Abstract
Seed dormancy is an important agronomic trait under the control of complex genetic and environmental interactions, which have not been yet comprehensively understood. From the field screening of rice mutant library generated by a Ds transposable element, we identified a pre-harvest sprouting (PHS) mutant dor1. This mutant has a single insertion of Ds element at the second exon of OsDOR1 (LOC_Os03g20770), which encodes a novel seed-specific glycine-rich protein. This gene successfully complemented the PHS phenotype of dor1 mutant and its ectopic expression enhanced seed dormancy. Here, we demonstrated that OsDOR1 protein binds to the GA receptor protein, OsGID1 in rice protoplasts, and interrupts with the formation OsGID1-OsSLR1 complex in yeast cells. Co-expression of OsDOR1 with OsGID1 in rice protoplasts attenuated the GA-dependent degradation of OsSLR1, the key repressor of GA signaling. We showed the endogenous OsSLR1 protein level in the dor1 mutant seeds is significantly lower than that of wild type. The dor1 mutant featured a hypersensitive GA-response of α-amylase gene expression during seed germination. Based on these findings, we suggest that OsDOR1 is a novel negative player of GA signaling operated in the maintenance of seed dormancy. Our findings provide a novel source of PHS resistance.
Key message
OsDOR1, the causal gene for the rice PHS mutant dor1, is a novel positive regulator of seed dormancy through interaction with the GID1-SLR1 complex and stabilization of the SLR1 protein in rice seeds.
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References
Agrawal GK, Yamazaki M, Kobayashi M, Hirochika R, Miyao A, Hirochika H (2001) Screening of the rice viviparous mutants generated by endogenous retrotransposon Tos17 insertion. Tagging of a zeaxanthin epoxidase gene and a novel ostatc gene. Plant Physiol 125(3):1248–1257. https://doi.org/10.1104/pp.125.3.1248
Cao D, Hussain A, Cheng H, Peng J (2005) Loss of function of four DELLA genes leads to light- and gibberellin-independent seed germination in Arabidopsis. Planta 223(1):105–113. https://doi.org/10.1007/s00425-005-0057-3
Cao H, Gong R, Yuan S, Su Y, Lv W, Zhou Y, Zhang Q, Deng X, Tong P, Liang S, Wang X, Hong Y (2021) Phospholipase Dα6 and phosphatidic acid regulate gibberellin signaling in rice. EMBO Rep 22(10):e51871. https://doi.org/10.15252/embr.202051871
Du W, Cheng J, Cheng Y, Wang L, He Y, Wang Z, Zhang H (2015) Physiological characteristics and related gene expression of after-ripening on seed dormancy release in rice. Plant Biol (stuttg) 17(6):1156–1164. https://doi.org/10.1111/plb.12371
Du L, Xu F, Fang J, Gao S, Tang J, Fang S, Wang H, Tong H, Zhang F, Chu J, Wang G, Chu C (2018) Endosperm sugar accumulation caused by mutation of PHS8/ISA1 leads to pre-harvest sprouting in rice. Plant J 95(3):545–556. https://doi.org/10.1111/tpj.13970
Fang J, Chai C, Qian Q, Li C, Tang J, Sun L, Huang Z, Guo X, Sun C, Liu M, Zhang Y, Lu Q, Wang Y, Lu C, Han B, Chen F, Cheng Z, Chu C (2008) Mutations of genes in synthesis of the carotenoid precursors of ABA lead to pre-harvest sprouting and photo-oxidation in rice. Plant J 54(2):177–189. https://doi.org/10.1111/j.1365-313X.2008.03411.x
Finkelstein R, Reeves W, Ariizumi T, Steber C (2008) Molecular aspects of seed dormancy. Annu Rev Plant Biol 59:387–415. https://doi.org/10.1146/annurev.arplant.59.032607.092740
Fujino K, Sekiguchi H, Matsuda Y, Sugimoto K, Ono K, Yano M (2008) Molecular identification of a major quantitative trait locus, qLTG3-1, controlling low-temperature germinability in rice. Proc Natl Acad Sci U S A 105(34):12623–12628. https://doi.org/10.1073/pnas.0805303105
Fujino K, Obara M, Sato K (2014) Diversification of the plant-specific hybrid glycine-rich protein (HyGRP) genes in cereals. Front Plant Sci 5:489. https://doi.org/10.3389/fpls.2014.00489
Gomi K, Sasaki A, Itoh H, Ueguchi-Tanaka M, Ashikari M, Kitano H, Matsuoka M (2004) GID2, an F-box subunit of the SCF E3 complex, specifically interacts with phosphorylated SLR1 protein and regulates the gibberellin-dependent degradation of SLR1 in rice. Plant J 37(4):626–634. https://doi.org/10.1111/j.1365-313x.2003.01990.x
Gu XY, Kianian SF, Foley ME (2006) Dormancy genes from weedy rice respond divergently to seed development environments. Genetics 172(2):1199–1211. https://doi.org/10.1534/genetics.105.049155
Gu XY, Foley ME, Horvath DP, Anderson JV, Feng J, Zhang L, Mowry CR, Ye H, Suttle JC, Kadowaki K, Chen Z (2011) Association between seed dormancy and pericarp color is controlled by a pleiotropic gene that regulates abscisic acid and flavonoid synthesis in weedy red rice. Genetics 189(4):1515–1524. https://doi.org/10.1534/genetics.111.131169
Guo X, Hou X, Fang J, Wei P, Xu B, Chen M, Feng Y, Chu C (2013) The rice GERMINATION DEFECTIVE 1, encoding a B3 domain transcriptional repressor, regulates seed germination and seedling development by integrating GA and carbohydrate metabolism. Plant J 75(3):403–416. https://doi.org/10.1111/tpj.12209
Han JH, Jung YJ, Lee HJ, Jung HS, Lee KO, Kang H (2013) The RNA chaperone and protein chaperone activity of Arabidopsis glycine-rich RNA-binding protein 4 and 7 is determined by the propensity for the formation of high molecular weight complexes. Protein J 32(6):449–455. https://doi.org/10.1007/s10930-013-9504-3
Harberd NP, Belfield E, Yasumura Y (2009) The angiosperm gibberellin-GID1-DELLA growth regulatory mechanism: how an “inhibitor of an inhibitor” enables flexible response to fluctuating environments. Plant Cell 21(5):1328–1339. https://doi.org/10.1105/tpc.109.066969
Hauvermale AL, Tuttle KM, Takebayashi Y, Seo M, Steber CM (2015) Loss of Arabidopsis thaliana seed dormancy is associated with increased accumulation of the GID1 GA hormone receptors. Plant Cell Physiol 56(9):1773–1785. https://doi.org/10.1093/pcp/pcv084
Hirano K, Asano K, Tsuji H, Kawamura M, Mori H, Kitano H, Ueguchi-Tanaka M, Matsuoka M (2010) Characterization of the molecular mechanism underlying gibberellin perception complex formation in rice. Plant Cell 22(8):2680–2696. https://doi.org/10.1105/tpc.110.075549
Huh SM, Hwang YS, Shin YS, Nam MH, Kim DY, Yoon IS (2013) Comparative transcriptome profiling of developing caryopses from two rice cultivars with differential dormancy. J Plant Physiol 170(12):1090–1100. https://doi.org/10.1016/j.jplph.2013.03.003
Ikeda A, Ueguchi-Tanaka M, Sonoda Y, Kitano H, Koshioka M, Futsuhara Y, Matsuoka M, Yamaguchi J (2001) slender rice, a constitutive gibberellin response mutant, is caused by a null mutation of the SLR1 gene, an ortholog of the height-regulating gene GAI/RGA/RHT/D8. Plant Cell 13(5):999–1010. https://doi.org/10.1105/tpc.13.5.999
Itoh H, Ueguchi-Tanaka M, Sato Y, Ashikari M, Matsuoka M (2002) The gibberellin signaling pathway is regulated by the appearance and disappearance of SLENDER RICE1 in nuclei. Plant Cell 14(1):57–70. https://doi.org/10.1105/tpc.010319
Iuchi S, Suzuki H, Kim YC, Iuchi A, Kuromori T, Ueguchi-Tanaka M, Asami T, Yamaguchi I, Matsuoka M, Kobayashi M, Nakajima M (2007) Multiple loss-of-function of Arabidopsis gibberellin receptor AtGID1s completely shuts down a gibberellin signal. Plant J 50(6):958–966. https://doi.org/10.1111/j.1365-313X.2007.03098.x
Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6(13):3901–3907
Karrer EE, Litts JC, Rodriguez RL (1991) Differential expression of alpha-amylase genes in germinating rice and barley seeds. Plant Mol Biol 16(5):797–805. https://doi.org/10.1007/BF00015072
Kim CM, Piao HL, Park SJ, Chon NS, Je BI, Sun B, Park SH, Park JY, Lee EJ, Kim MJ, Chung WS, Lee KH, Lee YS, Lee JJ, Won YJ, Yi G, Nam MH, Cha YS, Yun DW, Eun MY, Han CD (2004) Rapid, large-scale generation of Ds transposant lines and analysis of the Ds insertion sites in rice. Plant J 39(2):252–263. https://doi.org/10.1111/j.1365-313X.2004.02116.x
Kim JS, Park SJ, Kwak KJ, Kim YO, Kim JY, Song J, Jang B, Jung CH, Kang H (2007) Cold shock domain proteins and glycine-rich RNA-binding proteins from Arabidopsis thaliana can promote the cold adaptation process in Escherichia coli. Nucleic Acids Res 35(2):506–516. https://doi.org/10.1093/nar/gkl1076
Kim JY, Kim WY, Kwak KJ, Oh SH, Han YS, Kang H (2010a) Glycine-rich RNA-binding proteins are functionally conserved in Arabidopsis thaliana and Oryza sativa during cold adaptation process. J Exp Bot 61(9):2317–2325. https://doi.org/10.1093/jxb/erq058
Kim JY, Kim WY, Kwak KJ, Oh SH, Han YS, Kang H (2010b) Zinc finger-containing glycine-rich RNA-binding protein in Oryza sativa has an RNA chaperone activity under cold stress conditions. Plant Cell Environ 33(5):759–768. https://doi.org/10.1111/j.1365-3040.2009.02101.x
Kim S, Park SI, Kwon H, Cho MH, Kim BG, Chung JH, Nam MH, Song JS, Kim KH, Yoon IS (2021) The rice abscisic acid-responsive RING finger E3 Ligase OsRF1 targets OsPP2C09 for degradation and confers drought and salinity tolerance in rice. Front Plant Sci 12:797940. https://doi.org/10.3389/fpls.2021.797940
Lee SE, Yoon IS, Hwang YS (2020) Aquaporin activity of barley tonoplast intrinsic proteins is involved in the delay of the coalescence of protein storage vacuoles in aleurone cells. J Plant Physiol 251:153186. https://doi.org/10.1016/j.jplph.2020.153186
Liao Y, Bai Q, Xu P, Wu T, Guo D, Peng Y, Zhang H, Deng X, Chen X, Luo M, Ali A, Wang W, Wu X (2018) Mutation in rice abscisic acid2 results in cell death, enhanced disease-resistance, altered seed dormancy and development. Front Plant Sci 9:405. https://doi.org/10.3389/fpls.2018.00405
Lin Q, Wu F, Sheng P, Zhang Z, Zhang X, Guo X, Wang J, Cheng Z, Wang J, Wang H, Wan J (2015) The SnRK2-APC/C(TE) regulatory module mediates the antagonistic action of gibberellic acid and abscisic acid pathways. Nat Commun 6:7981. https://doi.org/10.1038/ncomms8981
Liu X, Hu P, Huang M, Tang Y, Li Y, Li L, Hou X (2016) The NF-YC-RGL2 module integrates GA and ABA signalling to regulate seed germination in Arabidopsis. Nat Commun 7:12768. https://doi.org/10.1038/ncomms12768
Liu X, Wang J, Yu Y, Kong L, Liu Y, Liu Z, Li H, Wei P, Liu M, Zhou H, Bu Q, Fang J (2019) Identification and characterization of the rice pre-harvest sprouting mutants involved in molybdenum cofactor biosynthesis. New Phytol 222(1):275–285. https://doi.org/10.1111/nph.15607
Livne S, Weiss D (2014) Cytosolic activity of the gibberellin receptor GIBBERELLIN INSENSITIVE DWARF1A. Plant Cell Physiol 55(10):1727–1733. https://doi.org/10.1093/pcp/pcu104
Ma Y, Liu L, Zhu C, Sun C, Xu B, Fang J, Tang J, Luo A, Cao S, Li G, Qian Q, Xue Y, Chu C (2009) Molecular analysis of rice plants harboring a multi-functional T-DNA tagging system. J Genet Genomics 36(5):267–276. https://doi.org/10.1016/S1673-8527(08)60114-9
Ma B, Yin CC, He SJ, Lu X, Zhang WK, Lu TG, Chen SY, Zhang JS (2014) Ethylene-induced inhibition of root growth requires abscisic acid function in rice (Oryza sativa L.) seedlings. PLoS Genet 10(10):e1004701. https://doi.org/10.1371/journal.pgen.1004701
Ma L, Cheng K, Li J, Deng Z, Zhang C, Zhu H (2021) Roles of plant glycine-rich RNA-binding proteins in development and stress responses. Int J Mol Sci. https://doi.org/10.3390/ijms22115849
Mangeon A, Junqueira RM, Sachetto-Martins G (2010) Functional diversity of the plant glycine-rich proteins superfamily. Plant Signal Behav 5(2):99–104. https://doi.org/10.4161/psb.5.2.10336
McGinnis KM, Thomas SG, Soule JD, Strader LC, Zale JM, Sun TP, Steber CM (2003) The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15(5):1120–1130. https://doi.org/10.1105/tpc.010827
Murase K, Hirano Y, Sun TP, Hakoshima T (2008) Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456(7221):459–463. https://doi.org/10.1038/nature07519
Nakashima K, Fujita Y, Kanamori N, Katagiri T, Umezawa T, Kidokoro S, Maruyama K, Yoshida T, Ishiyama K, Kobayashi M, Shinozaki K, Yamaguchi-Shinozaki K (2009) Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy. Plant Cell Physiol 50(7):1345–1363. https://doi.org/10.1093/pcp/pcp083
Park SJ, Kwak KJ, Oh TR, Kim YO, Kang H (2009) Cold shock domain proteins affect seed germination and growth of Arabidopsis thaliana under abiotic stress conditions. Plant Cell Physiol 50(4):869–878. https://doi.org/10.1093/pcp/pcp037
Sasaki K, Kim MH, Kanno Y, Seo M, Kamiya Y, Imai R (2015) Arabidopsis cold shock domain protein 2 influences ABA accumulation in seed and negatively regulates germination. Biochem Biophys Res Commun 456(1):380–384. https://doi.org/10.1016/j.bbrc.2014.11.092
Shimada A, Ueguchi-Tanaka M, Nakatsu T, Nakajima M, Naoe Y, Ohmiya H, Kato H, Matsuoka M (2008) Structural basis for gibberellin recognition by its receptor GID1. Nature 456(7221):520–523. https://doi.org/10.1038/nature07546
Sugimoto K, Takeuchi Y, Ebana K, Miyao A, Hirochika H, Hara N, Ishiyama K, Kobayashi M, Ban Y, Hattori T, Yano M (2010) Molecular cloning of Sdr4, a regulator involved in seed dormancy and domestication of rice. Proc Natl Acad Sci U S A 107(13):5792–5797. https://doi.org/10.1073/pnas.0911965107
Suzuki M, Ketterling MG, Li QB, McCarty DR (2003) Viviparous1 alters global gene expression patterns through regulation of abscisic acid signaling. Plant Physiol 132(3):1664–1677. https://doi.org/10.1104/pp.103.022475
Ueguchi-Tanaka M, Ashikari M, Nakajima M, Itoh H, Katoh E, Kobayashi M, Chow TY, Hsing YI, Kitano H, Yamaguchi I, Matsuoka M (2005) GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437(7059):693–698. https://doi.org/10.1038/nature04028437:693
Ueguchi-Tanaka M, Nakajima M, Katoh E, Ohmiya H, Asano K, Saji S, Hongyu X, Ashikari M, Kitano H, Yamaguchi I, Matsuoka M (2007) Molecular interactions of a soluble gibberellin receptor, GID1, with a rice DELLA protein, SLR1, and gibberellin. Plant Cell 19(7):2140–2155. https://doi.org/10.1105/tpc.106.043729
Walia RR, Xue LC, Wilkins K, El-Manzalawy Y, Dobbs D, Honavar V (2014) RNABindRPlus: a predictor that combines machine learning and sequence homology-based methods to improve the reliability of predicted RNA-binding residues in proteins. PLoS One 9(5):e97725. https://doi.org/10.1371/journal.pone.0097725
Wang Q, Lin Q, Wu T, Duan E, Huang Y, Yang C, Mou C, Lan J, Zhou C, Xie K, Liu X, Zhang X, Guo X, Wang J, Jiang L, Wan J (2020) OsDOG1L-3 regulates seed dormancy through the abscisic acid pathway in rice. Plant Sci 298:110570. https://doi.org/10.1016/j.plantsci.2020.110570
Xia B, Ke H, Inouye M (2001) Acquirement of cold sensitivity by quadruple deletion of the cspA family and its suppression by PNPase S1 domain in Escherichia coli. Mol Microbiol 40(1):179–188. https://doi.org/10.1046/j.1365-2958.2001.02372.x
Xu T, Han JH, Kang H (2013) Structural features important for the RNA chaperone activity of zinc finger-containing glycine-rich RNA-binding proteins from wheat (Triticum avestivum) and rice (Oryza sativa). Phytochemistry 94:28–35. https://doi.org/10.1016/j.phytochem.2013.05.019
Xu F, Tang J, Gao S, Cheng X, Du L, Chu C (2019) Control of rice pre-harvest sprouting by glutaredoxin-mediated abscisic acid signaling. Plant J 100(5):1036–1051. https://doi.org/10.1111/tpj.14501
Xu P, Chen H, Li T, Xu F, Mao Z, Cao X, Miao L, Du S, Hua J, Zhao J, Guo T, Kou S, Wang W, Yang HQ (2021) Blue light-dependent interactions of CRY1 with GID1 and DELLA proteins regulate gibberellin signaling and photomorphogenesis in Arabidopsis. Plant Cell 33(7):2375–2394. https://doi.org/10.1093/plcell/koab124
Yang Y, Karlson D (2013) AtCSP1 regulates germination timing promoted by low temperature. FEBS Lett 587(14):2186–2192. https://doi.org/10.1016/j.febslet.2013.05.039
Yang L, Jiang Z, Jing Y, Lin R (2020) PIF1 and RVE1 form a transcriptional feedback loop to control light-mediated seed germination in Arabidopsis. J Integr Plant Biol 62(9):1372–1384. https://doi.org/10.1111/jipb.12938
Yano K, Aya K, Hirano K, Ordonio RL, Ueguchi-Tanaka M, Matsuoka M (2015) Comprehensive gene expression analysis of rice aleurone cells: probing the existence of an alternative gibberellin receptor. Plant Physiol 167(2):531–544. https://doi.org/10.1104/pp.114.247940
Ye H, Feng J, Zhang L, Zhang J, Mispan MS, Cao Z, Beighley DH, Yang J, Gu XY (2015) Map-based cloning of seed dormancy1-2 identified a gibberellin synthesis gene regulating the development of endosperm-imposed dormancy in rice. Plant Physiol 169(3):2152–2165. https://doi.org/10.1104/pp.15.01202
Ye H, Beighley DH, Feng J, Gu XY (2013) Genetic and physiological characterization of two clusters of quantitative trait Loci associated with seed dormancy and plant height in rice. G3 (Bethesda) 3(2):323–331. https://doi.org/10.1534/g3.112.005041
Yoshida H, Tanimoto E, Hirai T, Miyanoiri Y, Mitani R, Kawamura M, Takeda M, Takehara S, Hirano K, Kainosho M, Akagi T, Matsuoka M, Ueguchi-Tanaka M (2018) Evolution and diversification of the plant gibberellin receptor GID1. Proc Natl Acad Sci U S A 115(33):E7844–E7853. https://doi.org/10.1073/pnas.1806040115
Zhao B, Zhang H, Chen T, Ding L, Zhang L, Ding X, Zhang J, Qian Q, Xiang Y (2022) Sdr4 dominates pre-harvest sprouting and facilitates adaptation to local climatic condition in Asia cultivated rice. J Integr Plant Biol. https://doi.org/10.1111/jipb.13266
Zhong M, Zeng B, Tang D, Yang J, Qu L, Yan J, Wang X, Li X, Liu X, Zhao X (2021) The blue light receptor CRY1 interacts with GID1 and DELLA proteins to repress GA signaling during photomorphogenesis in Arabidopsis. Mol Plant 14(8):1328–1342. https://doi.org/10.1016/j.molp.2021.05.011
Acknowledgements
We are grateful to the late Dr. MY Eun (National Institute of Agricultural Sciences, South Korea) for generation and large-scale field phenotyping of the rice Ds transposant mutant population. We sincerely thank to Dr. HS Kang (Chonnam National University, South Korea) for providing BX04 cell-based chaperone assay system and valuable discussion on the function of plant GRP proteins.
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This research was funded by grants (PJ01001501, PJ01321801 and PJ01486502) to ISY from the Agenda program of the Rural Development Administration.
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ISY, SYK and SMH conceived and wrote the original draft. GSL maintained the rice PHS Ds mutants. SMH, MHC, and JSS generated and analyzed transgenic rice materials. SYK, SMH and HJH performed experiments and data analysis. Y-SH analyzed subcellular localization in barley aleurone protoplasts. MHN and JHJ analyzed ABA content. Y-SH, B-G Kim, HSJ and K-HK reviewed the manuscript. ISY supervised this study. All authors contributed to manuscript revision, read, and approved the submitted version.
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Kim, S., Huh, S.M., Han, H.J. et al. A rice seed-specific glycine-rich protein OsDOR1 interacts with GID1 to repress GA signaling and regulates seed dormancy. Plant Mol Biol 111, 523–539 (2023). https://doi.org/10.1007/s11103-023-01343-7
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DOI: https://doi.org/10.1007/s11103-023-01343-7