Cyclic nucleotides as second messengers in plants

Introduction

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.

Hypothesis

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.

Implications for Biotechnology

It would also provide a new means of targeted engineering of signalling outputs, highly relevant for plant biotechnology.

Proposed Methodology

To systematically explore this radical hypothesis, I propose to generate (opto)genetic tools to:

1. Monitor cellular cAMP/GMP levels.
2. Specifically manipulate cellular cAMP/GMP levels.

Our vRootchip microfluidics set-up allows us to:

3. Survey the plant signalling landscape and identify pathways involving cAMP/GMP.
4. Identify thus-far elusive cAMP/cGMP targets.

As a blueprint for the use of the generated tools and knowledge, we plan to:

5. Elucidate the role of cGMP in phytohormone jasmonate signalling.

Expected Outcomes

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.

Challenges and Feasibility

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.