CHH methylation of genes associated with fatty acid and jasmonate biosynthesis contributes to cold tolerance in autotetraploids of Poncirus trifoliata

Abstract

Polyploids have elevated stress tolerance, but the underlying mechanisms remain largely elusive. In this study, we showed that naturally occurring tetraploid plants of trifoliate orange (Poncirus trifoliata (L.) Raf.) exhibited enhanced cold tolerance relative to their diploid progenitors. Transcriptome analysis revealed that whole‐genome duplication was associated with higher expression levels of a range of well‐characterized cold stress‐responsive genes. Global DNA methylation profiling demonstrated that the tetraploids underwent more extensive DNA demethylation in comparison with the diploids under cold stress. CHH methylation in the promoters was associated with up‐regulation of related genes, whereas CG, CHG, and CHH methylation in the 3'‐regions was relevant to gene down‐regulation. Of note, genes involved in unsaturated fatty acids (UFAs) and jasmonate (JA) biosynthesis in the tetraploids displayed different CHH methylation in the gene flanking regions and were prominently up‐regulated, consistent with greater accumulation of UFAs and JA when exposed to the cold stress. Collectively, our findings explored the difference in cold stress response between diploids and tetraploids at both transcriptional and epigenetic levels, and gained new insight into the molecular mechanisms underlying enhanced cold tolerance of the tetraploid. These results contribute to uncovering a novel regulatory role of DNA methylation in better cold tolerance of polyploids.

Polyploidization: A Biological Force That Enhances Stress Resistance

“…Similarly, the decrease in CHH methylation downstream of two crucial JA synthesis genes, PtrLOX3 and PtrAOC2, also led to their upregulation in tetraploids. This pattern suggested that tetraploids, due to more extensive DNA demethylation, synthesized UFAs more effectively and relayed JA signaling more efficiently, mounting a more intense response to cold stress in tetraploids than in diploids [109]. In addition, exposure to stressful environments induced epigenetic alterations that might persist even after the stress has subsided, thus establishing a 'stress memory'.…”

Celebrating the discovery of DNA demethylase

“…In a research article, (Li et al, 2022) show that BRAHMA, a chromatin remodeler, recruits a histone deacetylase to modulate root system architecture in response to phosphate starvation in Arabidopsis . (Wang, Zuo, et al, 2022) reveal how global demethylation contributes to the enhanced cold tolerance in the polyploid plant trifoliate orange ( Poncirus trifoliata ) compared with its diploid progenitors. Moreover, the ABA signaling pathway has central functions in stress responses and new reports in this issue reveal how epigenetic regulation interacts with ABA signaling.…”

“…Moreover, the ABA signaling pathway has central functions in stress responses and new reports in this issue reveal how epigenetic regulation interacts with ABA signaling. (Wang et al, 2022) identify DEMETHYLATION REGULATOR 1 as a regulator of DNA methylation in the nuclear and mitochondrial genomes acting upstream of ROS1 and responding to ABA. In addition, (Tang et al, 2022) reveal how removal of the RNA modification N6‐methyladenosine by an RNA demethylase modulates ABA responses.…”

“…For example, (Zhou et al, 2022) review how R‐loops, which comprise an RNA:DNA duplex and a displaced single strand of DNA, form and are resolved, and how they interact with other known epigenetic regulatory mechanisms including DNA, RNA, and histone modifications. In addition, (Wang et al, 2022) examine Hi‐C data for rice mutants lacking a key methyltransferase and reveal key similarities between topologically associated domains in rice and Arabidopsis .…”

“…(Huang et al, 2023) use stringent criteria to re‐annotate long microRNAs (lmiRNAs, 24 nucleotides in length) in rice, revealing that most lmiRNAs are derived from MITEs and providing insight on the evolution of lmiRNAs, their targets, and their regulatory mechanisms, particularly in stress responses. Intriguingly, research by (Wang et al, 2022) suggests that we have more to learn about epigenetic mechanisms, finding that activation of transposable elements induced by nitrogen starvation seems independently to occur against known epigenetic mechanisms such as DNA and histone methylation.…”