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R-loops act as a master regulatory switch modulating transcription of cold-responsive genes in rice

ABSTRACT: Cold is a major naturally occurring stress that usually causes complex symptoms and severe yield loss in plants. R-loops can function in a series of biological processes, including normal development and stress responses, in plants. However, how R-loops function in cold responses is still largely unknown in plants, especially in cold sensitive rice. Herein, we conducted DRIP-seq in combination with other newly generated omics data (RNA-seq, DNase-seq, ChIP-seq and MNase-seq) in rice with or without cold treatment. We found that cold treatment caused R-loop dynamics across the genome, indicating that R-loops are cold sensitive non-B DNA structures. Moreover, cold biased R-loops had high GC content and novel motifs the binding of distinct TFs as compared to CK biased R-loops, indicative of occurrence of differential biological implications of R-loop dynamics in response to cold stress. More importantly, we for the first time to provide evidence showing that, in addition to the direct involvement of R-loops in the regulation of cold-responsive gene transcription, R-loops can indirectly modulate transcription of subsets of cold-responsive genes through R-loop overlapping TF-centered or cis-regulatory element related regulatory networks and lncRNAs in rice. Thus, our study for the first time provides evidence showing functions of R-loop dynamics in rice cold responses. It also provides some potential R-loop loci for genetic and epigenetic manipulation towards breeding of enhanced cold tolerance rice varieties.

ORGANISM(S): Oryza sativa Japonica Group

PROVIDER: GSE217841 | GEO | 2023/09/26

REPOSITORIES: GEO

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Project description:Background: Rice grain production is susceptible to a changing environment that imposes both biotic and abiotic stress conditions. Cold episodes are becoming more frequent in the last years and directly affect rice yield in areas with a temperate climate. Rice is particularly susceptible to cold stress during the reproductive phase, especially in anthers during post-meiotic stages which, in turn, affect pollen production. However, a number of rice cultivars with a certain degree of tolerance to cold have been described, which may represent a good breeding resource for improvement of susceptible commercial varieties. Plants experiencing cold stress activate a molecular response in order to reprogram many metabolic pathways to face these hostile conditions. Results: Here we performed RNA-seq analysis using cold-stressed post-meiotic anther samples from a cold-tolerant, Erythroceros Hokkaido (ERY), and a cold-susceptible commercial cultivar Sant´Andrea (S.AND). Both cultivars displayed an early common molecular response to cold, although the changes in expression levels are much more drastic in the tolerant one. Comparing our datasets, obtained after one-night cold stress, with other similar genome-wide studies showed very few common deregulated genes, leading to the conclusion that molecular responses in cold-stressed anthers strongly depend on conditions and the duration of the cold treatments. Cold-tolerant ERY exhibits specific molecular responses related to ethylene metabolism, which appears to be activated after cold stress. On the other hand, S.AND cold-treated plants showed a general downregulation of photosystem I and II genes, supporting a role of photosynthesis and chloroplasts in cold responses in anthers, which has remained elusive. Conclusions: Our study revealed that a number of ethylene-related transcription factors, as putative master regulators of cold responses, were upregulated in ERY providing promising candidates to confer tolerance to susceptible cultivars. Our results also suggest that the photosynthesis machinery might be a good target to improve cold tolerance in anthers. In summary, our study provides valuable candidates for further analysis and molecular breeding for cold-tolerant rice cultivars.

Project description:Chilling stress is a major abiotic stress that affects rice growth and development. Rice seedlings are quite sensitive to chilling stress and this harms global rice production. Comprehensive studies of the molecular mechanisms for response to low temperature are of fundamental importance to chilling tolerance improvement. The number of identified cold regulated genes (CORs) in rice is still very small. Circadian clock is an endogenous timer that enables plants to cope with forever changing surroundings including light–dark cycles imposed by the rotation of the planet. Previous studies have demonstrated that the circadian clock regulates stress tolerances in plants show circadian clock regulation of plant stress tolerances. However, little is known about coordination of the circadian clock in rice chilling tolerance. In this study, we investigated rice responses to chilling stress under conditions with natural light-dark cycles. We demonstrated that chilling stress occurring at nighttime significantly decreased chlorophyll content and photosynthesis efficiency in comparison with that occurring at daytime. Transcriptome analysis characterized novel CORs in indica rice, and suggested that circadian clock obviously interferes with cold effects on key genes in chlorophyll (Chl) biosynthesis pathway and photosynthesis-antenna proteins. Expression profiling revealed that chilling stress during different Zeitberger times (ZTs) at nighttime repressed the expression of those genes involved Chl biosynthesis and photosynthesis, whereas stress during ZTs at daytime increases their expression dramatically. Moreover, marker genes OsDREBs for chilling tolerance were regulated differentially by the chilling stress occurring at different ZTs. The phase and amplitude of oscillation curves of core clock component genes such as OsLHY and OsPRR1 are regulated by chilling stress, suggesting the role of chilling stress as an input signal to the rice circadian clock. Our work revealed impacts of circadian clock on chilling responses in rice, and proved that the effects on the fitness costs are varying with the time in a day when the chilling stress occurs.

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R-loops act as a master regulatory switch modulating transcription of cold-responsive genes in rice

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