CYNIPS · Cyclic nucleotides as second messengers in plants

Multicellularity in plants and animals arose independently, as reflected in dramatically different signalling mechanism make-ups. Intracellular signalling’s central paradigm in animals is the concept of ‘second messengers’- most prominently cAMP and cGMP. Contrastingly, in plants, cAMP/cGMP are not part of mainstream ideas on signalling.Our recent, unexpected identification of cAMP and cGMP acting in the canonical signalling for the phytohormone auxin inspired a paradigm-shifting hypothesis that cAMP and cGMP act as largely unappreciated versatile second messengers in multiple plant signalling pathways. This would dramatically expand the modes of plant intracellular signalling, opening possibilities for additional regulations and crosstalks. It would also provide a new means of targeted engineering of signalling outputs, highly relevant for plant biotechnology.To systematically explore this radical hypothesis, I propose to generate (opto)genetic tools to (i) monitor and (ii) specifically manipulate cellular cAMP/GMP levels. Our vRootchip microfluidics set-up allows us to (iii) survey the plant signalling landscape and identify pathways involving cAMP/GMP further supported by (iv) identification of thus-far elusive cAMP/cGMP targets. As a blueprint for the use of the generated tools and knowledge, we plan (v) to elucidate the role of cGMP in phytohormone jasmonate signalling. Together, these approaches will establish cAMP/cGMP as bona fide second messengers in plants. We provide a rich resource to investigate their involvement in any chosen signalling mechanism or cellular response, while offering tools to manipulate their signalling output for both fundamental discoveries and targeted applications.This strategy poses considerable intellectual and methodological challenges, but our robust initial results, including functionality of cAMP/cGMP sensors, show a conceptual breakthrough is feasible, dramatically expanding our current view on plant signalling and beyond.