The unusual combination of the above topics is likely to beg the question, how on earth can these possibly be related? Though, it is through cell signalling that these 4 topics are undoubtedly connected. Additionally, some of the molecules involved that are detailed here may have great economic potential for the agricultural industry.
UVA has a wavelength of 315-400nm and encompasses 95% of the Earth’s radiation from the sun [1]. UVA can initiate various types of DNA damage and can induce photoaging of the skin by penetrating the dermis in humans and interacting with proteins and lipids [2]. However, compared to UVB, very little is known about UVA radiation, and there is no general consensus in the literature about its effects on plants either. Stomata, the pores on the underside of leaves (leaf epidermis), facilitate evapotranspiration. Water vapour loss through the stomata provides the driving force for water and mineral nutrient uptake from the roots to the aerial parts of the plant. As a result, stomata contribute to leaf cooling and offer plants a limited ability in withstanding periods of reduced water availability [3].
We know that in the presence of UVA, light-induced stomatal opening is inhibited and so the stomata close. We also know that the canonical mammalian cyclic guanosine monophosphate (cGMP) signalling system has influenced rationales towards plant signalling, see Figure 1 for a diagrammatic representation of this pathway, but it was previously unknown for sure whether cGMP signalling took place in plants or not. cGMP is an ubiquitous intracellular (IC) second messenger or a signalling molecule found almost everywhere in the body [4]. Protein kinase G (PKG) is its main signal transducer, as it phosphorylates key downstream components and mediates the cGMP signal [5]. Alongside PKG, cGMP-regulated phosphodiesterases (PDEs) and ion channels also contribute [6]. Soluble guanylate cyclase (sGC) stimulates the synthesis of cGMP, and PDE5 degrades cGMP to its constituents: GMP and GTP (guanosine monophosphate and triphosphate). Many pharmacological PDE5 inhibitor compounds can interfere with cGMP signalling and are considered valuable in the pharmaceutical industry, such as Viagra [7].
Figure 1: The canonical cGMP mammalian signalling pathway. Image from [7].
UVA induces reversible decreases in cytosolic cGMP in guard cells, cells that surround the stomata, and it has been confirmed that this response was exclusive to light in the UVA range. But what is the role of the UVA response? Does it have physiological significance? The highest ratios of UVA to blue light are met when the sun is on the horizon or at its midday zenith. This suggests UVA acts as a “brake” on stomatal opening, leading to increased water use efficiency (WUE), which could be the natural physiological significance of this process. Plant fitness in dry environments is greatest for individuals with the highest WUE, as stomata contribute to the control of WUE in plants [8, 9].
Through genetic manipulation of several key genes involved in photosynthesis and the regulation of stomatal opening and closing, the photosynthesis and WUE of plants can be improved [10]. Thus, advances in understanding fundamental processes surrounding stomatal regulation are important for developing plants with improved photosynthesis and WUE. This is a critical priority for regions facing periods of increased drought or diminished groundwater resources, as well as for developing means to increase biomass and crop harvest, which will be important in the future to feed our exponentially growing population [11, 12]. This is especially important as climate change including altered precipitation patterns, elevated CO2, and rising temperatures has been predicted to bring periods of increased water shortage [13].
As previously mentioned, PED5 inhibitors are of high value in the pharmaceutical industry. Nitric oxide (NO) is released during sexual arousal, triggering cGMP synthesis, leading to smooth muscle relaxation and increased penile blood flow [14]. PDE5 inhibitors (i.e. Viagra) competitively compete with cGMP for PDE5 binding to inhibit cGMP hydrolysis, enhancing NO. NO increases cGMP in smooth muscle cells, prolonging an erection [14]. NO has a role in controlling stomatal aperture by inducing stomatal closure [15]. As PDE activity, cGMP signalling, and NO presence have been proven in plants and involved in the mode of action of PDE5 and its inhibitors, could PDE5 inhibitors be present as well?
The discovery of plant-based PDE5 inhibitor analogues could yield great opportunities for the use of plants as factories in the production of these molecules. Alternatively, even if plants don’t produce these molecules, there are advantages for their use on plants instead. Small concentrations of Viagra dissolved in a vase of water have been found to double the shelf life of cut flowers, allowing them to stand up straight for up to a week over their natural life span, and when tested on strawberries and other perishables, their shelf life was dramatically increased as well. Testing with NO yielded the same effect, perhaps through its induction of stomatal closure, to improve WUE [16]. There is economic potential for the use of these molecules to increase the shelf life of various plant-based produce just waiting to be exploited, and so further research regarding this and stomatal regulation is warranted.
Mia Georgiou
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