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

Abstract

Summary 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.

SlTLFP8 reduces water loss to improve water‐use efficiency by modulating cell size and stomatal density via endoreduplication

“…In the short term, plants respond to drought by the influence of stomatal movement on stomatal aperture. For example, stomata open and close, which is mainly regulated by the levels of hormone ABA (He et al, 2018; Li, Han, Su, Guo, & Zhang, 2019; J Li et al, 2017; S. Qi et al, 2019; J. Wang et al, 2018), light (Isner et al, 2019) and nutrient conditions (Schaefer et al, 2018). During evolution, plants adapt to a drought environment by changing stomatal traits, such as stomatal size and stomatal density (Bertolino, Caine, & Gray, 2019; Dow, Bergmann, & Berry, 2014).…”

Light-Mediated Signaling and Metabolic Changes Coordinate Stomatal Opening and Closure

“…In contrast to the well-reported effects of UV-B light, much less is known about the roles of UV-A radiation (315-400 nm) on stomatal movement. Recently, it was shown that Arabidopsis epidermis illuminated with UV-A in combination with blue and red light demonstrated greatly decreased stomatal aperture than those illuminated with only blue and red light, and that the effect was strong at 3 h post exposure and decreases with time (Isner et al, 2019). It is noted that UV-A irradiation could not trigger closure in stomata that had previously been opened by blue and red light illumination.…”

“…Taken together, UV-B and UV-A light signaling acts in concert to limit stomatal opening in periods of strong solar irradiance. Although it was shown that the photoreceptor UVR8 mediates the perception of both UV-B and UV-A wavelengths (Rai et al, 2020), UV-A-mediated stomatal closure does not require UVR8 (Isner et al, 2019). Considering that CRY1 and CRY2 also act as photoreceptors for UVA radiation (Lin et al, 1995), further studies are needed to elucidate how CRY1/2 integrate blue and UV-A light signals to regulate stomatal responses and how decreased cGMP levels mediate the inhibition of blue/red light-induced stomatal opening.…”

Nitrated Nucleotides: New Players in Signaling Pathways of Reactive Nitrogen and Oxygen Species in Plants

“…However, the molecular mechanisms of cGMP signal transduction to cellular effectors, including cGMP-dependent kinases G, are still poorly characterized (Świeżawska et al, 2018). Recent reports described the identification of cGMPdependent protein kinase with a role in mediating gibberellin responses in rice (Shen et al, 2019) and a plant cGMPactivated phosphodiesterase involved in the UVA-induced cGMP degradation in Arabidopsis stomata (Isner et al, 2019). Signaling pathways involved in the regulation of stomatal movements by external stimuli and phytohormones comprise, beside cGMP, diverse components like NO, ROS, cytosolic pH, calcium ions and phospholipids (Daszkowska-Golec and Szarejko, 2013;Gayatri et al, 2013;Agurla et al, 2014;Agurla and Raghavendra, 2016).…”