Epigenetic marks include Histone Post-Translational Modifications and DNA methylation which are known to participate in the programming of gene expression in plants and animals. These epigenetic marks may be subjected to dynamic changes in response to endogenous and/or external stimuli and can have an impact on phenotypic plasticity. Studying how plant genomes can be epigenetically shaped under stressed conditions has become an essential issue in order to better understand the molecular mechanisms underlying plant stress responses and enabling epigenetic in addition to genetic factors to be considered when breeding crop plants. In this perspective, we discuss the contribution of epigenetic mechanisms to our understanding of plant responses to biotic and abiotic stresses. This regulation of gene expression in response to environment raises important biological questions for perennial species such as grapevine which is asexually propagated and grown worldwide in contrasting terroirs and environmental conditions. However, most species used for epigenomic studies are annual herbaceous plants, and epigenome dynamics has been poorly investigated in perennial woody plants, including grapevine. In this context, we propose grape as an essential model for epigenetic and epigenomic studies in perennial woody plants of agricultural importance.

Although epigenetic modifications have been intensely investigated over the last decade due to their role in crop adaptation to rapid climate change, it is unclear which epigenetic changes are heritable and therefore transmitted to their progeny. The identification of epigenetic marks that are transmitted to the next generations is of primary importance for their use in breeding and for the development of new cultivars with a broad-spectrum of tolerance/resistance to abiotic and biotic stresses. In this review, we discuss general aspects of plant responses to environmental stresses and provide an overview of recent findings on the role of transgenerational epigenetic modifications in crops. In addition, we take the opportunity to describe the aims of EPI-CATCH, an international COST action consortium composed by researchers from 28 countries. The aim of this COST action launched in 2020 is: (1) to define standardized pipelines and methods used in the study of epigenetic mechanisms in plants, (2) update, share, and exchange findings in epigenetic responses to environmental stresses in plants, (3) develop new concepts and frontiers in plant epigenetics and epigenomics, (4) enhance dissemination, communication, and transfer of knowledge in plant epigenetics and epigenomics.

Non-cell autonomous RNA silencing can spread from cell to cell and over long distances in animals and plants. However, the genetic requirements and signals involved in plant mobile gene silencing are poorly understood. Here, we identified a DICER-LIKE2 (DCL2)-dependent mechanism for systemic spread of posttranscriptional RNA silencing, also known as posttranscriptional gene silencing (PTGS), in Nicotiana benthamiana. Using a suite of transgenic DCL RNAi lines coupled with a GFP reporter, we demonstrated that N. benthamiana DCL1, DCL2, DCL3, and DCL4 are required to produce microRNAs and 22, 24, and 21nt small interfering RNAs (siRNAs), respectively. All investigated siRNAs produced in local incipient cells were present at low levels in distal tissues. Inhibition of DCL2 expression reduced the spread of gene silencing, while suppression of DCL3 or DCL4 expression enhanced systemic PTGS. In contrast to DCL4 RNAi lines, DCL2-DCL4 double-RNAi lines developed systemic PTGS similar to that observed in DCL2 RNAi. We further showed that the 21 or 24 nt local siRNAs produced by DCL4 or DCL3 were not involved in long-distance gene silencing. Grafting experiments demonstrated that DCL2 was required in the scion to respond to the signal, but not in the rootstock to produce/send the signal. These results suggest a coordinated DCL genetic pathway in which DCL2 plays an essential role in systemic PTGS in N. benthamiana, while both DCL4 and DCL3 attenuate systemic PTGS. We discuss the potential role of 21, 22, and 24 nt siRNAs in systemic PTGS.

Summary: Fruit formation comprises a series of developmental transitions among which the fruit set process is essential in determining crop yield. Yet, our understanding of the epigenetic landscape remodelling associated with the flower‐to‐fruit transition remains poor. We investigated the epigenetic and transcriptomic reprogramming underlying pollination‐dependent and auxin‐induced flower‐to‐fruit transitions in the tomato (Solanum lycopersicum) using combined genomewide transcriptomic profiling, global ChIP‐sequencing and whole genomic DNA bisulfite sequencing (WGBS). Variation in the expression of the overwhelming majority of genes was associated with change in histone mark distribution, whereas changes in DNA methylation concerned a minor fraction of differentially expressed genes. Reprogramming of genes involved in processes instrumental to fruit set correlated with their H3K9ac or H3K4me3 marking status but not with changes in cytosine methylation, indicating that histone posttranslational modifications rather than DNA methylation are associated with the remodelling of the epigenetic landscape underpinning the flower‐to‐fruit transition. Given the prominent role previously assigned to DNA methylation in reprogramming key genes of the transition to ripening, the outcome of the present study supports the idea that the two main developmental transitions in fleshy fruit and the underlying transcriptomic reprogramming are associated with different modes of epigenetic regulations.

Plants exhibit remarkable abilities to learn, communicate, memorize, and develop stimulus‐dependent decision‐making circuits. Unlike animals, plant memory is uniquely rooted in cellular, molecular, and biochemical networks, lacking specialized organs for these functions. Consequently, plants can effectively learn and respond to diverse challenges, becoming used to recurring signals. Artificial intelligence (AI) and machine learning (ML) represent the new frontiers of biological sciences, offering the potential to predict crop behavior under environmental stresses associated with climate change. Epigenetic mechanisms, serving as the foundational blueprints of plant memory, are crucial in regulating plant adaptation to environmental stimuli. They achieve this adaptation by modulating chromatin structure and accessibility, which contribute to gene expression regulation and allow plants to adapt dynamically to changing environmental conditions. In this review, we describe novel methods and approaches in AI and ML to elucidate how plant memory occurs in response to environmental stimuli and priming mechanisms. Furthermore, we explore innovative strategies exploiting transgenerational memory for plant breeding to develop crops resilient to multiple stresses. In this context, AI and ML can aid in integrating and analyzing epigenetic data of plant stress responses to optimize the training of the parental plants.