Chloroplast evolution, structure and functions

Abstract

In this review, we consider a selection of recent advances in chloroplast biology. These include new findings concerning chloroplast evolution, such as the identification of Chlamydiae as a third partner in primary endosymbiosis, a second instance of primary endosymbiosis represented by the chromatophores found in amoebae of the genus Paulinella, and a new explanation for the longevity of captured chloroplasts (kleptoplasts) in sacoglossan sea slugs. The controversy surrounding the three-dimensional structure of grana, its recent resolution by tomographic analyses, and the role of the CURVATURE THYLAKOID1 (CURT1) proteins in supporting grana formation are also discussed. We also present an updated inventory of photosynthetic proteins and the factors involved in the assembly of thylakoid multiprotein complexes, and evaluate findings that reveal that cyclic electron flow involves NADPH dehydrogenase (NDH)- and PGRL1/PGR5-dependent pathways, both of which receive electrons from ferredoxin. Other topics covered in this review include new protein components of nucleoids, an updated inventory of the chloroplast proteome, new enzymes in chlorophyll biosynthesis and new candidate messengers in retrograde signaling. Finally, we discuss the first successful synthetic biology approaches that resulted in chloroplasts in which electrons from the photosynthetic light reactions are fed to enzymes derived from secondary metabolism.

Figure 1.. The helical model of thylakoid architecture

A fretwork of stroma lamellae, which wind around the ascending grana stacks as a right-handed helix connects to individual grana discs via narrow membrane protrusions (indicated by dotted circles in the side view). Adapted with permission [31] 2014. Journal of Experimental Botany doi:10.1093/jxb/eru090.

Figure 2.. Model for the different roles of PGRL1 in cyclic electron flow in vascular plants and green algae

In the vascular plant Arabidopsis, cyclic electron flow (CEF) around photosystem I (PSI) operates via two partially redundant pathways, an NDH-dependent and the PGRL1/PGR5-dependent pathway. Only the latter is inhibited by AA. Note that both the PGRL1/PGR5 and the NDH complex (via Lhca5 and 6) can physically interact with PSI in Arabidopsis and accept electrons only from ferredoxin (Fd) [43,71]. In the green alga Chlamydomonas, CEF can be mediated by a PSI-Cyt b₆f-PGRL1-ANR1-CAS supercomplex [70,150]. FNR, ferredoxin NADP⁺ oxidoreductase; Pc, plastocyanin; PQ, plastoquinone; C, D and E, stromal subunits of PSI. Adapted with permission 2013 Journal of Experimental Botany doi:10.1093/jxb/eru090.

Figure 3.. Schematic representation of a light-driven metabolon introduced into the thylakoids

Photosystem I (PSI) receives electrons from photosystem II via plastocyanin (PC) and directs them to ferredoxin (Fd), which give them either to the ferredoxin NADP⁺ oxidoreductase (FNR) for NADPH production or directly to the two P450 enzymes (P450s). The two membrane-bound P450s hydroxylate the substrate in two consecutive steps, and this is followed by glycosylation by a soluble glucosyltransferase (GT) to form the final stable product. The novel aspect of this approach is that photosynthetic reducing power, in the form of reduced ferredoxin, is used directly by a novel biosynthetic pathway to produce the product without the need for numerous energy consuming metabolic conversions.