, Shen C, Qian Q, Geisler M, Jiang DA, Qi Y. 2015. The auxin response factor, OsARF19, controls rice leaf angles through positively regulating OsGH 3-5 and OsBRI 1. Plant, Cell & Environment 38: 638-654.
Zhao J, Chen H, Ren D, Tang H, Qiu R, Feng J, Long Y, Niu B, Chen D, Zhong T et al. 2015. Genetic interactions between diverged alleles of Early heading date 1 (Ehd1) and Heading date 3a (Hd3a)/RICE FLOWERING LOCUS T1 (RFT1) control differential heading and contribute to regional adaptation in rice (Oryza sativa). New Phytologist 208: 936-948.
Zhu S, Wang J, Cai M, Zhang H, Wu F, Xu Y, Li C, Cheng Z, Zhang X, Guo X et al. 2017. The OsHAPL1-DTH8-Hd1 complex functions as the transcription regulator to repress heading date in rice. Journal of Experimental Botany 68: 553-568.