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      Reconsidering plant memory: Intersections between stress recovery, RNA turnover, and epigenetics

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          Abstract

          Have plants learned to forget stress? This review proposes benefits to forgetfulness and finds key roles for RNA turnover.

          Abstract

          Plants grow in dynamic environments where they can be exposed to a multitude of stressful factors, all of which affect their development, yield, and, ultimately, reproductive success. Plants are adept at rapidly acclimating to stressful conditions and are able to further fortify their defenses by retaining memories of stress to enable stronger or more rapid responses should an environmental perturbation recur. Indeed, one mechanism that is often evoked regarding environmental memories is epigenetics. Yet, there are relatively few examples of such memories; neither is there a clear understanding of their duration, considering the plethora of stresses in nature. We propose that this field would benefit from investigations into the processes and mechanisms enabling recovery from stress. An understanding of stress recovery could provide fresh insights into when, how, and why environmental memories are created and regulated. Stress memories may be maladaptive, hindering recovery and affecting development and potential yield. In some circumstances, it may be advantageous for plants to learn to forget. Accordingly, the recovery process entails a balancing act between resetting and memory formation. During recovery, RNA metabolism, posttranscriptional gene silencing, and RNA-directed DNA methylation have the potential to play key roles in resetting the epigenome and transcriptome and in altering memory. Exploration of this emerging area of research is becoming ever more tractable with advances in genomics, phenomics, and high-throughput sequencing methodology that will enable unprecedented profiling of high-resolution stress recovery time series experiments and sampling of large natural populations.

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          Most cited references127

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          A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening.

          A major component in the regulatory network controlling fruit ripening is likely to be the gene at the tomato Colorless non-ripening (Cnr) locus. The Cnr mutation results in colorless fruits with a substantial loss of cell-to-cell adhesion. The nature of the mutation and the identity of the Cnr gene were previously unknown. Using positional cloning and virus-induced gene silencing, here we demonstrate that an SBP-box (SQUAMOSA promoter binding protein-like) gene resides at the Cnr locus. Furthermore, the Cnr phenotype results from a spontaneous epigenetic change in the SBP-box promoter. The discovery that Cnr is an epimutation was unexpected, as very few spontaneous epimutations have been described in plants. This study demonstrates that an SBP-box gene is critical for normal ripening and highlights the likely importance of epialleles in plant development and the generation of natural variation.
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            Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants.

            Small, non-coding RNAs are a distinct class of regulatory RNAs in plants and animals that control a variety of biological processes. In plants, several classes of small RNAs with specific sizes and dedicated functions have evolved through a series of pathways. The major classes of small RNAs include microRNAs (miRNAs) and small interfering RNAs (siRNAs), which differ in their biogenesis. miRNAs control the expression of cognate target genes by binding to reverse complementary sequences, resulting in cleavage or translational inhibition of the target RNAs. siRNAs have a similar structure, function, and biogenesis as miRNAs but are derived from long double-stranded RNAs and can often direct DNA methylation at target sequences. Besides their roles in growth and development and maintenance of genome integrity, small RNAs are also important components in plant stress responses. One way in which plants respond to environmental stress is by modifying their gene expression through the activity of small RNAs. Thus, understanding how small RNAs regulate gene expression will enable researchers to explore the role of small RNAs in biotic and abiotic stress responses. This review focuses on the regulatory roles of plant small RNAs in the adaptive response to stresses. This article is part of a Special Issue entitled: Plant gene regulation in response to abiotic stress. Copyright © 2011 Elsevier B.V. All rights reserved.
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              Functions of microRNAs in plant stress responses.

              The discovery of microRNAs (miRNAs) as gene regulators has led to a paradigm shift in the understanding of post-transcriptional gene regulation in plants and animals. miRNAs have emerged as master regulators of plant growth and development. Evidence suggesting that miRNAs play a role in plant stress responses arises from the discovery that miR398 targets genes with known roles in stress tolerance. In addition, the expression profiles of most miRNAs that are implicated in plant growth and development are significantly altered during stress. These later findings imply that attenuated plant growth and development under stress may be under the control of stress-responsive miRNAs. Here we review recent progress in the understanding of miRNA-mediated plant stress tolerance. Copyright © 2012 Elsevier Ltd. All rights reserved.
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                Author and article information

                Journal
                Sci Adv
                Sci Adv
                SciAdv
                advances
                Science Advances
                American Association for the Advancement of Science
                2375-2548
                February 2016
                19 February 2016
                : 2
                : 2
                : e1501340
                Affiliations
                Australian Research Council Centre of Excellence in Plant Energy Biology, Research School of Biology, Australian National University Canberra, Acton, Australian Capital Territory 0200, Australia.
                Author notes
                [* ]Corresponding author. E-mail: barry.pogson@ 123456anu.edu.au
                Author information
                http://orcid.org/0000-0002-3655-0130
                http://orcid.org/0000-0001-6746-0181
                Article
                1501340
                10.1126/sciadv.1501340
                4788475
                26989783
                4672f634-a1b5-4f56-9922-22720a126d54
                Copyright © 2016, The Authors

                This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.

                History
                : 27 September 2015
                : 08 December 2015
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100006067, Centre of Excellence in Plant Energy Biology, Australian Research Council;
                Award ID: ID0EF1AG3646
                Award ID: CE140100008
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000980, Grains Research and Development Corporation;
                Award ID: ID0EK6AG3656
                Award ID: GRS184
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000980, Grains Research and Development Corporation;
                Award ID: ID0EGNBG3657
                Award ID: GRS10683
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100006067, Centre of Excellence in Plant Energy Biology, Australian Research Council;
                Award ID: ID0E1UBG3658
                Award ID: CE140100008
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000923, Australian Research Council;
                Award ID: ID0E4ZBG3659
                Award ID: DE150101206
                Award Recipient :
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                Abel Bellen

                rna metabolism,gene silencing,epigenetics,dna methylation,rna turnover,abiotic stress,plants,arabidopsis,stress recovery,plant memory

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