SO Signaling In Plants
Because of SO’s extremely high reactivity in aqueous and organic solutions, and the abundance of ROS scavengers in cells, SO has been estimated to have half-life of 200 ns in biological environments (Gorman & Rodgers, 1992). Therefore, responses to intracellular sources of SO are likely due to interactions with biomolecules close to the site of production that initiate a chloroplast-to-nucleus retrograde signal. These may be β-carotene near PSII reaction centers, lipids of chloroplast membranes, or proteins embedded in the thylakoid membrane (Wagner et al., 2004; Przybyla et al., 2008; Ramel et al., 2012b). InA. thaliana , there appears to be more than one distinct pathway for SO retrograde signaling (Figure 2), but detection of SO by the EXECUTOR1 protein in the grana margins or carotenoid signaling in the grana core are of particular importance.
SO Sensing by EXECUTER1. EXECUTER1 (EX1) and its homolog EXECUTER2 (EX2) were originally discovered as a result of work with the conditional flu mutant (Meskauskiene et al., 2001), and they modulate most of the phenotypes generated by SO induction in flu . The amount of SO that accumulates in L:D:L-exposed flu mutants varies depending upon the duration of the dark period and the light intensity of re-exposure (Lee et al. 2007; Hou et al. 2019). As a result, this mutant can be utilized to study both programmed cell death (PCD) in response to high SO dosages, or stress acclimation programs activated by sub-lethal SO doses. Experiments with the flu mutant demonstrate that EX1 plays a role in both of these processes, and reduces or blocks the majority of phenotypes caused by flu (e.g. Lee et al., 2007; Zhang et al., 2014). Exposing flu to 8h of darkness followed by reillumination halts plant growth, induces the formation of lesions on foliage, modulates expression of a large set of SO-responsive genes (SORGs), and activates multiple hormone signaling pathways (Ochsenbein et al., 2006; Lee et al., 2007; Przybyla et al., 2008). Introducing the ex1 loss-of function mutation into theflu background inhibited lesion formation, restored growth, and blocked the induction of ~80% of SORGs, whereas EX2 was not required for induction of most SORGs (Lee et al., 2007). EX1 also contributes to the effects of SO on hormone signaling. Przybyla and coworkers (2006) demonstrated that exposing flu to L:D:L shift induced enzymatic lipid peroxidation and accumulation of the oxylipin hormones 12-oxo phytodienoic acid (OPDA) and jasmonic acid, whereas these responses were inhibited in the flu/ex1 double mutant (Przybyla et al., 2008). The L:D:L shift also has been shown to cause a rapid upregulation of ENHANCED DISEASE SUSCEPTIBILITY1(EDS1 ) and salicylic acid (SA) accumulation, which consequently activated expression of genes encoding pathogenesis-related (PR) proteins PR1 and PR5 (Ochsenbein et al., 2006). In protoplasts, SA contributed to the cell death phenotype observed influ (Danon et al., 2005). Zheng and coworkers (2014) subsequently showed that PR1 induction was compromised in theflu /ex1/ex2 triple mutant, suggesting that induction of SA signaling by SO is dependent upon EX1.
The complex molecular processes through which EX1 and EX2 mediate plant responses to SO are not yet fully resolved, but recent studies have made major advances in deciphering them. The EX1 and EX2 proteins are localized to the non-appressed region of the thylakoid membrane called the grana margin (Wang et al., 2016), where, prior to stimulation by SO, they complex with several other proteins, including GENOMES UNCOUPLED4 (GUN4) and GUN5, proteins involved in tetrapyrrole synthesis (Li et al. 2023). In response to SO accumulation, EX1 undergoes oxidative modification, disassociates from the complex, and accumulates in the nucleus, where it interacts directly with WRKY transcription factors and gene promoters to activate expression of SORGs (Li et al. 2023). In parallel, exposure to SO also causes a dose-dependent decline in EX1 abundance that requires a functional copy of the thylakoid membrane-bound metalloprotease FtsH2 (Wang et al., 2016; Dogra et al., 2017). Inactivation of FtsH2 repressed induction of ~85% of EX1-dependent SORGs in flu , implying that proteolysis of EX1 by FtsH2 is important to its function in SO-responsive signaling (Dogra et al., 2017). Like EX1, EX2 can also undergo oxidative modification by SO and proteolysis by FtsH2, and the presence of a functional copy of EX2 slows down proteolysis of EX1 and decreases expression of EX1-dependent SORGs (Dogra et al., 2022). These results suggest that EX2 acts as a negative modulator of EX1 signaling, tapping the brakes on this system by competing with EX1 to interact with SO or FtsH2.
Further work is needed to determine how and why proteolysis of EX1 promotes EX1-dependent regulation. The EX1 proteins found in the nucleus after SO induction are full-length (Li et al. 2023), and so it appears that there are two separate pools of EX1 in the cell—one that moves to the nucleus to act as a transcriptional activator, and one that remains in the chloroplast to be degraded. Somehow these pools act synergistically to promote SORG expression. Another important question that remains to be resolved is the source of ROS that oxidizes EX1 and EX2 after SO induction. The typical site of SO production occurs from active PSII in the appressed thylakoid (grana core) during photosynthesis. However, the reactive nature and short half-life of SO (Gorman and Rodgers, 1992) severely reduce the likelihood of this ROS traveling from the grana core to the grana margin. It is possible that SO in the grana core triggers production of other more stable ROS that move to the grana margins to modify EX1 and EX2. Alternatively, it has been proposed that there is an additional mechanism to generate SO in the grana margin via chlorophyll precursors or damaged PSII subunits sent to the grana margins for repair (Wang et al., 2016; Dogra and Kim, 2020). EX1 and EX2 coprecipitate with multiple proteins including the PSII D1 and D2 proteins and proteins involved in chlorophyll synthesis, including GUN4, GUN5, and Pchlide oxidoreductases (Dogra et al., 2022; Li et al. 2023). GUN4 and GUN5 are upstream of Pchlide synthesis in the chlorophyll synthesis pathway, whereas Pchlide oxidoreductases convert Pchlide to chlorophyllide, and so the balance of activities among these enzymes could regulate Pchlide accumulation. GUN4 has been implicated in SO generation (Tabrizi et al., 2016), and together with GUN5, it may promote Pchlide synthesis and SO generation in the grana margins, causing oxidation of EX1 and activation of EX1 signaling. Additional studies are needed to confirm the source of ROS at the grana margins and the functional significance of EX1’s multiple interaction partners.
Carotenoids and Other SO Signaling Pathways. In addition to the EXECUTOR pathway, which can mediate stress-responsive programmed cell death or at lower SO dosages enable stress acclimation, β-carotene derivatives also play a role in acclimation to high light stress (Ramel et al., 2012a, 2013). The ch1 mutant, which accumulates excess SO in the grana core, is commonly used to study the role of carotenoids in SO signaling. The reaction of SO with carotenoid scavengers near the reaction center of PSII yields aldehydes and endoperoxides through oxidative modification (Ramel et al., 2012a). Specifically, oxidation of the carotenoid β-carotene by SO gives rise to β-cyclocitral (β-CC), a volatile, highly reactive electrophilic compound that can then diffuse out of the chloroplast to signal for an acclimation response to high light stress (Ramel et al., 2012a). Importantly, β-CC generation occurs in the grana core of the thylakoid membrane where active PSII reside, whereas EX1 and EX2 are localized in the grana margins, where damaged D1 and D2 proteins of the PSII reaction centers are sent for repair (Dogra and Kim, 2020). Thus, the β-CC and EXECUTER pathways are not initiated in the same area, or by the same SO-generating mechanism, and remain relatively distinct from one another.
Pretreating A. thaliana with β-CC upregulated genes associated with oxidative stress, hormone signaling, and detoxification, and rendered plants more tolerant to high light exposure in a dose-dependent manner (Ramel et al., 2012a). It has been proposed that the protein METHYLENE BLUE SENSITIVITY (MBS1) is activated downstream of β-CC to transduce the signal to the nucleus for regulation of plant growth and development under high light stress (Shumbe et al., 2017). In addition, D’Alessandro and colleagues (2018) identified Scarecrow-Like14(SLC14 ) as another downstream mediator of the SO signal transduced by β-CC that acts independently of MBS1. SLC14, a GRAS family transcription factor, further regulates the expression of NAC transcription factors, and a transgenic line overexpressing SLC14was found to have enhanced resilience to high light stress, indicatingSLC14 is involved in photooxidative adaptation. However, the authors also discovered that only 30% of gene expression changes inch1 mutants under high light stress were due to β-CC (Shumbe et al., 2017). Therefore, it is likely that multiple pathways of SO signaling exist for adaptation under high light stress and defense against other abiotic and biotic stressors. Consistent with this hypothesis, Wang and coworkers (2020) report the existence of an EX1-dependent signaling pathway that is negatively regulated by a protein in the chloroplast stroma, SAFEGAURD1, that is degraded in response to SO (SAFE1). SAFE1 protects the grana margins from damage by SO in flu plants, and loss of function of SAFE1 in aflu /ex1 background restores the cell death phenotype and many of the transcriptional responses to SO that are seen in flubut normally suppressed by ex1 . Another EX1-independent response factor is OXIDATIVE SIGNAL INDUCIBLE1 (OXI1), a kinase that mediates SO-responsive cell death in the ch1 mutant, probably through a jasmonate-dependent signaling mechanism (Shumbe et al. 2016). It is unclear whether carotenoid signaling promotes OXI1 signaling. Further studies are needed to characterize EX1-independent pathways, examine the potential interconnections among the different SO signaling pathways, and definitively establish their roles in wild-type responses to SO and SO-generating stresses. However, markers associated with known SO signaling pathways give us a good starting point to identify stresses that activate SO signaling in plants.