Short- and Long-Term Effects of UVA on Arabidopsis Are Mediated by a Novel cGMP Phosphodiesterase

Although UVA radiation (315–400 nm) represents 95% of the UV radiation reaching the earth’s surface, surprisingly little is known about its effects on plants [1]. We show that in Arabidopsis, short-term exposure to UVA inhibits the opening of stomata, and this requires a reduction in the cytosolic level of cGMP. This process is independent of UVR8, the UVB receptor. A cGMP-activated phosphodiesterase (AtCN-PDE1) was responsible for the UVA-induced decrease in cGMP in Arabidopsis. AtCN-PDE1-like proteins form a clade within the large HD-domain/PDEase-like protein superfamily, but no eukaryotic members of this subfamily have been functionally characterized. These genes have been lost from the genomes of metazoans but are otherwise conserved as single-copy genes across the tree of life. In longer-term experiments, UVA radiation increased growth and decreased water-use efficiency. These experiments revealed that PDE1 is also a negative regulator of growth. As the PDE1 gene is ancient and not represented in animal lineages, it is likely that at least one element of cGMP signaling in plants has evolved differently to the system present in metazoans. •UVA inhibits stomatal opening, and this requires a reduction in the cytosolic cGMP•UVA-induced decrease in cGMP was caused by a cGMP phosphodiesterase (AtcnPDE1)•UVA radiation increased growth and decreased water use efficiency•cnPDE1 is ancient and has been lost from animal lineages Isner et al. show that UVA radiation inhibits stomatal opening in Arabidopsis. This requires a reduction in cytosolic cGMP, mediated by a cGMP-activated phosphodiesterase (AtCN-PDE1) that is conserved across the tree of life, except in metazoans, where it has been lost. They also show that UVA increases growth and decreases water use efficiency.