A novel Arabidopsis gene RGAT1 is required for GA-mediated tapetum and pollen development.
DELLA
RGA
RGAT1
gibberellin
male sterility
pollen
programmed cell death
tapetum development
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
07 2021
07 2021
Historique:
received:
07
09
2020
accepted:
22
02
2021
pubmed:
5
3
2021
medline:
11
6
2021
entrez:
4
3
2021
Statut:
ppublish
Résumé
The phytohormone gibberellin (GA) is critical for anther development. RGA, a member of the DELLA family of proteins that are central GA signalling repressors, is a key regulator of male fertility in plants. However, the downstream genes in GA-RGA-mediated anther development remain to be characterised. We identified RGA Target 1 (RGAT1), a novel Arabidopsis gene, that functions as an important RGA-regulated target in pollen development. RGAT1 is predominantly expressed in the tapetum and microspores during anther stages 8-11, and can be directly activated by RGA and suppressed by GA in inflorescence apices. Both loss of function and gain of function of RGAT1 led to abnormal tapetum development, resulting in abortive pollen and short siliques. In RGAT1-knockdown and overexpression lines, pollen abortion occurred at stage 10. Loss of RGAT1 function induced the premature degeneration of tapetal cells with defective ER-derived tapetosomes, while RGAT1 overexpression delayed tapetum degeneration. TUNEL assay confirmed that RGAT1 participates in timely tapetal programmed cell death. Moreover, reducing RGAT1 expression partially rescued the tapetal developmental defects in GA-deficient ga1-3 mutant. Our findings revealed that RGAT1 is a direct target of RGA and plays an essential role in GA-mediated tapetum and pollen development.
Substances chimiques
Arabidopsis Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
137-151Informations de copyright
© 2021 The Authors New Phytologist © 2021 New Phytologist Foundation.
Références
Achard P, Herr A, Baulcombe DC, Harberd NP. 2004. Modulation of floral development by a gibberellin-regulated microRNA. Development 131: 3357-3365.
Aya K, Hiwatashi Y, Kojima M, Sakakibara H, Ueguchi-Tanaka M, Hasebe M, Matsuoka M. 2011. The Gibberellin perception system evolved to regulate a pre-existing GAMYB-mediated system during land plant evolution. Nature Communications 2: 544.
Aya K, Ueguchi-Tanaka M, Kondo M, Hamada K, Yano K, Nishimura M, Matsuoka M. 2009. Gibberellin modulates anther development in rice via the transcriptional regulation of GAMYB. The Plant Cell 21: 1453-1472.
Bao SJ, Hua CM, Shen LS, Yu H. 2020. New insights into gibberellin signaling in regulating flowering in Arabidopsis. Journal of Integrative Plant Biology 62: 118-131.
Cao DN, Cheng H, Wu W, Soo HM, Peng JR. 2006. Gibberellin mobilizes distinct DELLA-dependent transcriptomes to regulate seed germination and floral development in Arabidopsis. Plant Physiology 142: 509-525.
Cheng H, Qin LJ, Lee S, Fu XD, Richards DE, Cao DN, Luo D, Harberd NP, Peng JR. 2004. Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function. Development 131: 1055-1064.
Daneva A, Gao Z, Van Durme M, Nowack MK. 2016. Functions and regulation of programmed cell death in plant development. Annual Review of Cell and Developmental Biology 32: 441-468.
Daviere JM, Achard P. 2013. Gibberellin signaling in plants. Development 140: 1147-1151.
De Lucas M, Daviere JM, Rodríguez-Falcón M, Pontin M, Iglesias-Pedraz JM, Lorrain S, Fankhauser C, Blázquez MA, Titarenko E, Prat S. 2008. A molecular framework for light and gibberellin control of cell elongation. Nature 451: 480-484.
Dill A, Jung HS, Sun TP. 2001. The DELLA motif is essential for gibberellin-induced degradation of RGA. Proceedings of the National Academy of Sciences, USA 98: 14162-14167.
Feng S, Martinez C, Gusmaroli G, Wang Y, Zhou J, Wang F, Chen L, Yu L, Iglesias-Pedraz JM, Kircher S. 2008. Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451: 475.
Goldberg RB, Beals TP, Sanders PM. 1993. Anther development: basic principles and practical applications. The Plant Cell 5: 1217-1229.
Gómez JF, Talle B, Wilson ZA. 2015. Anther and pollen development: a conserved developmental pathway. Journal of Integrative Plant Biology 57: 876-891.
Gómez MD, Fuster-Almunia C, Ocaña-Cuesta J, Alonso JM, Pérez-Amador MA. 2019. RGL2 controls flower development, ovule number and fertility in Arabidopsis. Plant Science 281: 82-92.
Gubler F, Kalla R, Roberts JK, Jacobsen JV. 1995. Gibberellin-regulated expression of a myb gene in barley aleurone cells: evidence for Myb transactivation of a high-pI alpha-amylase gene promoter. The Plant Cell 7: 1879-1891.
Himmelbach A, Hoffmann T, Leube M, Höhener B, Grill E. 2002. Homeodomain protein ATHB6 is a target of the protein phosphatase ABI1 and regulates hormone responses in Arabidopsis. EMBO Journal 21: 3029-3038.
Hou XL, Hu WW, Shen LS, Lee LYC, Tao Z, Han JH, Yu H. 2008. Global identification of DELLA target genes during Arabidopsis flower development. Plant Physiology 147: 1126-1142.
Hsieh K, Huang AHC. 2005. Lipid-rich tapetosomes in brassica tapetum are composed of oleosin-coated oil droplets and vesicles, both assembled in and then detached from the endoplasmic reticulum. The Plant Journal 43: 889-899.
Hu YL, Zhou LM, Huang MK, He XM, Yang YH, Liu Xu, Li YG, Hou XL. 2018. Gibberellins play an essential role in late embryogenesis of Arabidopsis. Nature Plants 4: 289-298.
Jacobsen SE, Olszewski NE. 1991. Characterization of the arrest in anther development associated with gibberellin deficiency of the gib-1 mutant of tomato. Plant Physiology 97: 409-414.
Lee S, Cheng H, King KE, Wang W, He YW, Hussain A, Lo J, Harberd NP, Peng JR. 2002. Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Genes & Development 16: 646-658.
Li N, Zhang DS, Liu HS, Yin CS, Li XX, Liang WQ, Yuan Z, Xu B, Chu HW, Wang J et al. 2006. The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. The Plant Cell 18: 2999-3014.
Liu B, De Storme N, Geelen D. 2017. Gibberellin induces diploid pollen formation by interfering with meiotic cytokinesis. Plant Physiology 173: 338-353.
Liu X, Hu PW, Huang MK, Tang Y, Li YG, Li L, Hou XL. 2016. The NF-YC-RGL2 module integrates GA and ABA signalling to regulate seed germination in Arabidopsis. Nature Communications 7: 12768.
Millar AA, Gubler F. 2005. The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. The Plant Cell 17: 705-721.
Murase K, Hirano Y, Sun TP, Hakoshima T. 2008. Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456: 459.
Parish RW, Li SF. 2010. Death of a tapetum: a programme of developmental altruism. Plant Science 178: 73-89.
Peng JR, Carol P, Richards DE, King KE, Cowling RJ, Murphy GP, Harberd NP. 1997. The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes & Development 11: 3194-3205.
Phan HA, Iacuone S, Li SF, Parish RW. 2011. The MYB80 transcription factor is required for pollen development and the regulation of tapetal programmed cell death in Arabidopsis thaliana. The Plant Cell 23: 2209-2224.
Plackett ARG, Ferguson AC, Powers SJ, Wanchoo-Kohli A, Phillips AL, Wilson ZA, Hedden P, Thomas SG. 2014. DELLA activity is required for successful pollen development in the Columbia ecotype of Arabidopsis. New Phytologist 201: 825-836.
Plackett ARG, Thomas SG, Wilson ZA, Hedden P. 2011. Gibberellin control of stamen development: a fertile field. Trends in Plant Science 16: 568-578.
Quilichini TD, Douglas CJ, Samuels AL. 2014. New views of tapetum ultrastructure and pollen exine development in Arabidopsis thaliana. Annals of Botany 114: 1189-1201.
Regan SM, Moffatt BA. 1990. Cytochemical analysis of pollen development in wild-type Arabidopsis and a male-sterile mutant. The Plant Cell 2: 877-889.
Roeder AH, Yanofsky MF. 2006. Fruit development in Arabidopsis. The Arabidopsis book 4: e0075.
Sanders PM, Bui AQ, Weterings K, McIntire KN, Goldberg RB. 1999. Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sexual Plant Reproduction 11: 297-322.
Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D. 2006. Highly specific gene silencing by artificial microRNAs in Arabidopsis. The Plant Cell 18: 1121-1133.
Silverstone AL, Mak PYA, Martinez EC, Sun TP. 1997. The new RGA locus encodes a negative regulator of gibberellin response in Arabidopsis thaliana. Genetics 146: 1087-1099.
Song SS, Qi TC, Huang H, Xie DX. 2013. Regulation of stamen development by coordinated actions of jasmonate, auxin, and gibberellin in Arabidopsis. Molecular Plant 6: 1065-1073.
Ueguchi-Tanaka M, Ashikari M, Nakajima M, Itoh H, Katoh E, Kobayashi M, Chow TY, Yue-ie CH, Kitano H, Yamaguchi I. 2005. GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437: 693.
Uzair M, Xu DW, Schreiber L, Shi JX, Liang WQ, Kung KH, Chen MJ, Luo ZJ, Yu J, Zhang DB. 2019. PERSISTENT TAPETAL CELL 2 is required for normal tapetal programmed cell death and pollen wall patterning. Plant Physiology 182: 962-967.
Vizcay-Barrena G, Wilson ZA. 2006. Altered tapetal PCD and pollen wall development in the Arabidopsis ms1 mutant. Journal of Experimental Botany 57: 2709-2717.
Wang B, Fang R, Chen F, Han J, Zhu Q. 2020. A novel ccch-type zinc-finger protein saw1 activates osga20ox3 to regulate gibberellin homeostasis and anther development in rice. Journal of Integrative Plant Biology 62: 1594-1606.
Wang ZP, Wang SB, Li DW, Zhang Q, Li L, Zhong CH, Liu YF, Huang HW. 2018. Optimized paired-sgrna/cas9 cloning and expression cassette triggers high-efficiency multiplex genome editing in kiwifruit. Plant Biotechnology Journal 16: 1424-1433.
Wen CK, Chang C. 2002. Arabidopsis RGL1 encodes a negative regulator of gibberellin responses. The Plant Cell 14: 87-100.
Xie HT, Wan ZY, Li S, Zhang Y. 2014. Spatiotemporal production of reactive oxygen species by NADPH oxidase is critical for tapetal programmed cell death and pollen development in Arabidopsis. The Plant Cell 26: 2007-2023.
Yoshida H, Hirano K, Sato T, Mitsuda N, Nomoto M, Maeo K, Koketsu E, Mitani R, Kawamura M, Ishiguro S. 2014. DELLA protein functions as a transcriptional activator through the DNA binding of the indeterminate domain family proteins. Proceedings of the National Academy of Sciences, USA 111: 7861-7866.
Zentella R, Zhang ZL, Park M, Thomas SG, Endo A, Murase K, Fleet CM, Jikumaru Y, Nambara E, Kamiya Y et al. 2007. Global analysis of della direct targets in early gibberellin signaling in Arabidopsis. The Plant Cell 19: 3037-3057.
Zheng ZF, Xia Q, Dauk M, Shen WY, Selvaraj G, Zou JT. 2003. Arabidopsis AtGPAT1, a member of the membrane-bound glycerol-3-phosphate acyltransferase gene family, is essential for tapetum differentiation and male fertility. The Plant Cell 15: 1872-1887.