High salinity, an adverse environmental factor affecting about 20% of irrigated arable land worldwide, inhibits plant growth and development by causing oxidative stress, damaging cellular components, and disturbing global metabolism. However, whether and how reactive oxygen species disturb the metabolism of salt-stressed plants remain elusive. Here, we report that salt-induced hydrogen peroxide (H₂O₂) inhibits the activity of plastid triose phosphate isomerase (pdTPI) to promote methylglyoxal (MG) accumulation and stimulates the sulfenylation of pdTPI at cysteine 74. We also show that MG is a key factor limiting the plant growth, as a decrease in MG levels completely rescued the stunted growth and repressed salt stress tolerance of the pdtpi mutant. Furthermore, targeting CATALASE 2 into chloroplasts to prevent salt-induced overaccumulation of H₂O₂ conferred salt stress tolerance, revealing a role for chloroplastic H₂O₂ in salt-caused plant damage. In addition, we demonstrate that the H₂O₂-mediated accumulation of MG in turn induces H₂O₂ production, thus forming a regulatory loop that further inhibits the pdTPI activity in salt-stressed plants. Our findings, therefore, illustrate how salt stress induces MG production to inhibit the plant growth.

Osmotic stress severely affects plant growth and development, resulting in massive loss of crop quality and quantity worldwide. The 70-kDa heat shock proteins (HSP70s) are highly conserved molecular chaperones that play essential roles in cellular processes including abiotic stress responses. However, whether and how plastid-targeted heat shock cognate 70 kDa protein (cpHSC70-1) participates in plant osmotic stress response remain elusive. Here, we report that the expression of cpHSC70-1 is significantly induced upon osmotic stress treatment. Phenotypic analyses reveal that the plants with cpHSC70-1 deficiency are sensitive to osmotic stress and the plants overexpressing cpHSC70-1 exhibit enhanced tolerance to osmotic stress. Consistently, the expression of the stress-responsive genes is lower in cphsc70-1 mutant but higher in 35S:: cpHSC70-1 lines than that in wild-type plants when challenged with osmotic stress. Further, the cphsc70-1 plants have less APX and SOD activity, and thus more ROS accumulation than the wild type when treated with mannitol, but the opposite is observed in the overexpression lines. Overall, our data reveal that cpHSC70-1 is induced and functions positively in plant response to osmotic stress by promoting the expression of the stress-responsive genes and reducing ROS accumulation.

Climate change is resulting in more frequent and rapidly changing temperatures at both extremes that severely affect the growth and production of plants, particularly crops. Oxidative stress caused by high temperatures is one of the most damaging factors for plants. However, the role of hydrogen peroxide (H₂O₂) in modulating plant thermotolerance is largely unknown, and the regulation of photorespiration essential for C3 species remains to be fully clarified. Here, we report that heat stress promotes H₂O₂ accumulation in chloroplasts and that H₂O₂ stimulates sulfenylation of the chloroplast-localized photorespiratory enzyme 2-phosphoglycolate phosphatase 1 (PGLP1) at cysteine 86, inhibiting its activity and promoting the accumulation of the toxic metabolite 2-phosphoglycolate. We also demonstrate that PGLP1 has a positive function in plant thermotolerance, as PGLP1 antisense lines have greater heat sensitivity and PGLP1-overexpressing plants have higher heat-stress tolerance than the wild type. Together, our results demonstrate that heat-induced H₂O₂ in chloroplasts sulfenylates and inhibits PGLP1 to modulate plant thermotolerance. Furthermore, targeting CATALASE2 to chloroplasts can largely prevent the heat-induced overaccumulation of H₂O₂ and the sulfenylation of PGLP1, thus conferring thermotolerance without a plant growth penalty. These findings reveal that heat-induced H₂O₂ in chloroplasts is important for heat-caused plant damage.

Arabidopsis thaliana (Arabidopsis) Ataxia Telangiectasia Mutated (ATM) kinase plays a vital role in orchestrating leaf senescence; however, the precise mechanisms remain elusive. Here, our study demonstrates that ATM kinase activity is essential for mitigating age- and reactive oxygen species-induced senescence, as restoration of wild-type ATM reverses premature senescence in the atm mutant, while a kinase-dead ATM variant is ineffective. ATM physically interacts with and phosphorylates Mitogen-Activated Protein Kinase Phosphatase 2 (MKP2) to enhance stability under oxidative stress. Mutations in putative phosphorylation sites S15/154 on MKP2 disrupt its phosphorylation, stability, and senescence-delaying function. Moreover, mutation of mitogen-activated protein kinase 6, a downstream target of MKP2, alleviates the premature senescence phenotype of the atm mutant. Notably, the dual-specificity protein phosphatase 19 (HsDUSP19), a predicted human counter protein of MPK2, interacts with both ATM and HsATM and extends leaf longevity in Arabidopsis when overexpressed. These findings elucidate the molecular mechanisms underlying the role of ATM in leaf senescence and suggest that the ATM-MKP2 module is likely evolutionarily conserved in regulating the aging process across eukaryotes.