Abstract
Key message
We reported that DGS1 plays a positive role in regulating grain size in rice and was regulated by OsBZR1.
Abstract
Grain size is an important agronomic trait that contributes to grain yield. However, the underlying molecular mechanisms that determine final grain size are still largely unknown. We isolated a rice mutant showing reduced grain size in a 60Co-irradiated variety Nanjing 35 population. We named the mutant decreased grain size1 (dgs1). Map-based cloning and subsequent transgenic CRISPR and complementation assays indicated that a mutation had occurred in LOC_Os03g49900 and that the DGS1 allele regulated grain size. DGS1 encodes a protein with a 7-transmembrane domain and C3HC4 type RING domain. It was widely expressed, especially in young tissues. DGS1 is a membrane-located protein. OsBZR1 (BRASSINAZOLE-RESISTANT1), a core transcription activator of BR signaling, also plays a positive role in grain size. We provided preliminary evidence that OsBZR1 can bind to the DGS1 promoter to activate expression of DGS1.
Similar content being viewed by others
References
Bai MY, Zhang LY, Gampala SS, Zhu SW, Song WY, Chong K, Wang ZY (2007) Functions of OsBZR1 and 14–3-3 proteins in brassinosteroid signaling in rice. Proc Natl Acad Sci U S A 104:13839–13844. https://doi.org/10.1073/pnas.0706386104
Chen SB, Tao LZ, Zeng LR, Vega-Sanchez ME, Umemura K, Wang GL (2006) A highly efficient transient protoplast system for analyzing defence gene expression and protein-protein interactions in rice. Mol Plant Pathol 7:417–427. https://doi.org/10.1111/j.1364-3703.2006.00346.x
Cheung MY et al (2007) Expression of a RING-HC protein from rice improves resistance to Pseudomonas syringae pv. tomato DC3000 in transgenic Arabidopsis thaliana. J Exp Bot 58:4147–4159. https://doi.org/10.1093/jxb/erm272
Disch S, Anastasiou E, Sharma VK, Laux T, Fletcher JC, Lenhard M (2006) The E3 ubiquitin ligase BIG BROTHER controls Arabidopsis organ size in a dosage-dependent manner. Curr Biol 16:272–279. https://doi.org/10.1016/j.cub.2005.12.026
Dong H et al (2017) Ubiquitylation activates a peptidase that promotes cleavage and destabilization of its activating E3 ligases and diverse growth regulatory proteins to limit cell proliferation in Arabidopsis. Gene Dev 31:197–208. https://doi.org/10.1101/gad.292235.116
Duan EC et al (2019) OsSHI1 regulates plant architecture through modulating the transcriptional activity of IPA1 in rice. Plant Cell 31:1026–1042. https://doi.org/10.1105/tpc.19.00023
Fan C et al (2006) GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein. Theor Appl Genet 112:1164–1171. https://doi.org/10.1007/s00122-006-0218-1
Freemont PS, Hanson IM, Trowsdale J (1991) A novel cysteine-rich sequence motif. Cell 64:483–484. https://doi.org/10.1016/0092-8674(91)90229-r
Gao XY et al (2019) Rice qGL3/OsPPKL1 functions with the GSK3/SHAGGY-like kinase OsGSK3 to modulate brassinosteroid signaling. Plant Cell 31:1077–1093. https://doi.org/10.1105/tpc.18.00836
Hardtke CS, Okamoto H, Stoop-Myer C, Deng XW (2002) Biochemical evidence for ubiquitin ligase activity of the Arabidopsis COP1 interacting protein 8 (CIP8). Plant J 30:385–394. https://doi.org/10.1046/j.1365-313x.2002.01298.x
He JX, Gendron JM, Sun Y, Gampala SSL, Gendron N, Sun CQ, Wang ZY (2005) BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science 307:1634–1638. https://doi.org/10.1126/science.1107580
Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6:271–282. https://doi.org/10.1046/j.1365-313x.1994.6020271.x
Hu Z et al (2012) A Kelch motif-containing serine/threonine protein phosphatase determines the large grain QTL trait in rice. J Integr Plant Biol 54:979–990. https://doi.org/10.1111/jipb.12008
Hu ZJ et al (2018) A novel QTL qTGW3 encodes the GSK3/SHAGGY-like kinase OsGSK5/OsSK41 that interacts with OsARF4 to negatively regulate grain size and weight in rice. Mol Plant 11:736–749. https://doi.org/10.1016/j.molp.2018.03.005
Ishimaru K et al (2013) Loss of function of the IAA-glucose hydrolase gene TGW6 enhances rice grain weight and increases yield. Nat Genet 45:707–711. https://doi.org/10.1038/ng.2612
Jiang WB, Huang HY, Hu YW, Zhu SW, Wang ZY, Lin WH (2013) Brassinosteroid regulates seed size and shape in Arabidopsis. Plant Physiol 162:1965–1977. https://doi.org/10.1104/pp.113.217703
Jofuku KD, Omidyar PK, Gee Z, Okamuro JK (2005) Control of seed mass and seed yield by the floral homeotic gene APETALA2. Proc Natl Acad Sci U S A 102:3117–3122. https://doi.org/10.1073/pnas.0409893102
Kawasaki T, Nam J, Boyes DC, Holt BF 3rd, Hubert DA, Wiig A, Dangl JL (2005) A duplicated pair of Arabidopsis RING-finger E3 ligases contribute to the RPM1- and RPS2-mediated hypersensitive response. Plant J 44:258–270. https://doi.org/10.1111/j.1365-313X.2005.02525.x
Ko JH, Yang SH, Han KH (2006) Upregulation of an Arabidopsis RING-H2 gene, XERICO, confers drought tolerance through increased abscisic acid biosynthesis. Plant J 47:343–355. https://doi.org/10.1111/j.1365-313X.2006.02782.x
Koiwai H, Tagiri A, Katoh S, Katoh E, Ichikawa H, Minami E, Nishizawa Y (2007) RING-H2 type ubiquitin ligase EL5 is involved in root development through the maintenance of cell viability in rice. Plant J 51:92–104. https://doi.org/10.1111/j.1365-313X.2007.03120.x
Lei Y, Lu L, Liu HY, Li S, Xing F, Chen LL (2014) CRISPR-P: a web tool for synthetic single-guide RNA design of CRISPR-system in plants. Mol Plant 7:1494–1496. https://doi.org/10.1093/mp/ssu044
Li QF, Lu J, Yu JW, Zhang CQ, He JX, Liu QQ (2018) The brassinosteroid-regulated transcription factors BZR1/BES1 function as a coordinator in multisignal-regulated plant growth. Bba-Gene Regul Mech 1861:561–571. https://doi.org/10.1016/j.bbagrm.2018.04.003
Li Y et al (2011) Natural variation in GS5 plays an important role in regulating grain size and yield in rice. Nat Genet 43:1266–1269. https://doi.org/10.1038/ng.977
Li Y, Zheng L, Corke F, Smith C, Bevan MW (2008) Control of final seed and organ size by the DA1 gene family in Arabidopsis thaliana. Genes Dev 22:1331–1336. https://doi.org/10.1101/gad.463608
Liu JF et al (2017) GW5 acts in the brassinosteroid signalling pathway to regulate grain width and weight in rice. Nat Plants 3:17043. https://doi.org/10.1038/nplants.2017.43
Liu K, Wang L, Xu Y, Chen N, Ma Q, Li F, Chong K (2007) Overexpression of OsCOIN, a putative cold inducible zinc finger protein, increased tolerance to chilling, salt and drought, and enhanced proline level in rice. Planta 226:1007–1016. https://doi.org/10.1007/s00425-007-0548-5
Mao H et al (2010) Linking differential domain functions of the GS3 protein to natural variation of grain size in rice. Proc Natl Acad Sci U S A 107:19579–19584. https://doi.org/10.1073/pnas.1014419107
McNellis TW, Torii KU, Deng XW (1996) Expression of an N-terminal fragment of COP1 confers a dominant-negative effect on light-regulated seedling development in Arabidopsis. Plant Cell 8:1491–1503. https://doi.org/10.1105/tpc.8.9.1491
McNellis TW, von Arnim AG, Deng XW (1994) Overexpression of Arabidopsis COP1 results in partial suppression of light-mediated development: evidence for a light-inactivable repressor of photomorphogenesis. Plant Cell 6:1391–1400. https://doi.org/10.1105/tpc.6.10.1391
Meng XB, Zhao WS, Lin RM, Wang M, Peng YL (2006) Molecular cloning and characterization of a rice blast-inducible RING-H2 type Zinc finger gene. DNA Seq 17:41–48. https://doi.org/10.1080/10425170500476509
Ohto MA, Fischer RL, Goldberg RB, Nakamura K, Harada JJ (2005) Control of seed mass by APETALA2. Proc Natl Acad Sci U S A 102:3123–3128. https://doi.org/10.1073/pnas.0409858102
Qi P et al (2012) The novel quantitative trait locus GL3.1 controls rice grain size and yield by regulating Cyclin-T1;3. Cell Res 22:1666–1680. https://doi.org/10.1038/cr.2012.151
Schruff MC, Spielman M, Tiwari S, Adams S, Fenby N, Scott RJ (2006) The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs. Development 133:251–261. https://doi.org/10.1242/dev.02194
Schumann U, Wanner G, Veenhuis M, Schmid M, Gietl C (2003) AthPEX10, a nuclear gene essential for peroxisome and storage organelle formation during Arabidopsis embryogenesis. Proc Natl Acad Sci U S A 100:9626–9631. https://doi.org/10.1073/pnas.1633697100
Si L et al (2016) OsSPL13 controls grain size in cultivated rice. Nat Genet 48:447–456. https://doi.org/10.1038/ng.3518
Song XJ, Huang W, Shi M, Zhu MZ, Lin HX (2007) A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat Genet 39:623–630. https://doi.org/10.1038/ng2014
Stone SL, Hauksdottir H, Troy A, Herschleb J, Kraft E, Callis J (2005) Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis. Plant Physiol 137:13–30. https://doi.org/10.1104/pp.104.052423
Takeda T et al (2003) The OsTB1 gene negatively regulates lateral branching in rice. Plant J 33:513–520. https://doi.org/10.1046/j.1365-313x.2003.01648.x
Tong HN et al (2012) Dwarf and low-tillering acts as a direct downstream target of a GSK3/SHAGGY-like kinase to mediate brassinosteroid responses in rice. Plant Cell 24:2562–2577. https://doi.org/10.1105/tpc.112.097394
Tsuge T et al (2001) Phytochrome-mediated control of COP1 gene expression in rice plants. Mol Genet Genomics 265:43–50. https://doi.org/10.1007/s004380000396
Waghmare S, Lileikyte E, Karnik R, Goodman JK, Blatt MR, Jones AME (2018) SNAREs SYP121 and SYP122 mediate the secretion of distinct cargo subsets. Plant Physiol 178:1679–1688. https://doi.org/10.1104/pp.18.00832
Wang S et al (2012) Control of grain size, shape and quality by OsSPL16 in rice. Nat Genet 44:950–954. https://doi.org/10.1038/ng.2327
Weng J et al (2008) Isolation and initial characterization of GW5, a major QTL associated with rice grain width and weight. Cell Res 18:1199–1209. https://doi.org/10.1038/cr.2008.307
Xia T et al (2013) The ubiquitin receptor DA1 interacts with the E3 ubiquitin ligase DA2 to regulate seed and organ size in Arabidopsis. Plant Cell 25:3347–3359. https://doi.org/10.1105/tpc.113.115063
Zhang C et al (2012a) Dynamics of brassinosteroid response modulated by negative regulator LIC in rice. PLoS Genet 8:651–664. https://doi.org/10.1371/journal.pgen.1002686
Zhang X et al (2012b) Rare allele of OsPPKL1 associated with grain length causes extra-large grain and a significant yield increase in rice. Proc Natl Acad Sci U S A 109:21534–21539. https://doi.org/10.1073/pnas.1219776110
Zhang Y et al (2007) SDIR1 is a RING finger E3 ligase that positively regulates stress-responsive abscisic acid signaling in Arabidopsis. Plant Cell 19:1912–1929. https://doi.org/10.1105/tpc.106.048488
Zhu XL et al (2015) Brassinosteroids promote development of rice pollen grains and seeds by triggering expression of Carbon Starved Anther, a MYB domain protein. Plant J 82:570–581. https://doi.org/10.1111/tpj.12820
Acknowledgements
We acknowledge support from the National Key Research and Development Program of China (2017YFD0100404), Jiangsu Science and Technology Development Program (BE2018388), and Key project for Jiangsu Agricultural New Variety Innovation (PZCZ201701). Additional support was provided by the Key Laboratory of Biology, Genetics and Breeding of Japonica Rice in the Mid-lower Yangtze River, and Jiangsu Collaborative Innovation Center for Modern Crop Production.
Author information
Authors and Affiliations
Contributions
JMW and LJ supervised this research; XJZ performed the experiments and wrote the manuscript; LJ revised the paper; SZZ, YPC, CLM, YSH, XL, JLJ participated in the experiments; JFY, QXH, CYY, MYC, THN, HD were involved in the data discussions; WHS, PW, SJL were involved in the generation of the transgenic plant. all authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zhu, X., Zhang, S., Chen, Y. et al. Decreased grain size1, a C3HC4-type RING protein, influences grain size in rice (Oryza sativa L.). Plant Mol Biol 105, 405–417 (2021). https://doi.org/10.1007/s11103-020-01096-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-020-01096-7