Role of the tomato fruit ripening regulator MADS-RIN in resistance to Botrytis cinerea infection

Abstract Tomato MADS-RIN (RIN) transcription factor has been shown to be a master activator regulating fruit ripening. Recent studies have revealed that in addition to activating many other cell wall genes, it also represses expression of XTH5, XTH8 and MAN4a, which are positively related to excess flesh softening and cell wall degradation, which might indicate it has a potential role in pathogen resistance of ripening fruit. In this study, both wild type (WT) and RIN-knockout (RIN-KO) mutant tomato fruit were infected with Botrytis cinerea, to investigate the function of RIN in defence against pathogen infection during ripening. The results showed that RIN-KO fruit were much more sensitive to B.cinerea infection with larger lesion sizes. Transcriptiome data and qRT-PCR assay indicate genes of phenylalanine ammonialyase (PAL) and chitinase (CHI) in RIN-KO fruit were reduced and their corresponding enzyme activities were decreased. Transcripts of genes encoding pathogenesis-related proteins (PRs), including PR1a, PRSTH2 and APETALA2/Ethylene Response Factor (AP2/ERF) including ERF.A1, Pti5, Pti6, ERF.A4 were reduced in RIN-KO fruit comparing to WT fruit. Moreover, in the absence of RIN the expression of genes encoding cell wall modifying enzymes XTH5, XTH8, MAN4a has been reported to be elevated, which is potentially correlated with cell wall properties. When present, RIN represses transcription of XTH5 by activating ERF.F4 a class II (repressor class) ERF gene family member and ERF.F5. These results support the conclusion that RIN enhances ripening-related resistance to grey mould infection by upregulating pathogen-resistance genes and defense enzyme activies as well as reducing accumulation of transcripts encoding some cell wall enzymes.

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A DEMETER-like DNA demethylase governs tomato fruit ripening

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1503362112 ◽

2015 ◽

Vol 112 (34) ◽

pp. 10804-10809 ◽

Cited By ~ 126

Author(s):

Ruie Liu ◽

Alexandre How-Kit ◽

Linda Stammitti ◽

Emeline Teyssier ◽

Dominique Rolin ◽

...

Keyword(s):

Stress Responses ◽

Fruit Ripening ◽

Developmental Process ◽

Tomato Fruit ◽

Dna Demethylation ◽

Biochemical Processes ◽

Active Dna Demethylation ◽

Expression Of Genes ◽

Tomato Fruit Ripening ◽

Genes Encoding

In plants, genomic DNA methylation which contributes to development and stress responses can be actively removed by DEMETER-like DNA demethylases (DMLs). Indeed, in Arabidopsis DMLs are important for maternal imprinting and endosperm demethylation, but only a few studies demonstrate the developmental roles of active DNA demethylation conclusively in this plant. Here, we show a direct cause and effect relationship between active DNA demethylation mainly mediated by the tomato DML, SlDML2, and fruit ripening— an important developmental process unique to plants. RNAi SlDML2 knockdown results in ripening inhibition via hypermethylation and repression of the expression of genes encoding ripening transcription factors and rate-limiting enzymes of key biochemical processes such as carotenoid synthesis. Our data demonstrate that active DNA demethylation is central to the control of ripening in tomato.

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Infection Strategies Deployed by Botrytis cinerea, Fusarium acuminatum, and Rhizopus stolonifer as a Function of Tomato Fruit Ripening Stage

Frontiers in Plant Science ◽

10.3389/fpls.2019.00223 ◽

2019 ◽

Vol 10 ◽

Cited By ~ 15

Author(s):

Stefan Petrasch ◽

Christian J. Silva ◽

Saskia D. Mesquida-Pesci ◽

Karina Gallegos ◽

Casper van den Abeele ◽

...

Keyword(s):

Botrytis Cinerea ◽

Fruit Ripening ◽

Tomato Fruit ◽

Rhizopus Stolonifer ◽

Ripening Stage ◽

Fusarium Acuminatum ◽

Tomato Fruit Ripening

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Effect of high temperature on cell wall modifications associated with tomato fruit ripening

Postharvest Biology and Technology ◽

10.1016/0925-5214(92)90008-d ◽

1992 ◽

Vol 1 (3) ◽

pp. 257-264 ◽

Cited By ~ 16

Author(s):

Elizabeth J. Mitcham ◽

Roy E. McDonald

Keyword(s):

Cell Wall ◽

High Temperature ◽

Fruit Ripening ◽

Tomato Fruit ◽

Tomato Fruit Ripening

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NAC transcription factors SNAC4 and SNAC9 synergistically regulate tomato fruit ripening by affecting expression of genes involved in ethylene and abscisic acid metabolism and signal transduction

Postharvest Biology and Technology ◽

10.1016/j.postharvbio.2021.111555 ◽

2021 ◽

Vol 178 ◽

pp. 111555

Author(s):

Sen Yang ◽

Jiaqian Zhou ◽

Christopher B. Watkins ◽

Caie Wu ◽

Yanchun Feng ◽

...

Keyword(s):

Signal Transduction ◽

Transcription Factors ◽

Abscisic Acid ◽

Fruit Ripening ◽

Acid Metabolism ◽

Tomato Fruit ◽

Nac Transcription Factors ◽

Expression Of Genes ◽

Tomato Fruit Ripening ◽

Abscisic Acid Metabolism

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45Ca mobility and distribution during ripening and maturation of Rutgers and RIN tomatoes

Agricultural and Food Science ◽

10.23986/afsci.72217 ◽

1986 ◽

Vol 58 (1) ◽

pp. 27-32

Author(s):

L. R. Howard ◽

A. Uusi-Rauva ◽

J. J. Laine

Keyword(s):

Cell Wall ◽

Fruit Ripening ◽

Early Stage ◽

Tomato Fruit ◽

Tissue Levels ◽

Tomato Fruit Ripening ◽

Soluble Calcium ◽

Low Levels

Radioisotope 45Ca was used to examine changes in levels of bound and soluble calcium during tomato fruit ripening, and the distribution of calcium in different regions of Rutgers and Rin (non-ripening) tomato tissue. Levels of cell wallmiddle lamella bound 45Ca decreased readily in pericarp tissue during ripening of Rutgers tomatoes with only as mall decrease being observed in RIN fruit. No significant increase in soluble 45Ca was observed for either genotype during ripening. Decreasing levels of bound and soluble 45Ca were observed from calyx to blossom end of pericarp tissue in Rutgers and RIN fruits. Low levels of bound 45Ca were found in the inner locular walls at an early stage of tomato ripening. The implication of low levels of cell wall bound calcium in relation to catabolic changes associated with ripening are discussed.

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Fruit Ripening in Sour Cherry: Changes in Expression of Genes Encoding Expansins and other Cell-wall-modifying Enzymes

Journal of the American Society for Horticultural Science ◽

10.21273/jashs.128.1.0016 ◽

2003 ◽

Vol 128 (1) ◽

pp. 16-22 ◽

Cited By ~ 17

Author(s):

Sang-Dong Yoo ◽

Zhifang Gao ◽

Claudio Cantini ◽

Wayne H. Loescher ◽

Steven van Nocker

Keyword(s):

Cell Wall ◽

Fruit Ripening ◽

Pectate Lyase ◽

Sour Cherry ◽

Xyloglucan Endotransglycosylase ◽

Model Species ◽

Cell Wall Modification ◽

Fruit Species ◽

Expression Of Genes ◽

Genes Encoding

A preliminary understanding of developmental processes among divergent species is essential to evaluate the applicability of information from model species to plants of agricultural importance. In tomato (Lycopersicon esculentum Mill.), where the molecular biology associated with fruit ripening has been studied most extensively, tissue softening is due at least in part to the activity of proteins called expansins, in concert with enzymatic activities that modify the pectin and xyloglucan components of the cell wall. We evaluated the potential for the concerted action of expansins and other cell wall-modifying enzymes during ripening in a highly divergent fruit species, sour cherry (Prunus cerasus L.). We identified a family of four expansin genes that was strongly upregulated at the advent of ripening. Activation of these genes was accompanied by strong upregulation of gene(s) encoding potential pectin methylesterases, pectate lyase(s), and xyloglucan endotransglycosylase(s). Initiation of ripening and gene induction were also associated with a rapid decrease in cell wall weight. These results suggest that expansin and several other distinct activities could be involved in ripening-associated cell wall modification in cherries.

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