Harnessing epigenome modifications for better crops

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Carpel size, grain filling, and morphology determine individual grain weight in wheat. Journal of Experimental Botany 66, 6715–6730. Harnessing epigenome modifications for better crops James Giovannoni US Department of Agriculture Robert W. Holley Center and Boyce Thompson Institute, Tower Road, Cornell University campus, Ithaca, NY 14853, USA ; or Chemical DNA modifications such as methylation influence translation of the DNA code to specific genetic outcomes. While such modifications can be heritable, others are transient, and their overall contribution to plant genetic diversity remains intriguing but uncertain. In this issue, Gouil and colleagues (pages 2655–2664) characterize the epigenome phenomenon termed ‘paramutation’ underlying a tomato photosynthesis-related gene defect, and in doing so expand our understanding of how epigenome modifications are conferred with exciting implications for crop improvement. It has long been recognized that DNA harbors information of richer texture and fidelity than the DNA sequence alone. Just as recorded texts contain information while volume, emphasis and accent contribute to the ultimate meaning conveyed by language, DNA sequence presents the genetic code while epigenome modifications influence specific conversion of this code into phenotypic traits. Epigenome contributions to genetic diversity and outcomes are gaining in appreciation as genomes and their modifications become ever more readily characterized and cataloged. As examples, whole genome sequencing and genomic DNA–protein interaction studies have revealed that many genomes, including those of important crops, include large repertoires of DNA- and RNA-derived mobile genetic elements rendered silent via chemical modifications, including cytosine methylation and methylation or acetylation of DNA-associated histone proteins (Cui and Cao, 2014). Also heritable epigenome reprogramming is critical in plant embryo development (Schmitz and Ecker, 2012), while developmental epigenome changes contribute to fruit maturation and ripening (Zhong et al., 2013), with additional modifications acquired in response to stress conditions. Recent evidence suggests the existence of molecular mechanisms in place to erase these induced modifications prior to meiotic transfer (Iwasaki and Paszkowski, 2014). A number of epialleles (stable genetic variants in DNA methylation patterns, but not DNA sequence) have been reported (Weigel and Colot, 2012), confirming that some heritable genetic diversity is anchored in the epigenome. The realization that a number of genetic diseases are traceable to the epigenome, including some cancers (Timp and Feinberg, 2013), has accelerated interest and inquiry into mechanisms of epigenome modification and resulting manifestations that can contribute to illness. Similarly, research in plants is spurred on by the knowledge that a clearer mechanistic picture of epigenome mechanisms will facilitate our understanding of their relative contributions to crop genetic diversity and open doors to their use for crop improvement. Paramutation facilitates genetic diversity via epigenome modification Paramutation has been studied extensively in maize, though examples have been reported in additional species, including © The Author 2016. Published by Oxford University Press on behalf of the Society for Experimental Biology. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Insight 2536 | Box 1. Endogenous paramutation and targeted gene silencing Endogenous paramutation and targeted gene silencing – e.g. virus-induced gene silencing (VIGS) – confer siRNA-mediated DNA methylation changes on susceptible loci. In this example the hypomethylated and transcriptionally active (*) P allele is converted to the hypomethylated and inactive p allele by either mechanism. A range of genetic outcomes could be achieved through differential methylation highlighting the potential for targeted epigenome and trait engineering. Tomato as a model for epigenome analysis While maize is among the most important staple crops and a model for plant genetics, the cultivated tomato (Solanum lycopersicum) offers a number of advantages for experimentation. These include a smaller and less repetitive sequenced genome; the ability to create stable inbred and true-breeding lines; efficient means of stable and transient DNA transformation; and a large collection of characterized genetic mutations, variants and inter-fertile wild species facilitating genetic analyses (The Tomato Genome Consortium, 2012 and references therein). Gouil et al. (2016) took advantage of these features in characterizing the paramutagenic tomato sulf locus, which manifests as sectors of chlorosis (i.e. yellowing, thus the sulfurea designation) in sulf/+ leaves where paramutat (...truncated)