RNA-Seq Study Reveals AP2-Domain-Containing Signalling Regulators Involved in Initial Imbibition of Seed Germination in Rice
#These authors contributed equally to this work
Received date: 2019-08-24
Accepted date: 2019-11-20
Online published: 2020-03-31
A number of internal signals are required for seed germination. However, the precise signalling responses in the initial imbibition of seed germination are not yet fully understood in rice. In this study, the RNA sequencing (RNA-Seq) approach was conducted in 8 h imbibed seeds to understand the signalling responses in the initial imbibition of rice seed germination. A total of 563 differentially expressed genes (DEGs) with at least 4-fold change were identified in 8 h imbibed seeds compared to dry seeds. MapMan analysis revealed that the majority of signalling response-related DEGs were hormone- and transcription factor-related genes, in which the largest number of DEGs belong to the AP2-domain-containing regulators, and their expressions were significantly induced in the initial imbibition of seed germination in rice. Moreover, at least five AP2-domain-containing transcription factor OsDREBs were identified in the initial imbibition of rice seed germination, and the expressions of 251 DEGs were putatively regulated by OsDREBs through the dehydration-responsive element (DRE) cis-element assay. It suggested that the OsDREBs might play important roles in the regulation of initial seed imbibition in rice. The identified genes provide a valuable resource to study the signalling regulation of seed germination in the future.
Yongqi He, Jia Zhao, Defeng Feng, Zhibo Huang, Jiaming Liang, Yufei Zheng, Jinping Cheng, Jifeng Ying, Zhoufei Wang . RNA-Seq Study Reveals AP2-Domain-Containing Signalling Regulators Involved in Initial Imbibition of Seed Germination in Rice[J]. Rice Science, 2020 , 27(4) : 302 -314 . DOI: 10.1016/j.rsci.2020.05.006
| [1] | Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. 2003. Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell, 15: 63-78. |
| [2] | Beaudoin N, Serizet C, Gosti F, Giraudat J. 2000. Interactions between abscisic acid and ethylene signaling cascades. Plant Cell, 12(7): 1103-1116. |
| [3] | Bewley J D. 1997. Seed germination and dormancy. Plant Cell, 9(7): 1055-1066. |
| [4] | Challam C, Ghosh T, Rai M, Tyagi W. 2015. Allele mining across DREB1A and DREB1B in diverse rice genotypes suggest a highly conserved pathway inducible by low temperature. J Genet, 94: 231-238. |
| [5] | Chen J Q, Meng X P, Zhang Y, Xia M, Wang X P. 2008. Over-expression of OsDREB genes lead to enhanced drought tolerance in rice. Biotechnol Lett, 30(12): 2191-2198. |
| [6] | Chen Y F, Randlett M D, Findell J L, Schaller G E. 2002. Localization of the ethylene receptor ETR1 to the endoplasmic reticulum of Arabidopsis. J Biol Chem, 277: 19861-19866. |
| [7] | Chew W, Hrmova M, Lopato S. 2013. Role of homeodomain leucine zipper (HD-Zip) IV transcription factors in plant development and plant protection from deleterious environmental factors. Int J Mol Sci, 14(4): 8122-8147. |
| [8] | Chiwocha S D, Cutler A J, Abrams S R, Ambrose S J, Yang J, Ross A R, Kermode A R. 2005. The etr1-2 mutation in Arabidopsis thaliana affects the abscisic acid, auxin, cytokinin and gibberellin metabolic pathways during maintenance of seed dormancy, moist-chilling and germination. Plant J, 42(1): 35-48. |
| [9] | 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. |
| [10] | Dametto A, Sperotto R A, Adamski J M, Blasi É A R, Cargnelutti D, de Oliveira L F V, Ricachenevsky F K, Fregonezi J N, Mariath J E A, da Cruz R P, Margis R, Fett J P. 2015. Cold tolerance in rice germinating seeds revealed by deep RNAseq analysis of contrasting indica genotypes. Plant Sci, 238: 1-12. |
| [11] | Dave A, Hernández M L, He Z, Andriotis V M E, Vaistij F E, Larson T R, Graham I A. 2011. 12-oxo-phytodienoic acid accumulation during seed development represses seed germination in Arabidopsis. Plant Cell, 23(2): 583-599. |
| [12] | Ding Z J, Yan J Y, Li G X, Wu Z C, Zhang S Q, Zheng S J. 2014. WRKY41 controls Arabidopsis seed dormancy via direct regulation of ABI3 transcript levels not downstream of ABA. Plant J, 79(5): 810-823. |
| [13] | Feng C Z, Chen Y, Wang C, Kong Y H, Wu W H, Chen Y F. 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(4): 654-668. |
| [14] | Frey A, Effroy D, Lefebvre V, Seo M, Perreau F, Berger A, Sechet J, To A, North H M, Marion-Poll A. 2012. Epoxycarotenoid cleavage by NCED5 fine-tunes ABA accumulation and affects seed dormancy and drought tolerance with other NCED family members. Plant J, 70(3): 501-512. |
| [15] | Ghassemian M, Nambara E, Cutler S, Kawaide H, Kamiya Y, McCourt P. 2000. Regulation of abscisic acid signaling by the ethylene response pathway in Arabidopsis. Plant Cell, 12(7): 1117-1126. |
| [16] | Gong W, Shen Y P, Ma L G, Pan Y, Du Y L, Wang D H, Yang J Y, Hu L D, Liu X F, Dong C X, Ma L, Chen Y H, Yang X Y, Gao Y, Zhu D M, Tan X L, Mu J Y, Zhang D B, Liu Y L, Dinesh-Kumar S P, Li Y, Wang X P, Gu H Y, Qu L J, Bai S N, Lu Y T, Li J Y, Zhao J D, Zuo J R, Huang H, Deng X W, Zhu Y X. 2004. Genome-wide ORFeome cloning and analysis of Arabidopsis transcription factor genes. Plant Physiol, 135(2): 773-782. |
| [17] | Graeber K, Nakabayashi K, Miatton E, Leubner-Metzger G, Soppe W J J. 2012. Molecular mechanisms of seed dormancy. Plant Cell Environ, 35(10): 1769-1786. |
| [18] | Gutterson N, Reuber T L. 2004. Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol, 7(4): 465-471. |
| [19] | He D L, Wang Q, Wang K, Yang P F. 2015. Genome-wide dissection of the microRNA expression profile in rice embryo during early stages of seed germination. PLoS One, 10(12): e0145424. |
| [20] | He Y A, Li Y P, Cui L X, Xie L X, Zheng C K, Zhou G H, Zhou J J, Xie X Z. 2016. Phytochrome B negatively affects cold tolerance by regulating OsDREB1 gene expression through phytochrome interacting factor-like protein OsPIL16 in rice. Front Plant Sci, 7: 1963. |
| [21] | He Y Q, Cheng J P, He Y, Yang B, Cheng Y H, Yang C, Zhang H S, Wang Z F. 2019. Influence of isopropylmalate synthase OsIPMS1 on seed vigour associated with amino acid and energy metabolism in rice. Plant Biotechnol J, 17(2): 322-337. |
| [22] | Huang Y, Feng C Z, Ye Q, Wu W H, Chen Y F. 2016. Arabidopsis WRKY6 transcription factor acts as a positive regulator of abscisic acid signaling during seed germination and early seedling development. PLoS Genet, 12(2): e1005833. |
| [23] | Inahashi H, Shelley I J, Yamauchi T, Nishiuchi S, Takahashi- Nosaka M, Matsunami M, Ogawa A, Noda Y, Inukai Y. 2018. OsPIN2, which encodes a member of the auxin efflux carrier proteins, is involved in root elongation growth and lateral root formation patterns via the regulation of auxin distribution in rice. Physiol Plant, 164(2): 216-225. |
| [24] | Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg S L. 2013. TopHat2: Accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol, 14(4): R36. |
| [25] | Kim J H, Hyun W Y, Nguyen H N, Jeong C Y, Xiong L, Hong S W, Lee H. 2015. AtMyb7, a subgroup 4 R2R3 Myb, negatively regulates ABA-induced inhibition of seed germination by blocking the expression of the bZIP transcription factor ABI5. Plant Cell Environ, 38(3): 559-571. |
| [26] | Kizis D, Lumbreras V, Pagès M. 2001. Role of AP2/EREBP transcription factors in gene regulation during abiotic stress. FEBS Lett, 498: 187-189. |
| [27] | Kucera B, Cohn M A, Leubner-Metzger G. 2005. Plant hormone interactions during seed dormancy release and germination. Seed Sci Res, 15: 281-307. |
| [28] | Lee K, Lee H G, Yoon S, Kim H U, Seo P J. 2015. The Arabidopsis MYB96 transcription factor is a positive regulator of ABSCISIC ACID-INSENSITIVE4 in the control of seed germination. Plant Physiol, 168(2): 677-689. |
| [29] | Lee S, Cheng H, King K E, Wang W, He Y, Hussain A, Lo J, Harberd N P, Peng J. 2002. Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Gene Dev, 16(5): 646-658. |
| [30] | Li B, Dewey C N. 2011. RSEM: Accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform, 12: 323. |
| [31] | Linkies A, Leubner-Metzger G. 2012. Beyond gibberellins and abscisic acid: How ethylene and jasmonates control seed germination. Plant Cell Rep, 31(2): 253-270. |
| [32] | Liu X D, Zhang H, Zhao Y, Feng Z Y, Li Q, Yang H Q, Luan S, Li J M, He Z H. 2013. Auxin controls seed dormancy through stimulation of abscisic acid signaling by inducing ARF-mediated ABI3 activation in Arabidopsis. Proc Natl Acad Sci USA, 110: 15485-15490. |
| [33] | Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods, 25(4): 402-408. |
| [34] | Magnani E, Sjolander K, Hake S. 2004. From endonucleases to transcription factors: Evolution of the AP2 DNA binding domain in plants. Plant Cell, 16(9): 2265-2277. |
| [35] | Mahender A, Anandan A, Pradhan S K. 2015. Early seedling vigour, an imperative trait for direct-seeded rice: An overview on physio-morphological parameters and molecular markers. Planta, 241(5): 1027-1050. |
| [36] | Matilla A J, Matilla-Vazquez M A. 2008. Involvement of ethylene in seed physiology. Plant Sci, 175: 87-97. |
| [37] | Narsai R, Secco D, Schultz M D, Ecker J R, Lister R, Whelan J. 2017. Dynamic and rapid changes in the transcriptome and epigenome during germination and in developing rice ( Oryza sativa) coleoptiles under anoxia and re-oxygenation. Plant J, 89(4): 805-824. |
| [38] | Nee G, Xiang Y, Soppe W J J. 2017. The release of dormancy, a wake-up call for seeds to germinate. Curr Opin Plant Biol, 35: 8-14. |
| [39] | 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. |
| [40] | Preston J, Tatematsu K, Kanno Y, Hobo T, Kimura M, Jikumaru Y, Yano R, Kamiya Y, Nambara E. 2009. Temporal expression patterns of hormone metabolism genes during imbibition of Arabidopsis thaliana seeds: A comparative study on dormant and non-dormant accessions. Plant Cell Physiol, 50(10): 1786-1800. |
| [41] | Ren H, Park M Y, Spartz A K, Wong J H, Gray W M. 2018. A subset of plasma membrane-localized PP2C.D phosphatases negatively regulate SAUR-mediated cell expansion in Arabidopsis. PLoS Genet, 14(6): e1007455. |
| [42] | Reyes J L, Chua N H. 2007. ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant J, 49(4): 592-606. |
| [43] | Rushton P J, Somssich I E, Ringler P, Shen Q X J. 2010. WRKY transcription factors. Trends Plant Sci, 15(5): 247-258. |
| [44] | Schuler M A, Werck-Reichhart D. 2003. Functional genomics of P450s. Annu Rev Plant Biol, 54: 629-667. |
| [45] | Shimono M, Koga H, Akagi A, Hayashi N, Goto S, Sawada M, Kurihara T, Matsushita A, Sugano S, Jiang C J, Kaku H, Inoue H, Takatsuji H. 2012. Rice WRKY45 plays important roles in fungal and bacterial disease resistance. Mol Plant Pathol, 13(1): 83-94. |
| [46] | Shinozaki K, Yamaguchi-Shinozaki K. 2000. Molecular responses to dehydration and low temperature: Differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol, 3(3): 217-223. |
| [47] | Shu K, Zhang H W, Wang S F, Chen M L, Wu Y R, Tang S Y, Liu C Y, Feng Y Q, Cao X F, Xie Q. 2013. ABI4 regulates primary seed dormancy by regulating the biogenesis of abscisic acid and gibberellins in Arabidopsis. PLoS Genet, 9(6): e1003577. |
| [48] | 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. |
| [49] | Spartz A K, Ren H, Park M Y, Grandt K N, Lee S H, Murphy A S, Sussman M R, Overvoorde P J, Gray W M. 2014. SAUR inhibition of PP2C-D phosphatases activates plasma membrane H+-ATPases to promote cell expansion in Arabidopsis. Plant Cell, 26(5): 2129-2142. |
| [50] | Stortenbeker N, Bemer M. 2019. The SAUR gene family: The plant’s toolbox for adaptation of growth and development. J Exp Bot, 70(1): 17-27. |
| [51] | Subbiah V, Reddy K J. 2010. Interactions between ethylene, abscisic acid and cytokinin during germination and seedling establishment in Arabidopsis. J Biosci, 35(3): 451-458. |
| [52] | Tao Z, Kou Y J, Liu H B, Li X H, Xiao J H, Wang S P. 2011. OsWRKY45 alleles play different roles in abscisic acid signalling and salt stress tolerance but similar roles in drought and cold tolerance in rice. J Exp Bot, 62(14): 4863-4874. |
| [53] | Thomashow M F. 2001. So what’s new in the field of plant cold acclimation? Lots! Plant Physiol, 125(1): 89-93. |
| [54] | Usadel B, Poree F, Nagel A, Lohse M, Czedik-Eysenberg A, Stitt M. 2009. A guide to using MapMan to visualize and compare omics data in plants: A case study in the crop species, maize. Plant Cell Environ, 32(9): 1211-1229. |
| [55] | Viana V E, Marini N, Finatto T, Ezquer I, Busanello C, dos Santos R S, Pegoraro C, Colombo L, Costa de Oliveira A. 2017. Iron excess in rice: From phenotypic changes to functional genomics of WRKY transcription factors. Genet Mol Res, 16(3): gmr16039694. |
| [56] | Wang L L, Guo M X, Li Y, Ruan W Y, Mo X R, Wu Z C, Sturrock C J, Yu H, Lu C G, Peng J R, Mao C Z. 2018. LARGE ROOT ANGLE1, encoding OsPIN2, is involved in root system architecture in rice. J Exp Bot, 69(3): 385-397. |
| [57] | Wang Z F, Wang J F, Bao Y M, Wu Y Y, Zhang H S. 2011. Quantitative trait loci controlling rice seed germination under salt stress. Euphytica, 178(3): 297-307. |
| [58] | Ward J M, Smith A M, Shah P K, Galanti S E, Yi H, Demianski A J, van der Graaff E, Keller B, Neff M M. 2006. A new role for the Arabidopsis AP2 transcription factor, LEAFY PETIOLE, in gibberellin-induced germination is revealed by the misexpression of a homologous gene, SOB2/DRN-LIKE. Plant Cell, 18(1): 29-39. |
| [59] | Wei T, He Z L, Tan X Y, Liu X, Yuan X, Luo Y F, Hu S N. 2015. An integrated RNA-Seq and network study reveals a complex regulation process of rice embryo during seed germination. Biochem Biophy Res Commun, 464(1): 176-181. |
| [60] | Wilson R L, Kim H, Bakshi A, Binder B M. 2014. The ethylene receptors ETHYLENE RESPONSE1 and ETHYLENE RESPONSE2 have contrasting roles in seed germination of Arabidopsis during salt stress. Plant Physiol, 165(3): 1353-1366. |
| [61] | Wuriyanghan H, Zhang B, Cao W H, Ma B, Lei G, Liu Y F, Wei W, Wu H J, Chen L J, Chen H W, Cao Y R, He S J, Zhang W K, Wang X J, Chen S Y, Zhang J S. 2009. The ethylene receptor ETR2 delays floral transition and affects starch accumulation in rice. Plant Cell, 21(5): 1473-1494. |
| [62] | Yau C P, Wang L, Yu M, Zee S Y, Yip W K. 2004. Differential expression of three genes encoding an ethylene receptor in rice during development, and in response to indole-3-acetic acid and silver ions. J Exp Bot, 55: 547-556. |
| [63] | Yaish M W, El-kereamy A, Zhu T, Beatty P H, Good A G, Bi Y M, Rothstein S J. 2010. The APETALA-2-like transcription factor OsAP2-39 controls key interactions between abscisic acid and gibberellin in rice. PLoS Genet, 6(9): e1001098. |
| [64] | Yamauchi Y, Takeda-Kamiya N, Hanada A, Ogawa M, Kuwahara A, Seo M, Kamiya Y, Yamaguchi S. 2007. Contribution of gibberellin deactivation by AtGA2ox2 to the suppression of germination of dark-imbibed Arabidopsis thaliana seeds. Plant Cell Physiol, 48(3): 555-561. |
| [65] | Yang J Y, Chung M C, Tu C Y, Leu W M. 2002. OSTF1: A HD-GL2 family homeobox gene is developmentally regulated during early embryogenesis in rice. Plant Cell Physiol, 43(6): 628-638. |
| [66] | Yu M, Yau C P, Yip W K. 2017. Differentially localized rice ethylene receptors OsERS1 and OsETR2 and their potential role during submergence. Plant Signal Behav, 12(8): e1356532. |
| [67] | Zhang A P, Qian Q, Gao Z Y. 2018. Research advances on rice seed vigor. Chin J Rice Sci, 32(3): 296-303. (in Chinese with English abstract) |
| [68] | Zhang S X, Haider I, Kohlen W, Jiang L, Bouwmeester H, Meijer A H, Schluepmann H, Liu C M, Ouwerkerk P B F. 2012. Function of the HD-Zip I gene Oshox22 in ABA-mediated drought and salt tolerances in rice. Plant Mol Biol, 80: 571-585. |
| [69] | Zheng Y, Schumaker K S, Guo Y. 2012. Sumoylation of transcription factor MYB30 by the small ubiquitin-like modifier E3 ligase SIZ1 mediates abscisic acid response in Arabidopsis thaliana. Proc Natl Acad Sci USA, 109: 12822-12827. |
| [70] | Zou X L, Neuman D, Shen Q J. 2008. Interactions of two transcriptional repressors and two transcriptional activators in modulating gibberellin signaling in aleurone cells. Plant Physiol, 148: 176-186. |
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