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Journal of Integrative Agriculture  2023, Vol. 22 Issue (1): 139-148    DOI: 10.1016/j.jia.2022.09.010
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PpMAPK6 regulates peach bud endodormancy release through interactions with PpDAM6

ZHANG Yu-zheng1, 2, 3, XU Chen1, 2, 3, LU Wen-li1, 2, 3, WANG Xiao-zhe1, 2, 3, WANG Ning1, 2, 3, MENG Xiang-guang1, 2, 3, FANG Yu-hui1, 2, 3, TAN Qiu-ping1, 2, 3, CHEN Xiu-de1, 2, 3, FU Xi-ling1, 2, 3, LI Ling1, 2, 3

1 College of Horticultural Science and Engineering, Shandong Agricultural University, Tai’an 271018, P.R.China

2 State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai’an 271018, P.R.China

3 Shandong Collaborative Innovation Center for Fruit & Vegetable Production with High Quality and Efficiency, Tai’an 271018, P.R.China

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摘要  

休眠相关的MADS-box (DAM)基因PpDAM6在芽休眠解除过程中起关键作用,在休眠解除过程中表达降低。然而,其在调控桃花芽内休眠解除中的互作网络仍不够完善。在本研究中,我们使用酵母双杂交(Y2H)技术,桃休眠相关SSHcDNA文库中鉴定了一种丝裂原活化蛋白激酶PpMAPK6,它与PpDAM6相互作用。PpMAPK6主要位于细胞核中。进一步的Y2H和双分子荧光互补(BiFC)实验验证了PpMAPK6通过结合PpDAM6MADS-box结构域与PpDAM6相互作用。实时荧光定量PCR (qRT-PCR)分析结果表明,在3个不同需冷量的品种(春捷,中油5号,青州蜜桃)PpMAPK6的表达趋势与PpDAM6相反。此外,ABA抑制PpMAPK6在花中的表达,促进PpDAM6在花中的表达。结果表明,PpMAPK6可能通过与PpDAM6相互作用使其磷酸化,从而加速其降解。桃花内休眠解除过程中随着ABA含量的降低,PpMAPK6的表达量增加,进而降低了PpDAM6的表达量,促进桃花芽内休眠解除



Abstract  

The MADS-box (DAM) gene PpDAM6, which is related to dormancy, plays a key role in bud endodormancy release, and the expression of PpDAM6 decreases during endodormancy release.  However, the interaction network that governs its regulation of the endodormancy release of flower buds in peach remains unclear.  In this study, we used yeast two-hybrid (Y2H) assays to identify a mitogen-activated protein kinase, PpMAPK6, that interacts with PpDAM6 in a peach dormancy-associated SSHcDNA library.  PpMAPK6 is primarily located in the nucleus, and Y2H and bimolecular fluorescence complementation (BiFC) assays verified that PpMAPK6 interacts with PpDAM6 by binding to the MADS-box domain of PpDAM6.  Quantitative real-time PCR (qRT-PCR) analysis showed that the expression of PpMAPK6 was opposite that of PpDAM6 in the endodormancy release of three cultivars with different chilling requirements (Prunus persica ‘Chunjie’, Prunus persica var. nectarina ‘Zhongyou 5’, Prunus persica ‘Qingzhou peach’).  In addition, abscisic acid (ABA) inhibited the expression of PpMAPK6 and promoted the expression of PpDAM6 in flower buds.  The results indicated that PpMAPK6 might phosphorylate PpDAM6 to accelerate its degradation by interacting with PpDAM6.  The expression of PpMAPK6 increased with decreasing ABA content during endodormancy release in peach flower buds, which in turn decreased the expression of PpDAM6 and promoted endodormancy release.

Keywords:  peach       endodormancy release        PpDAM6        PpMAPK6        ABA  
Received: 07 February 2022   Accepted: 25 August 2022
Fund: This work was partially supported by the National Key Research and Development Plan (2018YFD1000104), the National Natural Science Foundation of China (318720415) and the Agricultural Improved Seed Project Grant of Shandong, China (2020LZGC007 and 2020LZGC00702) and the Fruit Industry Technology System Project of Shandong, China (SDAIT-06-04). 

About author:  ZHANG Yu-zheng, E-mail: 2227144914@qq.com; Correspondence FU Xi-ling, E-mail: xilingfu@sdau.edu.cn; LI Ling, E-mail: liling217@sdau.edu.cn

Cite this article: 

ZHANG Yu-zheng, XU Chen, LU Wen-li, WANG Xiao-zhe, WANG Ning, MENG Xiang-guang, FANG Yu-hui, TAN Qiu-ping, CHEN Xiu-de, FU Xi-ling, LI Ling. 2023.

PpMAPK6 regulates peach bud endodormancy release through interactions with PpDAM6 . Journal of Integrative Agriculture, 22(1): 139-148.

Balogh E, Halász J, Soltész A, Erös-Honti Z, Gutermuth Á, Szalay L, Höhn M, Vágújfalvi A, Galiba G, Hegedüs A. 2019. Identification,structural and functional characterization of dormancy regulator genes in apricot (Prunus armeniaca L.). Frontiers in Plant Science, 10, 402.
Bielenberg D G, Wang Y, Li Z G, Zhebentyayeva T, Fan S H, Reighard G L, Scorza R, Abbott A G. 2008. Sequencing andannotation of the evergrowing locus in peach [Prunus persica (L.) Batsch] reveals a cluster of six MADS-boxtranscription factors as candidate genes for regulation of terminal bud formation. Tree Genetics & Genomes, 4, 495–507.
Chen M, Liu X, Jiang S, Wen B, Yang C, Xiao W, Fu X, Li D, Chen X, Gao D, Li L. 2018. Transcriptomic and functional analyses reveal that PpGLK1 regulates chloroplast development in peach (Prunus persica). Frontiers in Plant Science, 9, 34–34. 
Cheng N, Ji M L, Zhang Z J, Li L, Gao D. 2020. Cloning, expression and bioinformatics analysis of MPK3 gene in peach. Journal of Nuclear Agricultural Sciences, 34, 468–476. (in Chinese)
Cooke J E, Eriksson M E, Junttila O. 2012. The dynamic nature of bud dormancy in trees: Environmental control and molecular mechanisms. Plant Cell and Environment, 35, 1707–1728. 
Danquah A, de Zélicourt A, Boudsocq M,Neubauer J, Frei Dit Frey N, Leonhardt N, Pateyron S, Gwinner F, Tamby J P, Ortiz-Masia D, Marcote M J, Hirt H, Colcombet J. 2015. Identification and characterization of an ABA-activated MAP kinase cascade in Arabidopsis thaliana. The Plant Journal, 82, 232–244.
Du P Y, Wang D L, Tan Q P, Liu L, Fu X L, Chen X D, Xiao W, Li D M, Zhu C Y, Li L. 2016. Expression analysis of MAPK genes involved in nectarine floral buds during dormancy release. Plant Physiology Journal, 52, 216–224.
Galletti R, Ferrari S, De Lorenzo G. 2011. Arabidopsis MPK3 and MPK6 play different roles in basal and oligogalacturonide- or flagellin-induced resistance against Botrytis cinerea. Plant Physiology, 157, 804–814. 
Gao D S, Shu H R, Li X L. 2002. Study on the relationship between H2O2 content change and natural dormancy of several deciduous fruit trees. Acta Horticulturae Sinica, 29, 209–209. (in Chinese)
Goyal R K, Tulpan D, Chomistek N, Fundora D G, West C, Ellis B E, Foroud N A. 2018. Analysis of MAPK and MAPKK gene families in wheat and related Triticeae species. BMC Genomics, 19, 178–178. 
Hao X, Chao W, Yang Y, Horvath D. 2015. Coordinated expression of FLOWERING LOCUS T and DORMANCY ASSOCIATED MADS-BOX-like genes in leafy spurge. PLoS ONE, 10, e0126030.
He P, Shan L, Lin N C, Martin G B, Kemmerling B, Nurnberger T, Sheen J. 2006. Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell, 125, 563–575.
Hisayo Y, Tomomi O, Hiroaki J, Yukari H, Ryuta S, Ryutaro T. 2011. Expressional regulation of PpDAM5 and PpDAM6, peach (Prunus persica) dormancy-associated MADS-box genes, by low temperature and dormancy-breaking reagent treatment. Journal of Experimental Botany, 10, 3481–3488. 
Hu D, Sun C, Ma Q, You C, Cheng L, Hao Y. 2016. MdMYB1 regulates anthocyanin and malate accumulation by directly facilitating their transport into vacuoles in apples. Plant Physiology, 170, 1315–1330.
Jiménez S, Lawton-Rauh A L, Reighard G L, Abbott A G, Bielenberg D G. 2009. Phylogenetic analysis and molecular evolution of the dormancy associated MADS-box genes from peach. BMC Plant Biology, 9, 81.
Jin X, Zhu L, Yao Q, Meng X, Ding G, Wang D, Xie Q, Tong Z, Tao C, Yu L, Li H, Wang X. 2017. Expression profiling of mitogen-activated protein kinase genes reveals their evolutionary and functional diversity in different rubber tree (Hevea brasiliensis) cultivars. Genes (Basel), 8, 261. 
Jonak C, Okresz L, Bogre L, Hirt H. 2002. Complexity, cross talk and integration of plant MAP kinase signalling. Current Opinion in Plant Biology, 5, 415–424. 
José A C, Ruiz D, Egea J. 2011. Dormancy in temperate fruit trees in a global warming context: A review. Scientia Horticulturae, 130, 357–372.
Lang G A, Early J D, Martin G C, Darnell R L. 1987. Endo-, para-, and ecodormancy: Physiological terminology and classification for dormancy research. Hortscience, 22, 371–377.
Li H, Ding Y, Shi Y, Zhang X, Zhang S, Gong Z, Yang S. 2017. MPK3- and MPK6-mediated ICE1 phosphorylation negatively regulates ICE1 stability and freezing tolerance in Arabidopsis. Developmental Cell, 43, 630. 
Liu Y. 2012. Roles of mitogen-activated protein kinase cascades in ABA signaling. Plant Cell Reports, 31, 1–12.
Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2–∆∆Ct method. Methods, 4, 402–408.
Luo J, Zhao L L, Gong S Y, Sun X, Peng L, Qin L X, Ying Z, Xu W L, Li X B. 2011. A cotton mitogen-activated protein kinase (GhMPK6) is involved in ABA-induced CAT1 expression and H2O2 production. Journal of Genetics and Genomics, 38, 557–565.
Meng X, Xu J, He Y, Yang K, Mordorski B, Liu Y, Zhang S. 2013. Phosphorylation of an ERF transcription factor by Arabidopsis MPK3/MPK6 regulates plant defense gene induction and fungal resistance. The Plant Cell, 25, 1126–1142.
Niu Q F, Li J, Cai D Y, Qian M, Jia H, Bai S, Sayed H, Liu G, Teng Y, Zheng X. 2016. Dormancy-associated MADS-box genes and microRNAs jointly control dormancy transition in pear (Pyrus pyrifolia white pear group) flower bud. Journal of Experimental Botany, 67, 239–257.
Richardson W C, Badrakh T, Roundy B A, Aanderud Z T, Petersen S L, Allen P S, Madsen M D. 2019. Influence of an abscisic acid (ABA) seed coating on seed germination rate and timing of Bluebunch Wheatgrass. Ecology and Evolution, 9, 7438–7447. 
Rios G, Leida C, Conejero A, Badenes M L. 2014. Epigenetic regulation of bud dormancy events in perennial plants. Frontiers in Plant Science, 5, 247–247.
Sasaki R, Yamane H, Ooka T, Jotatsu H, Kitamura Y, Akagi T, Tao R. 2011. Functional and expressional analyses of PmDAM genes associated with endodormancy in Japanese apricot. Plant Physiology, 157,485–497.
Singh R K, Maurya JP, Azeez A, Miskolczi P, Tylewicz S, Stojkovič K, Delhomme N, Busov V, Bhalerao R P. 2018. A genetic network mediating the control of bud break in hybrid aspen. Nature Communications, 9, 4173.
Sorensson C, Lenman M, Veidevilg J, Schopper S, Ljungdahl T, Grotli M, Andreasson E. 2012. Determination of primary sequence specificity of Arabidopsis MAPKs MPK3 and MPK6 leads to identification of new substrates. Biochemical Journal, 446, 271–278.
Tuan P A, Bai S L, Saito T, Ito A, Moriguchi T. 2017. Dormancy-associated MADS-box (DAM) and the abscisic acid pathway regulate pear endodormancy through a feedback mechanism. Plant and Cell Physiology, 58, 1378–1390.
Vergara R, Noriega X, Aravena K, Prieto H, Perez F J. 2017. ABA represses the expression of cell cycle genes and may modulate the development of endodormancy in grapevine buds. Frontiers in Plant Science, 8, 812.
Wang D, Gao Z, Du P, Xiao W, Tan Q, Chen X, Li L, Gao D. Expression of ABA metabolism-related genes suggests similarities and differences between seed dormancy and bud dormancy of peach (Prunus persica). Frontiers in Plant Science, 6, 1248.
Wang H, Li L, Tan Y, Li D M, Tan Q P, Chen X D. 2011. Changes of carbohydrate subduction and related gene expression in nectarine buds during dormancy. Plant Physiology Journal, 47, 595–600. 
Wang H, Ngwenyama N, Liu Y, Walker J C, Zhang S. 2007. Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. The Plant Cell, 19, 63–73.
Wang H B, Wang X D, Gao D S. 2009. Physiological changes of peach varieties with different cooling requirements during bud dormancy induction. Journal of Fruit Science, 26, 445–449.
Wang P, Du Y, Zhao X, Miao Y, Song C P. 2013. The MPK6-ERF6-ROS-responsive cis-acting element7/GCC box complex modulates oxidative gene transcription and the oxidative response in Arabidopsis. Plant Physiology, 161, 1392–1408.
Wang Q, Xu G, Zhao X, Zhang Z, Wang X, Liu X, Xiao W, Fu X, Chen X, Gao D, Li D, Li L. 2020. Transcription factor TCP20 regulates peach bud endodormancy by inhibiting DAM5/DAM6 and interacting with ABF2. Journal of Experimental Botany, 71, 1585–1597.
Wells C E, Vendramin E, Tarodo S J, Verde I, Bielenberg D G. 2015. A genome-wide analysis of MADS-box genes in peach [Prunus persica (L.) Batsch]. BMC Plant Biology, 15, 41–41.
Xing Y, Jia W, Zhang J. 2009. AtMKK1 and AtMPK6 are involved in abscisic acid and sugar signaling in Arabidopsis seed germination. Plant Molecular Biology, 70, 725–736.
Xing Y, Jia W, Zhang J. 2010. AtMKK1 mediates ABA-induced CAT1 expression and H2O2 production via AtMPK6-coupled signaling in Arabidopsis. The Plant Journal, 54, 440–451.
Yamane H, Ooka T, Jotatsu H, Hosaka Y, Sasaki R, Tao R. 2011a. Expressional regulation of PpDAM5 and PpDAM6, peach (Prunus persica) dormancy-associated MADS-box genes, by low temperature and dormancy-breaking reagent treatment. Journal of Experimental Botany, 62, 3481–3488. 
Yamane H, Tao R, Ooka T, Jotatsu H, Sasaki R, Yonemori K. 2011b. Comparative analyses of dormancy-associated MADS-box genes, PpDAM5 and PpDAM6, in low- and high-chill peaches (Prunus persica L.). Journal of the Japanese Society for Horticultural Science, 80, 276–283.
Yamane H, Wada M, Honda C, Matsuura T, Ikeda Y, Hirayama T, Osako Y, Gao-Takai M, Kojima M, Sakakibara H, Tao R. 2019. Overexpression of Prunus DAM6 inhibits growth, represses bud break competency of dormant buds and delays bud outgrowth in apple plants. PLoS ONE, 14, e0214788.
Zhao F, Zheng Y F, Zeng T, Sun R, Yang J Y, Li Y, Bai S. 2017. Phosphorylation of SPOROCYTELESS/NOZZLE by the MPK3/6 kinase is required for anther development. Plant Physiology, 173, 2265–2277.
Zhao K, Zhou Y, Ahmad S, Yong X, Xie X, Han Y, Li Y, Sun L, Zhang Q. 2018. PmCBFs synthetically affect PmDAM6 by alternative promoter binding and protein complexes towards the dormancy of bud for Prunus mume. Scientific Reports, 8, 4527.
Zheng C, Halaly T, Acheampong A K, Takebayashi Y, Jikumaru Y, Kamiya Y, Or E. 2015. Abscisic acid (ABA) regulates grape bud dormancy, and dormancy release stimuli may act through modification of ABA metabolism. Journal of Experimental Botany, 66, 1527–1542. 
Zhou J, Wang X, He Y, Sang T, Wang P, Dai S, Zhang S, Meng X. 2020. Differential phosphorylation of the transcription factor WRKY33 by the protein kinases CPK5/CPK6 and MPK3/MPK6 cooperatively regulates camalexin biosynthesis in Arabidopsis. The Plant Cell, 32, 2621–2638.

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