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DNA methylation is a conserved epigenetic mark that plays important roles in maintaining genome stability and regulating gene expression. As sessile organisms, plants have evolved sophisticated regulatory systems to endure or respond to diverse adverse abiotic environmental challenges, i.e., abiotic stresses, such as extreme temperatures (cold and heat), drought and salinity. Plant stress responses are often accompanied by changes in chromatin modifications at diverse responsive loci, such as 5-methylcytosine (5mC) and N 6 -methyladenine (6mA) DNA methylation. Some abiotic stress responses are memorized for several hours or days through mitotic cell divisions and quickly reset to baseline levels after normal conditions are restored, which is referred to as somatic memory. In some cases, stress-induced chromatin marks are meiotically heritable and can impart the memory of stress exposure from parent plants to at least the next stress-free offspring generation through the mechanisms of transgenerational epigenetic inheritance, which may offer the descendants the potential to be adaptive for better fitness. In this review, we briefly summarize recent achievements regarding the establishment, maintenance and reset of DNA methylation, and highlight the diverse roles of DNA methylation in plant responses to abiotic stresses. Further, we discuss the potential role of DNA methylation in abiotic stress-induced somatic memory and transgenerational inheritance. Future research directions are proposed to develop stress-tolerant engineered crops to reduce the negative effects of abiotic stresses.

Global warming has profound effects on plant growth and fitness. Plants have evolved sophisticated epigenetic machinery to respond quickly to heat, and exhibit transgenerational memory of the heat-induced release of post-transcriptional gene silencing (PTGS). However, how thermomemory is transmitted to progeny and the physiological relevance are elusive. Here we show that heat-induced HEAT SHOCK TRANSCRIPTION FACTOR A2 (HSFA2) directly activates the H3K27me3 demethylase RELATIVE OF EARLY FLOWERING 6 (REF6), which in turn derepresses HSFA2. REF6 and HSFA2 establish a heritable feedback loop, and activate an E3 ubiquitin ligase, SUPPRESSOR OF GENE SILENCING 3 (SGS3)-INTERACTING PROTEIN 1 (SGIP1). SGIP1-mediated SGS3 degradation leads to inhibited biosynthesis of trans-acting siRNA (tasiRNA). The REF6-HSFA2 loop and reduced tasiRNA converge to release HEAT-INDUCED TAS1 TARGET 5 (HTT5), which drives early flowering but attenuates immunity. Thus, heat induces transmitted phenotypes via a coordinated epigenetic network involving histone demethylases, transcription factors, and tasiRNAs, ensuring reproductive success and transgenerational stress adaptation.

Breeding crops with resistance is an efficient way to control diseases. However, increased resistance often has a fitness penalty. Thus, simultaneously increasing disease resistance and yield potential is a challenge in crop breeding. In this study, we found that downregulation of microRNA-156 (miR-156) and overexpression of Ideal Plant Architecture1 ( IPA1 ) and OsSPL7 , two target genes of miR-156, enhanced disease resistance against bacterial blight caused by Xanthomonas oryzae pv. oryzae ( Xoo ), but reduced rice yield. We discovered that gibberellin signalling might be partially responsible for the disease resistance and developmental defects in IPA1 overexpressors. We then generated transgenic rice plants expressing IPA1 with the pathogen-inducible promoter of OsHEN1 ; these plants had both enhanced disease resistance and enhanced yield-related traits. Thus, we have identified miR-156– IPA1 as a novel regulator of the crosstalk between growth and defence, and we have established a new strategy for obtaining both high disease resistance and high yield. Breeding crops with both high yield and disease resistance remains challenging. A study has now identified microRNA-156– Ideal Plant Architecture1 ( IPA1 ) as a regulator of the crosstalk between growth and defence in rice and overcame the trade-off by pathogen-induced expression of IPA1 .

Super hybrid rice varieties with ideal plant architecture (IPA) have been critical in enhancing food security worldwide. However, the molecular mechanisms underlying their improved yield remain unclear. Here, we report the identification of a QTL, qWS8/ipa1 - 2D , in the super rice Yongyou12 (YY12) and related varieties. In-depth genetic molecular characterization of qWS8 / ipa1-2D reveals that this newly identified QTL results from three distal naturally occurring tandem repeats upstream of IPA1 , a key gene/locus previously shown to shape rice ideal plant architecture and greatly enhance grain yield. The qWS8/ipa1-2D locus is associated with reduced DNA methylation and a more open chromatin state at the IPA1 promoter, thus alleviating the epigenetic repression of IPA1 mediated by nearby heterochromatin. Our findings reveal that IPA traits can be fine-tuned by manipulating IPA1 expression and that an optimal IPA1 expression/dose may lead to an ideal yield, demonstrating a practical approach to efficiently design elite super rice varieties. Breeding of rice with ideal plant architecture has increased rice yield worldwide. Here Zhang et al . show that, in the super rice variety YY12, this ideal plant architecture trait arose from three distal tandem repeats that are associated with an open chromatin state and increased expression of the IPA1 gene.

Lipids and lipid metabolites play important roles in plant-microbe interactions. Despite the extensive studies of lipases in lipid homeostasis and seed oil biosynthesis, the involvement of lipases in plant immunity remains largely unknown. In particular, GDSL esterases/lipases, characterized by the conserved GDSL motif, are a subfamily of lipolytic enzymes with broad substrate specificity. Here, we functionally identified two GDSL lipases, OsGLIP1 and OsGLIP2, in rice immune responses. Expression of OsGLIP1 and OsGLIP2 was suppressed by pathogen infection and salicylic acid (SA) treatment. OsGLIP1 was mainly expressed in leaf and leaf sheath, while OsGLIP2 showed high expression in elongating internodes. Biochemical assay demonstrated that OsGLIP1 and OsGLIP2 are functional lipases that could hydrolyze lipid substrates. Simultaneous down-regulation of OsGLIP1 and OsGLIP2 increased plant resistance to both bacterial and fungal pathogens, whereas disease resistance in OsGLIP1 and OsGLIP2 overexpression plants was significantly compromised, suggesting that both genes act as negative regulators of disease resistance. OsGLIP1 and OsGLIP2 proteins mainly localize to lipid droplets and the endoplasmic reticulum (ER) membrane. The proper cellular localization of OsGLIP proteins is indispensable for their functions in immunity. Comprehensive lipid profiling analysis indicated that the alteration of OsGLIP gene expression was associated with substantial changes of the levels of lipid species including monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG). We show that MGDG and DGDG feeding could attenuate disease resistance. Taken together, our study indicates that OsGLIP1 and OsGLIP2 negatively regulate rice defense by modulating lipid metabolism, thus providing new insights into the function of lipids in plant immunity.

The heat tolerance of rice and tomato plants is increased by overexpression of the ERECTA gene. The detrimental effects of global warming on crop productivity threaten to reduce the world's food supply 1 , 2 , 3 . Although plant responses to changes in temperature have been studied 4 , genetic modification of crops to improve thermotolerance has had little success to date. Here we demonstrate that overexpression of the Arabidopsis thaliana receptor-like kinase ERECTA (ER) in Arabidopsis , rice and tomato confers thermotolerance independent of water loss and that Arabidopsis er mutants are hypersensitive to heat. A loss-of-function mutation of a rice ER homolog and reduced expression of a tomato ER allele decreased thermotolerance of both species. Transgenic tomato and rice lines overexpressing Arabidopsis ER showed improved heat tolerance in the greenhouse and in field tests at multiple locations in China during several seasons. Moreover, ER -overexpressing transgenic Arabidopsis , tomato and rice plants had increased biomass. Our findings could contribute to engineering or breeding thermotolerant crops with no growth penalty.

Plants must effectively defend against biotic and abiotic stresses to survive in nature. However, this defense is costly and is often accompanied by significant growth inhibition. How plants coordinate the fluctuating growth-defense dynamics is not well understood and remains a fundamental question. Jasmonate (JA) and gibberellic acid (GA) are important plant hormones that mediate defense and growth, respectively. Binding of bioactive JA or GA ligands to cognate receptors leads to proteasome-dependent degradation of specific transcriptional repressors (the JAZ or DELLA family of proteins), which, at the resting state, represses cognate transcription factors involved in defense (e.g., MYCs) or growth [e.g. phytochrome interacting factors (PIFs)]. In this study, we found that the coi1 JA receptor mutants of rice (a domesticated monocot crop) and Arabidopsis (a model dicot plant) both exhibit hallmark phenotypes of GA-hypersensitive mutants. JA delays GA-mediated DELLA protein degradation, and the della mutant is less sensitive to JA for growth inhibition. Overexpression of a selected group of JAZ repressors in Arabidopsis plants partially phenocopies GA-associated phenotypes of the coi1 mutant, and JAZ9 inhibits RGA (a DELLA protein) interaction with transcription factor PIF3. Importantly, the pif quadruple (pifq) mutant no longer responds to JA-induced growth inhibition, and overexpression of PIF3 could partially overcome JA-induced growth inhibition. Thus, a molecular cascade involving the COI1–JAZ–DELLA–PIF signaling module, by which angiosperm plants prioritize JA-mediated defense over growth, has been elucidated.

Recurrent heat stress and pathogen invasion seriously threaten crop production, and abiotic stress often antagonizes biotic stress response against pathogens. However, the molecular mechanisms of trade-offs between thermotolerance and defense remain obscure. Here, we identify a rice thermo-sensitive mutant that displays a defect in floret development under high temperature with a mutation in S UPPRESSOR OF GENE SILENCING 3a ( OsSGS3a ). OsSGS3a interacts with its homolog OsSGS3b and modulates the biogenesis of trans -acting small interfering RNA (tasiRNA) targeting AUXIN RESPONSE FACTORS ( ARFs ). We find that OsSGS3a/b positively, while OsARF3a/b and OsARF3la/lb negatively modulate thermotolerance. Moreover, OsSGS3a negatively, while OsARF3a/b and OsARF3la/lb positively regulate disease resistance to the bacterial pathogen Xanthomonas oryzae pv. oryzae ( Xoo ) and the fungal pathogen Magnaporthe oryzae ( M. oryzae ). Taken together, our study uncovers a previously unknown trade-off mechanism that regulates distinct immunity and thermotolerance through the OsSGS3-tasiRNA-OsARF3 module, highlighting the regulation of abiotic-biotic stress response trade-off in plants. Gu et al. report that the OsSGS3-tasiRNA-OsARF3 module plays an important role in coordinating the trade-off between heat tolerance and disease resistance, which positively regulates thermotolerance but negatively modulates immunity in rice.

Zuhua He and colleagues identify the gene underlying a quantitative trait locus for grain-filling in rice, which contributes to grain weight. The gene, GIF1 , encodes a protein with cell-wall invertase activity and may have been under selection during rice domestication. Grain-filling, an important trait that contributes greatly to grain weight, is regulated by quantitative trait loci and is associated with crop domestication syndrome 1 , 2 , 3 , 4 . However, the genes and underlying molecular mechanisms controlling crop grain-filling remain elusive. Here we report the isolation and functional analysis of the rice GIF1 ( GRAIN INCOMPLETE FILLING 1 ) gene that encodes a cell-wall invertase required for carbon partitioning during early grain-filling. The cultivated GIF1 gene shows a restricted expression pattern during grain-filling compared to the wild rice allele, probably a result of accumulated mutations in the gene's regulatory sequence through domestication. Fine mapping with introgression lines revealed that the wild rice GIF1 is responsible for grain weight reduction. Ectopic expression of the cultivated GIF1 gene with the 35S or rice Waxy promoter resulted in smaller grains, whereas overexpression of GIF1 driven by its native promoter increased grain production. These findings, together with the domestication signature that we identified by comparing nucleotide diversity of the GIF1 loci between cultivated and wild rice, strongly suggest that GIF1 is a potential domestication gene and that such a domestication-selected gene can be used for further crop improvement.

This brief article highlights the key findings of the study conducted by Sha et al. (Nature, doi:10.1038/s41586-023-06205-2, 2023), focusing on the cloning of the RBL1 gene from rice, which is associated with lesion mimic mutant (LMM) traits. The RBL1 gene encodes a cytidine diphosphate diacylglycerol (CDP-DAG) synthase and plays a crucial role in regulating cell death and immunity by controlling phosphatidylinositol biosynthesis. The rbl1 mutant shows autoimmunity with multi-pathogen resistance but with severe yield penalty. Using genome editing techniques, the research team successfully generated an elite allele of RBL1 that not only restores rice yield but also provides broad-spectrum resistance against both bacterial and fungal pathogens. These findings demonstrate the potential of utilizing genome editing to enhance crop productivity and pathogen resistance.