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Plant adenylate cyclases have come full circle

Nature Plants volume 9, pages 1389–1397 (2023)Cite this article

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Abstract

In bacteria, fungi and animals, 3′-5′-cyclic adenosine monophosphate (cAMP) and adenylate cyclases (ACs), enzymes that catalyse the formation of 3′,5′-cAMP from ATP, are recognized as key signalling components. In contrast, the presence of cAMP and its biological roles in higher plants have long been a matter of controversy due to the generally lower amounts in plant tissues compared with that in animal and bacterial cells, and a lack of clarity on the molecular nature of the generating and degrading enzymes, as well as downstream effectors. While treatment with 3′,5′-cAMP elicited many plant responses, ACs were, however, somewhat elusive. This changed when systematic searches with amino acid motifs deduced from the conserved catalytic centres of annotated ACs from animals and bacteria identified candidate proteins in higher plants that were subsequently shown to have AC activities in vitro and in vivo. The identification of active ACs moonlighting within complex multifunctional proteins is consistent with their roles as molecular tuners and regulators of cellular and physiological functions. Furthermore, the increasing number of ACs identified as part of proteins with different domain architectures suggests that there are many more hidden ACs in plant proteomes and they may affect a multitude of mechanisms and processes at the molecular and systems levels.

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Fig. 1: ACs moonlighting in proteins with diverse domain architecture.
Fig. 2: Plant ACs act as molecular tuners in localized signalling environments.
Fig. 3: Plant ACs regulate key biological processes.

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Acknowledgements

We acknowledge technical and logistical support provided by the Wenzhou Municipal Key Lab for Applied Biomedical and Biopharmaceutical Informatics and the Zhejiang Bioinformatics International Science and Technology Cooperation Center. This research was supported by grants from the National Natural Science Foundation of China (32100581) and the International Collaborative Research Program of Wenzhou-Kean University (ICRP202202) awarded to A.W.

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Authors and Affiliations

  1. Department of Biology, College of Science, Mathematics and Technology, Wenzhou-Kean University, Wenzhou, Zhejiang Province, China

    Aloysius Wong, Wei Chi, Jia Yu, Chuyun Bi, Xuechen Tian & Yixin Yang

  2. Wenzhou Municipal Key Lab for Applied Biomedical and Biopharmaceutical Informatics, Wenzhou, Zhejiang Province, China

    Aloysius Wong, Chuyun Bi, Xuechen Tian & Yixin Yang

  3. Zhejiang Bioinformatics Internatiosnal Science and Technology Cooperation Center, Wenzhou, Zhejiang Province, China

    Aloysius Wong, Chuyun Bi, Xuechen Tian & Yixin Yang

  4. Department of Chemistry, Biology and Biotechnology, University of Perugia, Perugia, Italy

    Chris Gehring

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Contributions

A.W. and C.G. conceived the idea, analysed the data and wrote the paper. W.C., and J.Y. analysed the data and generated the supplementary table. Y.Y. analysed the data and wrote the paper. C.B. and X.T. analysed the data and generated the figures.

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Correspondence to Aloysius Wong or Chris Gehring.

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Nature Plants thanks Lo Lomovatskaya, Ruqiang Xu and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary Information

Supplementary Table 1.

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Wong, A., Chi, W., Yu, J. et al. Plant adenylate cyclases have come full circle. Nat. Plants 9, 1389–1397 (2023). https://doi.org/10.1038/s41477-023-01486-x

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