Casein kinase 1 AELs promote senescence by enhancing ethylene biosynthesis through phosphorylating WRKY22 transcription factor
Guo-Qing Zhu
Shanghai Collaborative Innovation Center of Agri-Seeds, Joint Center for Single Cell Biology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, 200240 China
Search for more papers by this authorLi Qu
Shanghai Collaborative Innovation Center of Agri-Seeds, Joint Center for Single Cell Biology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, 200240 China
Search for more papers by this authorCorresponding Author
Hong-Wei Xue
Shanghai Collaborative Innovation Center of Agri-Seeds, Joint Center for Single Cell Biology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, 200240 China
Author for correspondence:
Hong-Wei Xue
Email:[email protected]
Search for more papers by this authorGuo-Qing Zhu
Shanghai Collaborative Innovation Center of Agri-Seeds, Joint Center for Single Cell Biology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, 200240 China
Search for more papers by this authorLi Qu
Shanghai Collaborative Innovation Center of Agri-Seeds, Joint Center for Single Cell Biology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, 200240 China
Search for more papers by this authorCorresponding Author
Hong-Wei Xue
Shanghai Collaborative Innovation Center of Agri-Seeds, Joint Center for Single Cell Biology, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, 200240 China
Author for correspondence:
Hong-Wei Xue
Email:[email protected]
Search for more papers by this authorSee also the Commentary on this article by Mei & Wang, 244: 5–6.
Summary
- Leaf senescence is a complex process regulated by developmental and environmental factors, and plays a pivotal role in the development and life cycle of higher plants. Casein kinase 1 (CK1) is a highly conserved serine/threonine protein kinase in eukaryotes and functions in various cellular processes including cell proliferation, light signaling and hormone effects of plants. However, the biological function of CK1 in plant senescence remains unclear.
- Through systemic genetic and biochemical studies, we here characterized the function of Arabidopsis EL1-like (AEL), a CK1, in promoting leaf senescence by stimulating ethylene biosynthesis through phosphorylating transcription factor WRKY22. Seedlings lacking or overexpressing AELs presented delayed or accelerated leaf senescence, respectively.
- AELs interact with and phosphorylate WRKY22 at Thr57, Thr60 and Ser69 residues to enhance whose transactivation activity. Being consistent, increased or suppressed phosphorylation of WRKY22 resulted in the promoted or delayed leaf senescence. WRKY22 directly binds to promoter region and stimulates the transcription of 1-amino-cyclopropane-1-carboxylate synthase 7 gene to promote ethylene level and hence leaf senescence.
- Our studies demonstrated the crucial role of AEL-mediated phosphorylation in regulating ethylene biosynthesis and promoting leaf senescence by enhancing WRKY22 transactivation activity, which helps to elucidate the fine-controlled ethylene biosynthesis and regulatory network of leaf senescence.
Open Research
Data availability
The data in this study are included in the main text or in the Supporting Information.
Supporting Information
Filename | Description |
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nph19785-sup-0001-Supinfo.docxWord 2007 document , 4.3 MB |
Fig. S1 Arabidopsis EL1-like promote dark-induced leaf senescence. Fig. S2 Arabidopsis EL1-like interact with WRKY22. Fig. S3 WRKY22 involves the Arabidopsis EL1-like effect on dark-induced leaf senescence. Fig. S4 Arabidopsis EL1-like phosphorylates WRKY22. Fig. S5 Arabidopsis EL1-like phosphorylate WRKY22 at the N-terminal region. Fig. S6 Residues Thr57, Thr60 and Ser69 of WRKY22 are major phosphosites by Arabidopsis EL1-like. Fig. S7 Real-time quantitative polymerase chain reaction and western blot analysis of WRKY22 expression in different transgenic materials. Fig. S8 Thr57, Thr60 and Ser69 residues of WRKY22 are essential for dark-induced senescence. Fig. S9 WRKY22 binds to 1-amino-cyclopropane-1-carboxylate synthase 7 promoter. Fig. S10 Biacore analysis revealed that phosphorylation does not affect the DNA binding ability of WRKY22. Fig. S11 WRKY22 promotes 1-amino-cyclopropane-1-carboxylate synthase 7 transcription through binding promoter. Table S1 Primers used in this study. Please note: Wiley is not responsible for the content or functionality of any Supporting Information supplied by the authors. Any queries (other than missing material) should be directed to the New Phytologist Central Office. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- Allen JJ, Li MQ, Brinkworth CS, Paulson JL, Wang D, Hubner A, Chou WH, Davis RJ, Burlingame AL, Messing RO et al. 2007. A semisynthetic epitope for kinase substrates. Nature Methods 4: 511–516.
- Bakshi M, Oelmuller R. 2014. WRKY transcription factors: Jack of many trades in plants. Plant Signaling & Behavior 9: e27700.
- Buchanan-Wollaston V, Earl S, Harrison E, Mathas E, Navabpour S, Page T, Pink D. 2003. The molecular analysis of leaf senescence-a genomics approach. Plant Biotechnology Journal 1: 3–22.
- Cai YH, Chen XJ, Xie K, Xing QK, Wu YW, Li J, Du CH, Sun ZX, Guo ZJ. 2014. Dlf1, a WRKY transcription factor, is involved in the control of flowering time and plant height in rice. PLoS ONE 9: e102529.
- Cao J, Liu HR, Tan SY, Li ZH. 2023. Transcription factors-regulated leaf senescence: current knowledge, challenges and approaches. International Journal of Molecular Sciences 24: 9245.
- Chai JY, Liu J, Zhou J, Xing D. 2014. Mitogen-activated protein kinase 6 regulates NPR1 gene expression and activation during leaf senescence induced by salicylic acid. Journal of Experimental Botany 65: 6513–6528.
- Chen F, Hu Y, Vannozzi A, Wu KC, Cai HY, Qin Y, Mullis A, Lin ZG, Zhang LS. 2017. The WRKY transcription factor family in model plants and crops. Critical Reviews in Plant Sciences 36: 311–335.
- Chen H, Lai ZB, Shi JW, Xiao Y, Chen ZX, Xu XP. 2010. Roles of Arabidopsis WRKY18, WRKY40 and WRKY60 transcription factors in plant responses to abscisic acid and abiotic stress. BMC Plant Biology 10: 281.
- Chen HH, Qu L, Xu ZH, Zhu JK, Xue HW. 2018. EL1-like casein kinases suppress ABA signaling and responses by phosphorylating and destabilizing the ABA receptors PYR/PYLs in Arabidopsis. Molecular Plant 11: 706–719.
- Chen WQ, Provart NJ, Glazebrook J, Katagiri F, Chang HS, Eulgem T, Mauch F, Luan S, Zou GZ, Whitham SA et al. 2002. Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14: 559–574.
- Cheng HT, Liu HB, Deng Y, Xiao JH, Li XH, Wang SP. 2015. The WRKY45-2 WRKY13 WRKY42 transcriptional regulatory cascade is required for rice resistance to fungal pathogen. Plant Physiology 167: 1087–1099.
- Cheng XK, Zhao YX, Jiang QS, Yang J, Zhao WS, Taylor IA, Peng YL, Wang DL, Liu JF. 2019. Structural basis of dimerization and dual W-box DNA recognition by rice WRKY domain. Nucleic Acids Research 47: 4308–4318.
- Cho H, Ryu H, Rho S, Hill K, Smith S, Audenaert D, Park J, Han S, Beeckman T, Bennett MJ et al. 2014. A secreted peptide acts on BIN2-mediated phosphorylation of ARFs to potentiate auxin response during lateral root development. Nature Cell Biology 16: 66–76.
- Chujo T, Miyamoto K, Ogawa S, Masuda Y, Shimizu T, Kishi-Kaboshi M, Takahashi A, Nishizawa Y, Minami E, Nojiri H et al. 2014. Overexpression of phosphomimic mutated OsWRKY53 leads to enhanced blast resistance in rice. PLoS ONE 9: e98737.
- Clough SJ, Bent AF. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16: 735–743.
- Eulgem T, Rushton PJ, Robatzek S, Somssich IE. 2000. The WRKY superfamily of plant transcription factors. Trends in Plant Science 5: 199–206.
- Felix G, Grosskopf DG, Regenass M, Boller T. 1991. Rapid changes of protein phosphorylation are involved in transduction of the elicitor signal in plant cells. Proceedings of the National Academy of Sciences, USA 88: 8831–8834.
- Gan SS, Amasino RM. 1997. Making sense of senescence (molecular genetic regulation and manipulation of leaf senescence). Plant Physiology 113: 313–319.
- Guo Y, Cai Z, Gan S. 2004. Transcriptome of Arabidopsis leaf senescence. Plant, Cell & Environment 27: 521–549.
- Guo YF, Gan SS. 2014. Translational researches on leaf senescence for enhancing plant productivity and quality. Journal of Experimental Botany 65: 3901–3913.
- Han L, Li GJ, Yang KY, Mao GH, Wang RQ, Liu YD, Zhang SQ. 2010. Mitogen-activated protein kinase 3 and 6 regulate Botrytis cinerea-induced ethylene production in Arabidopsis. The Plant Journal 64: 114–127.
- Hao YJ, Song QX, Chen HW, Zou HF, Wei W, Kang XS, Ma BA, Zhang WK, Zhang JS, Chen SY. 2010. Plant NAC-type transcription factor proteins contain a NARD domain for repression of transcriptional activation. Planta 232: 1033–1043.
- Hortensteiner S, Feller U. 2002. Nitrogen metabolism and remobilization during senescence. Journal of Experimental Botany 53: 927–937.
- Huang H, Liu B, Liu LY, Song SS. 2017. Jasmonate action in plant growth and development. Journal of Experimental Botany 68: 1349–1359.
- Kim J, Kim JH, Lyu JI, Woo HR, Lim PO. 2018. New insights into the regulation of leaf senescence in Arabidopsis. Journal of Experimental Botany 69: 787–799.
- Knippschild U, Gocht A, Wolff S, Huber N, Lohler J, Stoter M. 2005. The casein kinase 1 family: participation in multiple cellular processes in eukaryotes. Cellular Signalling 17: 675–689.
- Lee IC, Hong SW, Whang SS, Lim PO, Nam HG, Koo JC. 2011. Age-dependent action of an ABA-inducible receptor kinase, RPK1, as a positive regulator of senescence in Arabidopsis leaves. Plant & Cell Physiology 52: 651–662.
- Li G, Meng X, Wang R, Mao G, Han L, Liu Y, Zhang S. 2012. Dual-level regulation of ACC synthase activity by MPK3/MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis. PLoS Genetics 8: e1002767.
- Lim PO, Kim HJ, Nam HG. 2007. Leaf senescence. Annual Review of Plant Biology 58: 115–136.
- Lim PO, Woo HR, Nam HG. 2003. Molecular genetics of leaf senescence in Arabidopsis. Trends in Plant Science 8: 272–278.
- Lin JF, Wu SH. 2004. Molecular events in senescing Arabidopsis leaves. The Plant Journal 39: 612–628.
- Liu YD, Zhang SQ. 2004. Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16: 3386–3399.
- Llorca CM, Potschin M, Zentgraf U. 2014. bZIPs and WRKYs: two large transcription factor families executing two different functional strategies. Frontiers in Plant Science 5: 169.
- Lohman KN, Gan SS, John MC, Amasino RM. 1994. Molecular analysis of natural leaf senescence in Arabidopsis thaliana. Physiologia Plantarum 92: 322–328.
- Mao GH, Meng XZ, Liu YD, Zheng ZY, Chen ZX, Zhang SQ. 2011. Phosphorylation of a WRKY transcription factor by two pathogen-responsive mapks drives phytoalexin biosynthesis in Arabidopsis. Plant Cell 23: 1639–1653.
- Matsuoka D, Yasufuku T, Furuya T, Nanmori T. 2015. An abscisic acid inducible Arabidopsis MAPKKK, MAPKKK18 regulates leaf senescence via its kinase activity. Plant Molecular Biology 87: 565–575.
- Mayr B, Montminy M. 2001. Transcriptional regulation by the phosphorylation-dependent factor CREB. Nature Reviews Molecular Cell Biology 2: 599–609.
- Miao Y, Laun T, Zimmermann P, Zentgraf U. 2004. Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant Molecular Biology 55: 853–867.
- Niu F, Cui X, Zhao P, Sun M, Yang B, Deyholos MK, Li Y, Zhao X, Jiang YQ. 2020. WRKY42 transcription factor positively regulates leaf senescence through modulating SA and ROS synthesis in Arabidopsis thaliana. The Plant Journal 104: 171–184.
- Noh YS, Amasino RM. 1999. Identification of a promoter region responsible for the senescence-specific expression of SAG12. Plant Molecular Biology 41: 181–194.
- Qu L, Liu MY, Zheng LL, Wang X, Xue HW. 2023. Data-independent acquisition-based global phosphoproteomics reveal the diverse roles of casein kinase 1 in plant development. Science Bulletin 68: 2077–2093.
- Qu L, Wei Z, Chen HH, Liu T, Liao K, Xue HW. 2021. Plant casein kinases phosphorylate and destabilize a cyclin-dependent kinase inhibitor to promote cell division. Plant Physiology 187: 917–930.
- Ren GD, Zhou Q, Wu SX, Zhang YF, Zhang LG, Huang JR, Sun ZF, Kuai BK. 2010. Reverse genetic identification of CRN1 and its distinctive role in chlorophyll degradation in Arabidopsis. Journal of Integrative Plant Biology 52: 496–504.
- Schaller GE, Kieber JJ. 2002. Ethylene. Arabidopsis Book 1: e0071.
- Schippers JH, Schmidt R, Wagstaff C, Jing HC. 2015. Living to die and dying to live: the survival strategy behind leaf senescence. Plant Physiology 169: 914–930.
- Schweiger R, Schwenkert S. 2014. Protein–protein interactions visualized by bimolecular fluorescence complementation in tobacco protoplasts and leaves. Journal of Visualized Experiments 85: 51327.
- Sun GL, Mei YY, Deng DW, Xiong L, Sun LF, Zhang XY, Wen ZW, Liu S, You X, Nasrullah et al. 2017. N-terminus-mediated degradation of ACS7 is negatively regulated by senescence signaling to allow optimal ethylene production during leaf development in Arabidopsis. Frontiers in Plant Science 8: 2066.
- Tan ST, Dai C, Liu HT, Xue HW. 2013. Arabidopsis casein kinase1 proteins CK1.3 and CK1.4 phosphorylate cryptochrome2 to regulate blue light signaling. Plant Cell 25: 2618–2632.
- Tan ST, Xue HW. 2014. Casein kinase 1 regulates ethylene synthesis by phosphorylating and promoting the turnover of ACS5. Cell Reports 9: 1692–1702.
- Tsuchisaka A, Yu GX, Jin HL, Alonso JM, Ecker JR, Zhang XM, Gao S, Theologis A. 2009. A combinatorial interplay among the 1-aminocyclopropane-1-carboxylate isoforms regulates ethylene biosynthesis in Arabidopsis thaliana. Genetics 183: 979–1003.
- Van Camp W. 2005. Yield enhancement genes: seeds for growth. Current Opinion in Biotechnology 16: 147–153.
- Venerando A, Ruzzene M, Pinna LA. 2014. Casein kinase: the triple meaning of a misnomer. Biochemical Journal 460: 141–156.
- Wang F, Zhu DM, Huang X, Li S, Gong YN, Yao QF, Fu XD, Fan LM, Deng XW. 2009. Biochemical insights on degradation of Arabidopsis DELLA proteins gained from a cell-free assay system. Plant Cell 21: 2378–2390.
- Wang NN, Li Y, Chen YH, Lu R, Zhou L, Wang Y, Zheng Y, Li XB. 2021. Phosphorylation of WRKY16 by MPK3-1 is essential for its transcriptional activity during fiber initiation and elongation in cotton (Gossypium hirsutum). Plant Cell 33: 2736–2752.
- Wang S, Han SY, Zhou XG, Zhao CJ, Guo LA, Zhang JQ, Liu F, Huo QX, Zhao WS, Guo ZJ et al. 2023. Phosphorylation and ubiquitination of OsWRKY31 are integral to OsMKK10-2-mediated defense responses in rice. Plant Cell 35: 2391–2412.
- Wang YQ, Cui X, Yang B, Xu ST, Wei XY, Zhao PY, Niu FF, Sun MT, Wang C, Cheng H et al. 2020. WRKY55 transcription factor positively regulates leaf senescence and the defense response by modulating the transcription of genes implicated in the biosynthesis of reactive oxygen species and salicylic acid in Arabidopsis. Development 147: dev189647.
- Woo HR, Kim HJ, Lim PO, Nam HG. 2019. Leaf senescence: systems and dynamics aspects. Annual Review of Plant Biology 70: 347–376.
- Woo HR, Koo HJ, Kim J, Jeong H, Yang JO, Lee IH, Jun JH, Choi SH, Park SJ, Kang B et al. 2016. Programming of plant leaf senescence with temporal and inter-organellar coordination of transcriptome in Arabidopsis. Plant Physiology 171: 452–467.
- Xiong L, Xiao D, Xu XX, Guo ZX, Wang NN. 2014. The non-catalytic N-terminal domain of ACS7 is involved in the post-translational regulation of this gene in Arabidopsis. Journal of Experimental Botany 65: 4397–4408.
- Yoo SD, Cho YH, Sheen J. 2007. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nature Protocols 2: 1565–1572.
- Zentgraf U, Doll J. 2019. Arabidopsis WRKY53, a node of multi-layer regulation in the network of senescence. Plants 8: 578.
- Zhang W, Wen CK. 2010. Preparation of ethylene gas and comparison of ethylene responses induced by ethylene, ACC, and ethephon. Plant Physiology and Biochemistry 48: 45–53.
- Zhang XW, Xu RR, Liu YK, You CX, An JP. 2023. MdVQ10 promotes wound-triggered leaf senescence in association with MdWRKY75 and undergoes antagonistic modulation of MdCML15 and MdJAZs in apple. The Plant Journal 115: 1599–1618.
- Zhang YS, Liu J, Chai JY, Xing D. 2016. Mitogen-activated protein kinase 6 mediates nuclear translocation of ORE3 to promote ORE9 gene expression in methyl jasmonate-induced leaf senescence. Journal of Experimental Botany 67: 83–94.
- Zhou JG, Wang XY, He YX, Sang T, Wang PC, Dai SJ, Zhang SQ, Meng XZ. 2020. Differential phosphorylation of the transcription factor WRKY33 by the protein kinases CPK5/CPK6 and MPK3/MPK6 cooperatively regulates camalexin biosynthesis in Arabidopsis. Plant Cell 32: 2621–2638.
- Zhou X, Jiang YJ, Yu DQ. 2011. WRKY22 transcription factor mediates dark-induced leaf senescence in Arabidopsis. Molecules and Cells 31: 303–313.