Endogenous cAMP elevation in Brassica napus causes changes in phytohormone levels

ABSTRACT

In higher plants, the regulatory roles of cAMP (cyclic adenosine 3′,5′-monophosphate) signaling remain elusive until now. Cellular cAMP levels are generally much lower in higher plants than in animals and transiently elevated for triggering downstream signaling events. Moreover, plant adenylate cyclase (AC) activities are found in different moonlighting multifunctional proteins, which may pose additional complications in distinguishing a specific signaling role for cAMP. Here, we have developed rapeseed (Brassica napus L.) transgenic plants that overexpress an inducible plant-origin AC activity for generating high AC levels much like that in animal cells, which served the genetic model disturbing native cAMP signaling as a whole in plants. We found that overexpression of the soluble AC activity had significant impacts on the contents of indole-3-acetic acid (IAA) and stress phytohormones, i.e. jasmonic acid (JA), abscisic acid (ABA), and salicylic acid (SA) in the transgenic plants. Acute induction of the AC activity caused IAA overaccumulation, and upregulation of TAA1 and CYP83B1 in the IAA biosynthesis pathways, but also simultaneously the hyper-induction of PR4 and KIN2 expression indicating activation of JA and ABA signaling pathways. We observed typical overgrowth phenotypes related to IAA excess in the transgenic plants, including significant increases in plant height, internode length, width of leaf blade, petiole length, root length, and fresh shoot biomass, as well as the precocious seed development, as compared to wild-type plants. In addition, we identified a set of 1465 cAMP-responsive genes (CRGs), which are most significantly enriched in plant hormone signal transduction pathway, and function mainly in relevance to hormonal, abiotic and biotic stress responses, as well as growth and development. Collectively, our results support that cAMP elevation impacts phytohormone homeostasis and signaling, and modulates plant growth and development. We proposed that cAMP signaling may be critical in configuring the coordinated regulation of growth and development in higher plants.

KEYWORDS:

• Adenylate cyclase
• cyclic AMP
• phytohormone
• signaling
• Brassica napus

Acknowledgments

The authors would like to thank Dr Shufen Zhang, Henan Academy of Agricultural Sciences, for kindly providing Brassica napus cv. P300 seeds.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Author contributions

Conceptualization, RX; methodology, RX, TL, WJ, SP, and YG; investigation, TL, WJ, SP, and YG; validation, TL, JL, XZ, and PL; writing – original draft, TL and RX; writing – review & editing, RX; visualization, TL, WJ, SP, and YG; supervision and funding acquisition, RX and HZ. All the authors have read and approved the final manuscript.

Data availability statement

All data generated or analyzed during this study are included in this article and its supplementary information files.

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/15592324.2024.2310963

Additional information

Funding

This work was supported by the Major Scientific Research Project of Henan Higher Education Institutions [No. 23A210016], the Key Technologies Research & Development Program of Henan Province [No. 202102110024], the Natural Science Foundation of Henan Province [No. 212300410276], and the Natural Science Foundation of China [No. 32101661].