Characterization of a tomato chlh mis-sense mutant reveals a new function of ChlH in fruit ripening

Tomato fruit ripening is a complex developmental process that is important for fruit quality and shelf life. Many factors, including ethylene and several key transcription factors, have been shown to play important roles in the regulation of tomato fruit ripening. However, our understanding of the regulation of tomato fruit ripening is still limited. Here, we describe mut26, an EMS-induced tomato (Solanum lycopersicum) mutant that exhibits chlorophyll-deficient phenotypes in various organs, including fruits. Genetic mapping and functional analyses revealed that a single-nucleotide substitution and a corresponding Pro398->Ser mis-sense mutation in SlChlH (GENOMES UNCOUPLED 5, GUN5), which encodes the H subunit of magnesium chelatase, are responsible for the defects in the mut26 strain. Transcript analyses towards the expression of many SlPhANGs revealed that mut26 is defective in plastid retrograde signalling during tomato fruit ripening initiation, namely the transition from mature green to breaker stage. mut26 exhibits delayed progression of fruit ripening characterized by reduced fruit ethylene emission, increased fruit firmness, reduced carotenoid content and delayed plastid conversion from chloroplast to chromoplast. Given that fruit ripening requires signalling from plastids to nucleus, these data support the hypothesis that GUN5-mediated plastid retrograde signalling promotes tomato fruit ripening. We further showed that the delayed fruit ripening of mut26 is not likely caused by reduced chlorophyll content. Taken together, we identified a new function of SlChlH in the promotion of tomato fruit ripening and ethylene biosynthesis, suggesting that GUN5-mediated plastid retrograde signalling plays a promotive role in tomato fruit ripening.