title: Warm temperatures induce transgenerational epigenetic release of RNA silencing by inhibiting siRNA biogenesis in Arabidopsis.
abstract: Owing to their sessile nature, plants have evolved sophisticated genetic and epigenetic regulatory systems to respond quickly and reversibly to daily and seasonal temperature changes. However, our knowledge of how plants sense and respond to warming ambient temperatures is rather limited. Here we show that an increase in growth temperature from 22 °C to 30 °C effectively inhibited transgene-induced posttranscriptional gene silencing (PTGS) in Arabidopsis. Interestingly, warmth-induced PTGS release exhibited transgenerational epigenetic inheritance. We discovered that the warmth-induced PTGS release occurred during a critical step that leads to the formation of double-stranded RNA (dsRNA) for producing small interfering RNAs (siRNAs). Deep sequencing of small RNAs and RNA blot analysis indicated that the 22-30 °C increase resulted in a significant reduction in the abundance of many trans-acting siRNAs that require dsRNA for biogenesis. We discovered that the temperature increase reduced the protein abundance of SUPPRESSOR OF GENE SILENCING 3, as a consequence, attenuating the formation of stable dsRNAs required for siRNA biogenesis. Importantly, SUPPRESSOR OF GENE SILENCING 3 overexpression released the warmth-triggered inhibition of siRNA biogenesis and reduced the transgenerational epigenetic memory. Thus, our study reveals a previously undescribed association between warming temperatures, an epigenetic system, and siRNA biogenesis.
authors.affiliation: National Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China.
authors.forename: Si-Hui
authors.initials: SH
authors.lastname: Zhong
authors.forename: Jun-Zhong
authors.initials: JZ
authors.lastname: Liu
authors.forename: Hua
authors.initials: H
authors.lastname: Jin
authors.forename: Lin
authors.initials: L
authors.lastname: Lin
authors.forename: Qun
authors.initials: Q
authors.lastname: Li
authors.forename: Ying
authors.initials: Y
authors.lastname: Chen
authors.forename: Yue-Xing
authors.initials: YX
authors.lastname: Yuan
authors.forename: Zhi-Yong
authors.initials: ZY
authors.lastname: Wang
authors.forename: Hai
authors.initials: H
authors.lastname: Huang
authors.forename: Yi-Jun
authors.initials: YJ
authors.lastname: Qi
authors.forename: Xiao-Ya
authors.initials: XY
authors.lastname: Chen
authors.forename: Hervé
authors.initials: H
authors.lastname: Vaucheret
authors.forename: Joanne
authors.initials: J
authors.lastname: Chory
authors.forename: Jianming
authors.initials: J
authors.lastname: Li
authors.forename: Zu-Hua
authors.initials: ZH
authors.lastname: He
mesh_terms: D017360:Arabidopsis / Q000502:physiology*; D029681:Arabidopsis Proteins / Q000378:metabolism*; D001483:Base Sequence; D044127:Epigenesis, Genetic / Q000502:physiology*; D018506:Gene Expression Regulation, Plant / Q000502:physiology*; D059014:High-Throughput Nucleotide Sequencing; D008969:Molecular Sequence Data; D030821:Plants, Genetically Modified; D011494:Protein Kinases / Q000378:metabolism; D034622:RNA Interference / Q000502:physiology*; D034741:RNA, Small Interfering / Q000096:biosynthesis* / Q000235:genetics; D060888:Real-Time Polymerase Chain Reaction; D017422:Sequence Analysis, DNA; D013696:Temperature
chemical_list: D029681:Arabidopsis Proteins; D034741:RNA, Small Interfering; C410507:SGS3 protein, Arabidopsis; D011494:Protein Kinases; C108270:BRI1 protein, Arabidopsis