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Cyclic AMP deficiency negatively affects cell growth and enhances stress-related responses in tobacco Bright Yellow-2 cells

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Abstract

Cyclic adenosine 3′,5′-monophosphate (cAMP) is a recognized second messenger; however, knowledge of cAMP involvement in plant physiological processes originates primarily from pharmacological studies. To obtain direct evidence for cAMP function in plants, tobacco Bright Yellow-2 (BY-2) cells were transformed with the cAMP sponge, which is a genetically encoded tool that reduces cAMP availability. BY-2 cells expressing the cAMP sponge (cAS cells), showed low levels of free cAMP and exhibited growth inhibition that was not proportional to the cAMP sponge transcript level. Growth inhibition in cAS cells was closely related to the precocious inhibition of mitosis due to a delay in cell cycle progression. The cAMP deficiency also enhanced antioxidant systems. Remarkable changes occurred in the cAS proteomic profile compared with that of wild-type (WT) cells. Proteins involved in translation, cytoskeletal organization, and cell proliferation were down-regulated, whereas stress-related proteins were up-regulated in cAS cells. These results support the hypothesis that BY-2 cells sense cAMP deficiency as a stress condition. Finally, many proteasome subunits were differentially expressed in cAS cells compared with WT cells, indicating that cAMP signaling broadly affects protein degradation via the ubiquitin/proteasome pathway.

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Acknowledgments

The authors thank Prof. M. Hofer (Boston Healthcare System, Brigham and Women’s Hospital and Harvard Medical School of Massachusetts, USA) for kindly providing “cAMP-sponge”. This work was financially supported by the Italian Ministry of University and Research (FIRB-Futuro in Ricerca n° RBFR10S1LJ_002).

Author contributions

Conceptualization, M.C.d.P.; Investigation, W.S., A.S., M.M., A.P. and F.O.; Methodology, L.V. and E.B.; Validation and data curation, W.S., C.V. and M.C.d.P.; Writing—original draft, W.S., C.V. and M.C.d.P.; Writing—review and editing, W.S., C.V., M.B:, L.V., E.B. and M.C.d.P.; Funding acquisition, E.B., L.V. and M.C.d.P.; Supervision, M.C.d.P.

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Authors and Affiliations

  1. Istituto di Bioscienze e Biorisorse, CNR, Via G. Amendola 165/A, 70126, Bari, Italy

    Wilma Sabetta & Emanuela Blanco

  2. Dipartimento di Biotecnologie e Scienze della Vita, Università degli Studi dell’Insubria, Via H. J. Dunant 3, 21100, Varese, Italy

    Candida Vannini, Milena Marsoni, Francesca Ortolani & Marcella Bracale

  3. Dipartimento di Biologia, Università degli Studi di Bari “Aldo Moro”, via E. Orabona 4, 70125, Bari, Italy

    Alessandra Sgobba, Annalisa Paradiso, Luigi Viggiano & Maria Concetta de Pinto

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  1. Wilma Sabetta
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Correspondence to Maria Concetta de Pinto.

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Fig. S1

Representative 2DE gels of WT and cAS cells (PDF 857 kb)

Table S1

Cell length and cell viability in WT and cAS lines (DOCX 13 kb)

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Sabetta, W., Vannini, C., Sgobba, A. et al. Cyclic AMP deficiency negatively affects cell growth and enhances stress-related responses in tobacco Bright Yellow-2 cells. Plant Mol Biol 90, 467–483 (2016). https://doi.org/10.1007/s11103-016-0431-5

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