Epigenetic stress memory: A new approach to study cold and heat stress responses in plants

Abstract

Understanding plant stress memory under extreme temperatures such as cold and heat could contribute to plant development. Plants employ different types of stress memories, such as somatic, intergenerational and transgenerational, regulated by epigenetic changes such as DNA and histone modifications and microRNAs (miRNA), playing a key role in gene regulation from early development to maturity. In most cases, cold and heat stresses result in short-term epigenetic modifications that can return to baseline modification levels after stress cessation. Nevertheless, some of the modifications may be stable and passed on as stress memory, potentially allowing them to be inherited across generations, whereas some of the modifications are reactivated during sexual reproduction or embryogenesis. Several stress-related genes are involved in stress memory inheritance by turning on and off transcription profiles and epigenetic changes. Vernalization is the best example of somatic stress memory. Changes in the chromatin structure of the Flowering Locus C (FLC) gene, a MADS-box transcription factor (TF), maintain cold stress memory during mitosis. FLC expression suppresses flowering at high levels during winter; and during vernalization, B3 TFs, cold memory cis-acting element and polycomb repressive complex 1 and 2 (PRC1 and 2) silence FLC activation. In contrast, the repression of SQUAMOSA promoter-binding protein-like (SPL) TF and the activation of Heat Shock TF (HSFA2) are required for heat stress memory. However, it is still unclear how stress memory is inherited by offspring, and the integrated view of the regulatory mechanisms of stress memory and mitotic and meiotic heritable changes in plants is still scarce. Thus, in this review, we focus on the epigenetic regulation of stress memory and discuss the application of new technologies in developing epigenetic modifications to improve stress memory.

The role of microRNAs in responses to drought and heat stress in peanut (Arachis hypogaea)

“…Focusing on the subgenome‐preferential expression of identified (Supporting Information S11; Tables S2 and S4) and validated miRNA target gene homoeologues and effectors in different tissue types (root, stem, flower, leaf, pods, and pegs), over short‐term time course treatments, and in wild relatives (Vinson et al., 2018; Yin et al., 2018) may reveal the adaptive nature of allopolyploid miRNA target gene losses and expression changes common to legumes. Further work is required to reveal the evolutionary innovations of MIRNA s in stress responses and nodulation (De Luis et al., 2012), and the roles of sRNAs in epigenetics of heat stress memory and male fertility (Bilichak & Kovalchuk, 2016; Malik & Zhao, 2022; Ramakrishnan et al., 2022), nucleolar dominance, genomic maintenance, and stability (Seijo et al., 2018). Such knowledge of sRNA functions can be applied to harness the genetic diversity of wild Arachis species to accelerate molecular breeding for value‐added agronomic traits.…”

“…We manually verified Tifrunner A genome TAS-L ncRNA XR_001589440.2:D7(-) and B genome TAS-L XR_002357732.1:D2/5/6(-) collectively act by a 21 2 hit mechanism to trigger phasiRNAs from PPR PHAS locus 6Q4537 (phase score 28.7) and numerous paralogs not yet annotated in Tifrunner reference genome v2.J5K5 (Supporting Information S6c,e). It is also remarkable that the same miR3514:PHAS-derived tasi-RNAs B02D5(-)/6(-) that target PPRs also target numerous En/Spm Transposase mRNAs (Supporting Informations S11 and S6e; Table S2; Figure S5), analogous to miR4392-triggered tasiRNAs in soybean The Plant Genome (Arikit et al, 2014) and miRNAs in Arabidopsis and rice that regulate transposable element RNA-dependent DNA methylation and receptor-like kinase activities in reproductive tissues (Creasey et al, 2014;Fei et al, 2016;Oliver et al, 2022) which are hypersensitive to heat stress that causes male sterility (Malik & Zhao, 2022) and may be involved in epigenetic heat stress memory (Ramakrishnan et al, 2022).…”

Role of Epigenetic Factors in Response to Stress and Establishment of Somatic Memory of Stress Exposure in Plants

“…Likewise, massive demethylation changes were observed in Arabidopsis plants exposed to heat stress [128]. Demethylation is possibly associated with the lower activity of RdDM machinery, including the downregulation of RNA-DIRECTED DNA METHYLATION 4 (RDM4) [129]. In turn, RDM4 regulates the expression of transcription factors responsive to cold stress [31].…”

The power of retrotransposons in high-throughput genotyping and sequencing

“…Numerous studies have investigated the activities of LTR retrotransposons under stress conditions ( Grandbastien, 1998 ; Pecinka et al., 2010 ; Tittel-Elmer et al., 2010 ; Ito et al., 2011 ; Butelli et al., 2012 ; Gaubert et al., 2017 ; Benoit et al., 2019 ; Cho et al., 2019 ; Papolu et al., 2021 ; Ramakrishnan et al., 2022 ). Mobile elements and endogenous retroviruses are important in the distribution of cis-regulatory elements, which contribute to genetic control in both the short (accumulation of hidden variability and processes of selection) and the long (adaptation and separation) term.…”