Abstract
Main conclusion
The SNF5-type protein BUSHY plays a role in the regulation of seed germination via the gibberellin pathway dependent on HUB1 in Arabidopsis thaliana.
Abstract
SWITCH/SUCROSE NONFERMENTING (SWI/SNF) complexes play diverse roles in plant development. Some components have roles in embryo development and seed maturation, however, whether the SNF5-type protein BUSHY (BSH), one of the components, plays a role in Arabidopsis seed related traits is presently unclear. In our study, we show that a loss-of-function mutation in BSH causes increased seed germination in Arabidopsis. BSH transcription was induced by the gibberellin (GA) inhibitor paclobutrazol (PAC) in the seed, and BSH regulates the expression of GA pathway genes, such as Gibberellin 3-Oxidase 1 (GA3OX1), Gibberellic Acid-Stimulated Arabidopsis 4 (GASA4), and GASA6 during seed germination. A genetic analysis showed that seed germination was distinctly improved in the bshga3ox1ga3ox2 triple mutant, indicating that BSH acts partially downstream of GA3OX1 and GA3OX2. Moreover, the regulation of seed germination by BSH in response to PAC is dependent on HUB1. These results provide new insights and clues to understand the mechanisms of phytohormones in the regulation of seed germination.
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Abbreviations
- BSH:
-
SNF5-type protein BUSHY
- GA:
-
Gibberellin
- HUB1:
-
HISTONE MONOUBIQUITINATION1
- PAC:
-
Paclobutrazol
- SWI/SNF:
-
SWITCH/SUCROSE NONFERMENTING complex
References
Alonso JM, Stepanova AN, Leisse TJ et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301(5633):653–657
Amedeo P, Habu Y, Afsar K, Mittelsten Scheid O, Paszkowski J (2000) Disruption of the plant gene MOM releases transcriptional silencing of methylated genes. Nature 405(6783):203–206
Aubert D, Chevillard M, Dorne AM, Arlaud G, Herzog M (1998) Expression patterns of GASA genes in Arabidopsis thaliana: the GASA4 gene is up-regulated by gibberellins in meristematic regions. Plant Mol Biol 36(6):871–883
Bassel GW, Lan H, Glaab E, Gibbs DJ, Gerjets T, Krasnogor N, Bonner AJ, Holdsworth MJ, Provart NJ (2011) Genome-wide network model capturing seed germination reveals coordinated regulation of plant cellular phase transitions. Proc Natl Acad Sci USA 108(23):9709–9714
Brzeski JPW, Olczak K, Jerzmanowski A (1999) Identification and analysis of the Arabidopsis thaliana BSH gene, a member of the SNF5 gene family. Nucleic Acids Res 27(11):6
Carrera-Castaño G, Calleja-Cabrera J, Pernas M, Gómez L, Oñate-Sánchez L (2020) An updated overview on the regulation of seed germination. Plants 9:703
Cao Y, Dai Y, Cui S, Ma L (2008) Histone H2B monoubiquitination in the chromatin of FLOWERING LOCUS C regulates flowering time in Arabidopsis. Plant Cell 20(10):2586–2602
Charron JB, He H, Elling AA, Deng XW (2009) Dynamic landscapes of four histone modifications during deetiolation in Arabidopsis. Plant Cell 21(12):3732–3748
Chen F, Nonogaki H, Bradford KJ (2002) A gibberellin-regulated xyloglucan endotransglycosylase gene is expressed in the endosperm cap during tomato seed germination. J Exp Bot 53(367):215–223
Chen H, Zhang J, Neff MM, Hong SW, Zhang H, Deng XW, Xiong L (2008) Integration of light and abscisic acid signaling during seed germination and early seedling development. Proc Natl Acad Sci USA 105(11):4495–4500
Cho JN, Ryu JY, Jeong YM, Park J, Song JJ, Amasino RM, Noh B, Noh YS (2012) Control of seed germination by light-induced histone arginine demethylation activity. Dev Cell 22(4):736–748
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743
Davies PJ (ed) (1995) Plant hormones: physiology, biochemistry and molecular biology, 2nd edn. Kluwer Academic Publishers
Finkelstein R, Reeves W, Ariizumi T, Steber C (2008) Molecular aspects of seed dormancy. Annu Rev Plant Biol 59:387–415
Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12(4):599–609
Finkelstein RR, Somerville CR (1990) Three classes of abscisic acid (ABA)-insensitive mutations of Arabidopsis define genes that control overlapping subsets of ABA responses. Plant Physiol 94(3):1172–1179
Fleury D, Himanen K, Cnops G, Nelissen H, Boccardi TM, Maere S, Beemster GTS, Neyt P, Anami S, Robles P, Micol JL, Inze D, Van Lijsebettens M (2007) The Arabidopsis thaliana homolog of yeast BRE1 has a function in cell cycle regulation during early leaf and root growth. Plant Cell 19(2):417–432
Ge W, Steber CM (2018) Positive and negative regulation of seed germination by the Arabidopsis GA hormone receptors, GID1a, b, and c. Plant Direct 2(9):e00083
Han SK, Sang Y, Rodrigues A, Biol F, Wu MF, Rodriguez PL, Wagner D (2012) The SWI2/SNF2 chromatin remodeling ATPase BRAHMA represses abscisic acid responses in the absence of the stress stimulus in Arabidopsis. Plant Cell 24(12):4892–4906
Hauvermale AL, Steber CM (2020) GA signaling is essential for the embryo-to-seedling transition during Arabidopsis seed germination, a ghost story. Plant Signal Behav 15(1):1705028
Hicke L (2001) Protein regulation by monoubiquitin. Nat Rev Mol Cell Biol 2(3):195–201
Hu M, Pei BL, Zhang LF, Li YZ (2014) Histone H2B monoubiquitination is involved in regulating the dynamics of microtubules during the defense response to Verticillium dahliae toxins in Arabidopsis. Plant Physiol 164(4):1857–1865
Jackson JP, Lindroth AM, Cao X, Jacobsen SE (2002) Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416(6880):556–560
Jacobsen SE, Olszewski NE (1993) Mutations at the SPINDLY locus of Arabidopsis alter gibberellin signal transduction. Plant Cell 5(8):887–896
Koornneef M, Bentsink L, Hilhorst H (2002) Seed dormancy and germination. Curr Opin Plant Biol 5(1):33–36
Koornneef M, Jorna ML, Brinkhorst-van der Swan DL, Karssen CM (1982) The isolation of abscisic acid (ABA) deficient mutants by selection of induced revertants in non-germinating gibberellin sensitive lines of Arabidopsis thaliana (L.) Heynh. Theor Appl Genet 61(4):385–393
Koornneef M, Van der Veen JH (1980) Induction and analysis of gibberrellin-sensitive mutants in Arabidopsis thaliana (L.). Theor Appl Genet 58:7
Liu Y, Koornneef M, Soppe WJ (2007) The absence of histone H2B monoubiquitination in the Arabidopsis hub1 (rdo4) mutant reveals a role for chromatin remodeling in seed dormancy. Plant Cell 19(2):433–444
Mitchum MG, Yamaguchi S, Hanada A, Kuwahara A, Yoshioka Y, Kato T, Tabata S, Kamiya Y, Sun TP (2006) Distinct and overlapping roles of two gibberellin 3-oxidases in Arabidopsis development. Plant J 45(5):804–818
Nambara E, Akazawa T, McCourt P (1991) Effects of the gibberellin biosynthetic inhibitor uniconazol on mutants of Arabidopsis. Plant Physiol 97(2):736–738
Noh YS, Amasino RM (2003) PIE1, an ISWI family gene, is required for FLC activation and floral repression in Arabidopsis. Plant Cell 15(7):1671–1682
Nonogaki H (2008) Repression of transcription factors by microRNA during seed germination and postgerminaiton: another level of molecular repression in seeds. Plant Signal Behav 3(1):65–67
Olszewski N, Sun TP, Gubler F (2002) Gibberellin signaling: biosynthesis, catabolism, and response pathways. Plant Cell 14(Suppl):61–80
Peeters AJ, Blankestijn-De Vries H, Hanhart CJ, Leon-Kloosterziel KM, Zeevaart JA, Koornneef M (2002) Characterization of mutants with reduced seed dormancy at two novel rdo loci and a further characterization of rdo1 and rdo2 in Arabidopsis. Physiol Plant 115(4):604–612
Penfield S, Gilday AD, Halliday KJ, Graham IA (2006) DELLA-mediated cotyledon expansion breaks coat-imposed seed dormancy. Curr Biol 16(23):2366–2370
Phelan ML, Sif S, Narlikar GJ, Kingston RE (1999) Reconstitution of a core chromatin remodeling complex from SWI/SNF subunits. Mol Cell 3(2):247–253
Qu J, Kang SG, Hah C, Jang JC (2016) Molecular and cellular characterization of GA-stimulated transcripts GASA4 and GASA6 in Arabidopsis thaliana. Plant Sci 246:1–10
Rajjou L, Duval M, Gallardo K, Catusse J, Bally J, Job C, Job D (2012) Seed germination and vigor. Annu Rev Plant Biol 63:507–533
Ren CW, Kermode AR (2000) An increase in pectin methyl esterase activity accompanies dormancy breakage and germination of yellow cedar seeds. Plant Physiol 124(1):231–242
Sanchez-Montesino R, Bouza-Morcillo L, Marquez J, Ghita M, Duran-Nebreda S, Gomez L, Holdsworth MJ, Bassel G, Onate-Sanchez L (2019) A regulatory module controlling GA-mediated endosperm cell expansion is critical for seed germination in Arabidopsis. Mol Plant 12(1):71–85
Sarnowska EA, Rolicka AT, Bucior E et al (2013) DELLA-interacting SWI3C core subunit of switch/sucrose nonfermenting chromatin remodeling complex modulates gibberellin responses and hormonal cross talk in Arabidopsis. Plant Physiol 163(1):305–317
Sarnowski TJ, Swiezewski S, Pawlikowska K, Kaczanowski S, Jerzmanowski A (2002) AtSWI3B, an Arabidopsis homolog of SWI3, a core subunit of yeast Swi/Snf chromatin remodeling complex, interacts with FCA, a regulator of flowering time. Nucleic Acids Res 30(15):3412–3421
Steber CM, Cooney SE, McCourt P (1998) Isolation of the GA-response mutant sly1 as a suppressor of ABI1-1 in Arabidopsis thaliana. Genetics 149(2):509–521
Sudarsanam P, Winston F (2000) The Swi/Snf family nucleosome-remodeling complexes and transcriptional control. Trends Genet 16(8):345–351
Tang X, Hou A, Babu M, Nguyen V, Hurtado L, Lu Q, Reyes JC, Wang A, Keller WA, Harada JJ, Tsang EW, Cui Y (2008) The Arabidopsis BRAHMA chromatin-remodeling ATPase is involved in repression of seed maturation genes in leaves. Plant Physiol 147(3):1143–1157
van Zanten M, Zoll C, Wang Z, Philipp C, Carles A, Li Y, Kornet NG, Liu Y, Soppe WJ (2014) HISTONE DEACETYLASE 9 represses seedling traits in Arabidopsis thaliana dry seeds. Plant J 80(3):475–488
Wang Z, Chen F, Li X, Cao H, Ding M, Zhang C, Zuo J, Xu C, Xu J, Deng X, Xiang Y, Soppe W, Liu Y (2016) Arabidopsis seed germination speed is controlled by SNL histone deacetylase-binding factor-mediated regulation of AUX1. Nat Commun 7:13412
Zhao J, Chen QH, Zhou S, Sun YH, Li XY, Li YZ (2020) H2Bub1 regulates RbohD-dependent hydrogen peroxide signal pathway in the defense responses to Verticillium dahliae toxins. Plant Physiol 182(1):640–657
Zheng J, Chen F, Wang Z, Cao H, Li X, Deng X, Soppe WJ, Li Y, Liu Y (2012) A novel role for histone methyltransferase KYP/SUVH4 in the control of Arabidopsis primary seed dormancy. New Phytol 193(3):605–616
Zhong C, Xu H, Ye S, Wang S, Li L, Zhang S, Wang X (2015) Gibberellic acid-sstimulated Arabidopsis6 serves as an integrator of gibberellin, abscisic acid, and glucose signaling during seed germination in Arabidopsis. Plant Physiol 169(3):2288–2303
Zhou S, Chen QH, Sun YH, Li YZ (2017) Histone H2B monoubiquitination regulates salt stress-induced microtubule depolymerization in Arabidopsis. Plant Cell Environ 40(8):1512–1530
Acknowledgements
We thank Dr. Wim J.J. Soppe very much for his great help on the improvement of the manuscript. This project was supported by the National Natural Science Foundation of China (grant numbers 31171164, 31870305, and 31571257).
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Wang, Z., Cao, H., Zhang, C. et al. The SNF5-type protein BUSHY regulates seed germination via the gibberellin pathway and is dependent on HUB1 in Arabidopsis. Planta 255, 34 (2022). https://doi.org/10.1007/s00425-021-03767-1
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DOI: https://doi.org/10.1007/s00425-021-03767-1