
OsbZIP09, a Unique OsbZIP Transcription Factor of Rice, Promotes Rather Than Suppresses Seed Germination by Attenuating Abscisic Acid Pathway
#These authors contributed equally to this work
Received date: 2020-11-12
Accepted date: 2021-01-28
Online published: 2021-07-28
We successfully identified a novel and unique OsbZIP transcription factor, OsbZIP09, whose mutants exhibited longer seeds and less severe pre-harvest sprouting than the wild type, but shared similar germination rate as the wild type under normal germination conditions. The expression of OsbZIP09 was induced by abscisic acid (ABA) and declined as the germination process. As a nucleus-localized transcription factor, the conserved binding motif of OsbZIP09 was identified via DNA affinity purification sequencing technique. Further evidences indicated that OsbZIP09 directly enhanced the expression of ABA catabolism gene ABA8ox1, thus reducing ABA accumulation. In addition, OsbZIP09 also directly bound to the promoter of LEA3 gene to inhibit its expression, thus further alleviating the suppressive effect of ABA on seed germination. These results demonstrated that OsbZIP09 likely functions as a brake of the ABA pathway to attenuate the inhibitory effect of ABA on rice seed germination via dual strategies.
Chuxin Wang, Chengchao Zhu, Yu Zhou, Min Xiong, Jindong Wang, Huang Bai, Chenya Lu, Changquan Zhang, Qiaoquan Liu, Qianfeng Li . OsbZIP09, a Unique OsbZIP Transcription Factor of Rice, Promotes Rather Than Suppresses Seed Germination by Attenuating Abscisic Acid Pathway[J]. Rice Science, 2021 , 28(4) : 358 -367 . DOI: 10.1016/j.rsci.2021.05.006
| [1] | Alves M S, Dadalto S P, Gonçalves A B, De Souza G B, Barros V A, Fietto L G. 2013. Plant bZIP transcription factors responsive to pathogens: A review. Int J Mol Sci, 14(4): 7815-7828. |
| [2] | Blauwkamp T A, Chang M V, Cadigan K M. 2008. Novel TCF- binding sites specify transcriptional repression by Wnt signalling. EMBO J, 27: 1436-1446. |
| [3] | Chen K, Li G J, Bressan R A, Song C P, Zhu J K, Zhao Y. 2020. Abscisic acid dynamics, signaling, and functions in plants. J Integr Plant Biol, 62(1): 25-54. |
| [4] | Cheng X Y, Wu Y, Guo J P, Du B, Chen R Z, Zhu L L, He G C. 2013. A rice lectin receptor-like kinase that is involved in innate immune responses also contributes to seed germination. Plant J, 76(4): 687-698. |
| [5] | Dröge-Laser W, Snoek B L, Snel B, Weiste C. 2018. TheArabidopsis bZIP transcription factor family: An update. Curr Opin Plant Biol, 45: 36-49. |
| [6] | Dröge-Laser W, Weiste C. 2018. The C/S 1 bZIP network: A regulatory hub orchestrating plant energy homeostasis. Trends Plant Sci, 23(5): 422-433. |
| [7] | Finkelstein R, Reeves W, Ariizumi T, Steber C. 2008. Molecular aspects of seed dormancy. Annu Rev Plant Biol, 59: 387-415. |
| [8] | Hellens R P, Allan A C, Friel E N, Bolitho K, Grafton K, Templeton M D, Karunairetnam S, Gleave A P, Laing W A. 2005. Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods, 1: 13. |
| [9] | Hossain M A, Cho J I, Han M, Ahn C H, Jeon J S, An G, Park P B. 2010. The ABRE-binding bZIP transcription factor OsABF2 is a positive regulator of abiotic stress and ABA signaling in rice. J Plant Physiol, 167(17): 1512-1520. |
| [10] | Jacobsen J V, Pearce D W, Poole A T, Pharis R P, Mander L N. 2002. Abscisic acid, phaseic acid and gibberellin contents associated with dormancy and germination in barley. Physiol Plant, 115(3): 428-441. |
| [11] | Joo J, Lee Y H, Song S I. 2019. OsbZIP42 is a positive regulator of ABA signaling and confers drought tolerance to rice. Planta, 249(5): 1521-1533. |
| [12] | Kawakatsu T, Takaiwa F. 2010. Differences in transcriptional regulatory mechanisms functioning for free lysine content and seed storage protein accumulation in rice grain. Plant Cell Physiol, 51(12): 1964-1974. |
| [13] | Kawakatsu T, Yamamoto M P, Touno S M, Yasuda H, Takaiwa F. 2009. Compensation and interaction between RISBZ1 and RPBF during grain filling in rice. Plant J, 59(6): 908-920. |
| [14] | Langmead B, Salzberg S L. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods, 9(4): 357-359. |
| [15] | Li Q F, Zhou Y, Xiong M, Ren X Y, Han L, Wang J D, Zhang C Q, Fan X L, Liu Q Q. 2020. Gibberellin recovers seed germination in rice with impaired brassinosteroid signalling. Plant Sci, 293: 110435. |
| [16] | Lu G J, Gao C X, Zheng X N, Han B. 2009. Identification of OsbZIP72 as a positive regulator of ABA response and drought tolerance in rice. Planta, 229(3): 605-615. |
| [17] | MacDonald B T, Tamai K, He X. 2009. Wnt/beta-catenin signaling: Components, mechanisms, and diseases. Dev Cell, 17: 9-26. |
| [18] | Machanick P, Bailey T L. 2011. MEME-ChIP: Motif analysis of large DNA datasets. Bioinformatics, 27(12): 1696-1697. |
| [19] | Martínez-Andújar C, Ordiz M I, Huang Z, Nonogaki M, Beachy R N, Nonogaki H. 2011. Induction of 9-cis-epoxycarotenoid dioxygenase in Arabidopsis thaliana seeds enhances seed dormancy. Proc Natl Acad Sci USA, 108(41): 17225-17229. |
| [20] | Miyakawa T, Fujita Y, Yamaguchi-Shinozaki K, Tanokura M. 2013. Structure and function of abscisic acid receptors. Trends Plant Sci, 18(5): 259-266. |
| [21] | Née G, Xiang Y, Soppe W J. 2017. The release of dormancy, a wake-up call for seeds to germinate. Curr Opin Plant Biol, 35: 8-14. |
| [22] | Nijhawan A, Jain M, Tyagi A K, Khurana J P. 2008. Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice. Plant Physiol, 146(2): 333-350. |
| [23] | Nonogaki H. 2019. Seed germination and dormancy: The classic story, new puzzles, and evolution. J Integr Plant Biol, 61(5): 541-563. |
| [24] | Nonogaki M, Sall K, Nambara E, Nonogaki H. 2014. Amplification of ABA biosynthesis and signaling through a positive feedback mechanism in seeds. Plant J, 78(3): 527-539. |
| [25] | O’Malley R C, Huang S C, Song L, Lewsey M G, Bartlett A, Nery J R, Galli M, Gallavotti A, Ecker J R. 2016. Cistrome and epicistrome features shape the regulatory DNA landscape. Cell, 165(5): 1280-1292. |
| [26] | Onodera Y, Suzuki A, Wu C Y, Washida H, Takaiwa F. 2001. A rice functional transcriptional activator, RISBZ1, responsible for endosperm-specific expression of storage protein genes through GCN4 motif. J Biol Chem, 276(17): 14139-14152. |
| [27] | Saika H, Okamoto M, Miyoshi K, Kushiro T, Shinoda S, Jikumaru Y, Fujimoto M, Arikawa T, Takahashi H, Ando M, Arimura S I, Miyao A, Hirochika H, Kamiya Y, Tsutsumi N, Nambara E, Nakazono M. 2007. Ethylene promotes submergence-induced expression of OsABA8ox1, a gene that encodes ABA 8′- hydroxylase in rice. Plant Cell Physiol, 48(2): 287-298. |
| [28] | Shu K, Liu X D, Xie Q, He Z H. 2016. Two faces of one seed: Hormonal regulation of dormancy and germination. Mol Plant, 9(1): 34-45. |
| [29] | Skubacz A, Daszkowska-Golec A, Szarejko I. 2016. The role and regulation of ABI5 (ABA-insensitive 5) in plant development, abiotic stress responses and phytohormone crosstalk. Front Plant Sci, 7: 1884. |
| [30] | Song S, Wang G F, Wu H, Fan X W, Liang L W, Zhao H, Li S L, Hu Y, Liu H Y, Ayaad M, Xing Y Z. 2020. OsMFT2 is involved in the regulation of ABA signaling mediated seed germination through interacting with OsbZIP23/66/72 in rice. Plant J, 103(2): 532-546. |
| [31] | Sornaraj P, Luang S, Lopato S, Hrmova M. 2016. Basic leucine zipper (bZIP) transcription factors involved in abiotic stresses: A molecular model of a wheat bZIP factor and implications of its structure in function. Biochim Biophy Acta: Genral Subjects, 1860: 46-56. |
| [32] | Sun Y, Fan X Y, Cao D M, Tang W, He K, Zhu J Y, He J X, Bai M Y, Zhu S, Oh E, Patil S, Kim T W, Ji H, Wong W H, Rhee S Y, Wang Z Y. 2010. Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev Cell, 19(5): 765-777. |
| [33] | Tong H N, Chu C C. 2018. Functional specificities of brassinosteroid and potential utilization for crop improvement. Trends Plant Sci, 23(11): 1016-1028. |
| [34] | Tong H N, Xiao Y H, Liu D P, Gao S P, Liu L C, Yin Y H, Jin Y, Qian Q, Chu C C. 2014. Brassinosteroid regulates cell elongation by modulating gibberellin metabolism in rice. Plant Cell, 26(11): 4376-4393. |
| [35] | Tuan P A, Kumar R, Rehal P K, Toora P K, Ayele B T. 2018. Molecular mechanisms underlying abscisic acid/gibberellin balance in the control of seed dormancy and germination in cereals. Front Plant Sci, 9: 668. |
| [36] | Wang C, Liu Q, Shen Y, Hua Y F, Wang J J, Lin J R, Wu M G, Sun T T, Cheng Z K, Mercier R, Wang K. 2019. Clonal seeds from hybrid rice by simultaneous genome engineering of meiosis and fertilization genes. Nat Biotechnol, 37(3): 283-286. |
| [37] | Wang Q, Lin Q B, Wu T, Duan E C, Huang Y S, Yang C Y, Mou C L, Lan J, Zhou C L, Xie K, Liu X, Guo X P, Wang J, Jiang L, Wan J M. 2020. OsDOG1L-3 regulates seed dormancy through the abscisic acid pathway in rice. Plant Sci, 298: 110570. |
| [38] | Wang Y F, Hou Y X, Qiu J H, Wang H M, Wang S, Tang L Q, Tong X H, Zhang J. 2020. Abscisic acid promotes jasmonic acid biosynthesis via a ‘SAPK10-bZIP72-AOC’ pathway to synergistically inhibit seed germination in rice (Oryza sativa). New Phytol, 228(4): 1336-1353. |
| [39] | Wu J H, Zhu C F, Pang J H, Zhang X R, Yang C L, Xia G X, Tian Y C, He C Z. 2014. OsLOL1, a C2C2-type zinc finger protein, interacts with OsbZIP58 to promote seed germination through the modulation of gibberellin biosynthesis in Oryza sativa. Plant J, 80(6): 1118-1130. |
| [40] | Xu H, Li X F, Zhang H, Wang L C, Zhu Z G, Gao J P, Li C S, Zhu Y. 2020. High temperature inhibits the accumulation of storage materials by inducing alternative splicing of OsbZIP58 during filling stage in rice. Plant Cell Environ, 43(8): 1879-1896. |
| [41] | Xu X, Wan W, Jiang G, Xi Y, Huang H, Cai J, Chang Y, Duan C G, Mangrauthia S K, Peng X, Zhu J K, Zhu G. 2019. Nucleocytoplasmic trafficking of theArabidopsis WD40 repeat protein XIW1 regulates ABI5 stability and abscisic acid responses. Mol Plant, 12(12): 1598-1611. |
| [42] | Yadukrishnan P, Datta S. 2020. Light and abscisic acid interplay in early seedling development. New Phytol, 229: 763-769. |
| [43] | Yamamoto M P, Onodera Y, Touno S M, Takaiwa F. 2006. Synergism between RPBF Dof and RISBZ1 bZIP activators in the regulation of rice seed expression genes. Plant Physiol, 141(4): 1694-1707. |
| [44] | Yan A, Chen Z. 2017. The pivotal role of abscisic acid signaling during transition from seed maturation to germination. Plant Cell Rep, 36(5): 689-703. |
| [45] | Yang J C, Zhang J H, Wang Z Q, Zhu Q S, Wang W. 2001. Hormonal changes in the grains of rice subjected to water stress during grain filling. Plant Physiol, 127(1): 315-323. |
| [46] | Yang W Q, Zhang W, Wang X X. 2017. Post-translational control of ABA signalling: The roles of protein phosphorylation and ubiquitination. Plant Biotechnol J, 15(1): 4-14. |
| [47] | Yang X, Yang Y N, Xue L J, Zou M J, Liu J Y, Chen F, Xue H W. 2011. Rice ABI5-like1 regulates abscisic acid and auxin responses by affecting the expression of ABRE-containing genes. Plant Physiol, 156(3): 1397-1409. |
| [48] | Yang Y M, Xu C N, Wang B M, Jia J Z. 2001. Effects of plant growth regulators on secondary wall thickening of cotton fibres. Plant Growth Regul, 35: 233-237. |
| [49] | Yu F F, Wu Y R, Xie Q. 2015. Precise protein post-translational modifications modulate ABI5 activity. Trends Plant Sci, 20(9): 569-575. |
| [50] | Zhang H Y, He H, Wang X C, Wang X F, Yang X Z, Li L, Deng X W. 2011. Genome-wide mapping of the HY5-mediated gene networks in Arabidopsis that involve both transcriptional and post-transcriptional regulation. Plant J, 65(3): 346-358. |
| [51] | Zhang Y, Liu T, Meyer C A, Eeckhoute J, Johnson D S, Bernstein B E, Nusbaum C, Myers R M, Brown M, Li W, Liu X S. 2008. Model- based analysis of ChIP-Seq (MACS). Genome Biol, 9(9): R137. |
| [52] | Zhao H Y, Nie K L, Zhou H P, Yan X J, Zhan Q D, Zheng Y, Song C P. 2020. ABI5 modulates seed germination via feedback regulation of the expression of the PYR/PYL/RCAR ABA receptor genes. New Phytol, 228(2): 596-608. |
| [53] | Zou M J, Guan Y C, Ren H B, Zhang F, Chen F. 2008. A bZIP transcription factor, OsABI5, is involved in rice fertility and stress tolerance. Plant Mol Biol, 66(6): 675-683. |
/
| 〈 |
|
〉 |