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.

Overexpression of receptor-like kinase ERECTA improves thermotolerance in rice and tomato

“…Following our previous studies of Arabidopsis heat and harmattan responses [19][20][21] , we report in this study that two ecotypes, Columbia-0 (Col-0) and Landsberg erecta (Ler), were substantially different from each other in their tolerance to prolonged extreme heat in greenhouse conditions (40 °C ; Fig. 1a).…”

Proteomic Study of Microsomal Proteins Reveals a Key Role for Arabidopsis Annexin 1 in Mediating Heat Stress-Induced Increase in Intracellular Calcium Levels

“…In recent years, there has been considerable progress in identifying the signaling steps that enable plants to respond to heat stress at the molecular level. These include: activation of bZIP transcription factors by heat-induced proteolytic cleavage (4); inhibition of transgene-induced post-transcriptional gene silencing (PTGS) by SUPPRESSOR OF GENE SILENCING 3 (SGS3) (5); accumulation of reactive oxygen species (ROS) by RBOHD activation (6); and reduced H2A.Z occupancy in nucleosomes of heat-regulated genes, which would be expected to stimulate transcription of these genes (7). Many reports also provide evidence that membrane-localized calcium channels can act as sensors for increased temperature in plant cells (8,9).…”

Elucidation of Abiotic Stress Signaling in Plants

“…Further, this moderate increase also resulted in the altered DNA methylation status of transgenes. Interestingly, this phenomenon exhibited transgenerational epigenetic memory, which persisted for three generations (Zhong et al 2013 ).…”

“…NRPD2, the second largest subunit of PolIV and PolV, is crucial for sRNA biogenesis and RdDM (Haag and Pikaard 2011 ;Zhang and Zhu 2011 ). One more report links the warm temperature and transgenerational epigenetic through siRNA-mediated regulation (Zhong et al 2013 ) wherein increase in ambient temperature from 22 to 30 °C leads to the reduction in the protein levels of SGS3, which inhibit the dsRNA formation step in the post-transcriptional gene silencing pathways induced by antisense sequences, small RNA and tasiRNA (Zhong et al 2013 ). Conversely, the overexpression of SGS3 abolished the warmth-induced inhibition of siRNA formation.…”