Polycomb-group protein SlMSI1 represses the expression of fruit-ripening genes to prolong shelf life in tomato

Abstract

Polycomb-group (PcG) protein MULTICOPY SUPPRESSOR OF IRA1 (MSI1) protein is an evolutionarily conserved developmental suppressor and plays a crucial role in regulating epigenetic modulations. However, the potential role and function of MSI1 in fleshy fruits remain unknown. In this study, SlMSI1 was cloned and transformed into tomato to explore its function. The quantitative real-time PCR results showed that SlMSI1 was highly expressed in flowers and fruits and that its transcript and protein levels were significantly decreased in fruits after the breaker stage. Additionally, SlMSI1-overexpressing transgenic tomatoes displayed abnormal non-ripening fruit formation, whereas its suppression promoted fruit ripening in transgenic tomatoes. Quantitative real-time PCR assays also showed that RIN and its regulons were decreased in SlMSI1 overexpression transgenic tomato fruits. Furthermore, RNA-seq analysis demonstrated that SlMSI1 inhibits fruit ripening by negatively regulating a large set of fruit-ripening genes in addition to RIN and its regulons. Finally, genetic manipulation of SlMSI1 and RIN successfully prolonged the fruit shelf life by regulating the fruit-ripening genes in tomato. Our findings reveal a novel regulatory function of SlMSI1 in fruit ripening and provide a new regulator that may be useful for genetic engineering and modification of fruit shelf life.

A critical evaluation of the role of ethylene and MADS transcription factors in the network controlling fleshy fruit ripening

“…(d) Appearance of F 1 hybrid fruits with the RIN / RIN ‐ KO genotypes (namely hybrid WT ( AC ) with rin G3‐6 and rin G3‐5 plants) and fruits with the RIN / rin genotype (namely hybrid WT ( AC ) with rin mutant plants (reproduced with permission from Ito et al ., ). (e) Ripening comparison between the WT , rin mutant, Sl MSI 1 overexpression lines L1, L2 and L29 and the recovery lines R1, R2 and R3 (the Sl MSI 1 overexpression lines L1, L2 and L29 complemented by overexpressing RIN in Sl MSI 1‐overexpression transgenic plants; reproduced with permission from D. D. Liu et al ., ).…”

“…c reproduced from Fig. a in D. D. Liu et al ., ). All overexpressing lines produced nonripening fruits, and looked very similar to rin mutant tomatoes (Fig.…”

“…(), an extremely interesting approach to the problem was taken by D. D. Liu et al . () who manipulated expression of tomato gene SlMSI1 ( Solyc01g104510 ) using a cDNA cloned from AC tomato. SlMSI1 belongs to a subfamily of WD‐40 repeat proteins which are conserved developmental suppressors that affect DNA and histone methylation in many organisms.…”

The mode of action of remorin1 in regulating fruit ripening at transcriptional and post‐transcriptional levels

“…Current knowledge indicates that overexpression of SlNAC1 (NAM, ATAF and CUC) inhibited normal fruit ripening via reducing the expression of SlACS2 and SlACO1 (Ma et al ., ), and the transcription factor SlZFP2 (C 2 H 2 zinc finger protein) regulated fruit ripening through suppression of the ripening regulator CNR expression (Weng et al ., ). Likewise, MULTICOPY SUPPRESSOR OF IRA 1 ( SlMSI1 ) overexpression fruits failed to produce ethylene and displayed nonripening (Liu et al ., ). However, most ripening regulators are considered to localize to the nucleus.…”

Evaluation of multiple approaches to identify genome-wide polymorphisms in closely related genotypes of sweet cherry ( Prunus avium L.)

“…As delayed maturation of the fruit is the only observable phenotypic difference between ‘Glory’ and ‘Staccato,’ TRAP primers were designed to target flowering related genes with the presumption that during the ontogenic progression, these genes may influence fruit maturation. Relationship between VRN2 and Polycomb-group Proteins, which work in concert to regulate fruit maturation in tomato has been reported recently [48]. It is premature to comment on the direct role of VRN2 in regulating fruit maturation in non-climacteric sweet cherry based on this result.…”