title: Comparative metabolomic analysis reveals a reactive oxygen species-dominated dynamic model underlying chilling environment adaptation and tolerance in rice.
abstract: Cold, a major environmental stress for plants, has been studied intensively for decades. Its response system has been revealed, especially at the transcriptional level. The mechanisms underlying recovery growth and environmental adaptation, however, remain unknown. Taking advantage of a naturally existing system, two subspecies of Asian cultivated rice (Oryza sativa) with significant divergence in chilling tolerance, we analyzed representative japonica and indica varieties, Nipponbare and 93-11, using comparative metabolomic analysis at six time points covering chilling treatment and recovery. In total, 223 known metabolites were detected. During chilling treatment, significant biochemical changes were centered on antioxidation. During recovery, a wide-ranging chilling response was observed. Large-scale amino acid accumulation occurred, consistent with the appearance of chilling injury. At the mid-treatment stage, the accumulation of antioxidation-related compounds appeared earlier in Nipponbare than in 93-11, consistent with the higher reactive oxygen species (ROS) levels in japonica vs indica varieties. A significant contribution of ROS-mediated gene regulation, rather than the C-repeat binding factor/dehydration-responsive-element binding factor (CBF/DREB) regulon, to the more vigorous transcriptional stress response in Nipponbare was revealed by RNA-seq. Accordingly, during recovery, the induction of stress-tolerant-related metabolites was more active in the chilling-tolerant variety Nipponbare. Senescence-related compounds accumulated only in the chilling-sensitive variety 93-11. Our study uncovers the dynamic metabolic models underlying chilling response and recovery, and reveals a ROS-dominated rice adaptation mechanism to low-temperature environments.
authors.affiliation: Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China.
authors.forename: Jingyu
authors.initials: J
authors.lastname: Zhang
authors.affiliation: Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China.
authors.forename: Wei
authors.initials: W
authors.lastname: Luo
authors.affiliation: Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China.
authors.forename: Yuan
authors.initials: Y
authors.lastname: Zhao
authors.affiliation: Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China.
authors.forename: Yunyuan
authors.initials: Y
authors.lastname: Xu
authors.affiliation: Big Data Center, Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, 100101, China.
authors.forename: Shuhui
authors.initials: S
authors.lastname: Song
authors.affiliation: Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China.
authors.forename: Kang
authors.initials: K
authors.lastname: Chong
mesh_terms: D000222:Adaptation, Physiological; D000975:Antioxidants / Q000378:metabolism; D001483:Base Sequence; D004777:Environment; D005615:Freezing; D018506:Gene Expression Regulation, Plant; D055442:Metabolome; D055432:Metabolomics / Q000379:methods*; D008954:Models, Biological; D012275:Oryza / Q000235:genetics / Q000254:growth & development / Q000378:metabolism* / Q000502:physiology*; D010937:Plant Growth Regulators / Q000378:metabolism; D025341:Principal Component Analysis; D017382:Reactive Oxygen Species / Q000378:metabolism*; D020156:Salicylic Acid / Q000378:metabolism; D017423:Sequence Analysis, RNA; D013312:Stress, Physiological / Q000235:genetics; D014158:Transcription, Genetic
chemical_list: D000975:Antioxidants; D010937:Plant Growth Regulators; D017382:Reactive Oxygen Species; D020156:Salicylic Acid
keywords: chilling; environmental adaptation; metabolome; reactive oxygen species (ROS); rice (Oryza sativa)