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HY5 and ABI5 transcription factors physically interact to fine tune light and ABA signaling in Arabidopsis

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Abstract

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Cross-talk between light and ABA signaling is mediated by physical interaction between HY5 and ABI5 Arabidopsis.

Abstract

Plants undergo numerous transitions during their life-cycle and have developed a very complex network of signaling to integrate information from their surroundings to effectively survive in the ever-changing environment. Light signaling is one of the crucial factors that govern the plant growth and development from the very first step of that is from seedling germination to the flowering. Similarly, Abscisic acid (ABA) signaling transduces the signals from external unfavorable condition to the internal developmental pathways and is crucial for regulation of seed maturation, dormancy germination and early seedling development. These two fundamental factors coordinately regulate plant wellbeing, but the underlying molecular mechanisms that drive this regulation are poorly understood. Here, we identified that two bZIP transcription factors, ELONGATED HYPOCOTYLE 5 (HY5), a positive regulator of light signaling and ABA-INSENSITIVE 5 (ABI5), a positive regulator of ABA signaling interacts and integrates the two pathways together. Our phenotypic data suggest that ABI5 may act as a negative regulator during photomorphogenesis in contrast, HY5 acts as a positive regulator of ABA signaling in an ABA dependent manner. We further showed that over-expression of HY5 leads to ABA-hypersensitive phenotype and late flowering phenotype. Taken together, our data provides key insights regarding the mechanism of interaction between ABI5-HY5 that fine tunes the stress and developmental response in Arabidopsis.

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References

  • Abbas N, Maurya JP, Senapati D, Gangappa SN, Chattopadhyay S (2014) Arabidopsis CAM7 and HY5 physically interact and directly bind to the HY5 promoter to regulate its expression and thereby promote photomorphogenesis. Plant Cell 26:1036–1052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ang LH, Chattopadhyay S, Wei N, Oyama T, Okada K, Batschauer A, Deng XW (1998) Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. Mol Cell 1:213–222

    Article  CAS  PubMed  Google Scholar 

  • Aron D (1949) Copper enzymes isolated chloroplasts, polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  Google Scholar 

  • Beaudoin N, Serizet C, Gosti F, Giraudat J (2000) Interactions between abscisic acid and ethylene signaling cascades. Plant Cell 12:1103–1115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhatia C, Pandey A, Gaddam SR, Hoecker U, Trivedi PK (2018) Low temperature-enhanced flavonol synthesis requires light-associated regulatory components in Arabidopsis thaliana. Plant Cell Physiol 59:2099–2112

    Article  CAS  PubMed  Google Scholar 

  • Bursch K, Toledo-Ortiz G, Pireyre M, Lohr M, Braatz C, Johansson H (2020) Identification of BBX proteins as rate-limiting cofactors of HY5. Nat Plants 9:921–928

    Article  CAS  Google Scholar 

  • Chattopadhyay S, Ang LH, Puente P, Deng XW, Wei N (1998) Arabidopsis bZIP protein HY5 directly interacts with light-responsive promoters in mediating light control of gene expression. Plant Cell 10:673–683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen H, Xiong L (2008) Role of HY5 in abscisic acid response in seeds and seedlings. Plant Signal Behav 3:986–988

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen H, Zhang JY, Neff MM, Hong SW, Zhang HY, Deng XW, Xiong LM (2008) Integration of light and abscisic acid signaling during seed germination and early seedling development. Proc Natl Acad Sci USA 105:4495–4500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen QB, Bai L, Wang WJ, Shi HZ, Botella JR, Zhan QD, Liu K, Yang HQ, Song CP (2021) COP1 promotes ABA-induced stomatal closure by modulating the abundance of ABI/HAB and AHG3 phosphatases. New Phytol 229:2035–2049

    Article  CAS  PubMed  Google Scholar 

  • Datta S, Hettiarachchi C, Johansson H, Holm M (2007) SALT TOLERANCE HOMOLOG2 a B-box protein in Arabidopsis that activates transcription and positively regulates light-mediated development. Plant Cell 19:3242–3255de

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finkelstein RR, Lynch TJ (2000) The arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12:599–609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujii H, Verslues PE, Zhu J-K (2007) Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis. Plant Cell 19:485–494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gangappa SN, Botto JF (2016) The multifaceted roles of HY5 in plant growth and development. Mol Plant 9:1353–1365

    Article  CAS  PubMed  Google Scholar 

  • Gangappa SN, Crocco CD, Johansson H, Datta S, Hettiarachchi C, Holm M, Botto JF (2013) The Arabidopsis B-BOX protein BBX25 interacts with HY5, negatively regulating BBX22 expression to suppress seedling photomorphogenesis. Plant Cell 25:1243–1257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hardtke CS, Gohda K, Osterlund MT, Oyama T, Okada K, Deng XW (2000) HY5 stability and activity in Arabidopsis is regulated by phosphorylation in its COP1 binding domain. EMBO J 19:4997–5006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holtan HE, Bandong S, Marion CM, Adam L, Tiwari S, Shen Y, Maloof JN, Maszle DR, Ohto MA, Preuss S, Meister R, Petracek M, Repetti PP, Reuber TL, Ratcliffe OJ, Khanna R (2011) BBX32, an Arabidopsis B-Box protein, functions in light signaling by suppressing HY5-regulated gene expression and interacting with STH2/BBX21. Plant Physiol 156:2109–2123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jakoby M, Weisshaar B, Droge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7:106–111

    Article  CAS  PubMed  Google Scholar 

  • Ju L, Jing YX, Shi PT, Liu J, Chen JS, Yan JJ, Chu JF, Chen KM, Sun JQ (2019) JAZ proteins modulate seed germination through interaction with ABI5 in bread wheat and Arabidopsis. New Phytol 223:246–260

    Article  CAS  PubMed  Google Scholar 

  • Lau OS, Deng XW (2010) Plant hormone signaling lightens up: integrators of light and hormones. Curr Opin Plant Biol 13:571–577

    Article  CAS  PubMed  Google Scholar 

  • Lee J, He K, Stolc V, Lee H, Figueroa P, Gao Y, Tongprasit W, Zhao H, Lee I, Deng XW (2007) Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell 19:731–749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lim G-H, Hoey T, Zhu S, Clavel M, Yu K, Navarre D, Kachroo A, Deragon J-M, Kachroo P (2018) COP1, a negative regulator of photomorphogenesis, positively regulates plant disease resistance via double-stranded RNA binding proteins. Plos Pathog 14(3):e1006894

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu H, Stone SL (2013) Cytoplasmic degradation of the Arabidopsis transcription factor ABSCISIC ACID INSENSITIVE 5 is mediated by the RING-type E3 Ligase KEEP ON GOING. J Biol Chem 288:20267–20279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lopez-Molina L, Mongrand B, 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

    Article  CAS  PubMed  Google Scholar 

  • 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 50:1345–1363

    Article  CAS  PubMed  Google Scholar 

  • Nambara E, Hayama R, Tsuchiya Y, Nishimura M, Kawaide H, Kamiya Y, Naito S (2000) The role of ABI3 and FUS3 loci in Arabidopsis thaliana on phase transition from late embryo development to germination. Dev Biol 220:412–423

    Article  CAS  PubMed  Google Scholar 

  • Osterlund MT, Ang LH, Deng XW (1999) The role of COP1 in repression of Arabidopsis photomorphogenic development. Trends Cell Biol 9:113–118

    Article  CAS  PubMed  Google Scholar 

  • Paik I, Huq E (2019) Plant photoreceptors: multi-functional sensory proteins and their signaling networks. Semin Cell Dev Biol 92:114–121

    Article  CAS  PubMed  Google Scholar 

  • Pan JJ, Hu YR, Wang HP, Guo Q, Chen YI, Howe GA, Yu DQ (2020) Molecular mechanism underlying the synergetic effect of jasmonate on abscisic acid signaling during seed germination in Arabidopsis. Plant Cell 32:3846–3865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Podolec R, Ulm R (2018) Photoreceptor-mediated regulation of the COP1/SPA E3 ubiquitin ligase. Curr Opin Plant Biol 45:18–25

    Article  CAS  PubMed  Google Scholar 

  • Raghuram B, Sheikh AH, Rustagi Y, Sinha AK (2015) MicroRNA biogenesis factor DRB1 is a phosphorylation target of mitogen activated protein kinase MPK3 in both rice and Arabidopsis. FEBS J 282:521–536

    Article  CAS  PubMed  Google Scholar 

  • Rasmussen A, Mason MG, Cuyper CD, Brewer PB, Herold S, Agusti J, Geelen D, Greb T, Goormachtig S, Beeckman T (2012) Strigolactones suppress adventitious rooting in Arabidopsis and pea. Plant Physiol 158:1976–1987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schindler U, Menkens AE, Beckmann H, Ecker JR, Cashmore AR (1992) Heterodimerization between light-regulated and ubiquitously expressed Arabidopsis GBF bZIP proteins. EMBO J 11:1261–1273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sethi V, Raghuram B, Sinha AK, Chattopadhyay S (2014) A mitogen-activated protein kinase cascade module, MKK3-MPK6 and MYC2, is involved in blue light-mediated seedling development in Arabidopsis. Plant Cell 26:3343–3357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shang Y, Yan L, Liu ZQ, Cao Z, Mei C, Xin Q, Wu FQ, Wang XF, Du SY, Jiang T, Zhang XF, Zhao R, Sun HL, Liu R, Yu YT, Zhang DP (2010) The Mg-Chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition. Plant Cell 22:1909–1935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi QM, Yang X, Song L, Xue HW (2011) Arabidopsis MSBP1 is activated by HY5 and HYH and is involved in photomorphogenesis and brassinosteroid sensitivity regulation. Mol Plant 4:1092–1104

    Article  CAS  PubMed  Google Scholar 

  • Shu K, Chen F, Zhou WG, Luo XF, Dai YJ, Shuai HW, Yang WY (2018) ABI4 regulates the floral transition independently of ABI5 and ABI3. Mol Biol Rep 45:2727–2731

    Article  CAS  PubMed  Google Scholar 

  • Singh P, Sinha AK (2016) A positive feedback loop governed by SUB1A1 interaction with MITOGEN-ACTIVATED PROTEIN KINASE3 imparts submergence tolerance in rice. Plant Cell 28:1127–1143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh A, Ram H, Abbas N, Chattopadhyay S (2012) Molecular interactions of GBF1 with HY5 and HYH proteins during light-mediated seedling development in Arabidopsis thaliana. J Biol Chem 287:25995–26009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Skubacz A, Daszkowska-Golec A, Szarejko L (2016) The role and regulation of ABI5 (ABA-Insensitive 5) in plant development, abiotic stress responses and phytohormone crosstalk. Front Plant Sci 7:1884

    Article  PubMed  PubMed Central  Google Scholar 

  • Vishwakarma K, Upadhyay N, Kumar N, Yadav G, Singh J, Mishra RK, Kumar V, Verma R, Upadhyay RG, Pandey M, Sharma S (2017) Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front Plant Sci 8:161

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang YP, Li L, Ye TT, Lu YM, Chen X, Wu Y (2013) The inhibitory effect of ABA on floral transition is mediated by ABI5 in Arabidopsis. J Exp Bot 64:675–684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang WJ, Chen QB, Botella JR, Guo SY (2019) Beyond light: insights into the role of constitutively photomorphogenic1 in plant hormonal signaling. Front Plant Sci 10:557

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang TJ, Huang S, Zhang A, Guo P, Liu Y, Xu C, Cong W, Liu B, Xu XY (2021) JMJ17–WRKY40 and HY5–ABI5 modules regulate the expression of ABA-responsive genes in Arabidopsis. New Phytol 230:567–584

    Article  CAS  PubMed  Google Scholar 

  • Wit M, Galvao VC, Fankhauser C (2016) Light-mediated hormonal regulation of plant growth and development. Annu Rev Plant Biol 67(67):513–537

    Article  PubMed  CAS  Google Scholar 

  • Xu DQ, Li JG, Gangappa SN, Hettiarachchi C, Lin F, Andersson MX, Jiang Y, Deng XW, Holm M (2014) Convergence of light and ABA signaling on the ABI5 promoter. Plos Genet 10(2):e1004197

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xu DQ, Jiang Y, Li J, Holm M, Deng XW (2018) The B-Box domain protein BBX21 promotes photomorphogenesis. Plant Physiol 176:2365–2375

    Article  CAS  PubMed  Google Scholar 

  • Xu D, Wu D, Li XH, Jiang YE, Tian T, Chen QS, Ma L, Wang HY, Deng XW, Li G (2020) Light and abscisic acid coordinately regulate greening of seedlings(1)(OPEN). Plant Physiol 183:1281–1294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yadukrishnan P, Rahul PV, Datta S (2020a) HY5 suppresses, rather than promotes, abscisic acid-mediated inhibition of postgermination seedling development. Plant Physiol 184:574–578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yadukrishnan P, Rahul PV, Ravindran N, Bursch K, Johansson H, Datta S (2020b) CONSTITUTIVELY PHOTOMORPHOGENIC1 promotes ABA-mediated inhibition of post-germination seedling establishment. Plant J 103:481–496

    Article  CAS  PubMed  Google Scholar 

  • Yu YW, Wang J, Zhang ZJ, Quan RD, Zhang HW, Deng XW, Ma LG, Huang RF (2013) Ethylene promotes hypocotyl growth and HY5 degradation by enhancing the movement of COP1 to the nucleus in the light. Plos Genet 9(12):e1004025

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yu F, Li M, He DL, Yang PF (2021) Advances on post-translational modifications involved in seed germination. Front Plant Sci 12:362

    Article  Google Scholar 

  • Zhang HY, He H, Wang XC, Wang XF, Yang XZ, Li L, Deng XW (2011) Genome-wide mapping of the HY5-mediated genenetworks in Arabidopsis that involve both transcriptional and post-transcriptional regulation. Plant J 65:346–358

    Article  CAS  PubMed  Google Scholar 

  • Zhao X, Dou L, Gong Z, Wang X, Mao T (2019) BES1 hinders ABSCISIC ACID INSENSITIVE5 and promotes seed germination in Arabidopsis. New Phytol 221:908–918

    Article  CAS  PubMed  Google Scholar 

  • Zhao X, Heng Y, Wang X, Deng X, Xu D (2020) A positive feedback loop of BBX11–BBX21–HY5 promotes photomorphogenic development in Arabidopsis. Plant Commun 1:100045

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank Dr. Prabodh Kumar Trivedi and Dr. Chitra Bhatia for kindly providing the hy5-215 and OE-HY5 transgenic seeds. We would like to thank NIPGR confocal imaging facility, DNA sequencing facility and radioisotope division for their constant help and support.

Funding

The research work is supported by the core grant of National Institute of Plant Genome Research from Department of Biotechnology (DBT) Government of India. PKB thanks Department of Biotechnology, Govt. of India while DV thanks University Grants Commission, Govt. of India for fellowship. DS thanks Department of Science and Technology (DST), Govt. of India for inspire faculty position. AKS thanks Department of Biotechnology, Govt. of India for the TATA Innovation fellowship.

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PKB and AKS designed the research. PKB, DV and DS performed the experiments. PKB wrote the manuscript with inputs from DS. Final manuscript was edited and approved by AKS. All authors have read and approved the final manuscript.

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Correspondence to Alok Krishna Sinha.

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Bhagat, P.K., Verma, D., Sharma, D. et al. HY5 and ABI5 transcription factors physically interact to fine tune light and ABA signaling in Arabidopsis. Plant Mol Biol 107, 117–127 (2021). https://doi.org/10.1007/s11103-021-01187-z

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  • DOI: https://doi.org/10.1007/s11103-021-01187-z

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