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Journal of Integrative Agriculture  2023, Vol. 22 Issue (7): 2094-2110    DOI: 10.1016/j.jia.2023.04.039
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A cyclic effect of cAMP and calcium signaling contributes to jujube growth and development
WANG Li-xin1, 2*, WANG Lin-xia1, 3*, ZHANG Meng-ling1*, QU Ying-yue1*, YUAN Ye1, Ehsan SADEGHNEZHAD4, GAO Meng-jiao1, ZHAO Ruo-yu1, QI Chao-feng1, GUO Xiao-xue1, ZHU Wen-hui1, LI Rui-mei1, DAI Li1, 2, LIU Meng-jun1, 2, LIU Zhi-guo1, 2#
1 College of Horticulture, Hebei Agricultural University, Baoding 071001, P.R.China
2 Research Center of Chinese Jujube, Hebei Agricultural University, Baoding 071001, P.R.China
3 Key Laboratory of Resource Biology and Biotechnology in Western China, Ministry of Education/College of Life Sciences,
Northwest University, Xi’an 710069, P.R.China
4 Department of Plant Biology, Faculty of Biological Sciences, Tarbiat Modares University, Teheran 14115, Iran
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摘要  

3',5'-环磷酸腺苷(cAMP)是一种重要的代谢产物,特别在枣中高效积累。然而,cAMP在枣细胞中的功能尚未得到系统研究。因此,我们通过枣细胞悬浮系的建立、原生质体分离及荧光强度分析研究了cAMP与钙离子信号的关系。首先,外源cAMP处理可以促进枣的生长和内源cAMP的积累。通过对过表达腺苷酸环化酶(ZjAC)的转基因拟南芥转录组分析鉴定出60个与钙离子信号相关的差异表达基因(DEG),发现这些基因参与钙离子信号转导及细胞间/内的反应。另外,外源cAMP和钙离子促进剂A23187等药物处理可以诱导枣细胞中ZjAC的表达、cAMP的积累及钙离子向细胞质中的流入,而钙离子螯合剂EGTA或腺苷酸环化酶抑制剂bithionol处理抑制了这种增加。此外,外源cAMP处理可以激活钙离子通道及相关下游基因,如ZjCNGC2和ZjMAPK2、ZjMAPKK2、ZjMAPKK4。总之,该研究结果表明cAMP的合成依赖于钙离子信号内流,钙离子信号和cAMP之间的级联放大效应参与细胞内信号转导从而促进枣的生长发育。



Abstract  3´,5´-Cyclic adenosine monophosphate (cAMP) is an important metabolite that is specifically enriched in jujube. However, the effect of cAMP on jujube cellular responses has not been comprehensively studied. Here, we established jujube cell suspension cultures and investigated the calcium influx in response to cAMP treatment through protoplast isolation and fluorescence intensity. Firstly, cAMP treatment could promote jujube growth and increase the content of endogenous cAMP. Using transcriptome analysis with transgenic Arabidopsis plants overexpressing adenylate cyclase (ZjAC) as a positive control, we identified 60 calcium-related differential expressed genes (DEGs) that contributed to the calcium signaling and inter- or intra-cellular responses. Pharmacological treatments such as cAMP and the calcium ionophore A23187 could induce ZjAC expression, the accumulation of cAMP and calcium influx in jujube cells, while ethylene glycol tetraacetic acid (EGTA) or bithionol treatment inhibited these changes. Moreover, the calcium channels and transporters in calcium influx, such as the ZjCNGC2 channel and the mitogen activated protein (MAP) kinase pathway, could be activated by cAMP treatment. In summary, our findings demonstrated that cAMP biosynthesis is dependent on calcium influx and the amplifying effect between calcium and cAMP may be involved in intracellular signal induction, which might contribute to the growth and development of jujube.
Keywords:  cAMP        calcium        growth        suspension cells        protoplast        signaling        jujube  
Received: 22 December 2022   Accepted: 24 March 2023
Fund: This research was funded by the Provincial Supporting Program of Hebei for the Returned Oversea Scholars, China (C20210114), the Science and Technology Project of Hebei Education Department (QN2022017), the Fundamental Scientific Research Fund of Universities in Hebei Province (KY2021059), the China Agriculture Research System (CARS-30-2-07), the National Key Research and Development Project of China (2019YFD1001605), the Natural Science Foundation of Hebei Province (C2020204082), the Funds for Hebei Jujube Industry Technology Research Institute after Operation Performance (205676155H), and the Young Talent Project of Hebei Agricultural University Foundation (YJ201853).
About author:  #Correspondence LIU Zhi-guo, Tel/Fax: +86-312-7528962, E-mail: jujubeliu@163.com * These authors contributed equally to this study.

Cite this article: 

WANG Li-xin, WANG Lin-xia, ZHANG Meng-ling, QU Ying-yue, YUAN Ye, Ehsan SADEGHNEZHAD, GAO Meng-jiao, ZHAO Ruo-yu, QI Chao-feng, GUO Xiao-xue, ZHU Wen-hui, LI Rui-mei, DAI Li, LIU Meng-jun, LIU Zhi-guo. 2023. A cyclic effect of cAMP and calcium signaling contributes to jujube growth and development. Journal of Integrative Agriculture, 22(7): 2094-2110.

Ali R, Ma W, Lemtiri-Chlieh F, Tsaltas D, Leng Q, von Bodman S, Berkowitz G A. 2007. Death don’t have no mercy and neither does calcium: Arabidopsis CYCLIC NUCLEOTIDE GATED CHANNEL2 and innate immunity. Plant Cell, 19, 1081–1095.

Al-Younis I, Wong A, Lemtiri-Chlieh F, Schmockel S, Tester M, Gehring C, Donaldson L. 2018. The Arabidopsis thaliana K+-uptake permease 5 (AtKUP5) contains a functional cytosolic adenylate cyclase essential for K+ transport. Frontiers in Plant Science, 9, 1645.

Alqurashi M, Gehring C, Marondedze C. 2016. Changes in the Arabidopsis thaliana proteome implicate camp in biotic and abiotic stress responses and changes in energy metabolism. International Journal of Molecular Sciences, 17, 852.

Assmann S M. 1995. Cyclic AMP as a second messenger in higher plants (status and future prospects). Plant Physiology, 108, 885–889.

Bianchet C, Wong A, Quaglia M, Alqurashi M, Gehring C, Ntoukakis V, Pasqualini S. 2019. An Arabidopsis thaliana leucine-rich repeat protein harbors an adenylyl cyclase catalytic center and affects responses to pathogens. Journal of Plant Physiology, 232, 12–22.

Bindschedler L V, Minibayeva F, Gardner S L, Gerrish C, Davies D R, Bolwell G P. 2001. Early signalling events in the apoplastic oxidative burst in suspension cultured French bean cells involve cAMP and Ca2+. New Phytologist, 151, 185–194.

Blanco E, Fortunato S, Viggiano L, de Pinto M C. 2020. Cyclic AMP: A polyhedral signalling molecule in plants. International Journal of Molecular Sciences, 21, 4862.

Bu J, Zhao J, Liu M. 2016. Expression stabilities of candidate reference genes for RT-qPCR in Chinese jujube (Ziziphus jujuba Mill.) under a variety of conditions. PLoS ONE, 11, e0154212.

Charpentier M, Sun J, Vaz Martins T, Radhakrishnan G V, Findlay K, Soumpourou E, Thouin J, Very A A, Sanders D, Morris R J, Oldroyd G E. 2016. Nuclear-localized cyclic nucleotide-gated channels mediate symbiotic calcium oscillations. Science, 352, 1102–1105.

Cooke C J, Smith C J, Walton T J, Newton R P. 1994. Evidence that cyclic AMP is involved in the hypersensitive response of Medicago sativa to a fungal elicitor. Phytochemistry, 35, 889–895.

Curvetto N, Darjania L, Delmastro S. 1994. Effect of two cAMP analogues on stomatal opening in Vicia faba: Possible relationship with cytosolic calcium concentration. Plant Physiology and Biochemistry, 32, 365–372.

Cyong J C, Hanabusa K. 1980. Cyclic adenosine monophosphate in fruits of Zizyphus jujuba. Phytochemistry, 19, 2747–2748.

Duszyn M, Swiezawska B, Szmidt-Jaworska A, Jaworski K. 2019. Cyclic nucleotide gated channels (CNGCs) in plant signalling-current knowledge and perspectives. Journal of Plant Physiology, 241, 153035.

Ehsan H, Reichheld J P, Roef L, Witters E, Lardon F, Van Bockstaele D, Van Montagu M, Inze D, Van Onckelen H. 1998. Effect of indomethacin on cell cycle dependent cyclic AMP fluxes in tobacco BY-2 cells. FEBS Letters, 422, 165–169.

Gancedo J M. 2013. Biological roles of cAMP: Variations on a theme in the different kingdoms of life. Biological Reviews, 88, 645–668.

Gao M J, Wang L H, Li M, Sun P F, Sadeghnezhad E, Shi H Q, Qian J C, Liu Z G, Liu M J, Liu P, Wang L X. 2021. Physiological and transcriptome analysis accentuates microtubules and calcium signaling in Ziziphus jujuba Mill ‘Dongzao’ autotetraploids with sensitive cold tolerance. Scientia Horticulturae, 285, 110183.

Gehring C. 2010. Adenyl cyclases and cAMP in plant signaling-past and present. Cell Communication and Signaling, 8, 15.

Gehring C, Turek I S. 2017. Cyclic nucleotide monophosphates and their cyclases in plant signaling. Frontiers in Plant Science, 8, 1704.

Guan P, Shi W, Riemann M, Nick P. 2021. Dissecting the membrane-microtubule sensor in grapevine defence. Horticuture Research, 8, 260.

Ito M, Takahashi H, Sawasaki T, Ohnishi K, Hikichi Y, Kiba A. 2014. Novel type of adenylyl cyclase participates in tabtoxinine-β-lactam-induced cell death and occurrence of wildfire disease in Nicotiana benthamiana. Plant Signaling & Behavior, 9, e27420.

Jha S K, Sharma M, Pandey G K. 2016. Role of cyclic nucleotide gated channels in stress management in plants. Current Genomics, 17, 315–329.

Kaplan B, Sherman T, Fromm H. 2007. Cyclic nucleotide-gated channels in plants. FEBS Letters, 581, 2237–2246.

Kobylinska A, Borek S, Posmyk M M. 2018. Melatonin redirects carbohydrates metabolism during sugar starvation in plant cells. Journal of Pineal Research, 64, e12466.

Kudla J, Becker D, Grill E, Hedrich R, Hippler M, Kummer U, Parniske M, Romeis T, Schumacher K. 2018. Advances and current challenges in calcium signaling. New Phytologist, 218, 414–431.

Kurosaki F, Nishi A. 1993. Stimulation of calcium influx and calcium cascade by cyclic AMP in cultured carrot cells. Archives of Biochemistry and Biophysics, 302, 144–151.

Lemtiri-Chlieh F, Berkowitz G A. 2004. Cyclic adenosine monophosphate regulates calcium channels in the plasma membrane of Arabidopsis leaf guard and mesophyll cells. Journal of Biological Chemistry, 279, 35306–35312.

Li W, Luan S, Schreiber S L, Assmann S M. 1994. Cyclic AMP stimulates K+ channel activity in mesophyll cells of Vicia faba L. Plant Physiology, 106, 957–961.

Liang S, Sun J F, Luo Y M, Lv S S, Chen J J, Liu Y P, Hu X L. 2022. cAMP is a promising regulatory molecule for plant adaptation to heat stress. Life-Basel, 12, 885.

Liu M, Wang J, Wang L, Liu P, Zhao J, Zhao Z, Yao S, Stanica F, Liu Z, Wang L, Ao C, Dai L, Li X, Zhao X, Jia C. 2020. The historical and current research progress on jujube - A superfruit for the future. Horticulture Research, 7, 119.

Liu M J, Wang Y H. 1991. cAMP contents of Zizyphus jujuba Mill. Zizyphus spinosus Hu. and other twelve horticural plants. Journal of Hebei Agricultural University, 4, 20–23. (in Chinese)

Liu M J, Zhao J, Cai Q L, Liu G C, Wang J R, Zhao Z H, Liu P, Dai L, Yan G, Wang W J, Li X S, Chen Y, Sun Y D, Liu Z G, Lin M J, Xiao J, Chen Y Y, Li X F, Wu B, Ma Y, et al. 2014. The complex jujube genome provides insights into fruit tree biology. Nature Communications, 5, 5315.

Liu Q, Qiao F, Ismail A, Chang X, Nick P. 2013. The plant cytoskeleton controls regulatory volume increase. Biochimica et Biophysica Acta, 1828, 2111–2120.

Liu Z, Wang L, Xue C, Chu Y, Gao W, Zhao Y, Zhao J, Liu M. 2020. Genome-wide identification of MAPKKK genes and their responses to phytoplasma infection in Chinese jujube (Ziziphus jujuba Mill.). BMC Genomics, 21, 142.

Liu Z G, Yuan Y, Wang L L, Zhao X, Wang L X, Wang L H, Zhao Z H, Zhao X, Chu Y T, Gao Y N, Yang F Y, Wang Y L, Zhang Q, Zhao J, Liu M J. 2023. Three novel adenylate cyclase genes show significant biological functions in plant. Journal of Agricultural and Food Chemistry, 71, 1149–1161.

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, 402–408.

Lu M, Zhang Y, Tang S, Pan J, Yu Y, Han J, Li Y, Du X, Nan Z, Sun Q. 2016. AtCNGC2 is involved in jasmonic acid-induced calcium mobilization. Journal of Experimental Botany, 67, 809–819.

Ma W, Berkowitz G A. 2011. Ca2+ conduction by plant cyclic nucleotide gated channels and associated signaling components in pathogen defense signal transduction cascades. New Phytologist, 190, 566–572.

Ma Y, He K, Berkowitz G A. 2019. Editorial: From structure to signalsomes: New perspectives about membrane receptors and channels. Frontiers in Plant Science, 10, 682.

Moeder W, Garcia-Petit C, Ung H, Fucile G, Samuel M A, Christendat D, Yoshioka K. 2013. Crystal structure and biochemical analyses reveal that the Arabidopsis triphosphate tunnel metalloenzyme AtTTM3 is a tripolyphosphatase involved in root development. Plant Journal, 76, 615–626.

Moutinho A, Hussey P J, Trewavas A J, Malho R. 2001. cAMP acts as a second messenger in pollen tube growth and reorientation. Proceedings of the National Academy of Sciences of the United States of America, 98, 10481–10486.

Mustafa N R, de Winter W, van Iren F, Verpoorte R. 2011. Initiation, growth and cryopreservation of plant cell suspension cultures. Nature Protocols, 6, 715–742.

Ochoa-Villarreal M, Howat S, Hong S, Jang M O, Jin Y W, Lee E K, Loake G J. 2016. Plant cell culture strategies for the production of natural products. BMB Reports, 49, 149–158.

Proffitt R T, Tran J V, Reynolds C P. 1996. A fluorescence digital image microscopy system for quantifying relative cell numbers in tissue culture plates. Cytometry, 24, 204–213.

Qi L L, Kwiatkowski M, Chen H H, Hoermayer L, Sinclair S, Zou M X, del Genio C I, Kubes M F, Napier R, Jaworski K, Friml J. 2022. Adenylate cyclase activity of TIR1/AFB auxin receptors in plants. Nature, 611, 133.

Richards H, Das S, Smith C J, Pereira L, Geisbrecht A, Devitt N J, Games D E, van Geyschem J, Brenton A G, Newton R P. 2002. Cyclic nucleotide content of tobacco BY-2 cells. Phytochemistry, 61, 531–537.

Rosales-Mendoza S, Tello-Olea M A. 2015. Carrot cells: A pioneering platform for biopharmaceuticals production. Molecular Biotechnology, 57, 219–232.

Santos R B, Abranches R, Fischer R, Sack M, Holland T. 2016. Putting the spotlight back on plant suspension cultures. Frontiers in Plant Science, 7, 297.

Schripsema J, Meijer A H, van Iren F, ten Hoopen H J G, Verpoorte R. 1990. Dissimilation curves as a simple method for the characterization of growth of plant cell suspension cultures. Plant Cell Tissue and Organ Culture, 22, 55–64.

Su J, Cui W F, Zhu L C, Li B Y, Ma F W, Li M J. 2022. Response of carbohydrate metabolism-mediated sink strength to auxin in shoot tips of apple plants. Journal of Integrative Agriculture, 21, 422–433.

Swiezawska B, Jaworski K, Pawelek A, Grzegorzewska W, Szewczuk P, Szmidt-Jaworska A. 2014. Molecular cloning and characterization of a novel adenylyl cyclase gene, HpAC1, involved in stress signaling in Hippeastrum×hybridum. Plant Physiology and Biochemistry, 80, 41–52.

Trexler M M, McDonald K A, Jackman A P. 2005. A cyclical semicontinuous process for production of human α1-antitrypsin using metabolically induced plant cell suspension cultures. Biotechnology Progress, 21, 321–328.

Wang C K, Zhao Y W, Han P L, Yu J Q, Hao Y J, Xu Q, You X C, Hu D G. 2022. Auxin response factor gene MdARF2 is involved in ABA signaling and salt stress response in apple. Journal of Integrative Agriculture, 21, 2264–2274.

Wang L, Nick P. 2017. Cold sensing in grapevine - Which signals are upstream of the microtubular “thermometer”. Plant Cell and Environment, 40, 2844–2857.

Wang L, Sadeghnezhad E, Riemann M, Nick P. 2019. Microtubule dynamics modulate sensing during cold acclimation in grapevine suspension cells. Plant Science, 280, 18–30.

Wang L X, Li M, Liu Z G, Dai L, Zhang M L, Wang L L, Zhao J, Liu M J. 2020a. Genome-wide identification of CNGC genes in Chinese jujube (Ziziphus jujuba Mill.) and ZjCNGC2 mediated signalling cascades in response to cold stress. BMC Genomics, 21, 191.

Wang L X, Sadeghnezhad E, Nick P. 2020b. Upstream of gene expression: What is the role of microtubules in cold signalling? Journal of Experimental Botany, 71, 36–48.

Wu J, Qu H, Jin C, Shang Z, Wu J, Xu G, Gao Y, Zhang S. 2011. cAMP activates hyperpolarization-activated Ca2+ channels in the pollen of Pyrus pyrifolia. Plant Cell Reports, 30, 1193–1200.

Xu Z, Sun M, Jiang X, Sun H, Dang X, Cong H, Qiao F. 2018. Glycinebetaine biosynthesis in response to osmotic stress depends on jasmonate signaling in watermelon suspension cells. Frontiers in Plant Science, 9, 1469.

Yang H, Zhao Y L, Chen N, Liu Y P, Yang S Y, Du H W, Wang W, Wu J Y, Tai F J, Chen F, Hu X L. 2021. A new adenylyl cyclase, putative disease-resistance RPP13-like protein 3, participates in abscisic acid-mediated resistance to heat stress in maize. Journal of Experimental Botany, 72, 283–301.

Zelman A K, Dawe A, Gehring C, Berkowitz G A. 2012. Evolutionary and structural perspectives of plant cyclic nucleotide-gated cation channels. Frontiers in Plant Science, 3, 95.

Zhao J, Guo Y Q, Fujita K, Sakai K. 2004. Involvement of cAMP signaling in elicitor-induced phytoalexin accumulation in Cupressus lusitanica cell cultures. New Phytologist, 161, 723–733.

Zhao Y L, Du H W, Wang Y K, Wang H L, Yang S Y, Li C H, Chen N, Yang H, Zhang Y H, Zhu Y L, Yang L Y, Hu X L. 2021. The calcium-dependent protein kinase ZmCDPK7 functions in heat-stress tolerance in maize. Journal of Integrative Plant Biology, 63, 510–527.

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