Altered Chloroplast Development and Delayed Fruit Ripening Caused by Mutations in a Zinc Metalloprotease at the lutescent2 Locus of Tomato    

Abstract

The chloroplast is the site of photosynthesis in higher plants but also functions as the center of synthesis for primary and specialized metabolites including amino acids, fatty acids, starch, and diverse isoprenoids. Mutants that disrupt aspects of chloroplast function represent valuable tools for defining structural and biochemical regulation of the chloroplast and its interplay with whole-plant structure and function. The lutescent1 (l1) and l2 mutants of tomato (Solanum lycopersicum) possess a range of chlorophyll-deficient phenotypes including reduced rates of chlorophyll synthesis during deetiolation and enhanced rates of chlorophyll loss in leaves and fruits as they age, particularly in response to high-light stress and darkness. In addition, the onset of fruit ripening is delayed in lutescent mutants by approximately 1 week although once ripening is initiated they ripen at a normal rate and accumulation of carotenoids is not impaired. The l2 locus was mapped to the long arm of chromosome 10 and positional cloning revealed the existence of a premature stop codon in a chloroplast-targeted zinc metalloprotease of the M50 family that is homologous to the Arabidopsis (Arabidopsis thaliana) gene ETHYLENE-DEPENDENT GRAVITROPISM DEFICIENT AND YELLOW-GREEN1. Screening of tomato germplasm identified two additional l2 mutant alleles. This study suggests a role for the chloroplast in mediating the onset of fruit ripening in tomato and indicates that chromoplast development in fruit does not depend on functional chloroplasts.

Network Inference Analysis Identifies an APRR2-Like Gene Linked to Pigment Accumulation in Tomato and Pepper Fruits

“…This is in contrast to observations with GLK2 overexpressors reported by Powell et al (2012), where no obvious effect on the timing of ripening was reported. Our results suggest that the APRR2-Like gene product may form part of a ripening signal mechanism involving the plastid compartment (Barry et al, 2012). The mechanism of action clearly demands further investigation.…”

Proteomic Analysis of Chloroplast-to-Chromoplast Transition in Tomato Reveals Metabolic Shifts Coupled with Disrupted Thylakoid Biogenesis Machinery and Elevated Energy-Production Components

“…This indicates that chromoplastogenesis involves profound changes in signaling events whose details and interactions remain to be elucidated. The demonstration that chromoplasts can develop from altered chloroplasts in lutescent2 tomato fruit mutants (Barry et al, 2012) indicates that the differentiation of chromoplasts and the associated signaling events do not depend on functional chloroplasts. However, although with some delay, chromoplast formation always accompanies fruit ripening.…”

“…Interestingly, the FtsH and EGY1 proteins decrease in abundance, mostly between the B and R stages, which correlates well with the dismantling of the thylakoid membranes, while SECA was present only at the MG stage, indicating an early end to the provision of material for thylakoid biogenesis. Recently the lutescent2 mutant of tomato has been identified as mutated for a homolog of EGY1 of Arabidopsis (Barry et al, 2012). The mutation is responsible for an altered chloroplast development and delay in fruit ripening but this not precluded chromoplast differentiation, indicating that chromoplast development does not depend on functional chromoplasts (Barry et al, 2012).…”

“…Recently the lutescent2 mutant of tomato has been identified as mutated for a homolog of EGY1 of Arabidopsis (Barry et al, 2012). The mutation is responsible for an altered chloroplast development and delay in fruit ripening but this not precluded chromoplast differentiation, indicating that chromoplast development does not depend on functional chromoplasts (Barry et al, 2012). A signal recognition particle subunit (SRP54, Solyc09g009940) involved in the integration of the light-harvesting chlorophyll a/b protein into the thylakoid membrane (Li et al, 1995;Rutschow et al, 2008) is present at the MG stage and then absent, giving another indication of the disappearance of photosynthetic protein import during the chloroplast-tochromoplast transition.…”

Comparative study of salt stress-induced physiological and molecular responses in tomato (Solanum lycopersicum L.)

“…It has been revealed that tomato L2 encodes an ortholog of Arabidopsis EGY1, which is a membrane-bound, chloroplast-targeted protease and a member of zincdependent M50 metalloprotease family, required for normal plastid development since it mediates chlorophyll accumulation (Chen et al, 2005). These evidences suggest that L2/EGY1 homologs may have a role in mediating chloroplast responses such as proteolysis of thylakoid membrane proteins during photosystem assembly or in response to environmental changes (Barry et al, 2012). Simirarly to role of Deg proteases, FtsH protease, an ATP-dependent zinc metalloprotease, play a role in light-induced turnover of D1 protein in thylakoid membranes maintaining PSII reaction centre integrity (Lindhal et al, 2000).…”