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      How Stress Facilitates Phenotypic Innovation Through Epigenetic Diversity

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          Abstract

          Climate adaptation through phenotypic innovation will become the main challenge for plants during global warming. Plants exhibit a plethora of mechanisms to achieve environmental and developmental plasticity by inducing dynamic alterations of gene regulation and by maximizing natural variation through large population sizes. While successful over long evolutionary time scales, most of these mechanisms lack the short-term adaptive responsiveness that global warming will require. Here, we review our current understanding of the epigenetic regulation of plant genomes, with a focus on stress-response mechanisms and transgenerational inheritance. Field and laboratory-scale experiments on plants exposed to stress have revealed a multitude of temporally controlled, mechanistic strategies integrating both genetic and epigenetic changes on the genome level. We analyze inter- and intra-species population diversity to discuss how methylome differences and transposon activation can be harnessed for short-term adaptive efforts to shape co-evolving traits in response to qualitatively new climate conditions and environmental stress.

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          1,135 Genomes Reveal the Global Pattern of Polymorphism in Arabidopsis thaliana

          Summary Arabidopsis thaliana serves as a model organism for the study of fundamental physiological, cellular, and molecular processes. It has also greatly advanced our understanding of intraspecific genome variation. We present a detailed map of variation in 1,135 high-quality re-sequenced natural inbred lines representing the native Eurasian and North African range and recently colonized North America. We identify relict populations that continue to inhabit ancestral habitats, primarily in the Iberian Peninsula. They have mixed with a lineage that has spread to northern latitudes from an unknown glacial refugium and is now found in a much broader spectrum of habitats. Insights into the history of the species and the fine-scale distribution of genetic diversity provide the basis for full exploitation of A. thaliana natural variation through integration of genomes and epigenomes with molecular and non-molecular phenotypes.
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            Major Impacts of Widespread Structural Variation on Gene Expression and Crop Improvement in Tomato

            Structural variants (SVs) underlie important crop improvement and domestication traits. However, resolving the extent, diversity, and quantitative impact of SVs has been challenging. We used long-read nanopore sequencing to capture 238,490 SVs in 100 diverse tomato lines. This panSV genome, along with 14 new reference assemblies, revealed large-scale intermixing of diverse genotypes, as well as thousands of SVs intersecting genes and cis-regulatory regions. Hundreds of SV-gene pairs exhibit subtle and significant expression changes, which could broadly influence quantitative trait variation. By combining quantitative genetics with genome editing, we show how multiple SVs that changed gene dosage and expression levels modified fruit flavor, size, and production. In the last example, higher order epistasis among four SVs affecting three related transcription factors allowed introduction of an important harvesting trait in modern tomato. Our findings highlight the underexplored role of SVs in genotype-to-phenotype relationships and their widespread importance and utility in crop improvement.
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              Transposable elements and the epigenetic regulation of the genome.

              Overlapping epigenetic mechanisms have evolved in eukaryotic cells to silence the expression and mobility of transposable elements (TEs). Owing to their ability to recruit the silencing machinery, TEs have served as building blocks for epigenetic phenomena, both at the level of single genes and across larger chromosomal regions. Important progress has been made recently in understanding these silencing mechanisms. In addition, new insights have been gained into how this silencing has been co-opted to serve essential functions in 'host' cells, highlighting the importance of TEs in the epigenetic regulation of the genome.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                15 January 2021
                2020
                : 11
                : 606800
                Affiliations
                Department of Molecular Biology, Max Planck Institute for Developmental Biology , Tübingen, Germany
                Author notes

                Edited by: Marco Catoni, University of Birmingham, United Kingdom

                Reviewed by: Frédéric Pontvianne, UMR5096 Laboratoire Génome et Développement des Plantes, France; German Martinez, Swedish University of Agricultural Sciences, Sweden; Marie Mirouze, Institut de Recherche Pour le Développement (IRD), France

                *Correspondence: Hajk-Georg Drost, hajk-georg.drost@ 123456tuebingen.mpg.de

                This article was submitted to Plant Cell Biology, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2020.606800
                7843580
                33519857
                33e17076-87fb-4816-aeff-02ee94441dad
                Copyright © 2021 Srikant and Drost.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 15 September 2020
                : 16 December 2020
                Page count
                Figures: 2, Tables: 0, Equations: 0, References: 114, Pages: 14, Words: 0
                Funding
                Funded by: Max-Planck-Gesellschaft 10.13039/501100004189
                Categories
                Plant Science
                Hypothesis and Theory

                Plant science & Botany
                epigenetics (dna methylation),epigenomics,transposable element,abiotic stress,energy stress,plant engineering,methylome diversity,natural variation in plants

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