Integrative analysis in Pinus revealed long‐term heat stress splicing memory

Abstract

SUMMARY Due to the current climate change, many studies have described main drivers in abiotic stress. Recent findings suggest that alternative splicing (AS) has a critical role in controlling plant responses to high temperature. AS is a mechanism that allows organisms to create an assortment of RNA transcripts and proteins using a single gene. However, the most important roles of AS in stress could not be rigorously addressed because research has been focused on model species, covering only a narrow phylogenetic and lifecycle spectrum. Thus, AS degree of diversification among more dissimilar taxa in heat response is still largely unknown. To fill this gap, the present study employs a systems biology approach to examine how the AS landscape responds to and ‘remembers’ heat stress in conifers, a group which has received little attention even though their position can solve key evolutionary questions. Contrary to angiosperms, we found that potential intron retention may not be the most prevalent type of AS. Furthermore, our integrative analysis with metabolome and proteome data places splicing as the main source of variation during the response. Finally, we evaluated possible acquired long‐term splicing memory in a diverse subset of events, and although this mechanism seems to be conserved in seed plants, AS dynamics are divergent. These discoveries reveal the particular way of remembering past temperature changes in long‐lived plants and open the door to include species with unique features to determine the extent of conservation in gene expression regulation.

Proteomics research in forest trees: A 2012-2022 update

“…The use of a two-phase stress experimental design further confirmed the importance of sHSPs after initial heat stress and found changes in activated methyl cycle enzymes and H2A-H2B histone dimers associated with stress memory. Lamelas et al (2020b) also described changes in spliceosome-related proteins during heat stress and recovery, suggesting alternative splicing as an important mechanism mediating stress response and memory, which was further characterized by Roces et al (2022). Furthermore, the combined study of nuclear and chloroplast proteomes revealed the importance of proteins related to retrograde and anterograde signaling and to RNA metabolism rearrangement mediated by microRNAs, revealing a new layer of regulation in heat stress response (Lamelas et al, 2022).…”

“… Lamelas et al. (2020b) also described changes in spliceosome-related proteins during heat stress and recovery, suggesting alternative splicing as an important mechanism mediating stress response and memory, which was further characterized by Roces et al. (2022) .…”

The Integration of Data from Different Long-Read Sequencing Platforms Enhances Proteoform Characterization in Arabidopsis

“…Systems biology studies different layers of complexity of organisms in a high throughput manner, what we call omics, and then integrates them to obtain an accurate picture of an organism’s biology through its development or under different environmental conditions. Such an approach has been successfully applied in plant sciences to study, for example, the response to different types of stress in tree species [ 1 , 2 , 3 , 4 , 5 , 6 , 7 ], Arabidopsis thaliana [ 8 , 9 ] or Chlamydomonas reinhardtii [ 10 , 11 ]. However, the integration of different omic levels is a rather challenging task.…”

Co-expression network of heat-response transcripts: A glimpse into how splicing factors impact rice basal thermotolerance

“…As a result, AS allows for increased flexibility during responses to changing environmental conditions ( Syed et al, 2012 ; Staiger and Brown, 2013 ; Filichkin et al, 2015 ). Several studies have contributed to our knowledge of crucial AS regulations upon HS ( Jiang et al, 2017 ; Ling et al, 2018 ; Sanyal et al, 2018 ; Vitoriano and Calixto, 2021 ; Roces et al, 2022 ). For example, we analysed rice response to HS and identified 2,162 differentially alternatively spliced (DAS) genes, many of which code for key regulators of gene expression, confirming that AS is a major part of the HS response ( Vitoriano and Calixto, 2021 ).…”