YUAN Ye1, ZHAO Xin1, LI Jia-Min2, LIU Zhi-Guo3,*, LIU Meng-Jun1,3,*
1 College of Horticulture, Hebei Agricultural University, Baoding 071000, China;
2 College of Food Science and Technology, Hebei Agricultural University, Baoding 071000, China;
3 Research Center of Chinese Jujube, Hebei Agricultural University, Baoding 071000, China
Abstract:Adenylyl cyclase (AC), the key enzyme for the synthesis of 3',5'-cyclic adenosine monophosphate (cAMP), is of vital role in the cyclic adenosine monophosphate messenger system. AC has been systematically studied in animals and microorganisms. While the research of AC in plants started late and proceeded not as fast as that in animals. Nevertheless, with the continuous development and progress of science and technology, visible research progresses have been made in the field of AC enzyme activity verification, AC gene mining, structural characterization and biological function analysis of AC protein in plants, but there is no relevant systematic review report. Therefore, this study systematically summarized the progresses on plant ACs to provide references for the further study of AC metabolism in plants.
袁野, 赵馨, 李佳敏, 刘志国, 刘孟军. 植物腺苷酸环化酶研究进展[J]. 农业生物技术学报, 2022, 30(11): 2212-2223.
YUAN Ye, ZHAO Xin, LI Jia-Min, LIU Zhi-Guo, LIU Meng-Jun. Research Progress on Plant Adenylyl Cyclase. 农业生物技术学报, 2022, 30(11): 2212-2223.
[1] 刘孟军, 王永蕙. 1991. 枣和酸枣等14种园艺植物cAMP含量的研究[J]. 河北农业大学学报, 14(4): 20-23.
(Liu M J, Wang Y H.1991. cAMP contents of Zizyphus jujuba Mill. Zizyphus spinosus Hu. and other twelve horticural plants[J]. Journal of Hebei Agricultural University, 14(4): 20-23.)
[2] 薛晓芳, 赵爱玲, 任海燕, 等. 2020. 枣种质资源果实cAMP和cGMP含量分析[J]. 食品工业科技, 42(04): 208-214.
(Xue X F, Zhao A L, Ren H Y, et al.2020. Analysis of cAMP and cGMP contents in fruits of Chinese jujube germplasm resources[J]. Science and Technology of Food Industry, 42(04): 208-214.)
[3] 赵爱玲, 李登科, 王永康, 等. 2009. 枣树不同品种,发育时期和器官的cAMP和cGMP含量研究[J]. 园艺学报, 36(08): 1134-1139.
(Zhao A L, Li D K, Wang Y K, et al.2009. Study on the contents of cAMP and cGMP in different cultivars, growing periods and organs in Chinese jujube[J]. Acta Horticulturae Sinica, 36(08): 1134-1139.)
[4] Al-Azzawi M J, Hall J L.1976. Cytochemical localization of adenyl cyclase activity in maize root tips[J]. Plant Science Letters, 6(5): 285-289.
[5] Alberini C M, Ghirardi M, Huang Y Y, et al.2010. A molecular switch for the consolidation of long-term memory: cAMP-inducible gene expression[J]. Annals of the New York Academy of Sciences, 758(1): 261-286.
[6] Alvarez R, Moore T C, Vandepeute J.1974. Formation of adenosine 5'-phosphorofluoridate and the assay of adenyl cyclase in barley seeds[J]. Plant Physiology, 53(2): 144-148.
[7] Al-Younis I, Moosa B, Kwiatkowski M, et al.2021. Functional crypto-adenylate cyclases operate in complex plant proteins[J]. Frontiers in Plant Science, 12: 711749.
[8] Al-Younis I, Wong A, Gehring C.2015. The Arabidopsis thaliana K+-uptake permease 7 (AtKUP7) contains a functional cytosolic adenylate cyclase catalytic centre[J]. FEBS Letters, 589(24): 3848-3852.
[9] Al-Younis I, Wong A, Lemtiri-Chlieh F, et al.2018. The Arabidopsis thaliana K+-Uptake Permease 5 (AtKUP5) contains a functional cytosolic adenylate cyclase essential for K+ transport[J]. Frontiers in Plant Science, 9: 1645.
[10] Andrew W, Martino B, Stefan B, et al.2018. SWISS-MODEL: Homology modelling of protein structures and complexes[J]. Nucleic Acids Research, 46(W1): W296-W303.
[11] Ashton A R, Polya G M.1978. Cyclic adenosine 3':5'-monophosphate in axenic rye grass endosperm cell cultures[J]. Plant Physiology, 61(5): 718-722.
[12] Assmann S M.1995. Cyclic AMP as a second messenger in higher plants (status and future prospects)[J]. Plant Physiology, 108(3): 885-889.
[13] Bianchet C, Wong A, Quaglia M, et al.2018. An Arabidopsis thaliana leucine-rich repeat protein harbors an adenylyl cyclase catalytic center and affects responses to pathogens[J]. Journal of Plant Physiology, 232: 12-22.
[14] Bieger B, Essen L.2001. Structural analysis of adenylate cyclases from in their monomeric state[J]. The EMBO Journal, 20: 433-445.
[15] Brown E, Newton R.1981. Cyclic AMP and higher plants[J]. Phytochemistry, 20(11): 2453-2463.
[16] Carricarte V, Bianchini G M, Muschietti J P, et al.1988. Adenylate-cyclase activity in a higher-plant, asfalfa (Medicago-sativa)[J]. Biochemical Journal, 249(3): 807-811.
[17] Chatukuta P, Dikobe T, Kawadza D, et al.2018. An Arabidopsis clathrin assembly protein with a predicted role in plant defense can function as an adenylate cyclase[J]. Biomolecules, 8(2): 15.
[18] Curvetto N, Drjania L, Delmastro S.1994. Effect of two cAMP analogues on stomatal openingin Vicia faba. possible relationship with cytosolic calcium concentration[J]. Plant Physiology and Biochemistry (France), 32(3): 365-372.
[19] Cyong J C, Hanabusa K.1980. Cyclic adenosine monophosphate in fruits of Zizyphus jujuba[J]. Phytochemistry, 19(12): 2747-2748.
[20] Dias F V, Serrazina S, Vitorino M, et al.2019. A role for diacylglycerol kinase 4 in signalling crosstalk during Arabidopsis pollen tube growth[J]. The New Phytologist, 222(3): 1434-1446.
[21] Derici M K, Sadi G, Cenik B, et al.2019. Differential expressions and functions of phosphodiesterase enzymes in different regions of the rat heart[J]. European Journal of Pharmacology, 844: 118-129.
[22] Duszyn M, Świeżawska-Boniecka B, Skorupa M, et al.2022. BdGUCD1 and cyclic GMP are required for responses of Brachypodium distachyon to Fusarium pseudograminearum in the mechanism involving jasmonate[J]. International Journal of Molecular Sciences, 23(5): 2674.
[23] Duszyn M, Świeżawska B, Szmidt-Jaworska A, et al.2019. Cyclic nucleotide gated channels (CNGCs) in plant signalling-current knowledge and perspectives[J]. Journal of Plant Physiology, 241: 153035.
[24] Drum C L, Yan S Z, Bard J, et al.2002. Structural basis for the activation of anthrax adenylyl cyclase exotoxin by calmodulin[J]. Nature, 415(6870): 396.
[25] Ehsan H, Reichheld J P, Roef L, et al.1998. Effect of indomethacin on cell cycle dependent cyclic AMP fluxes in tobacco BY-2 cells[J]. FEBS Letters, 422(2): 165-169.
[26] Gallagher D T, Smith N N, Kim S K, et al.2006. Structure of the class Ⅳ adenylyl cyclase reveals a novel fold[J]. Journal of Molecular Biology, 362(1): 114-122.
[27] Gallagher D T, Kim S K, Robinson H, et al.2011. Active-site structure of class Ⅳ adenylyl cyclase and transphyletic mechanism[J]. Journal of Molecular Biology, 405(3): 787-803.
[28] Gehring C.2010. Adenyl cyclase and cAMP in plant signaling- past and present[J]. Cell Communication and Signaling, 8: 15.
[29] Giannattasio M, Macchia V.1973. Adenylate-cyclase and cyclic 3′5′-AMP-diesterase in Jerusalem artichoke tubers[J]. Plant Science Letters, 1(6): 259-264.
[30] Glaser P, Sakamoto H, Bellalou J, et al.1988. Secretion of cyclolysin, the calmodulin-sensitive adenylate cyclase-haemolysin bifunctional protein of Bordetella pertussis[J]. EMBO Journal, 7(12): 3997-4004.
[31] Goelet P, Castellucci V F, Schacher S, et al.1986. The long and the short of long-term memory-a molecular framework[J]. Nature, 322(6078): 419-422.
[32] Guo Q, Shen Y, Lee Y S, et al.2005. Structural basis for the interaction of Bordetella pertussis adenylyl cyclase toxin with calmodulin[J]. The EMBO Journal, 24(18): 3190-3201.
[33] Han M, Wu W, Wu W H, et al.2016. Potassium transporter KUP7 is involved in K+ acquisition and translocation in Arabidopsis root under K+-limited conditions[J]. Molecular Plant, 9(3): 437-446.
[34] Hilton G M, Nesius K K.1978. Localization of adenyl cyclase in meristems of young pea hypocotyls[J]. Physiologia Plantarum, 42(1): 49-52.
[35] Ito M, Takahashi H, Sawasaki T, et al.2014. Novel type of adenylyl cyclase participates in tabtoxinine-β-lactam-induced cell death and occurrence of wildfire disease in Nicotiana benthamiana[J]. Plant Signaling & Behavior, 9(1): e27420.
[36] Johnson R A, Welden J.1977. Characteristics of the enzymatic hydrolysis of 5'-adenylylimidodiphosphate: Implications for the study of adenylate cyclase[J]. Archives of Biochemistry & Biophysics, 183(1): 216-227.
[37] Jumper J, Evans R, Pritzel A, 2021. et al. Highly accurate protein structure prediction with AlphaFold[J]. Nature, 596(7873): 583-589.
[38] Kasahara M, Suetsugu N, Urano Y, et al.2016. An adenylyl cyclase with a phosphodiesterase domain in basal plants with a motile sperm system[J]. Scientific Reports, 6: 39232.
[39] Kotera E, Tasaka M, Shikanai T.2005. A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts[J]. Nature, 433(7023): 326-330.
[40] Krishna G, Weiss B, Brodie B B.1968. A simple, sensitive method for the assay of adenyl cyclase[J]. Journal of Pharmacology & Experimental Therapeutics, 163(2): 379.
[41] Lefkimmiatis K, Moyer M P, Curci S, et al.2009. "cAMP sponge": A buffer for cyclic adenosine 3', 5'-monophosphate[J]. PLOS ONE, 4(11): e7649.
[42] Legendre L, Derckel J P, Wrisez F, et al.1997. Evidence for the existence of cAMP in lily plant flower tissues[J]. Phytochemistry, 44(5), 769-774.
[43] Lemtiri-Chlieh F, Berkowitz G A.2004. Cyclic adenosine monophosphate regulates calcium channels in the plasma membrane of Arabidopsis leaf guard and mesophyll cells[J]. Journal of Biological Chemistry, 279(34): 35306-35312.
[44] Leppla S H.1984. Bacillus anthracis calmodulin-dependent adenylate cyclase: Chemical and enzymatic properties and interactions with eucaryotic cells[J]. Advances in Cyclic Nucleotide & Protein Phosphorylation, 17: 189-198.
[45] Lu M, Zhang Y, Tang S, et al.2015. AtCNGC2 is involved in jasmonic acid-induced calcium mobilization[J]. Journal of Experimental Botany, 67(3): 809-819.
[46] Ludidi N, Gehring C.2003. Identification of a novel protein with guanylyl cyclase activity in Arabidopsis thaliana[J]. Journal of Biological Chemistry, 278(8): 6490-6494.
[47] Ma W, Qi Z, Smigel A, et al.2009. Ca2+, cAMP and transduction of non-self perception during plant immune responses[J]. Proceedings of the National Academy of Sciences, 106(49): 20995-21000.
[48] Maathuis F J M, Sanders D.2010. Mechanisms of potassium absorption by higher plant roots[J]. Physiologia Plantarum, 96(1): 158-168.
[49] May A, Chris G, Claudius M.2016. Changes in the Arabidopsis thaliana proteome implicate cAMP in biotic and abiotic stress responses and changes in energy metabolism[J]. International Journal of Molecular Sciences, 17(6): 852.
[50] Miller J J, Galsky A G.1974. Radioimmunological evidence for the presence of cyclic-AMP in Hordeum seeds[J]. Phytochemistry, 13(8): 1295-1296.
[51] Mou T C, Masada N, Cooper D M F, et al.2009. Structural basis for inhibition of mammalian adenylyl cyclase by calcium[J]. Biochemistry, 48(15): 3387-3397.
[52] Moutinho A, Hussey P J, Trewavas A J, et al.2001. cAMP acts as a second messenger in pollen tube growth and reorientation[J]. Proceedings of the National Academy of Sciences of the USA, 98(18): 10481-10486.
[53] Pacini B, Petrigliano A, Diffley P, et al.1993. Adenylyl cyclase activity in roots of Pisum sativum[J]. Phytochemistry, 34(4): 899-903.
[54] Ramachandran J.1971. A new simple method for separation of adenosine 3′,5′-cyclic monophosphate from other nucleotides and its use in the assay of adenyl cyclase[J]. Analytical Biochemistry, 43(1): 227-239.
[55] Rougier M, Jnoud N, Dumas C.1988. Localization of adenylate cyclase activity in Populus: Its relation to pollen-pistil recognition and incompatibility[J]. Sexual Plant Reproduction, 1(3): 140-149.
[56] Roy A, Kucukural A, Zhang Y.2010. I-TASSER: A unified platform for automated protein structure and function prediction[J]. Nature Protocols, 5(4): 725-738.
[57] Ruzvidzo O, Dikobe B T, Kawadza D T, et al.2013. Recombinant expression and functional testing of candidate adenylate cyclase domains[J]. Methods in Molecular Biology, 1016: 13-25.
[58] Ruzvidzo O, Gehring C, Wong A.2019. New perspectives on plant adenylyl cyclases[J]. Frontiers in Molecular Biosciences, 6: 136.
[59] Sabetta W, Vandelle E, Locato V, et al.2019. Genetic buffering of cyclic AMP in Arabidopsis thaliana compromises the plant immune response triggered by an avirulent strain of Pseudomonas syringae pv. tomato[J]. The Plant Journal, 98(4): 590-606.
[60] Sabetta W, Vannini C, Sgobba A, et al.2016. Cyclic AMP deficiency negatively affects cell growth and enhances stress-related responses in tobacco Bright Yellow-2 cells[J]. Plant Molecular Biology, 90(4-5): 467-483.
[61] Schulze W, Hinterberger U, Wollenberger A, et al.1977. Problems of the cytochemical demonstration of adenylate cyclase[J]. Acta Histochemica Et Cytochemica, 10(3): 371-378.
[62] Steegborn C, Litvin T N, Levin L R, et al.2004. Bicarbonate activation of adenylyl cyclase via promotion of catalytic active site closure and metal recruitment[J]. Nature Structural & Molecular Biology, 12(1): 32-37.
[63] Shah S, Peterkofsky A.1991. Characterization and generation of Escherichia coli adenylate cyclase deletion mutants[J]. Journal of Bacteriology, 173(10): 3238-3242.
[64] Sinha S C, Wetterer M, Sprang S R, et al.2005. Origin of asymmetry in adenylyl cyclases: Structures of Mycobacterium tuberculosis Rv1900c[J]. Embo Journal, 24(4): 663-673.
[65] Steegborn C, Litvin T N, Levin L R, et al.2005. Bicarbonate activation of adenylyl cyclase via promotion of catalytic active site closure and metal recruitment[J]. Nature Structural & Molecular Biology, 12(1): 32-37.
[66] Sutherland E W, Rall T W.1957. The properties of an adenine ribonucleotide produced with cellular particles, ATP, Mg++, and epinephrine or glucagon[J]. Journal of the American Chemical Society, 79(13): 3608-3608.
[67] Sutherland E W, Robison G A, Butcher R W.1968. Some aspects of the biological role of adenosine 3',5'-monophosphate (Cyclic AMP)[J]. Circulation, 37(2): 279-306.
[68] Świeżawska B, Jaworski K, Pawełek A, et alA.2014. Molecular cloning and characterization of a novel adenylyl cyclase gene, HpAC1, involved in stress signaling in Hippeastrum x hybridum[J]. Plant Physiology and Biochemistry, 80: 41-52.
[69] Świeżawska B, Duszyn M, Kwiatkowski M, et al.2020. Brachypodium distachyon triphosphate tunnel metalloenzyme 3 is both a triphosphatase and an adenylyl cyclase upregulated by mechanical wounding[J]. FEBS Letters, 594(6): 1101-1111.
[70] Tang W J, Hurley J H.1998. Catalytic mechanism and regulation of mammalian adenylyl cyclases[J]. Molecular Pharmacology, 54(2): 231-240.
[71] Tesmer J J, Sunahara R K, Gilman A G, et al.1997. Crystal structure of the catalytic domains of adenylyl cyclase in a complex with gsα·gtpγs[J]. Science, 278(5345): 1907-1916.
[72] Tews I, Findeisen F, Sinning I, et al.2005. The structure of a pH-sensing mycobacterial adenylyl cyclase holoenzyme[J]. Science, 308(5724): 1020-1023.
[73] Thomas L, Marondedze C, Ederli L, et al.2013. Proteomic signatures implicate cAMP in light and temperature responses in Arabidopsis thaliana[J]. Journal of Proteomics, 83: 47-59.
[74] Tresguerres M, Levin L R, Buck J.2011. Intracellular cAMP signaling by soluble adenylyl cyclase[J]. Kidney International, 79(12): 1277-1288.
[75] Trott O, Olson A J.2009. AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading[J]. Journal of Computational Chemistry, 31(2): 455-461.
[76] Wachstein M, Meisel E.1957. Histochemistry of hepatic phosphatases at physiologic pH[J]. American Journal of Clinical Pathology, 27(1): 13-22.
[77] Wissing J, Heim S, Wagner K G.1989. Diacylglycerol kinase from suspension cultured plant cells[J]. Plant Physiology, 90(4): 1546-1551.
[78] Witters E, Quanten L, Bloemen J, et al.2004. Product identification and adenylyl cyclase activity in chloroplasts of Nicotiana tabacum[J]. Rapid Communications in Mass Spectrometry, 18(4): 499-504.
[79] Witters E, Roef L, Newton R P, et al.1996. Quantitation of cyclic nucleotides in biological samples by negative electrospray tandem mass spectrometry coupled to ion suppression liquid chromatography[J]. Rapid Communications in Mass Spectrometry, 10(2): 225-231.
[80] Witters E, Vanhoutte K, Dewitte W, et al.2015. Analysis of cyclic nucleotides and cytokinins in minute plant samples using phase-system switching capillary electrospray-liquid chromatography-tandem mass spectrometry[J]. Phytochemical Analysis, 10(3): 143-151.
[81] Xu R Q, Guo Y H, Peng S, et al.2021. Molecular targets and biological functions of cAMP signaling in Arabidopsis[J]. Biomolecules, 11(5): 688.
[82] Yang H, Zhao Y L, Chen N, et al.2020. A new adenylyl cyclase, putative disease resistance RPP13-like protein 3, participates in abscisic acid-mediated heat stress resistance in maize[J]. Journal of Experimental Botany, 72(2): 283-301.
[83] Yang J, Yan R, Roy A, et al.2014. The I-TASSER suite: Protein structure and function prediction[J]. Nature Methods, 12(1): 7-8.
[84] Yount R G, Babcock D, Ballantyne W, et al.1971. Adenylyl imidiodiphosphate, an adenosine triphosphate analog containing a P-N-P linkage[J]. Biochemistry, 10(13): 2484-2489.
[85] Zajic G, Schacht J.1983. Cytochemical demonstration of adenylate cyclase with strontium chloride in the rat pancreas[J]. Journal of Histochemistry & Cytochemistry, 31(1): 25-28.
[86] Zelman A K, Dawe A, Gehring C, et al.2012. Evolutionary and structural perspectives of plant cyclic nucleotide-gated cation channels[J]. Frontiers in Plant Science, 3: 95.
[87] Zhang G, Liu Y, Ruoho A E, et al.1997. Structure of the adenylyl cyclase catalytic core[J]. Nature, 386(6622): 247-253.