Thermopriming triggers splicing memory in Arabidopsis.

Yu Ling,A S N Reddy,Moussa Benhamed,Mohamed Atia,Christoph Gehring,Martin Crespi,Jeremie Bazin,Magdy M Mahfouz,Alaguraj Veluchamy,Natalia Serrano,Morad Mokhtar,Yong H Woo,Ge Gao

doi:10.1093/jxb/ery062

Abstract

Abiotic and biotic stresses limit crop productivity. Exposure to a non-lethal stress, referred to as priming, can allow plants to survive subsequent and otherwise lethal conditions; the priming effect persists even after a prolonged stress-free period. However, the molecular mechanisms underlying priming are not fully understood. Here, we investigated the molecular basis of heat-shock memory and the role of priming in Arabidopsis thaliana. Comprehensive analysis of transcriptome-wide changes in gene expression and alternative splicing in primed and non-primed plants revealed that alternative splicing functions as a novel component of heat-shock memory. We show that priming of plants with a non-lethal heat stress results in de-repression of splicing after a second exposure to heat stress. By contrast, non-primed plants showed significant repression of splicing. These observations link 'splicing memory' to the ability of plants to survive subsequent and otherwise lethal heat stress. This newly discovered priming-induced splicing memory may represent a general feature of heat-stress responses in plants and other organisms as many of the key components are conserved among eukaryotes. Furthermore, this finding could facilitate the development of novel approaches to improve plant survival under extreme heat stress.

Highlights

Plants adapt to ever-changing environmental conditions by fine-tuning their molecular responses at the genome, epigenome, transcriptome, epitranscriptome, metabolome, and proteome levels to ensure survival and reproductive success (Burgess et al, 2016; Hatfield and Prueger, 2015)
We propose that Alternative splicing (AS) may contribute to heat stress-induced memory and test this hypothesis using our newly developed heat acclimation protocol in which heat stress-induced priming d leads to memory establishment that allows plants to survive a subsequent and otherwise lethal heat shock. te In particular, we investigated the genome-wide differential gene expression and alternative splicing patterns that mediate the establishment of priming and memory and identified a group of genes with p sustained activation levels that are implicated in the establishment of heat stress-induced memory to Acce establish a link between alternative splicing and heat stress-induced memory
To investigate the transcriptional and post-transcriptional regulation of heat stress priming and memory, we developed a comprehensive heat stress-induced priming platform in Arabidopsis

Summary

INTRODUCTION

Plants adapt to ever-changing environmental conditions by fine-tuning their molecular responses at the genome, epigenome, transcriptome, epitranscriptome, metabolome, and proteome levels to ensure survival and reproductive success (Burgess et al, 2016; Hatfield and Prueger, 2015). The activation of the second group is sustained after relief of the stress; these genes play a major role in heat stress-mediated memory (Stief et al, 2014). The interplay between transcriptional and post-transcriptional regulation of gene expression is mediated at t different levels and epigenetic factors are thought to play a role in establishing heat stress memory ip (Avramova, 2015; Brzezinka et al, 2016; Hu et al, 2015). Te In particular, we investigated the genome-wide differential gene expression and alternative splicing patterns that mediate the establishment of priming and memory and identified a group of genes with p sustained activation levels that are implicated in the establishment of heat stress-induced memory to Acce establish a link between alternative splicing and heat stress-induced memory We propose that AS may contribute to heat stress-induced memory and test this hypothesis using our newly developed heat acclimation protocol in which heat stress-induced priming d leads to memory establishment that allows plants to survive a subsequent and otherwise lethal heat shock. te In particular, we investigated the genome-wide differential gene expression and alternative splicing patterns that mediate the establishment of priming and memory and identified a group of genes with p sustained activation levels that are implicated in the establishment of heat stress-induced memory to Acce establish a link between alternative splicing and heat stress-induced memory

RESULTS

DISCUSSION

METHODS