A DEMETER-like DNA demethylase governs tomato fruit ripening

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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Critical roles of DNA demethylation in the activation of ripening-induced genes and inhibition of ripening-repressed genes in tomato fruit

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1705233114 ◽

2017 ◽

Vol 114 (22) ◽

pp. E4511-E4519 ◽

Cited By ~ 107

Author(s):

Zhaobo Lang ◽

Yihai Wang ◽

Kai Tang ◽

Dengguo Tang ◽

Tatsiana Datsenka ◽

...

Keyword(s):

Dna Methylation ◽

Fruit Ripening ◽

Tomato Fruit ◽

Dna Demethylation ◽

Epigenetic Mark ◽

Loss Of Function ◽

Active Dna Demethylation ◽

Tomato Fruit Ripening ◽

Induced Genes ◽

Environmental Responses

DNA methylation is a conserved epigenetic mark important for genome integrity, development, and environmental responses in plants and mammals. Active DNA demethylation in plants is initiated by a family of 5-mC DNA glycosylases/lyases (i.e., DNA demethylases). Recent reports suggested a role of active DNA demethylation in fruit ripening in tomato. In this study, we generated loss-of-function mutant alleles of a tomato gene, SlDML2, which is a close homolog of the Arabidopsis DNA demethylase gene ROS1. In the fruits of the tomato mutants, increased DNA methylation was found in thousands of genes. These genes included not only hundreds of ripening-induced genes but also many ripening-repressed genes. Our results show that SlDML2 is critical for tomato fruit ripening and suggest that active DNA demethylation is required for both the activation of ripening-induced genes and the inhibition of ripening-repressed genes.

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

Food Quality and Safety ◽

10.1093/fqsafe/fyab028 ◽

2021 ◽

Author(s):

Hui Zheng ◽

Rong Jin ◽

Zimeng Liu ◽

Cui Sun ◽

Yanna Shi ◽

...

Keyword(s):

Cell Wall ◽

Botrytis Cinerea ◽

Fruit Ripening ◽

Tomato Fruit ◽

Grey Mould ◽

Pathogen Resistance ◽

Ethylene Response Factor ◽

Expression Of Genes ◽

Tomato Fruit Ripening ◽

Genes Encoding

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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Tomato fruit ripening factor NOR controls leaf senescence

10.1101/436899 ◽

2018 ◽

Author(s):

Xuemin Ma ◽

Salma Balazadeh ◽

Bernd Mueller-Roeber

Keyword(s):

Leaf Senescence ◽

Stress Responses ◽

Fruit Ripening ◽

Higher Plants ◽

Tomato Fruit ◽

Leaf Age ◽

Nac Transcription Factors ◽

Tomato Fruit Ripening ◽

Elevated Expression ◽

Senescence Associated Genes

AbstractNAC transcription factors (TFs) are important regulators of expressional reprogramming during plant development, stress responses and leaf senescence. NAC TFs also play important roles in fruit ripening. In tomato (Solanum lycopersicum), one of the best characterized NAC involved in fruit ripening is NON-RIPENING (NOR) and the non-ripening (nor) mutation has been widely used to extend fruit shelf life in elite varieties. Here, we show that NOR additionally controls leaf senescence. Expression of NOR increases with leaf age, and developmental as well as dark-induced senescence are delayed in the nor mutant, while overexpression of NOR promotes leaf senescence. Genes associated with chlorophyll degradation as well as senescence-associated genes (SAGs) show reduced and elevated expression, respectively, in nor mutants and NOR overexpressors. Overexpression of NOR also stimulates leaf senescence in Arabidopsis thaliana. In tomato, NOR supports senescence by directly and positively regulating the expression of several senescence-associated genes including, besides others, SlSAG15 and SlSAG113, SlSGR1 and SlYLS4. Finally, we find that another senescence control NAC TF, namely SlNAP2, acts upstream of NOR to regulate its expression. Our data support a model whereby NAC TFs have often been recruited by higher plants for both, the control of leaf senescence and fruit ripening.

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SlGRAS4 accelerates fruit ripening by regulating ethylene biosynthesis genes and SlMADS1 in tomato

Horticulture Research ◽

10.1038/s41438-020-00431-9 ◽

2021 ◽

Vol 8 (1) ◽

Author(s):

Yudong Liu ◽

Yuan Shi ◽

Deding Su ◽

Wang Lu ◽

Zhengguo Li

Keyword(s):

Transcription Factors ◽

Stress Responses ◽

Fruit Ripening ◽

Tomato Fruit ◽

Ethylene Biosynthesis ◽

Negative Regulator ◽

Carotenoid Content ◽

Total Carotenoid Content ◽

Tomato Fruit Ripening ◽

Transcriptional Regulatory Mechanisms

AbstractGRAS proteins are plant-specific transcription factors that play crucial roles in plant development and stress responses. However, their involvement in the ripening of economically important fruits and their transcriptional regulatory mechanisms remain largely unclear. Here, we demonstrated that SlGRAS4, encoding a transcription factor of the GRAS family, was induced by the tomato ripening process and regulated by ethylene. Overexpression of SlGRAS4 accelerated fruit ripening, increased the total carotenoid content and increased PSY1 expression in SlGRAS4-OE fruit compared to wild-type fruit. The expression levels of key ethylene biosynthesis genes (SlACS2, SlACS4, SlACO1, and SlACO3) and crucial ripening regulators (RIN and NOR) were increased in SlGRAS4-OE fruit. The negative regulator of tomato fruit ripening, SlMADS1, was repressed in OE fruit. Exogenous ethylene and 1-MCP treatment revealed that more endogenous ethylene was derived in SlGRAS4-OE fruit. More obvious phenotypes were observed in OE seedlings after ACC treatment. Yeast one-hybrid and dual-luciferase assays confirmed that SlGRAS4 can directly bind SlACO1 and SlACO3 promoters to activate their transcription, and SlGRAS4 can also directly repress SlMADS1 expression. Our study identified that SlGRAS4 acts as a new regulator of fruit ripening by regulating ethylene biosynthesis genes in a direct manner. This provides new knowledge of GRAS transcription factors involved in regulating 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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Global increase in DNA methylation during orange fruit development and ripening

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1815441116 ◽

2019 ◽

Vol 116 (4) ◽

pp. 1430-1436 ◽

Cited By ~ 37

Author(s):

Huan Huang ◽

Ruie Liu ◽

Qingfeng Niu ◽

Kai Tang ◽

Bo Zhang ◽

...

Keyword(s):

Dna Methylation ◽

Fruit Ripening ◽

Tomato Fruit ◽

Dna Demethylation ◽

Epigenetic Mark ◽

Dna Hypermethylation ◽

Active Dna Demethylation ◽

Orange Fruit ◽

Global Increase ◽

Genomic Regions

DNA methylation is an important epigenetic mark involved in many biological processes. The genome of the climacteric tomato fruit undergoes a global loss of DNA methylation due to active DNA demethylation during the ripening process. It is unclear whether the ripening of other fruits is also associated with global DNA demethylation. We characterized the single-base resolution DNA methylomes of sweet orange fruits. Compared with immature orange fruits, ripe orange fruits gained DNA methylation at over 30,000 genomic regions and lost DNA methylation at about 1,000 genomic regions, suggesting a global increase in DNA methylation during orange fruit ripening. This increase in DNA methylation was correlated with decreased expression of DNA demethylase genes. The application of a DNA methylation inhibitor interfered with ripening, indicating that the DNA hypermethylation is critical for the proper ripening of orange fruits. We found that ripening-associated DNA hypermethylation was associated with the repression of several hundred genes, such as photosynthesis genes, and with the activation of hundreds of genes, including genes involved in abscisic acid responses. Our results suggest important roles of DNA methylation in orange fruit ripening.

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