Heat-induced methylglyoxal impairs plant thermotolerance by repressing cpHSC70-1-mediated chloroplast protein import via post-translational modification.
It is demonstrated that heat stress induces the accumulation of the photorespiratory metabolite 2-phosphoglycolate (2PG), which inhibits the activity of plastid triose phosphate isomerase (pdTPI), leading to increased MG levels.
Abstract
Global warming threatens agricultural productivity, making it crucial to understand how plants perceive and respond to heat stress. Although various metabolic pathways are known to participate in plant heat responses, the role of metabolites in post-translational regulation under heat stress remains poorly understood. Here, we report that methylglyoxal (MG) functions as a negative modulator of plant thermotolerance. We demonstrate that heat stress induces the accumulation of the photorespiratory metabolite 2-phosphoglycolate (2PG), which inhibits the activity of plastid triose phosphate isomerase (pdTPI), leading to increased MG levels. Through a proteomic approach, we identified the chloroplast chaperone cpHSC70-1 as a primary target of MG. MG modifies cpHSC70-1 at a conserved arginine residue (R373), inhibiting its ATPase activity and consequently impairing chloroplast protein import under heat stress. Genetic evidence confirms that the 2PG-pdTPI module controls MG accumulation, and that MG exerts its thermosensitive effect through cpHSC70-1. Our work reveals a photorespiratory metabolite-driven post-translational regulatory pathway, elucidating a novel mechanism for metabolic control of plant thermotolerance.
It is shown that salt stress–induced ABA accumulation up-regulates Heat Shock Factor 4 (CmHSFA4), a gene that is known to enhance chrysanthemum salt tolerance, and an ABA-SnRK2.2-ABF1/BRM signaling module that integrates phosphorylation-dependent protein stabilization and degradation with histone methylation dynamics to fine-tune salt stress–responsive gene expression in chrysanthemum is revealed.
Xinhui Wang, Han Wang, Hongyu Wei et al.· Science Advances· 0 citations
The critical role of phase separation in plant heat stress tolerance is revealed and it is demonstrated that N-acetyltransferase 10 (NAT10), which encodes of the cytosine N4 acetyltransferase protein, contributes to heat resistance.
Wan-long Zhang, Yanxiao Bu, Yubing Jiao et al.· Molecular Plant· 0 citations
Heterologous expression of CsAlaDC establishes a functional ethylamine-theanine metabolic branch in tomato and enhances thermotolerance through coordination with the GABA metabolic network, offering a promising strategy to improve both stress resilience and nutritional quality in crops.
Qianying Wang, Jingbo Yu, Peng Mao et al.· Plant Physiology· 0 citations
High-temperature stress impairs plant growth and alters secondary metabolism. Polymethoxyflavones (PMFs) are citrus-specific flavonoids with important nutritional benefits; however, their transcriptional responses to heat stress remain poorly understood. Here, five-month-old ‘Ponkan’ citrus seedlings were exposed to 40 °C for 6, 11, and 21 days. HPLC analysis showed that the accumulation of four major PMFs (sinensetin, nobiletin, tangeretin, and 5-demethylnobiletin) was significantly reduced in leaves under heat stress. RNA-seq identified 3424 differentially expressed genes shared across all three time points, which were enriched in pathways associated with microtubule cytoskeleton organization, cell cycle regulation, and glyoxylate and dicarboxylate metabolism. Further analysis of the PMF biosynthetic pathway revealed that 14 of 18 key structural genes, including CHS, CHI, FNSII, and OMT family members, were downregulated by heat treatment. In addition, several bHLH, AP2/EREBP, and MYB transcription factors, known regulators of flavonoid biosynthesis, exhibited expression patterns closely associated with PMF accumulation. RT-qPCR analysis validated the transcriptome results. Collectively, these findings suggest that heat stress suppresses PMF accumulation through coordinated repression of PMF biosynthetic genes and their potential regulators. This study provides new insights into the molecular basis of heat-responsive PMF metabolism and offers potential targets for maintaining citrus nutritional quality under elevated temperatures.
Xiaojuan Liu, Zhenkun Liao, Honglu Hu et al.· Horticulturae· 0 citations
The GmSNAT1 gene, which encodes a key enzyme involved in soybean melatonin biosynthesis, is crucial for abiotic stress tolerance. In the present study, the molecular mechanism by which GmSNAT1 enhances cold tolerance is elucidated. The cold tolerance of plants was significantly increased by GmSNAT1 overexpression and reduced by CRISPR/Cas9-mediated knockout, a phenotype that was effectively rescued by exogenous melatonin. Integrated transcriptomic, physiological, and biochemical analyses revealed that the GmSNAT1-mediated melatonin pathway activates calcium signaling; coordinates the crosstalk between auxin, abscisic acid, and ethylene; and mobilizes transcription factor networks to orchestrate bidirectional physiological responses. Additionally, the activation of antioxidant systems for reactive oxygen species scavenging and the upregulation of photosynthesis-related genes to maintain photosynthetic stability were explored. The physical interaction between GmSNAT1 and the plant sulfotyrosine peptide receptor GmPSYR1 was confirmed using co-immunoprecipitation, bimolecular fluorescence complementation, and yeast two-hybrid assays. This interaction may be involved in cold stress signal transduction, regulation of root development, and redox homeostasis through GmPSYR1. Collectively, these findings demonstrate that cold adaptation in soybeans is synergistically enhanced by GmSNAT1 via a multidimensional axis encompassing melatonin synthesis, signal transduction, and physiological protection, thereby providing a novel molecular target for breeding cold-tolerant crops.
C. Ren, Tong Cheng, Wenjie Zhang et al.· Plant Physiology· 0 citations
ABSTRACT Global warming is increasing the frequency of extreme heat events, threatening forest resilience. However, the physiological and molecular mechanisms underlying heat tolerance of ectomycorrhizal (ECM) inoculation in conifers remain poorly understood. This study investigates how the ECM fungus Cenococcum geophilum enhances thermotolerance in Pinus massoniana seedlings. We found that ECM inoculation significantly improved plant biomass and photosynthesis under both normal and high temperatures. Under heat stress, ECM symbiosis reduced oxidative damage by elevating the activities of antioxidant enzymes (superoxide dismutase [SOD], catalase [CAT], and peroxidase [POD]) and promoting nitric oxide (NO) accumulation via enhanced nitrate reductase (NR)- and nitric oxide synthase (NOS)-dependent pathways. Furthermore, ECM colonization reprogrammed proline metabolism, stimulating its biosynthesis through Δ1-pyrroline-5-carboxylate synthetase (P5CS) and ornithine aminotransferase (OAT) while tissue-specifically regulating proline dehydrogenase (ProDH), thereby supporting osmotic adjustment in roots and energy maintenance in shoots. Transcriptomic analyses revealed that ECM primed the host at 25°C by activating defense signaling, reinforcing epidermal structures, and enhancing starch and sucrose metabolism. Under heat stress, ECM induced extensive transcriptional reorganization, upregulating pathways related to membrane lipid remodeling, cell wall modification, and carbon reallocation, while downregulating energy-costly processes, such as oxidative phosphorylation and RNA polymerase activity. This shift reflects an ECM-driven resource reallocation strategy that suppresses ROS production and prioritizes cellular integrity. Collectively, our study demonstrates that C. geophilum establishes an integrated mechanism involving physiological, biochemical, and transcriptional adjustments to enhance heat tolerance in P. massoniana, providing mechanistic insight into ECM-mediated climate resilience and underscoring the potential of using ECM fungi as an ecological tool to promote forest adaptation in a warming world. IMPORTANCE This study elucidates how the ectomycorrhizal fungus Cenococcum geophilum systemically enhances heat tolerance in Pinus massoniana by acting as a natural “heat shield,” revealing a symbiotic mechanism where the fungus primes the plant's antioxidant defenses, reprograms proline metabolism in a tissue-specific manner, and boosts nitric oxide signaling. Crucially, transcriptomic analysis shows the fungus drives a strategic resource reallocation under heat stress by upregulating pathways for cellular integrity while downregulating energy-intensive processes to minimize oxidative damage. These findings establish a detailed mechanistic framework for fungal-mediated climate resilience, highlighting that enhancing natural partnerships with soil fungi can fortify existing forests against increasing heatwaves by optimizing internal stress management for forest adaptation, offering a practical tool for ecosystem management in a warming world. This study elucidates how the ectomycorrhizal fungus Cenococcum geophilum systemically enhances heat tolerance in Pinus massoniana by acting as a natural “heat shield,” revealing a symbiotic mechanism where the fungus primes the plant's antioxidant defenses, reprograms proline metabolism in a tissue-specific manner, and boosts nitric oxide signaling. Crucially, transcriptomic analysis shows the fungus drives a strategic resource reallocation under heat stress by upregulating pathways for cellular integrity while downregulating energy-intensive processes to minimize oxidative damage. These findings establish a detailed mechanistic framework for fungal-mediated climate resilience, highlighting that enhancing natural partnerships with soil fungi can fortify existing forests against increasing heatwaves by optimizing internal stress management for forest adaptation, offering a practical tool for ecosystem management in a warming world.
Taoxiang Zhang, Yi-Jian Zhou, Shihuan Zhong et al.· Applied and Environmental Mi...· 0 citations
