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.