Manipulation of Plastidial Protein Quality Control Components as a New Strategy to Improve Carotenoid Contents in Tomato Fruit.

Lucio D’Andrea,Manuel Rodriguez-Concepcion

doi:10.3389/fpls.2019.01071

Lucio D’Andrea, Manuel Rodriguez-Concepcion

Open Access

https://doi.org/10.3389/fpls.2019.01071

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Abstract

Carotenoids such as β-carotene (pro-vitamin A) and lycopene accumulate at high levels during tomato (Solanum lycopersicum L.) fruit ripening, contributing to the characteristic color and nutritional quality of ripe tomatoes. Besides their role as pigments in chromoplast-harboring tissues such as ripe fruits, carotenoids are important for photosynthesis and photoprotection in the chloroplasts of photosynthetic tissues. Interestingly, recent work in Arabidopsis thaliana (L.) Heynh. has unveiled a critical role of chloroplast protein quality control components in the regulation of carotenoid biosynthesis. The accumulation (i.e. degradation rate) and activity (i.e. folding status) of phytoene synthase (PSY) and other Arabidopsis biosynthetic enzymes is modulated by chaperones such as Orange (OR) and Hsp70 in coordination with the stromal Clp protease complex. OR and Clp protease were recently shown to also influence PSY stability and carotenoid accumulation in tomato. Here we show how manipulating the levels of plastid-localized Hsp70 in transgenic tomato plants can also impact the accumulation of carotenoids in ripe fruit. The resulting carotenoid profile and chromoplast ultrastructure, however, are different from those obtained in tomatoes from transgenic lines with increased OR activity. These results suggest that different chaperone families target different processes related to carotenoid metabolism and accumulation during tomato ripening. We further discuss other possible targets for future manipulation in tomato based on the knowledge acquired in Arabidopsis.

Highlights

Carotenoids are a group of isoprenoid molecules produced by all photosynthetic organisms and some non-photosynthetic bacteria and fungi (Rodriguez-Concepcion et al, 2018)
Tomato Chaperones, Proteases and Carotenoids synthesized and accumulated in plastids. They derive from geranylgeranyl diphosphate (GGPP), generated from prenyl diphosphate substrates synthetized by the methylerythritol 4-phosphate (MEP) pathway (Figure 1A)
It is unknown whether other ripening-induced chaperones that protect against protein misfolding and aggregation such as heat shock protein 21 (Hsp21) (Figure 1B) or Hsp70 (Figure 1C) are up-regulated in tomato as they are in Arabidopsis when Clp protease activity is blocked (Llamas et al, 2017)

Summary

INTRODUCTION

Carotenoids are a group of isoprenoid molecules produced by all photosynthetic organisms and some non-photosynthetic bacteria and fungi (Rodriguez-Concepcion et al, 2018) In plants they are essential as photoprotective pigments for photosynthesis and as precursors for the production of hormones (abscisic acid, strigolactones) and other signaling molecules. Levels of plastidial chaperones (often referred to as heatshock proteins) increase during natural fruit ripening in tomato (Figures 1B, C) and several other plant systems, presumably to deal with proteome changes and protein folding stress resulting from the chromoplast differentiation process (Bonk et al, 1996; Neta-Sharir et al, 2005; Barsan et al, 2012; Suzuki et al, 2015; Shukla et al, 2017; D’Andrea et al, 2018). We revise recent advances in our understanding of the connections between PQC and carotenoid accumulation and discuss how interference with PQC components can improve the carotenoid profile of tomato fruits, one of the most highly consumed vegetables worldwide

Learning From Arabidopsis

Translating to Tomato

Filling the Gaps

Looking Forward