Epigenetics has emerged as an important research field for crop improvement under the on-going climatic changes. Heritable epigenetic changes can arise independently of DNA sequence alterations and have been associated with altered gene expression and transmitted phenotypic variation. By modulating plant development and physiological responses to environmental conditions, epigenetic diversity—naturally, genetically, chemically, or environmentally induced—can help optimise crop traits in an era challenged by global climate change. Beyond DNA sequence variation, the epigenetic modifications may contribute to breeding by providing useful markers and allowing the use of epigenome diversity to predict plant performance and increase final crop production. Given the difficulties in transferring the knowledge of the epigenetic mechanisms from model plants to crops, various strategies have emerged. Among those strategies are modelling frameworks dedicated to predicting epigenetically controlled-adaptive traits, the use of epigenetics for in vitro regeneration to accelerate crop breeding, and changes of specific epigenetic marks that modulate gene expression of traits of interest. The key challenge that agriculture faces in the 21st century is to increase crop production by speeding up the breeding of resilient crop species. Therefore, epigenetics provides fundamental molecular information with potential direct applications in crop enhancement, tolerance, and adaptation within the context of climate change.

Transgenerationally heritable epialleles are defined by the stable propagation of alternative transcriptional states through mitotic and meiotic cell cycles. Given that the propagation of DNA methylation at CpG sites, mediated in Arabidopsis by MET1, plays a central role in epigenetic inheritance, we examined genomewide DNA methylation in partial and complete loss‐of‐function met1 mutants. We interpreted the data in relation to transgenerational epiallelic stability, which allowed us to classify chromosomal targets of epigenetic regulation into (i) single copy and methylated exclusively at CpGs, readily forming epialleles, and (ii) transposon‐derived, methylated at all cytosines, which may or may not form epialleles. We provide evidence that DNA sequence features such as density of CpGs and genomic repetitiveness of the loci predispose their susceptibility to epiallelic switching. The importance and predictive power of these genetic features were confirmed by analyses of common epialleles in natural Arabidopsis accessions, epigenetic recombinant inbred lines (epiRILs) and also verified in rice. Synopsis Why certain loci are able to stably switch between alternative epigenetic states (forming heritable epialleles), while others remain resistant to such switches seems to be predetermined by their genetic features, such as DNA sequence composition and repetitiveness. Low‐copy number loci enriched in CG dinucleotides form transgenerationally stable epialleles. High‐copy number loci depleted of CG nucleotides rapidly revert to one epiallelic form.

Phytohormones regulate many aspects of plant life by activating transcription factors (TFs) that bind sequence-specific response elements (REs) in regulatory regions of target genes. Despite their short length, REs are degenerate, with a core of just 3 to 4 bp. This degeneracy is paradoxical, as it reduces specificity and REs are extremely common in the genome. To study whether RE degeneracy might serve a biological function, we developed an algorithm for the detection of regulatory sequence conservation and applied it to phytohormone REs in 45 angiosperms. Surprisingly, we found that specific RE variants are highly conserved in core hormone response genes. Experimental evidence showed that specific variants act to regulate the magnitude and spatial profile of hormonal response in Arabidopsis (Arabidopsis thaliana) and tomato (Solanum lycopersicum). Our results suggest that hormone-regulated TFs bind a spectrum of REs, each coding for a distinct transcriptional response profile. Our approach has implications for precise genome editing and for rational promoter design.

Climate change has created an environment where heat stress conditions are becoming more frequent as temperatures continue to raise in crop production areas around the world. This situation leads to decreased crop production due to plant sensitivity to heat stress. Reproductive success is critically dependent on plants’ ability to produce functional pollen grains, which are the most thermo-sensitive tissue. Flavonols are plant secondary metabolites known for their potent antioxidative activity, essential for male fertility in several species including tomato, and implicated in heat stress tolerance. Since flavonols are highly abundant in fruits of the tomatohigh pigment 2(hp2) mutant, we tested the level of flavonols in pollen of this mutant, under the hypothesis that increased accumulation of flavonols would render pollen more tolerant to heat stress. Indeed, pollen from two alleles of thehp2mutant was found to have flavonols levels increased by 18 and 280% compared with wild-type (WT) under moderate chronic heat stress (MCHS) conditions. This mutant produced on average 7.8-fold higher levels of viable pollen and displayed better germination competence under heat stress conditions. The percentage of fully seeded fruits and the number of seeds per fruit were maintained in the mutant under heat stress conditions while decreased in wild-type plants. Our results strongly suggest that increased concentrations of pollen flavonols enhance pollen thermotolerance and reproductive success under heat stress conditions. Thus, the high flavonols trait may help frame the model for improving crop resilience to heat stress.