Review
Epigenetics for Plant Improvement: Current Knowledge and Modeling Avenues

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Trends

Broadening crop phenotypic diversity is a key issue facing the challenge of sustainable food security and crop adaptation to ongoing climate changes.

Chromatin marks and epigenetic regulatory mechanisms are essential to the control of plant developmental processes and in shaping plant phenotypic plasticity, including adaptive responses to environmental stresses.

Stability and heritability features of epigenetic marks and knowledge of epigenetic regulatory mechanisms are crucial for breeding applications.

Modeling epigenetic variations requires understanding epigenetic regulatory mechanisms to further predict their impact on plant performances.

Modeling epigenetic variations with a process-based approach could help to assess and quantify their impacts on plant performances and then to guide the decision to either induce or repress them. This modeling feedback is central to model-driven breeding strategies.

Crop modelers are urged to take epigenetic variations into account to assist breeding strategies.

Epigenetic variations are involved in the control of plant developmental processes and participate in shaping phenotypic plasticity to the environment. Intense breeding has eroded genetic diversity, and epigenetic diversity now emerge as a new source of phenotypic variations to improve adaptation to changing environments and ensure the yield and quality of crops. Here, we review how the characterization of the stability and heritability of epigenetic variations is required to drive breeding strategies, which can be assisted by process-based models. We propose future directions to hasten the elucidation of complex epigenetic regulatory networks that should help crop modelers to take epigenetic modifications into account and assist breeding strategies for specific agronomical traits.

Section snippets

Epigenetics as a New Source to Broaden Plant Phenotypic Diversity

Over the past century, integration of desired traits into crops has mainly relied on the use of natural or induced genetic variability [1]. Intense breeding programs have narrowed the range of cultivars, resulting in a considerable loss of genetic diversity [2]. Indeed, the recent completion of many important crop genomes has increased the efficiency of breeding by providing new tools, such as genome-wide association studies (GWAS), that help capture a substantial proportion of sequence-based

Epigenetics: Stability and/or Heritability of Chromatin Marks

Epigenetic information is mediated by DNA methylation and histone PTMs, the so-called chromatin marks (Box 1) that together with chromatin remodeling, small RNAs, and histone variants (Box 2), determine the conformational state of chromatin and, thus, also its transcriptional state [29]. However, the stability and heritability of chromatin marks vary and not all chromatin regulations are associated with epigenetic memory (Box 1).

DNA methylation represents a highly stable and heritable

Chromatin Changes Are Involved in the Control of Plant Development and in Environmental Responses

As mentioned above, chromatin marks, including DNA methylation and histone PTMs, have crucial roles during plant development. They are involved in the control of flowering time [16], seed and endosperm development [50], parental imprinting [25], fruit ripening 28, 51, symbiotic nodule organogenesis [52], and cell fate maintenance and reprogramming 53, 54. Impairing DNA methylation control leads to pleiotropic phenotypes consistent with multiple functions of these epigenetic mechanisms in plants

Epialleles Generate Heritable Phenotypic Variation

Evidence that epigenetic processes act on the variability of plant traits was first provided by the characterization of plant epialleles [84]. These were used to show that methylation imprints could lead to gene misexpression and, thus, to new phenotypes that are stable across generations. The Colourless Non Ripening (CNR) locus provides one of the best-characterized examples of epiallelic variation that impacts important agronomical traits. In the Cnr background, fruit ripening is dramatically

Exploiting Epigenetic Variations for Crop Improvement

Exploiting epigenetic variations for breeding applications, whether they control developmental processes or contribute to adaptation to various environments, clearly relies on their transmission features and on the plant propagation strategies (sexual versus clonal) (Table 1) [92]. For example, because 5mC patterns can be transmitted after mitosis and meiosis, DNA methylation marks could be useful in all crops, irrespective of their propagation mode. By contrast, because histone PTMs are more

Recent Advances in Modeling Epigenetics

Plant modelers face manifold challenges to predict plant performance from epigenetic variations, including the identification of the epigenetic marks and/or epigenetic regulatory mechanisms, characterization of the transmission features (especially in support of breeding schemes), and the quantification of linkages between epigenetic and phenotypic variations. Due to the difficulty of tracking epigenetic variations and characterizing epigenetic features, modeling approaches for predictive

Concluding Remarks and Future Perspectives

Epigenetic marks are involved in a range of plant developmental processes shaping plant phenotypic plasticity, including adaptive responses to environmental stresses. Therefore, their variations are expected to broaden plant phenotypic space to improve plant adaptation under ever-changing environmental conditions and/or to ensure crop yield and production quality (Figure 2, Key Figure). We have demonstrated that epigenetic variations could be exploited in predictive models should their

Acknowledgments

We thank E. Personeni for critical reading and comments on the manuscript. We are also grateful to the three anonymous reviewers for their constructive suggestions. This work was supported by the INRA divisions Environment and Agronomy, and Plant Biology and Breeding, and the University of Bordeaux, and the INRA-EA ‘Fruit and seed quality’ network.

Glossary

Chromatin marks
covalent modifications of the chromatin that include the methylation of the fifth carbon of cytosine (5mC) on the DNA molecules and histone post-translational modifications (PTMs). Histone PTMs include methylation, acetylation, ubiquitination, phosphorylation, sumoylation, and poly (ADP) ribosylation. Genes, transposable elements, heterochromatin, and so on are marked by a particular combination of epigenetic marks that define their epigenetic state. When inherited, stable

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    These authors contributed equally to this work.

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