The Arabidopsis Protein CONSERVED ONLY IN THE GREEN LINEAGE160 Promotes the Assembly of the Membranous Part of the Chloroplast ATP Synthase

Abstract

The chloroplast F 1 F o -ATP synthase/ATPase (cpATPase) couples ATP synthesis to the light-driven electrochemical proton gradient. The cpATPase is a multiprotein complex and consists of a membrane-spanning protein channel (comprising subunit types a, b, b9, and c) and a peripheral domain (subunits a, b, g, d, and «). We report the characterization of the Arabidopsis (Arabidopsis thaliana) CONSERVED ONLY IN THE GREEN LINEAGE160 (AtCGL160) protein (AtCGL160), conserved in green algae and plants. AtCGL160 is an integral thylakoid protein, and its carboxyl-terminal portion is distantly related to prokaryotic ATP SYNTHASE PROTEIN1 (Atp1/UncI) proteins that are thought to function in ATP synthase assembly. Plants without AtCGL160 display an increase in xanthophyll cycle activity and energy-dependent nonphotochemical quenching. These photosynthetic perturbations can be attributed to a severe reduction in cpATPase levels that result in increased acidification of the thylakoid lumen. AtCGL160 is not an integral cpATPase component but is specifically required for the efficient incorporation of the c-subunit into the cpATPase. AtCGL160, as well as a chimeric protein containing the amino-terminal part of AtCGL160 and Synechocystis sp. PCC6803 Atp1, physically interact with the c-subunit. We conclude that AtCGL160 and Atp1 facilitate the assembly of the membranous part of the cpATPase in their hosts, but loss of their functions provokes a unique compensatory response in each organism.

BIOGENESIS FACTOR REQUIRED FOR ATP SYNTHASE 3 Facilitates Assembly of the Chloroplast ATP Synthase Complex

“…2). Similar photosynthetic properties were also observed in other mutants with low accumulation of chloroplast ATP synthase (Rott et al, 2011;Zoschke et al, 2012;Rühle et al, 2014;Fristedt et al, 2015;Mao et al, 2015). Therefore, the results of our immunoblot and spectroscopy analyses indicate that bfa3 is a typical mutant with a specific impairment in ATP synthase accumulation.…”

“…Such moderate changes in the transcript accumulation of chloroplast ATP synthase genes are usually detected in other typical ATP synthase mutants. The maize atp4 mutant and Arabidopsis atcgl160 mutant exhibited reduced levels of atpH/F transcripts, but these mutations are not directly involved in the expression of atpH/F (Zoschke et al, 2012;Rühle et al, 2014;Fristedt et al, 2015). The reduced atpH/F transcript levels in these mutants suggest that an unknown regulatory mechanism may function at the transcriptional level, which is stimulated by low levels of chloroplast ATP synthase.…”

“…It has been shown that Alb4 physically interacts with the CF 1 b and CF 0 II subunits and promotes the assembly of CF 1 during its attachment to CF 0 in the thylakoid membrane (Benz et al, 2009). Arabidopsis (Arabidopsis thaliana) CGL160, a homolog of prokaryotic Atp1/UncI proteins, is thought to facilitate c-ring formation via interaction with the CF 0 II and CF 0 III subunits (Rühle et al, 2014). By contrast, stromal protein PAB specifically interacts with the g-subunit and facilitates the assembly of the g-subunit into the a 3 b 3 hexamer (Mao et al, 2015).…”

“…To date, only three assembly factors, Alb4, PAB, and CGL160, were shown to be involved in the assembly of chloroplast ATP synthase (Benz et al, 2009;Rühle et al, 2014;Fristedt et al, 2015;Mao et al, 2015). Alb4 is a YidC/ Oxa1/Alb3 family protein.…”

Assembly of F1F0-ATP synthases

“…Monomeric c subunits are assembled into a c 14 -ring by CGL160, which is similar to its bacterial counterpart Atp1/UncI. A c-subunit-containing subcomplex, which does not comigrate with other chloroplast ATP synthase subunits in 2D gel electrophoresis, might represent a true c 14 oligomer intermediate in CF 0 assembly [120]. CF 1 -CF 0 -containing intermediates have not been characterized in vivo, but the integral thylakoid membrane protein ALB4 has been proposed to stabilize or promote the assembly of CF 1 during its attachment to the CF 0 portion.…”