Cyclic GMP: the new kid on the plant cell signalling block

Cyclic guanosine monophosphate (cGMP) is a nucleotide consisting of three functional groups: a sugar, a nitrogenous base (guanine) and a single phosphate group. It should not be confused with non-cyclic GMP:

cGMP and GMP comparison

In Cyclic GMP one of the oxygen molecules on the phosphate group is bound to the sugar group (highlighted in red). Image credits: Wikimedia Commons users Diberri (cGMP) and Cacycle (GMP) distributed under CC BY-SA 3.0 licences (Links in references)

In animals cGMP can act as a signalling molecule involved in processes including smooth muscle contraction, phototransduction in the eye and blood vessel dilation. In all these cases nitric oxide (NO) is produced and this stimulates activity of a guanylate cyclase to produce cGMP from guanosine triphosphate (GTP).

Recently, evidence has been emerging that cGMP may have a role in plant cell signalling too. NO can induce increases in cGMP in a number of plant species including soybean (Glycine max) and Arabidopsis thaliana (1,2). Also, an NO-sensitive guanylate cyclase has been identified in A. thaliana (3) . So it seems that like animals, plants also have NO-dependent cGMP production.

NO is involved in many plant signalling processes including stomatal closure. Stomata are pores in the surface of plant leaves that allow gases such as carbon dioxide (CO2) to diffuse in and out of the leaf. Water also diffuses out of leaves through the stomata so plants regulate stomata opening and closing to avoid excessive water loss but at the same time balance the need for CO2 for photosynthesis. Abscisic acid (ABA) is a plant “stress” hormone and can induce stomatal closure mediated by NO. A guanylate cyclase inhibitor inhibits ABA-induced stomatal closure suggesting cGMP production is required for ABA-induced stomatal closure (Neill, 2002). However, cGMP treatment alone does not induce stomatal closure so although it is required, it is not sufficient (Neill, 2002). In animals cGMP can be nitrated to form 8-nitro-cGMP. Could 8-nitro-cGMP be the signalling molecule mediating stomatal closure instead?

In a recent paper Joudoi and colleagues showed for the first time that 8-nitro-cGMP is produced in plants (4). They then used a technique called immunocytochemistry to visualise 8-nitro-cGMP in Arabidopsis thaliana guard cells (the cells that frame the stomatal pore) after various treatments (see original paper for figures). They found that ABA can induce 8-nitro-cGMP synthesis in guard cells and that this synthesis is dependent on cGMP. They also found that 8-nitro-cGMP treatment was able to induce stomatal closure in wild type plants and in an NO-dependent guanylate cyclase mutant (nogc-1), which is also defective for normal ABA-induced stomatal closure).

To place 8-nitro-cGMP within the existing ABA-induced stomatal closure signalling pathway the authors examine 8-nitro-cGMP production in other situations. They found that 8-nitro-cGMP production is dependent on reactive oxygen species, which are induced by ABA, and they suggest that NO and reactive oxygen species react to create reactive nitrogen species that could then nitrate cGMP. The slac-1 mutant is defective in ABA-induced stomatal closure. 8-nitro-cGMP was unable to induce stomatal closure in slac-1. This suggests that 8-nitro-cGMP lies upstream of the SLAC-1 anion channel, which mediates stomatal closure by activating the movement of water molecules out of guard cells.

Model of ABA-induced stomatal closure during the day. ABA induces NO production leading to the activation of NOGC producing cGMP from GTP. Nitration of cGMP requires NO and reactive oxygen species (ROS). 8-nitro-cGMP induces SLAC1 leading to net movement of water out of the guard cells and stomatal closure. For a more detailed model see reference (4).

Model of ABA-induced stomatal closure during the day. ABA induces NO production leading to the activation of NOGC producing cGMP from GTP. Nitration of cGMP requires NO and reactive oxygen species (ROS). 8-nitro-cGMP induces SLAC1 leading to net movement of water out of the guard cells and stomatal closure. For a more detailed model see reference (4).

Alongside being required for 8-nitro-cGMP synthesis, cGMP itself can act as a signal molecule regulating stomata. While 8-nitro-cGMP can activate stomatal closure in the light, cGMP can activate stomatal opening in the dark. Therefore nitration of cGMP seems to be acting as a switch between stomatal opening and closing.

This research raises plenty of questions including: what does 8-nitro-cGMP interact with during the activation of stomatal closure? And how does cGMP activate stomatal opening in the dark? NO is involved in many signalling processes in plants including pathogen defence and programmed cell death. Are cGMP and 8-nitro-cGMP also involved in these processes?

This is exciting development and I’m looking forward to hearing more about cGMP and 8-nitro-cGMP in the future.

References:

1) Suita et al., (2009) Cyclic GMP acts as a common regulator for the transcriptional activation of the flavonoid biosynthetic pathway in soybean. Planta.

2) Dubovskaya et al., (2011) cGMP-dependent ABA-induced stomatal closure in the ABA-insensitive Arabidopsis mutant abi1-1. New Phytologist.

3) Mulaudzi et al., (2011) Identification of a novel Arabidopsis thaliana nitric oxide-binding molecule with guanylate cyclase activity in vitro. FEBS Letters.

4) Joudoi et al., (2013) Nitrated cyclic GMP modulates guard cell signaling in Arabidopsis. Plant Cell.

Image links: cGMP and GMP

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One thought on “Cyclic GMP: the new kid on the plant cell signalling block

  1. Pingback: Morsels for the mind – 26/7/2013 › Six Incredible Things Before Breakfast

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