Chloroplast Chaperonin: An Intricate Protein Folding Machine for Photosynthesis

Abstract

Group I chaperonins are large cylindrical-shaped nano-machines that function as a central hub in the protein quality control system in the bacterial cytosol, mitochondria and chloroplasts. In chloroplasts, proteins newly synthesized by chloroplast ribosomes, unfolded by diverse stresses, or translocated from the cytosol run the risk of aberrant folding and aggregation. The chloroplast chaperonin system assists these proteins in folding into their native states. A widely known protein folded by chloroplast chaperonin is the large subunit of ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco), an enzyme responsible for the fixation of inorganic CO2 into organic carbohydrates during photosynthesis. Chloroplast chaperonin was initially identified as a Rubisco-binding protein. All photosynthetic eucaryotes genomes encode multiple chaperonin genes which can be divided into α and β subtypes. Unlike the homo-oligomeric chaperonins from bacteria and mitochondria, chloroplast chaperonins are more complex and exists as intricate hetero-oligomers containing both subtypes. The Group I chaperonin requires proper interaction with a detachable lid-like co-chaperonin in the presence of ATP and Mg2+ for substrate encapsulation and conformational transition. Besides the typical Cpn10-like co-chaperonin, a unique co-chaperonin consisting of two tandem Cpn10-like domains joined head-to-tail exists in chloroplasts. Since chloroplasts were proposed as sensors to various environmental stresses, this diversified chloroplast chaperonin system has the potential to adapt to complex conditions by accommodating specific substrates or through regulation at both the transcriptional and post-translational levels. In this review, we discuss recent progress on the unique structure and function of the chloroplast chaperonin system based on model organisms Chlamydomonas reinhardtii and Arabidopsis thaliana. Knowledge of the chloroplast chaperonin system may ultimately lead to successful reconstitution of eukaryotic Rubisco in vitro.

Hetero‐oligomeric CPN60 resembles highly symmetric group‐I chaperonin structure revealed by Cryo‐EM

“…The chloroplast chaperonin was first recognized as a protein that transiently binds Rubisco large subunits before they assemble into the holoenzyme (Barraclough and Ellis, 1980;Hemmingsen and Ellis, 1986;Ellis et al, 1989). Two features set the chloroplast chaperonin apart from the prototypical E. coli GroEL/ES system: (i) its unique ability to assist in the folding and assembly of the Rubisco holoenzyme; and (ii) the hetero-oligomeric nature of chloroplast chaperonin and co-chaperonins, consisting of Cpn60a and Cpn60b subunits and co-chaperonin Cpn10 and Cpn20 subunits, respectively (Roy, 1989;Vitlin Gruber et al, 2013;Aigner et al, 2017;Zhao and Liu, 2017). We could obviously show that the recombinant chloroplast co-chaperonin subunits CPN11, CPN20 and CPN23 from Chlamydomonas form various hetero-oligomeric complexes when mixed in vitro (Tsai et al, 2012).…”

“…Unlike the homo-oligomeric chaperonin systems from bacteria (GroES/GroEL) and mitochondria (Hsp10/Hsp60), the chloroplast chaperonin system is much more complicated, as all genomes of photosynthetic eukaryotes encode multiple copies of chloroplast chaperonin and co-chaperonin genes (Hill and Hemmingsen, 2001;Weiss et al, 2009;Vitlin Gruber et al, 2013;Trosch et al, 2015;Zhao and Liu, 2017). Chloroplast chaperonins harbor two subunit subtypes, termed Cpn60a and Cpn60b, which share about 50% sequence identity.…”

Hetero-oligomeric CPN60 resembles highly symmetric group I chaperonin structure revealed by Cryo-EM

“…Unlike the homo-oligomeric chaperonin systems from bacteria (GroES/GroEL) and mitochondria (Hsp10/Hsp60), the chloroplast chaperonin system is much more complicated, as all genomes of photosynthetic eukaryotes encode multiple copies of chloroplast chaperonin and co-chaperonin genes (Hill and Hemmingsen, 2001;Trosch et al, 2015;Vitlin Gruber et al, 2013;Weiss et al, 2009;Zhao and Liu, 2017). Chloroplast chaperonins harbor two subunit subtypes, termed Cpn60α and Cpn60β, which share about 50% sequence identity.…”

“…The chloroplast chaperonin was first recognized as a protein that transiently binds Rubisco large subunits before they assemble into the holoenzyme (Barraclough and Ellis, 1980;Ellis et al, 1989;Hemmingsen and Ellis, 1986). Two features set the chloroplast chaperonin apart from the prototypical GroEL/ES system in Escherichia coli: (1) its irreplaceable ability to assist in the folding and assembly of the Rubisco holoenzyme; (2) the hetero-oligomeric nature of chloroplast chaperonin and co-chaperonins, consisting of Cpn60α-and Cpn60β-subunits and co-chaperonin Cpn10 and Cpn20-subunits, respectively (Aigner et al, 2017;Roy, 1989;Vitlin Gruber et al, 2013;Zhao and Liu, 2017). In a previous study the recombinant chloroplast co-chaperonin subunits CPN11, CPN20 and CPN23 from Chlamydomonas form various hetero-oligomeric complexes when mixed in vitro (Tsai et al, 2012).…”

Proteomic studies of honeybee- and manually-collected pollen

“…The Food Standards Agency's final report provides data on the concentration of arsenic in fruit and vegetables. Arsenic was in low concentration In plants, the chloroplast CPN60 was initially identified as a protein which is very important for folding of Rubisco assembly, the key enzyme responsible for respiration (Zhao, Liu, 2018). It was found data in literature that silencing CPN21 in grape seed led to grape seed abortion (Hanania et al, 2007).…”