Relationship of GUN1 to FUG1 in chloroplast protein homeostasis.

ABSTRACT

GUN1 integrates retrograde signals in chloroplasts but the underlying mechanism is elusive. FUG1, a chloroplast translation initiation factor, and GUN1 are co-expressed at the transcriptional level, and FUG1 co-immunoprecipitates with GUN1. We used mutants of GUN1 (gun1-103) and FUG1 (fug1-3) to analyse their functional relationship at the physiological and system-wide level, the latter including transcriptome and proteome analyses. Absence of GUN1 aggravates the effects of decreased FUG1 levels on chloroplast protein translation, resulting in transiently more pronounced phenotypes regarding photosynthesis, leaf colouration, growth and cold acclimation. The gun1-103 mutation also enhances variegation in the var2 mutant, increasing the fraction of white sectors, while fug1-3 suppresses the var2 phenotype. The transcriptomes of fug1-3 and gun1-103 plants are very similar, but absence of GUN1 alone has almost no effect on protein levels, whereas steady-state levels of chloroplast proteins are markedly decreased in fug1-3. In fug1 gun1 double mutants, effects on transcriptomes and particularly on proteomes are enhanced. Our results show that GUN1 function becomes critical when chloroplast proteostasis is perturbed by decreased rates of synthesis (fug1) or degradation (var2) of chloroplast proteins, or by low temperatures. The functions of FUG1 and GUN1 appear to be related, corroborating the view that GUN1 helps to maintain chloroplast protein homeostasis (proteostasis).