Abstract
Main conclusion
OsWRKY24 functions redundantly with OsWRKY53, while OsWRKY70 functions differently from OsWRKY53 in regulating grain size.
Abstract
Grain size is a key agronomic trait that affects grain yield and quality in rice (Oryza sativa L.). The transcription factor OsWRKY53 positively regulates grain size through brassinosteroid (BR) signaling and Mitogen-Activated Protein Kinase (MAPK) cascades. However, whether the OsWRKY53 homologs OsWRKY24 and OsWRKY70 also contribute to grain size which remains unknown. Here, we report that grain size in OsWRKY24 overexpression lines and oswrky24 mutants is similar to that of the wild type. However, the oswrky24 oswrky53 double mutant produced smaller grains than the oswrky53 single mutant, indicating functional redundancy between OsWRKY24 and OsWRKY53. In addition, OsWRKY70 overexpression lines displayed an enlarged leaf angle, reduced plant height, longer grains, and higher BR sensitivity, phenotypes similar to those of OsWRKY53 overexpression lines. Importantly, a systematic characterization of seed length in the oswrky70 single, the oswrky53 oswrky70 double and the oswrky24 oswrky53 oswrky70 triple mutant indicated that loss of OsWRKY70 also leads to increased seed length, suggesting that OsWRKY70 might play a role distinct from that of OsWRKY53 in regulating grain size. Taken together, these findings suggest that OsWRKY24 and OsWRKY70 regulate rice grain size redundantly and independently from OsWRKY53.
Data availability
All data generated or analyzed during this study are included in this published article (and its supplementary information files).
References
Che RH, Tong HN, Shi BH, Liu YQ, Fang SR, Liu DP, Xiao YH, Hu B, Liu LC, Wang HR, Zhao MF, Chu CC (2016) Control of grain size and rice yield by GL2-mediated brassinosteroid responses. Nat Plants 2:15195. https://doi.org/10.1038/nplants.2015.195
Chujo T, Takai R, Akimoto-Tomiyama C, Ando S, Minami E, Nagamura Y, Kaku H, Shibuya N, Yasuda M, Nakashita H, Umemura K, Okada A, Okada K, Nojiri H, Yamane H (2007) Involvement of the elicitor-induced gene OsWRKY53 in the expression of defense-related genes in rice. Biochim Biophys Acta 1769:497–505. https://doi.org/10.1016/j.bbaexp.2007.04.006
Fan CC, Xing YZ, Mao HL, Lu TT, Han B, Xu CG, Li XH, Zhang QF (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
Gao Y, Xue CY, Liu JM, He Y, Mei Q, Wei SH, Xuan YH (2021) Sheath blight resistance in rice is negatively regulated by WRKY53 via SWEET2a activation. Biochem Biophys Res Commun 585:117–123. https://doi.org/10.1016/j.bbrc.2021.11.042
Hiei Y, Obta 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 LF, Ye M, Li R, Lou YG (2015) OsWRKY53, a versatile switch in regulating herbivore-induced defense responses in rice. Plant Signal Behav 11:e1169357. https://doi.org/10.1080/15592324.2016.1169357
Jing SJ, Zhou X, Song Y, Yu DQ (2009) Heterologous expression of OsWRKY23 gene enhances pathogen defense and dark-induced leaf senescence in Arabidopsis. Plant Growth Regul 58:181–190. https://doi.org/10.1007/s10725-009-9366-z
Lan J, Lin QB, Zhou CL, Ren YK, Liu X, Miao R, Jing RN, Mou CL, Nguyen TH, Zhu XJ, Wang X, Zhang X, Guo XP, Liu SJ, Jiang L, Wan J (2020) Small grain and semi-dwarf 3, a WRKY transcription factor, negatively regulates plant height and grain size by stabilizing SLR1 expression in rice. Plant Mol Biol 104:429–450. https://doi.org/10.1007/s11103-020-01049-0
Li N, Li YH (2016) Signaling pathways of seed size control in plants. Curr Opin Plant Biol 33:23–32. https://doi.org/10.1016/j.pbi.2016.05.008
Li SJ, Zhou X, Chen LG, Huang WD, Yu DQ (2010) Functional characterization of Arabidopsis thaliana WRKY39 in heat stress. Mol Cells 29:475–483. https://doi.org/10.1007/s10059-010-0059-2
Li YB, Fan CC, Xing YZ, Jiang YH, Luo LJ, Sun L, Shao D, Xu CJ, Li XH, Xiao JH, He YQ, Zhang QF (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 R, Zhang J, Li JC, Zhou GX, Wang Q, Bian WB, Erb M, Lou YG (2015) Prioritizing plant defence over growth through WRKY regulation facilitates infestation by non-target herbivores. eLife 4:e04805. https://doi.org/10.7554/eLife.04805.001
Liu ZQ, Mei EY, Tian XJ, He ML, Tang JQ, Xu M, Liu JL, Song L, Li XX, Wang ZY, Guan QJ, Xu QJ, Bu QY (2021) OsMKKK70 regulates grain size and leaf angle in rice through the OsMKK4-OsMAPK6-OsWRKY53 signaling pathway. J Integr Plant Biol 00:1–15. https://doi.org/10.1111/jipb.13174
Ma XL, Zhang QY, Zhu QL, Liu W, Chen Y, Qiu R, Wang B, Yang ZF, Li HY, Lin YR, Xie YY, Shen RX, Chen SF, Wang Z, Chen YL, Guo JX, Chen LT, Zhao XC, Liu YG (2015) A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol Plant 8:1274–1284. https://doi.org/10.1016/j.molp.2015.04.007
Qi P, Lin YS, Song XJ, Shen JB, Huang W, Shan JX, Zhu MZ, Jiang LW, Gao JP, Lin HX (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
Qiao SL, Sun SY, Wang LL, Wu ZH, Li CX, Li XM, Wang T, Leng LN, Tian WS, Lu TG, Wang XL (2017) The RLA1/SMOS1 transcription factor functions with OsBZR1 to regulate brassinosteroid signaling and rice architecture. Plant Cell 29:292–309. https://doi.org/10.1105/tpc.16.00611
Qiu YP, Yu DQ (2009) Over-expression of the stress-induced OsWRKY45 enhances disease resistance and drought tolerance in Arabidopsis. Environ Exp Bot 65:35–47. https://doi.org/10.1016/j.envexpbot.2008.07.002
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
Song XJ, Kuroha T, Ayano M, Furuta T, Nagai K, Komeda N, Segami S, Miura K, Ogawa D, Kamura T, Suzuki T, Higashiyama T, Yamasaki M, Mori H, Inukai Y, Wu JZ, Kitano H, Sakakibara H, Jacobsen SE, Ashikari M (2015) Rare allele of a previously unidentified histone H4 acetyltransferase enhances grain weight, yield, and plant biomass in rice. Proc Natl Acad Sci USA 112:76–81. https://doi.org/10.1073/pnas.1421127112
Takeda S, Matsuoka M (2008) Genetic approaches to crop improvement: responding to environmental and population changes. Nat Rev Genet 9:444–457. https://doi.org/10.1038/nrg2342
Tian XJ, Li XF, Zhou WJ, Ren YK, Wang ZY, Liu ZQ, Tang JQ, Tong HN, Fang J, Bu QY (2017) Transcription factor OsWRKY53 positively regulates brassinosteroid signaling and plant architecture. Plant Physiol 175:1337–1349. https://doi.org/10.1104/pp.17.00946
Tian XJ, He ML, Mei EY, Zhang B, Tang JQ, Xu M, Liu JL, Li XF, Wang ZY, Tang WQ, Guan QJ, Bu QY (2021) WRKY53 integrates classic brassinosteroid signaling and the mitogen-activated protein kinase pathway to regulate rice architecture and seed size. Plant Cell 33:2753–2775. https://doi.org/10.1093/plcell/koab137
Tong H, Jin Y, Liu W, Li F, Fang J, Yin Y, Qian Q, Zhu L, Chu C (2009) DWARF AND LOW-TILLERING, a new member of the GRAS family, plays positive roles in brassinosteroid signaling in rice. Plant J58:803–816. https://doi.org/10.1111/j.1365-313X.2009.03825.x
Tong HN, Liu L, Jin Y, Du L, Yin Y, Qian Q, Zhu L, Chu CC (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
Wang SK, Wu K, Yuan QB, Liu XY, Liu ZB, Lin XY, Zeng RZ, Zhu HT, Dong GJ, Qian Q, Zhang GQ, Fu XD (2012) Control of grain size, shape and quality by OsSPL16 in rice. Nat Genet 44:950–954. https://doi.org/10.1038/ng.2327
Wang SK, Li S, Liu Q, Wu K, Zhang JQ, Wang SS, Wang Y, Chen XB, Zhang Y, Gao CX, Wang F, Huang HX, Fu XD (2015) The OsSPL16-GW7 regulatory module determines grain shape and simultaneously improves rice yield and grain quality. Nat Genet 47:949–954. https://doi.org/10.1038/ng.3352
Xia D, Zhou H, Liu RJ, Dan WH, Li PB, Wu B, Chen JX, Wang LQ, Gao GJ, Zhang QL, He YQ (2018) GL3.3, a novel QTL encoding a GSK3/SHAGGY-like kinase, epistatically interacts with GS3 to produce extra-long grains in rice. Mol Plant 1:754–756. https://doi.org/10.1016/j.molp.2018.03.006
Xie Z, Zhang ZL, Zou XL, Huang J, Ruas P, Thompson D, Shen QJ (2005) Annotations and functional analyses of the rice WRKY gene superfamily reveal positive and negative regulators abscisic acid signaling in aleurone cells. Plant Physiol 137:176–189. https://doi.org/10.1104/pp.104.054312
Xie Z, Zhang ZL, Zou XL, Yang GX, Komatsu S, Shen QJ (2006) Interactions of two abscisic-acid induced WRKY genes in repressing gibberellin signaling in aleurone cells. Plant J 46:231–242. https://doi.org/10.1111/j.1365-313X.2006.02694.x
Xie WY, Ke YG, Cao JB, Wang SP, Yuan M (2021) Knock out of transcription factor WRKY53 thickens sclerenchyma cell walls, confers bacterial blight resistance. Plant Physiol 187:1746–1761. https://doi.org/10.1093/plphys/kiab400
Xing YZ, Zhang QF (2010) Genetic and molecular bases of rice yield. Annu Rev Plant Biol 61:421–442. https://doi.org/10.1146/annurev-arplant-042809-112209
Yamasaki K, Kigawa T, Inoue M, Tateno M, Yamasaki T, Yabuki T, Aoki M, Seki E, Matsuda T, Tomo Y (2005) Solution structure of an Arabidopsis WRKY DNA binding domain. Plant Cell 17:944–956. https://doi.org/10.1105/tpc.104.026435
Zhang ZL, Xie Z, Zou XL, Casaretto J, Ho TD, Shen QJ (2004) A rice WRKY gene encodes a transcriptional repressor of the gibberellin signaling pathway in aleurone cells. Plant Physiol 134:1500–1513. https://doi.org/10.1104/pp.103.034967
Zhang CQ, Xu Y, Lu Y, Yu HX, Gu MH, Liu QQ (2011) The WRKY transcription factor OsWRKY78 regulates stem elongation and seed development in rice. Planta 234:541–554. https://doi.org/10.1007/s00425-011-1423-y
Zhang LY, Gu LK, Ringler P, Smith S, Rushton PJ, Shen QJ (2015) Three WRKY transcription factors additively repress abscisic acid and gibberellin signaling in aleurone cells. Plant Sci 236:214–222. https://doi.org/10.1016/j.plantsci.2015.04.014
Zuo JR, Li JY (2014) Molecular genetic dissection of quantitative trait loci regulating rice grain size. Annu Rev Genet 48:99–118. https://doi.org/10.1146/annurev-genet-120213-092138
Acknowledgements
This study was supported by the Natural Science Foundation of Heilongjiang (Grant No. JQ2020C003), National Natural Science Foundation of China-Heilongjiang Joint Fund (Grant No. U20A2025), Youth Innovation Promotion Association CAS (Grant No. 2021229).
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Tang, J., Mei, E., He, M. et al. Functions of OsWRKY24, OsWRKY70 and OsWRKY53 in regulating grain size in rice. Planta 255, 92 (2022). https://doi.org/10.1007/s00425-022-03871-w
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DOI: https://doi.org/10.1007/s00425-022-03871-w