Skip to main content
Log in

Current Views on Plant Adenylate Cyclases

  • REVIEWS
  • Published:
Russian Journal of Plant Physiology Aims and scope Submit manuscript

Abstract

Existence of adenylate cyclases in plants has long been considered unproven. It is only in the last two decades that biochemical properties of the enzyme and its molecular structure were clarified. This review focuses on specific functioning of plant adenylate cyclases integrated in multimolecular complexes as well as on physiological significance of this phenomenon in plant responses to stress. The problem of search for nucleotide sequences of plant adenylate cyclases and advances in the sequence decoding are considered.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.

Similar content being viewed by others

REFERENCES

  1. Alqurashi, M., Gehring, C., and Marondedze, C., Changes in the Arabidopsis thaliana proteome implicate cAMP in biotic and abiotic stress responses and changes in energy metabolism, Int. J. Mol. Sci., 2016, vol. 17, p. 852. https://doi.org/10.3390/ijms17060852

    Article  CAS  PubMed Central  Google Scholar 

  2. Gehring, C. and Turek, I., Cyclic nucleotide monophosphates and their cyclases in plant signaling, Front. Plant Sci., 2017. https://doi.org/10.3389/fpls.2017.01704

  3. Johnson, J.-L.F. and Leroux, M.R., cAMP and cGMP signaling: sensory systems with prokaryotic roots adopted by eukaryotic cilia, Trends Cell Biol., 2010, vol. 20, p. 435. https://doi.org/10.1016/j.tcb.2010.05.005

    Article  CAS  PubMed  Google Scholar 

  4. Swiezawska, B., Duszyn, M., Jaworski, K., and Szmidt-Jaworska, A., Downstream targets of cyclic nucleotides in plants, Front. Plant Sci., 2018, vol. 9, p. 1428. https://doi.org/10.3389/fpls.2018.01428

    Article  PubMed  PubMed Central  Google Scholar 

  5. Sutherland, E.W., Rall, T.W., and Mennon, T., Adenyl cyclase: distribution, preparation and properties, J. Biol. Chem., 1962, vol. 247, p. 1220.

    Article  Google Scholar 

  6. Hanoune, J., Pouille, Y., Tzavara, E., Shen, T., Lipskaya, M., Miyamoto, N., Suzuki, Y., and Defer, N., Adenylyl cyclases: structure, regulation, and function in an enzyme superfamily, Mol. Cell. Endocrinol., 1997, vol. 128, p. 179. https://doi.org/10.1016/s0303-7207(97)04013-6

    Article  CAS  PubMed  Google Scholar 

  7. Tesmer, J.G., Sunahara, R.K., Johnson, R.A., Gosselin, G., Gilman, A.G., and Sprang, S.A., Two-metal-ion catalysis in adenylyl cyclase, Science, 1999, vol. 285, p. 756. https://doi.org/10.1126/science.285.5428.756

    Article  CAS  PubMed  Google Scholar 

  8. Amrhein, N., Evidence against the occurrence of adenosine 3',5'-ceclic monophoshate in higher plants, Planta, 1974, vol. 118, p. 241.

    Article  CAS  Google Scholar 

  9. Spiteri, A., Viratelle, O.M., Raymond, P., Rancillac, M., Labouesse, J., and Prsdet, A., Artefactual origins of cyclic AMP in higher plant tissues, Plant Physiol., 1989, vol. 91, p. 624. https://doi.org/10.1104/pp.91.2.624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Ishikwa, I. and Homcy, C., The adenylyl cyclases as integrators of transmembrane signal transduction, Circ. Res., 1997, vol. 80, p. 297. https://doi.org/10.1161/01.RES.80.3.297

    Article  Google Scholar 

  11. Jasso-Chávez, R., Vega-Segura, A., El-Hafidi, M., Moreno-Sanchez, R., and Torres-Marquez, M.E., Kinetic and thermodynamic characterization of adenylyl cyclase from Euglena gracils, Arch. Biochem. Biophys., 2002, vol. 404, p. 48. https://doi.org/10.1016/s0003-9861(02)00235-7

    Article  PubMed  Google Scholar 

  12. Hellevuo, K., Berry, R., Sikela, J.M., and Tabakoff, B., Localization of the gene for a novel human adenylyl cyclase (ADCY7) to chromosome 16, Hum. Genet., 1995, vol. 95, p. 197. https://doi.org/10.1007/BF00209401

    Article  CAS  PubMed  Google Scholar 

  13. Ruzvidzo, O., Dikobe, D.T., Kawadza, D.T., Mabadahanye, G.H., Chatukuta, P., and Kwezi, L., Recombinant expression and functional testing of candidate adenylate cyclase domains, in Cyclic Nucleotide Signaling in Plants: Methods and Protocols, New York: Springer-Verlag, 2013, p. 13.

    Google Scholar 

  14. Defer, N., Best-Belpomme, M., and Hanoune, J., Tissue specificity and physiological relevance of various isoforms of adenylyl cyclase, Am. J. Physiol.: Renal Physiol., 2000, vol. 279, p. F400. https://doi.org/10.1152/ajprenal.2000.279.3.F400

    Article  CAS  Google Scholar 

  15. Halls, M.L. and Cooper, D.M.F., Regulation by Ca2+- signaling pathways of adenylyl cyclases, Cold Spring Harb. Perspect. Biol., 2011, vol. 3, p. a004143. https://doi.org/10.1101/cshperspect.a004143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Danchin, A., Adenylyl cyclases and guanylyl cyclases: role and classification, 2010. http://www.normalesup.org/ ‑adanchin/science/adenylyl cyclases.html.

  17. Kamenetsky, M., Middelhaufe, S., Bank, E.M., Levin, L.R., Buck, J., and Steegborn, C., Molecular details of cAMP generation in mammalian cells: a tale of two systems, J. Mol. Biol., 2006, vol. 362, p. 623. https://doi.org/10.1016/j.jmb.2006.07.045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Drum, C.L., Yan, S.Z., Bard, J., Shen, Y.Q., Lu, D., Soelaiman, S., Grabarek, Z., Bohm, A., and Tang, W.J., Structural basis for the activation of anthrax adenylyl cyclase exotoxin by calmodulin, Nature, 2002, vol. 415, p. 396. https://doi.org/10.1038/415396a

    Article  CAS  PubMed  Google Scholar 

  19. Baker, D.A. and Kelly, J.M., Structure, function and evolution of microbial adenylyl and guanylylcyclases, Mol. Microb., 2004, vol. 52, p. 1229. https://doi.org/10.1111/j.1365-2958.2004.04067.x

    Article  CAS  Google Scholar 

  20. Linder, J.U., Class III adenylyl cyclases: molecular mechanisms of catalysis and regulation, Cell Mol. Life Sci., 2006, vol. 63, p. 1736. https://doi.org/10.1007/s00018-006-6072-0

    Article  CAS  PubMed  Google Scholar 

  21. Téllez-Sosa, J., Soberón, N., Vega-Segura, A., Torres-Márquez, M.E., and Cevallos, M.A., The Rhizobium etlicya C product: characterization of a novel adenylatecyclase class, J. Bacteriol., 2002, vol. 84, p. 3560. https://doi.org/10.1128/JB.184.13.3560-3568.2002

    Article  CAS  Google Scholar 

  22. Steegborn, C., Structure, mechanism, and regulation of soluble adenylyl cyclases—similarities and differences to transmembrane adenylyl cyclases, Biochim. Biophys. Acta, Mol. Basis Dis., 2014, vol. 1842, p. 535. https://doi.org/10.1016/j.bbadis.2014.08.012

    Article  CAS  Google Scholar 

  23. Sunahara, R. and Taussig, R., Isoforms of mammalian adenylyl cyclase: multiplicities of signaling, Mol. Intervent., 2002, vol. 2, p. 168. https://doi.org/10.1124/mi.2.3.168

    Article  CAS  Google Scholar 

  24. Chang, J.C., Beuers, U., and Elferink, R., The emerging role of soluble adenylyl cyclase in primary biliary cholangitis, Dig. Dis., 2017, vol. 35, p. 217. https://doi.org/10.1159/000450914

    Article  PubMed  Google Scholar 

  25. Roa, J.N. and Tresguerres, M., Bicarbonate-sensing soluble adenylyl cyclase is present in the cell cytoplasm and nucleus of multiple shark tissues, Physiol. Rep., 2017, vol. 5, p. e13090. https://doi.org/10.14814/phy2.13090

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Wuttke, M.S., Buck, J., and Levin, L.R., Bicarbonat-regulated soluble adenylyl cyclase, J. Pancreas, 2001, vol. 2, p. 154.

    CAS  Google Scholar 

  27. Kobayashi, M., Buck, J., and Levin, L.R., Conservation of functional domain structure in bicarbonate-regulated “soluble” adenylyl cyclases in bacteria and eukaryotes, Dev. Genes Evol., 2004, vol. 214, p. 503. https://doi.org/10.1007/s00427-004-0432-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Kleinboelting, S., Diaz, A., Moniot, S., Heuvel, J., Weyand, M., Levin, L.R., Buck, J., and Steegborn, C., Crystal structures of human soluble adenylyl cyclase reveal mechanisms of catalysis and of its activation through bicarbonate, Proc. Natl. Acad. Sci. U.S.A., 2014, vol. 111, p. 3727. https://doi.org/10.1073/pnas.1322778111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Buck, J., Sinclair, M.L., Schapal, L., Cann, M.J., and Levin, L.R., Cytosolic adenylyl cyclase defines a unique signaling molecule in mammals, Proc. Natl. Acad. Sci. U.S.A., 1999, vol. 96, p. 79. https://doi.org/10.1073/pnas.96.1.79

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Zippin, J.H., Chen, Y., Nahirney, P., Kamenetsky, M., Wuttke, M.S., Fischman, D.A., Levin, L.R., and Buck, J., Compartmentalization of bicarbonate-sensitive adenylyl cyclase in distinct signaling microdomains, FASEB J., 2003, vol. 17, p. 82. https://doi.org/10.1096/fj.02-0598fje

    Article  CAS  PubMed  Google Scholar 

  31. Brown, E.G. and Newton, R.P., Occurrence of adenosine 3':5'-cyclic monophosphate in plant tissues, Photochemistry, 1973, vol. 12, p. 2685.

    Article  Google Scholar 

  32. Bhalta, S.C. and Chopra, R.N., Subcellular localization of adenylate cyclase in the shoot apices of Bryum argenteum Hedw., Ann. Bot., 1984, vol. 54, p. 195. https://doi.org/10.1093/oxfordjournals.aob.a086783

    Article  Google Scholar 

  33. Carricarte, V.C., Bianchin, G.M., and Muschietti, J.P., Adenilate cyclase activity in a higher plant, alfalfa (Medicago sativa), Biochem. J., 1988, vol. 249, p. 807. https://doi.org/10.1042/bj2490807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Gasumov, K.G., Shichijo, C., Bayramov, S.M., and Hashimoto, T., Membrane and soluble fractions of adenylyl cyclase from Sorghum bicolor seedlings positively react to the action of red and far red lights, Proc. First On-line Conf. on Photochemistry and Photobiology, 1997. http://www.photobiology.com/v1/contrib.htm.

  35. Lusini, P., Trabalzini, L., Franchi, G.G., Bovalini, L., and Martelli, P., Adenilate cyclase in roots of Ricinus comuis: stimulation by GTF and Mn2+, Phytochemistry, 1999, vol. 30, p. 109.

    Article  Google Scholar 

  36. Lomovatskaya, L.A., Romanenko, A.S., Filinova, N.V., and Salyaev, R.K., Influence of exopolysaccharides of the ring rot pathogen on the kinetic parameters of adenylate cyclases in potato plants, Dokl. Biol. Sci., 2011, vol. 441, p. 404.

    Article  CAS  Google Scholar 

  37. Tarchevskii, I.A., Signal’nye sistemy rastenii (Signaling Systems of Plants), Moscow: Nauka, 2002.

  38. Roelofs, J. and van Haastert, P.J., Deducing the origin of soluble adenylyl cyclase, a gene lost in multiple lineages, Mol. Biol. Evol., 2002, vol. 9, p. 2239. https://doi.org/10.1093/oxfordjournals.molbev.a004047

    Article  Google Scholar 

  39. Moutinho, A., Hussey, P. J., Trevawas, A.J., and Malho, R., Cyclic AMP act as a second messenger in pollen tube growth and reorientation, Proc. Natl. Acad. Sci. U.S.A., 2001, vol. 98, p. 10481. https://doi.org/10.1073/pnas.171104598

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Thomas, L., Marondedze, C., Ederli, L., Pasqualini, S., and Gehring, C., Proteomic signatures implicate cAMP in light and temperature responses in Arabidopsis thaliana, J. Proteomics, 2013, vol. 83, p. 47. https://doi.org/10.1016/j.jprot.2013.02.032

    Article  CAS  PubMed  Google Scholar 

  41. Di, D.W., Zhang, C., and Guo, G.Q., Involvement of secondary messengers and small organic molecules in auxin perception and signaling, Plant Cell Rep., 2015, vol. 34, p. 895. https://doi.org/10.1007/s00299-015-1767-z

    Article  CAS  PubMed  Google Scholar 

  42. Cooke, C.J., Smith, C.J., Walton, T.J., and Newton, R.P., Evidence that cyclic AMP is involved in the hypersensitive response of Medicago sativa to a fungal elicitor, Phytochemistry, 1994, vol. 35, p. 889. https://doi.org/10.1016/S0031-9422(00)90633-2

    Article  CAS  Google Scholar 

  43. Jiang, J., Fan, L.W., and Wu, W.H., Evidences for involvement of endogenous cAMP in Arabidopsis defense responses to Verticillium toxins, Cell Res., 2005, vol. 15, p. 585.

    Article  CAS  Google Scholar 

  44. Koumura, Y., Suzuki, T., Yoshikawa, S., Watanabe, M., and Iseki, M., The origin of photoactivated adenylyl cyclase (PAC), the Euglena blue-light receptor: phylogenetic analysis of orthologues of PAC subunits from several euglenoids andtrypanosome-type adenylyl cyclases from Euglena gracilis, Photochem. Photobiol. Sci., 2004, vol. 3, p. 580.

    Article  CAS  Google Scholar 

  45. Blain-Hartung, M., Rockwell, N.C., Moreno, M.V., Martin, S.S., Gan, F., Bryant, D.A., and Lagarias, J.C., Cyanobacteriochrome-based photoswitchable adenylyl cyclases (cPACs) for broad spectrum light regulation of cAMP levels in cells, J. Biol. Chem., 2018, vol. 293, p. 8473. https://doi.org/10.1074/jbc.RA118.002258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Yang, H., Zhao, Y., Chen, N., Liu, Y., Yang, S., Du, H., Wang, W., Wu, J., Tai, F., Chen, F., and Hu, X., A new adenylyl cyclase, putative disease-resistance RPP13-like protein 3, participates in abscisic acid-mediated resistance to heat stress in maize, J. Exp. Bot., 2021, vol. 72, p. 283. https://doi.org/10.1093/jxb/eraa431

    Article  CAS  PubMed  Google Scholar 

  47. Sim, W.-S. and Kim, H.-R., Effect of GA3 on the cyclic AMP biosynthesis in maize seedling, Plant Cell Physiol., 1987, vol. 28, p. 415. https://doi.org/10.1093/oxfordjournals.pcp.a077311

    Article  CAS  Google Scholar 

  48. Uematsu, K., Nakajima, M., Yamaguchi, I., Yoneyama, K., and Fuku, Y., Role of cAMP in gibberellin promotion of seed germination in Orobanche minor Smith, J. Plant Growth Regul., 2007, vol. 26, p. 45.

    Article  Google Scholar 

  49. Duc, N.M., Kim, H.R., and Chung, K.Y., Recent progress in understanding the conformational mechanism of heterotrimeric G protein activation, Biomol. Ther., 2017, vol. 25, p. 4. https://doi.org/10.4062/biomolther.2016.169

    Article  CAS  Google Scholar 

  50. Ito, M., Takahashi, H., Sawasaki, T., Ohnishi, K., Hikichi, Y., and Kiba, A., Novel type of adenylyl cyclase participates in tabtoxinine-β-lactam-induced cell death and occurrence of wildfire disease in Nicotiana benthamiana, Plant Signaling Behav., 2014, vol. 9, p. e27420. https://doi.org/10.4161/psb.27420

    Article  CAS  Google Scholar 

  51. Świeżawska, B., Jaworski, K., Pawełek, A., Grzegorzewska, W., Szewczuk, P., and Szmidt-Jaworska, A., Molecular cloning and characterization of a novel adenylyl cyclase gene, HpAC1, involved in stress signaling in Hippeastrum × hybridum, Plant Physiol. Biochem., 2014, vol. 80, p. 41. https://doi.org/10.1016/j.plaphy.2014.03.010

    Article  CAS  PubMed  Google Scholar 

  52. Ma, Y., Zhao, Y., Walker, R.K., and Berkowitz, G.A., Molecular steps in the immune signaling pathway evoked by plant elicitor peptides: Ca2+-dependent protein kinases, nitric oxide, and reactive oxygen species are downstream from the early Ca2+ signal, Plant Physiol., 2013, vol. 163, p. 1459. https://doi.org/10.1104/pp.113.226068

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Bindschedler, L.V., Minibayeva, F., Gardner, S.L., Gerrish, C., Davies, D.R., and Bolwell, G.P., Early signaling events in the apoplastic oxidative burst in suspension cultured French bean cells involve cAMP and Ca2+, New Phytol., 2001, vol. 151, p. 185. https://doi.org/10.1046/j.1469-8137.2001.00170.x

    Article  CAS  PubMed  Google Scholar 

  54. Bianchet, C., Wong, A., Quaglia, M., Alqurashi, M., Gehringa, C., Ntoukakise, V., and Pasqualinia, S., An Arabidopsis thaliana leucine-rich repeat protein harbors an adenylyl cyclase catalytic center and affects responses to pathogens, J. Plant Physiol., 2019, vol. 232, p. 12. https://doi.org/10.1016/j.jplph.2018.10.025

    Article  CAS  PubMed  Google Scholar 

  55. Chatukuta, P., Dikobe, B., Kawadza, D., Sehlabane, K., Takundwa, M., Wong, A., Gehring, C., and Ruzvidzo, O., An Arabidopsis clathrin assembly protein with a predicted role in plant defense can function as an adenylate cyclase, Biomolecules, 2018, vol. 8, p. 15. https://doi.org/10.3390/biom8020015

    Article  CAS  PubMed Central  Google Scholar 

  56. Newton, R.P., Roef, L., Witters, E., and van Onckelen, H., Tansley review no. 106: Cyclic nucleotides in higher plants: the enduring paradox, New Phytol., 1999, vol. 143, p. 427. https://doi.org/10.1046/j.1469-8137.1999.00478.x

    Article  CAS  PubMed  Google Scholar 

  57. Witters, E., Valcke, R., and van Onckelen, H., Cytoenzymological analysis of adenylyl cyclase activity and 3':5'-cAMP immunolocalization in chloroplasts of Nicotiana tabacum, New Phytol., 2005, vol. 168, p. 709. https://doi.org/10.1111/j.1469-8137.2005.01476.x

    Article  CAS  Google Scholar 

  58. Al-Younis, I., Moosa, B., Kwiatkowski, M., Jaworski, K., Wong, A., and Gehring, C., Functional crypto-adenylate cyclases operate in complex plant proteins, Front. Plant Sci., 2021. https://doi.org/10.3389/fpls.2021.711749

  59. Zhang, H., Gao, Z., Zheng, X., and Zhang, Z., The role of G-proteins in plant immunity, Plant Signaling Behav., 2012, vol. 7, p. 1284. https://doi.org/10.4161/psb.21431

    Article  CAS  Google Scholar 

  60. Guo, T. and Fang, Y., Functional organization and dynamics of the cell nucleus, Front. Plant Sci., 2014, vol. 5, p. 378. https://doi.org/10.3389/fpls.2014.00378

    Article  PubMed  PubMed Central  Google Scholar 

  61. Al-Younis, I., Wong, A., and Gehring, C., The Arabidopsis thaliana K+-uptake permease 7 (AtKUP7) contains afunctional cytosolic adenylate cyclase catalytic centre, FEBS Lett., 2015, vol. 589, p. 3848. https://doi.org/10.1016/j.febslet.2015.11.038

    Article  CAS  PubMed  Google Scholar 

  62. Kasahara, M., Suetsugu, N., Urano, Y., Yamamoto, C., Ohmori, M., Takada, Y., Okuda, S., Nishiyama, T., Sakayama, H., Kohchi, T., and Takahashi, F., An adenylyl cyclase with a phosphodiesterase domain in basal plants with a motile sperm system, Sci. Rep., 2016, vol. 6, p. 39232. https://doi.org/10.1038/srep39232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Yamamoto, C., Takahashi, F., Ooe, Y., Shirahata, H., Shibata, A., and Kasahara, M., Distribution of adenylyl cyclase/cAMP phosphodiesterase gene, CAPE, in streptophytes reproducing via motile sperm, Sci. Rep., 2021, vol. 11, p. 10054. https://doi.org/10.1038/s41598-021-89539-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Wong, A., Tian, X., Gehring, C., and Marondedze, C., Discovery of novel functional centers with rationally designed amino acid motifs, Comput. Struct. Biotechnol. J., 2018, vol. 16, p. 70. https://doi.org/10.1016/j.csbj.2018.02.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Gangwani, L., Khurana, J.P., and Maheshwari, S.C., Inhibition of chloroplast protein phosphorylation by cAMP in Lemna paucicostata 6746, Phytochemistry, 1996, vol. 41, p. 49. https://doi.org/10.1016/0031-9422(95)00616-8

    Article  CAS  Google Scholar 

  66. Kleinboelting, S., Miehling, J., and Steegborn, C., Crystal structure and enzymatic characterization of the putative adenylyl cyclase HpAC1 from Hippeastrum reveal dominant triphosphatase activity, J. Struct. Biol., 2020, vol. 212, p. 107649. https://doi.org/10.1016/j.jsb.2020.1-6

    Article  CAS  PubMed  Google Scholar 

  67. Gehring, C., Adenylyl cyclases and cAMP in plant signaling—past and present, Cell Commun. Signaling, 2010, vol. 8, p. 1.

    Article  Google Scholar 

  68. Wong, A. and Gehrin, C., Computational identification of candidate nucleotide cyclases in higher plants, in Cyclic Nucleotide Signaling in Plants: Methods and Protocols, Totowa, NJ: Humana, 2013.

    Google Scholar 

  69. Leipe, D.D., Koonin, E.V., and Aravind, L., STAND, a class of P-loop NTPases including animal and plant regulators of programmed cell death: multiple, complex domain architectures, unusual phyletic patterns, and evolution by horizontal gene transfer, J. Mol. Biol., 2004, vol. 343, p. 1. https://doi.org/10.1016/j.jmb.2004.08.023

    Article  CAS  PubMed  Google Scholar 

  70. Lomovatskaya, L.A., Romanenko, A.S., and Filinova, N.V., Plant adenylate cyclases: the effect of a biotic stressor on the kinetic parameters of transmembrane and “soluble” forms of adenylate cyclase, Biol. Membr., 2014, vol. 31, p. 129. https://doi.org/10.7868/S0233475514010071

    Article  CAS  Google Scholar 

  71. Pietrowska-Borek, M., Chadzinikolau, T., and Borek, S., Cyclic nucleotides and nucleotide cyclases in plants under stress, in Improvement of Crops in the Era of Climatic Changes, New York: Springer-Verlag, 2014.

    Google Scholar 

  72. Xu, R., Guo, Y., Peng, S., Liu, J., Li, P., Jia, W., and Zhao, J., Molecular targets and biological functions of cAMP signaling in Arabidopsis, Biomolecules, 2021, vol. 11, p. 688. https://doi.org/10.3390/biom11050688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to L. A. Lomovatskaya.

Ethics declarations

Conflict of interests. The authors declare that they have no conflicts of interest.

Statement on the welfare of humans or animals. This article does not contain any studies involving humans or animals performed by any of the authors.

Additional information

Translated by A. Bulychev

Abbreviations: AC—adenylate cyclase; cAMP—cyclic adenosine monophosphate; GPCR—G-protein-coupled receptors; MAMP/PAMP—microbe-/pathogen-associated molecular patterns; sAC—soluble adenylate cyclase; tAC—transmembrane adenylate cyclase.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lomovatskaya, L.A., Kuzakova, O.V. & Romanenko, A.S. Current Views on Plant Adenylate Cyclases. Russ J Plant Physiol 69, 45 (2022). https://doi.org/10.1134/S102144372202011X

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1134/S102144372202011X

Keywords:

Navigation