Post-transcriptional regulation of fruit ripening and disease resistance in tomato by the vacuolar protease SlVPE3

Weihao Wang,Jianghua Cai,Peiwen Wang,Guozheng Qin,Shiping Tian

doi:10.1186/s13059-017-1178-2

Abstract

BackgroundProteases represent one of the most abundant classes of enzymes in eukaryotes and are known to play key roles in many biological processes in plants. However, little is known about their functions in fruit ripening and disease resistance, which are unique to flowering plants and required for seed maturation and dispersal. Elucidating the genetic mechanisms of fruit ripening and disease resistance is an important goal given the biological and dietary significance of fruit.ResultsThrough expression profile analyses of genes encoding tomato (Solanum lycopersicum) cysteine proteases, we identify a number of genes whose expression increases during fruit ripening. RNA interference (RNAi)-mediated repression of SlVPE3, a vacuolar protease gene, results in alterations in fruit pigmentation, lycopene biosynthesis, and ethylene production, suggesting that SlVPE3 is necessary for normal fruit ripening. Surprisingly, the SlVPE3 RNAi fruit are more susceptible to the necrotrophic pathogen Botrytis cinerea. Quantitative proteomic analysis identified 314 proteins that differentially accumulate upon SlVPE3 silencing, including proteins associated with fruit ripening and disease resistance. To identify the direct SlVPE3 targets and mechanisms contributing to fungal pathogen resistance, we perform a screening of SlVPE3-interacting proteins using co-immunoprecipitation coupled with mass spectrometry. We show that SlVPE3 is required for the cleavage of the serine protease inhibitor KTI4, which contributes to resistance against the fungal pathogen B. cinerea.ConclusionsOur findings contribute to elucidating gene regulatory networks and mechanisms that control fruit ripening and disease resistance responses.

Highlights

Proteases represent one of the most abundant classes of enzymes in eukaryotes and are known to play key roles in many biological processes in plants
Expression of the protease SlVPE3 increases steadily during fruit ripening The tomato genome encodes more than 900 predicted proteases of diverse catalytic classes, based on the MEROPS protease database [26], but in this study we focused on cysteine proteases, a class that has been shown to take part in a variety of biological processes [27]
The transcript levels of a vacuolar processing enzyme (VPE) gene from Citrus sinensis have been observed to increase during fruit ripening [35], which when taken together with our results suggests that VPE proteins might contribute to ripening in a range of species

Summary

Introduction

Proteases represent one of the most abundant classes of enzymes in eukaryotes and are known to play key roles in many biological processes in plants. Little is known about their functions in fruit ripening and disease resistance, which are unique to flowering plants and required for seed maturation and dispersal. Fruit are highly specialized plant organs that play a central role in seed maturation and dispersal in angiosperms. They are valuable components of human diets, providing essential nutrients and a wide range of “bioactive” compounds that are important for human health [1]. Unlike the relatively well studied and defined changes in the fruit transcriptome during ripening, little is known about its post-transcriptional regulation

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Conclusion