Canonical transcriptional gene silencing may contribute to long‐term heat response and recovery through MOM1

• Published in: Plant, cell and environment Vol. 47; no. 1; pp. 372 - 382
• Main Authors: Torres, José Roberto, Botto, Javier F., Sanchez, Diego H.
• Format: Journal Article
• Language: English
• Published: Oxford Wiley Subscription Services, Inc 01.01.2024
• Subjects: Acclimation; Acclimatization; arabidopsis; DNA methylation; Epigenetics; Gene silencing; Genomic imprinting; Heat; Heat recovery; Heat stress; Heat tolerance; High temperature; Physiology; plant stress; silencing; stress recovery; Transcription activation; transcriptional gene silencing; Transcriptomes; Transcriptomics
• ISSN: 0140-7791; 1365-3040; 1365-3040
• DOI: 10.1111/pce.14722

Plant canonical transcriptional gene silencing (TGS) is involved in epigenetic mechanisms that mediate genomic imprinting and the suppression of transposable elements (TEs). It has been recognised that long‐term heat disrupts epigenetic silencing, with the ensuing activation of TEs. However, the physiological involvement of the TGS machinery under prolonged high temperatures has not yet been established. Here, we performed non‐lethal extended periodic heat stress and recovery treatments on Arabidopsis thaliana lines mutated on key TGS factors, analysing transcriptomic changes of coding‐protein genes and TEs. Plants bearing MET1, DRM2 and CMT3, and MOM1 mutated alleles showed novel transcriptional properties compatible with functionalities concerning the induction/repression of partially shared or private heat‐triggered transcriptome networks. Certain observations supported the idea that some responses are based on thermal de‐silencing. TEs transcriptional activation uncovered the interaction with specific epigenetic layers, which may play dedicated suppressing roles under determinate physiological conditions such as heat. Furthermore, physiological experimentation suggested that MOM1 is required to resume growth after stress. Our data thus provide initial evidence that at least one canonical TGS factor may contribute to plant acclimation and recovery from non‐lethal long‐term heat despite the stress‐induced epigenetic disturbance. Summary statement Plant stress physiology is epigenetically modulated. In turn, environmental cues transiently affect epigenetic pathways, such as long‐term heat which disrupts epigenetic suppression. However, the role of the transcriptional gene silencing (TGS) machinery under prolonged high temperatures has not yet been consistently established. Based on experimentation carried out with key Arabidopsis thaliana mutated lines, performing extensive transcriptomic analysis and additional physiological assessments, we provide here initial evidence suggesting that canonical TGS may contribute to plant acclimation and recovery from non‐lethal long‐term periodic heat despite the stress‐induced epigenetic disturbance.