Physiological Responses to SO in Plants
Plant responses to SO have primarily been studied using a) exogenous photosensitizers that induce SO such as Rose Bengal or Acridine Orange; b) high-light treatments that induce SO; and/or c) Arabidopsis thaliana mutants that exhibit elevated SO accumulation either constitutively (e.g. chlorina1 , or ch1 ) or conditionally (i.e. fluorescent in blue light , or flu ) (You et al., 2018; Dmitrieva et al., 2020). The flu mutant has a normal phenotype when grown under continuous light; however, if transferred to the dark, it accumulates a potent photosensitizer (protochlorophyllide, or Pchlide) in the chloroplast that generates SO when the plants are reilluminated (Meskauskiene et al., 2001; Op den Camp et al., 2003). The amount of SO that accumulates in flu mutants exposed to a Light:Dark:Light (L:D:L) shift can to some extent be modulated by manipulating the duration of the dark period and the light intensity after re-exposure (Lee et al. 2007; Hou et al. 2019). While these approaches cannot perfectly duplicate the timing, localization, and intensity of SO accumulation in wild-type plants experiencing stress, they have dramatically advanced our understanding of plant responses to high SO levels.
Cellular responses to SO vary depending upon the dosage of this ROS. Titers of SO and other ROS in cells are a product of the balance between generation and scavenging. Under optimal growing conditions, even though SO is continuously produced at PSII, it is quickly scavenged by nearby non-enzymatic antioxidants such as carotenoids or tocopherols, limiting its impact on the cell (Asada, 2006). While SO generation is a consequence photosynthesis even in healthy plants, elevated SO levels are observed in response to many environmental stresses that disrupt the photosynthetic machinery at PSII and/or PSI, such as high light, heat, heavy metals, mechanical injury, and osmotic stress (Pospíšil & Prasad, 2014; Chen & Fluhr, 2018). In extreme cases, SO accumulates to toxic levels that cause membrane rupture and consequent cell necrosis as a result of direct interaction of SO with membrane lipids, termed non-enzymatic lipid peroxidation. Between healthy baseline SO levels on one hand and levels that are high enough to cause necrosis on the other, intermediate doses trigger retrograde signaling for a spectrum of plant stress responses ranging from cellular acclimation to programmed cell death (PCD) (Dmitrieva et al., 2020).
The physiological impacts of SO also depend upon its localization. In the cytosol (and possibly also the nucleus), SO oxidizes mRNA and can thereby decrease expression of transcripts that have high turnover (Koh et al. 2021). In the chloroplast, SO damages the D1 protein in PSII, which can inhibit photosynthesis and retard growth unless rates of D1 repair and replacement are high (Dogra and Kim, 2020). SO in the chloroplast also activates retrograde signaling and transcriptional reprogramming, leading to stress acclimation or PCD (discussed in greater depth in the next section). SO localized at cellular membranes oxidizes membrane lipids, causing decreased integrity of the chloroplast membranes, vacuole leakage, and electrolyte leakage across the plasma membrane (Przybyla et al., 2008; Zhang et al. 2014; Koh et al., 2016); membrane damage can also cause cell death. Although it has yet to be tested in plant cells, artificial SO generation at membranes in mammalian cells strongly induces apoptosis, whereas SO accumulation in the mitochondria or nucleus causes less frequent cell death, via necrosis rather than PCD (Liang et al., 2020). In plants, SO-induced necrosis is considered to be relatively rare, and acclimation and even cell death in response to SO are thought to be genetically programmed and mediated through signaling (Op den Camp et al., 2003; Wagner et al. 2004). Research on SO signaling has focused primarily on the chloroplast as the source of signals because it is the greatest source of SO in the cell.