Abstract
Key message
A FT/TFL1 subfamily gene, rice CENTRORADIALIS 2, also known as RCN1, regulates seed germination and increase salt tolerance via ABA-mediated pathway. The ABA synthesis and metabolism related genes were changed relative expression levels.
Abstract
Seed germination is a complex biological process that is affected by many factors. Although a number of germination-related genes have been reported, the molecular mechanism of germination regulation has not yet been fully elucidated. Here, we reported that the rice OsCEN2 gene can negatively regulate seed germination. The germination speed of OsCEN2-RNAi seeds was significantly faster while that of OsCEN2-overexpression (OE) seeds was slower than that of the wild type (WT). The results of qRT-PCR showed that the OsCEN2 expression was increased in the early stage of seed germination. Exogenous application of abscisic acid (ABA) on seeds and seedlings showed that OsCEN2-OE seeds and seedlings were highly sensitive to ABA during germination and post-germination growth, respectively. The determination of endogenous ABA content in seeds also showed that the ABA content of OsCEN2-RNAi seeds was lower, while that of OsCEN2-OE seeds was higher. Moreover, the transgenic plants changed salt tolerance because of the altered ABA level. In addition, differences were also observed in the expression of genes related to ABA synthesis and metabolism in the seeds of OsCEN2-transgenic lines. This study reveals that OsCEN2 regulates the germination speed by affecting the content of ABA during seed germination and provides a theoretical basis for research on rice direct seeding.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
An JP, Li R, Qu FJ, You CX, Wang XF, Hao YJ (2018) An apple NAC transcription factor negatively regulates cold tolerance via CBF-dependent pathway. Journal of Plant Physiol 221:74–80. https://doi.org/10.1016/j.jplph.2017.12.009
Carles C, Bies-Etheve N, Aspart L, LeÂon-Kloosterziel KM, Koornneef M, Echeverria M, Delseny M (2002) Regulation of Arabidopsis thaliana Em genes: role of ABI5. Plant J 30:373–383. https://doi.org/10.1038/s41598-021-88874-5
Chen M, Penfield S (2018) Feedback regulation of COOLAIR expression controls seed dormancy and flowering time. Science 360:1014–1017. https://doi.org/10.1126/science.aar7361
Coelho CP, Minow MAA, Chalfun-Junior A, Colasanti J (2014) Putative sugarcane FT/TFL1 genes delay flowering time and alter reproductive architecture in Arabidopsis. Front Plant Sci 5:221. https://doi.org/10.3389/fpls.2014.00221
Corbineau F, Xia Q, Bailly C, El-Maarouf-Bouteau H (2014) Ethylene, a key factor in the regulation of seed dormancy. Front Plant Sci 5:539. https://doi.org/10.3389/fpls.2014.00539
Feng CZ, Chen Y, Wang C, Kong YH, Wu WH, Chen YF (2014) Arabidopsis RAV1 transcription factor, phosphorylated by SnRK2 kinases, regulates the expression of ABI3, ABI4, and ABI5 during seed germination and early seedling development. Plant J 80:654–668. https://doi.org/10.1111/tpj.12670
Finkelstein R (2013) Abscisic acid synthesis and response. Arabidopsis Book 11:e0166. https://doi.org/10.1199/tab.0166
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
Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12:599–609. https://doi.org/10.1105/tpc.12.4.599
Freiman A, Golobovitch S, Yablovitz Z, Belausov E, Dahan Y, Peer R, Avraham L, Freiman Z, Evenor D, Reuveni M, Sobolev V, Edelman M, Shahak Y, Samach A, Flaishman MA (2015) Expression of flowering locus T2 transgene from Pyrus communis L. delays dormancy and leaf senescence in Malus×domestica Borkh, and causes early flowering in tobacco. Plant Sci 241:164–176. https://doi.org/10.1016/j.plantsci.2015.09.012
Gubler F, Millar AA, Jacobsen JV (2005) Dormancy release, ABA and pre-harvest sprouting. Curr Opin Plant Biol 8:183–187. https://doi.org/10.1016/j.pbi.2005.01.011
Jiang DG, Chen WT, Dong JF, Li J, Yang F, Wu ZC, Zhou H, Wang WS, Zhuang CX (2018) Overexpression of miR164b-resistant OsNAC2 improves plant architecture and grain yield in rice. J Exp Bot 69:1533–1543. https://doi.org/10.1093/jxb/ery017
Jiang DG, Zhou LY, Chen WT, Ye NH, Xia JX, Zhuang CX (2019) Overexpression of a microRNA-targeted NAC transcription factor improves drought and salt tolerance in Rice via ABA-mediated pathways. Rice 12:76. https://doi.org/10.1186/s12284-019-0334-6
Jin S, Nasim Z, Susila H, Ahn JH (2021) Evolution and functional diversification of FLOWERING LOCUS T/TERMINAL FLOWER 1 family genes in plants. Semin Cell Dev Biol 109:20–30. https://doi.org/10.1016/j.semcdb.2020.05.007
Karlgrenet A, Gyllenstrand N, Källman T, Sundström JF, Moore D, Lascoux M, Lagercrantz U (2011) Evolution of the PEBP gene family in plants: functional diversification in seed plant evolution. Plant Physiol 156:1967–1977. https://doi.org/10.1104/pp.111.176206
Khan F, Upreti P, Singh R, Shukla PK, Shirke PA (2017) Physiological performance of two contrasting rice varieties under water stress. Physiol Mol Biol Plants 23:85–97. https://doi.org/10.1007/s12298-016-0399-2
Koramutla MK, Negi M, Ayele BT (2021) Roles of glutathione in mediating abscisic acid signaling and its regulation of seed dormancy and drought tolerance. Genes 12:1620. https://doi.org/10.3390/genes12101620
Kushiro T, Okamoto M, Nakabayashi K, Yamagishi K, Kitamura S, Asami T, Hirai N, Koshiba T, Kamiya Y, Nambara E (2004) The Arabidopsis cytochrome P450 CYP707A encodes ABA 8’-hydroxylases: key enzymes in ABA catabolism. EMBO J 23:1647–1656. https://doi.org/10.1038/sj.emboj.7600121
Lee SC, Luan S (2012) ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant Cell Environ 35:53–60. https://doi.org/10.1111/j.1365-3040.2011.02426.x
Li J, Jiang DG, Zhou H, Li F, Yang JW, Hong LF, Fu X, Li ZB, Liu ZL, Li JM, Zhuang CX (2011) Expression of RNA-interference/antisense transgenes by the cognate promoters of target genes is a better gene-silencing strategy to study gene functions in rice. PLoS ONE 6:e17444. https://doi.org/10.1371/journal.pone.0017444
Li XX, Yu B, Wu Q, Min Q, Zeng RF, Xie ZZ, Huang JL (2021) OsMADS23 phosphorylated by SAPK9 confers drought and salt tolerance by regulating ABA biosynthesis in rice. PLoS Genet 17:e1009699. https://doi.org/10.1371/journal.pgen.1009699
Lopez-Molina L, Mongrand S, Chua NH (2001) A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc Natl Acad Sci USA 98:4782–4787. https://doi.org/10.1073/pnas.081594298
Lopez-Molina L, Mongrand S, McLachlin DT, Chait BT, Chua NH (2002) ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J 32:317–328. https://doi.org/10.1046/j.1365-313X.2002.01430.x
Luo X, Chen T, Zeng XL, He DW, He YH (2019) Feedback regulation of FLC by FLOWERING LOCUS T (FT) and FD through a 5’ FLC promoter region in Arabidopsis. Mol Plant 12:285–288. https://doi.org/10.1016/j.molp.2019.01.013
Lv Y, Yang M, Hu D, Yang ZY, Ma SQ, Li XH, Xiong LZ (2017) The OsMYB30 transcription factor suppresses cold tolerance by interacting with a JAZ protein and suppressing β-Amylase expression. Plant Physiol 173:1475–1491. https://doi.org/10.1104/pp.16.01725
Mahender A, Anandan A, Pradhan SK (2015) Early seedling vigour, an imperative trait for direct-seeded rice: an overview on physio-morphological parameters and molecular markers. Planta 241:1027–1050. https://doi.org/10.1007/s00425-015-2273-9
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, Dong ZC, 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
Merlot S, Gosti F, Guerrier D, Vavasseur A, Giraudat J (2001) The ABI1 and ABI2 protein phosphatases 2C act in a negative feedback regulatory loop of the abscisic acid signalling pathway. Plant J 25:295–303. https://doi.org/10.1046/j.1365-313x.2001.00965.x
Miyazono KI, Miyakawa T, Sawano Y, Kubota K, Kang HJ, Asano A, Miyauchi Y, Takahashi M, Zhi Y, Fujita Y, Yoshida T, Kodaira KS, Yamaguchi-Shinozaki K, Tanokura M (2009) Structural basis of abscisic acid signaling. Nature 462:609–614. https://doi.org/10.1038/nature08583
Mohamed R, Wang CT, Ma C, Shevchenko O, Dye SJ, Puzey JR, Etherington E, Sheng XY, Meilan R, Strauss SH, Brunner AM (2010) Populus CEN/TFL1 regulates first onset of flowering, axillary meristem identity and dormancy release in Populus. Plant J 62:674–688. https://doi.org/10.1111/j.1365-313X.2010.04185.x
Morris WL, Carmen Alamar M, Lopez-Cobollo RM, Castillo Cañete J, Bennett M, Van der Kaay J, Stevens J, Kumar Sharma S, McLean K, Thompson AJ, Terry LA, Turnbull CGN, Bryan GJ, Taylor MA (2019) A member of the TERMINAL FLOWER 1/CENTRORADIALIS gene family controls sprout growth in potato tubers. J Exp Bot 70:835–843. https://doi.org/10.1093/jxb/ery387
Nakagawa M, Shimamoto K, Kyozuka J (2002) Overexpression of RCN1 and RCN2, rice TERMINAL FLOWER 1/CENTRORADIALIS homologs, confers delay of phase transition and altered panicle morphology in rice. Plant J 29:743–750. https://doi.org/10.1046/j.1365-313x.2002.01255.x
Nakamura S, Abe F, Kawahigashi H, Nakazono K, Tagiri A, Matsumoto T, Utsugi S, Ogawa T, Handa H, Ishida H, Mori M, Kawaura K, Ogihara Y, Miura H (2011) A wheat homolog of MOTHER OF FT AND TFL1 acts in the regulation of germination. Plant Cell 23:3215–3229. https://doi.org/10.1105/tpc.111.088492
Nonogaki H, Bassel GW, Derek Bewley J (2010) Germination-Still a mystery. Plant Sci 179:574–581. https://doi.org/10.1016/j.plantsci.2010.02.010
Piskurewicz U, Jikumaru Y, Nambara KN, E, Kamiya Y, Lopez-Molina L, (2008) The gibberellic acid signaling repressor RGL2 inhibits Arabidopsis seed germination by stimulating abscisic acid synthesis and ABI5 activity. Plant Cell 20:2729–2745. https://doi.org/10.1105/tpc.108.061515
Schmitz N, Abrams SR, Kermode AR (2002) Changes in ABA turnover and sensitivity that accompany dormancy termination of yellow-cedar (Chamaecyparis nootkatensis) seeds. J Exp Bot 53:89–101. https://doi.org/10.1093/jexbot/53.366.89
Song S, Wang GF, Wu H, Fan XW, Liang LW, Zhao H, Hu LSL, Y, Liu HY, Ayaad M, Xing YZ, (2020) OsMFT2 is involved in the regulation of ABA signaling-mediated seed germination through interacting with OsbZIP23/66/72 in rice. Plant J 103:532–546. https://doi.org/10.1111/tpj.14748
Shu K, Meng YJ, Shuai HW, Liu WG, Du JB, Liu J, Yang WY (2015) Dormancy and germination: How does the crop seed decide? Plant Biol 17:1104–1112. https://doi.org/10.1111/plb.12356
Shu K, Zhang HW, Wang SF, Chen ML, Wu YR, Tang SY, Liu CY, Feng YQ, Cao XF, Xie Q (2013) ABI4 regulates primary seed dormancy by regulating the biogenesis of abscisic acid and gibberellins in Arabidopsis. PLoS Genet 9:e1003577. https://doi.org/10.1371/journal.pgen.1003577
Söderman EM, Brocard IM, Lynch TJ, Finkelstein RR (2000) Regulation and function of the Arabidopsis ABA-insensitive4 gene in seed and abscisic acid response signaling networks. Plant Physiol 124:1752–1765. https://doi.org/10.1104/pp.124.4.1752
Sun L, Sun YF, Zhang M, Wang L, Ren J, Cui MM, Wang YP, Ji K, Li P, Li Q, Chen P, Dai SJ, Duan CR, Wu Y, Leng P (2012) Suppression of 9-cis-epoxycarotenoid dioxygenase, which encodes a key enzyme in abscisic acid biosynthesis, alters fruit texture in transgenic tomato. Plant Physiol 158:283–298. https://doi.org/10.1104/pp.111.186866
Wang J, Deng QW, Li YH, Yu YH, Liu X, Han YF, Luo XD, Wu XJ, Ju L, Sun JQ, Liu AH, Fang J (2020) Transcription factors Rc and OsVP1 coordinately regulate preharvest sprouting tolerance in red pericarp rice. J Agric Food Chem 68:14748–14757. https://doi.org/10.1021/acs.jafc.0c04748
Xi WY, Liu C, Liu C, Hou XL, Yu H (2010) MOTHER OF FT AND TFL1 regulates seed germination through a negative feedback loop modulating ABA Signaling in Arabidopsis. Plant Cell 22:1733–1748. https://doi.org/10.1105/tpc.109.073072
Yu L, Jiang JZ, Zhang C, Jiang LR, Ye NH, Lu YS, Yang GZ, Liu EE, Peng CL, He ZH, Peng XX (2010) Glyoxylate rather than ascorbate is an efficient precursor for oxalate biosynthesis in rice. J Exp Bot 61:1625–1634. https://doi.org/10.1093/jxb/erq028
Zhu GH, Ye NH, Zhang JH (2009) Glucose-induced delay of seed germination in rice is mediated by the suppression of ABA catabolism rather than an enhancement of ABA biosynthesis. Plant Cell Physiol 50:644–651. https://doi.org/10.1093/pcp/pcp022
Zhou H, Zhou M, Yang YZ, Li J, Zhu LY, Jiang DG, Dong JF, Liu QJ, Gu LF, Zhou LY, Feng MJ, Qin P, Hu XC, Song CL, Shi JF, Song XW, Ni ED, Wu XJ, Deng QY, Liu ZL, Chen MS, Liu YG, Cao XF, Zhuang CX (2014) RNase ZS1 processes UbL40 mRNAs and controls thermosensitive genic male sterility in rice. Nat Commun 5:4884. https://doi.org/10.1038/ncomms5884
Zou MJ, Guan YC, Ren HB, Zhang F, Chen F (2008) A bZIP transcription factor, OsABI5, is involved in rice fertility and stress tolerance. Plant Mol Biol 66:675–683. https://doi.org/10.1007/s11103-008-9298-4
Zou MJ, Guan YC, Ren HB, Zhang F, Chen F (2007) Characterization of alternative splicing products of bZIP transcription factors OsABI5. Biochem Biophys Res Commun 360:307–313. https://doi.org/10.1016/j.bbrc.2007.05.226
Acknowledgements
This work was supported by the Major Program of Guangdong Basic and Applied Research (grant no. 2019B030302006) and the National Natural Science Foundation of China (grant no. 31100872).
Author information
Authors and Affiliations
Contributions
CZ and DJ designed the research. YH and WC performed most experiments and analyzed experimental data. JT, XL, YZ, XG and JY conducted a part of experiments. HY wrote the manuscript, CZ and DJ revised the paper. All authors approved the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Matthias Wissuwa.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
He, Y., Chen, W., Tan, J. et al. Rice CENTRORADIALIS 2 regulates seed germination and salt tolerance via ABA-mediated pathway. Theor Appl Genet 135, 4245–4259 (2022). https://doi.org/10.1007/s00122-022-04215-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-022-04215-8