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      Ethylene and RIPENING INHIBITOR Modulate Expression of SlHSP17.7A, B Class I Small Heat Shock Protein Genes During Tomato Fruit Ripening


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          Heat shock proteins (HSPs) are ubiquitous and highly conserved in nature. Heat stress upregulates their gene expression and now it is known that they are also developmentally regulated. We have studied regulation of small HSP genes during ripening of tomato fruit. In this study, we identify two small HSP genes, SlHSP17.7A and SlHSP17.7B, localized on tomato Chr.6 and Chr.9, respectively. Each gene encodes proteins constituting 154 amino acids and has characteristic domains as in other sHSP genes. We found that SlHSP17.7A and SlHSP17.7B gene expression is low in the vegetative tissues as compared to that in the fruit. These sHSP genes are characteristically expressed in a fruit-ripening fashion, being upregulated during the ripening transition of mature green to breaker stage. Their expression patterns mirror that of the rate-limiting ethylene biosynthesis gene ACC (1-aminocyclopropane-1-carboxylic acid) synthase, SlACS2, and its regulator SlMADS-RIN. Exogenous application of ethylene to either mature green tomato fruit or tomato leaves suppressed the expression of both the SlHSP17.7A, B genes. Notably and characteristically, a transgenic tomato line silenced for SlACS2 gene and whose fruits produce ~50% less ethylene in vivo, had higher expression of both the sHSP genes at the fruit ripening transition stages [breaker (BR) and BR+3] than the control fruit. Moreover, differential gene expression of SlHSP17.7A versus SlHSP17.7B gene was apparent in the tomato ripening mutants— rin/rin, nor/nor, and Nr/Nr, with the expression of SlHSP17.7A being significantly reduced but that of SlHSP17.7B significantly upregulated as compared to the wild type (WT). These data indicate that ethylene negatively regulates transcriptional abundance of both these sHSPs. Transient overexpression of the ripening regulator SlMADS-RIN in WT and ACS2-AS mature green tomato fruits suppressed the expression of SlHSP17.7A but not that of SlHSP17.7B. Thus, ethylene directly or in tune with SlMADS-RIN regulates the transcript abundance of both these sHSP genes.

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          Most cited references55

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          Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response.

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            Molecular chaperones in cellular protein folding.

            F U Hartl (1996)
            The folding of many newly synthesized proteins in the cell depends on a set of conserved proteins known as molecular chaperones. These prevent the formation of misfolded protein structures, both under normal conditions and when cells are exposed to stresses such as high temperature. Significant progress has been made in the understanding of the ATP-dependent mechanisms used by the Hsp70 and chaperonin families of molecular chaperones, which can cooperate to assist in folding new polypeptide chains.
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              A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus.

              Tomato plants harboring the ripening-inhibitor (rin) mutation yield fruits that fail to ripen. Additionally, rin plants display enlarged sepals and loss of inflorescence determinacy. Positional cloning of the rin locus revealed two tandem MADS-box genes (LeMADS-RIN and LeMADS-MC), whose expression patterns suggested roles in fruit ripening and sepal development, respectively. The rin mutation alters expression of both genes. Gene repression and mutant complementation demonstrate that LeMADS-RIN regulates ripening, whereas LeMADS-MC affects sepal development and inflorescence determinacy. LeMADS-RIN demonstrates an agriculturally important function of plant MADS-box genes and provides molecular insight into nonhormonal (developmental) regulation of ripening.

                Author and article information

                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                30 June 2020
                : 11
                : 975
                [1] 1 Sustainable Agricultural Systems Laboratory, The Henry A. Wallace Beltsville Agricultural Research Center, United States Department of Agriculture-ARS , Beltsville, MD, United States
                [2] 2 Soybean Genomics and Improvement Laboratory, The Henry A. Wallace Beltsville Agricultural Research Center, United States Department of Agriculture-ARS , Beltsville, MD, United States
                Author notes

                Edited by: Carolina Andrea Torres, Washington State University, United States

                Reviewed by: Julia Vrebalov, Boyce Thompson Institute, United States; Niranjan Chakraborty, National Institute of Plant Genome Research (NIPGR), India

                *Correspondence: Autar K. Mattoo, autar.mattoo@ 123456usda.gov

                This article was submitted to Crop and Product Physiology, a section of the journal Frontiers in Plant Science

                Copyright © 2020 Upadhyay, Tucker and Mattoo

                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.

                : 15 April 2020
                : 16 June 2020
                Page count
                Figures: 8, Tables: 0, Equations: 0, References: 65, Pages: 15, Words: 7017
                Plant Science
                Original Research

                Plant science & Botany
                gene expression,ethylene,1-mcp,slmads-rin,small heat shock protein genes,tomato,tomato ripening mutants


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