Biogenesis of thylakoid networks in angiosperms: Knowns and unknowns

The Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture, Hebrew University of Jerusalem, 76100 Rehovot, Israel.
Plant Molecular Biology (Impact Factor: 4.26). 07/2011; 76(3-5):221-34. DOI: 10.1007/s11103-010-9693-5
Source: PubMed


Aerobic life on Earth depends on oxygenic photosynthesis. This fundamentally important process is carried out within an elaborate membranous system, called the thylakoid network. In angiosperms, thylakoid networks are constructed almost from scratch by an intricate, light-dependent process in which lipids, proteins, and small organic molecules are assembled into morphologically and functionally differentiated, three-dimensional lamellar structures. In this review, we summarize the major events that occur during this complex, largely elusive process, concentrating on those that are directly involved in network formation and potentiation and highlighting gaps in our knowledge, which, as hinted by the title, are substantial.

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    • "The phenotypes of these mutants were characterized by abnormal plastid biogenesis and, in most cases, early seedling lethality. The formation of bilayer structures in the thylakoid membrane is an energetically demanding process that depends on the presence of LHC or other membrane proteins, which must be delivered to and combined with the lipid phase [61]. Thus, they likely lack some membrane proteins (e.g., PSII proteins), which may lead to failed thylakoid membrane biogenesis. "
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    ABSTRACT: Chloroplast formation is associated with embryo development and seedling growth. However, the relationship between chloroplast differentiation and embryo development remains unclear. Five FtsHi genes that encode proteins with high similarity to FtsH proteins, but lack Zn2+-binding motifs, are present in the Arabidopsis genome. In this study, we showed that T-DNA insertion mutations in the Arabidopsis FtsHi4 gene resulted in embryo arrest at the globular-to-heart-shaped transition stage. Transmission electron microscopic analyses revealed abnormal plastid differentiation with a severe defect in thylakoid formation in the mutant embryos. Immunocytological studies demonstrated that FtsHi4 localized in chloroplasts as a thylakoid membrane-associated protein, supporting its essential role in thylakoid membrane formation. We further showed that FtsHi4 forms protein complexes, and that there was a significant reduction in the accumulation of D2 and PsbO (two photosystem II proteins) in mutant ovules. The role of FtsHi4 in chloroplast development was confirmed using an RNA-interfering approach. Additionally, mutations in other FtsHi genes including FtsHi1, FtsHi2, and FtsHi5 caused phenotypic abnormalities similar to ftshi4 with respect to plastid differentiation during embryogenesis. Taken together, our data suggest that FtsHi4, together with FtsHi1, FtsHi2, and FtsHi5 are essential for chloroplast development in Arabidopsis.
    Full-text · Article · Jun 2014 · PLoS ONE
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    • "While detailed information exists on signals initiating acclimation responses (recently reviewed by: Pogson et al., 2008; Kleine et al., 2009; Foyer et al., 2012; Pfannschmidt and Yang, 2012), much less is known about limiting steps, which ultimately determine complex accumulation in higher plants. Indications exist for regulation of photosynthetic complex biogenesis on the transcriptional level, on the level of mRNA maturation (especially in case of the chloroplast-encoded subunits), of mRNA translation, and on the level of complex assembly, which requires multiple auxiliary proteins (recently reviewed by: Adam et al., 2011; Schöttler et al., 2011; Lyska et al., 2013; Nickelsen and Rengstl, 2013). Complex stability and degradation may be highly regulated as well. "
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    Full-text · Article · May 2014 · Frontiers in Plant Science
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    • "The dynamin family member FZL is also localized at the envelope and thylakoids, and shows GTPase activity, but in FZL knock-out plants disruption of thylakoid ultrastructure is less severe (Gao et al., 2006) than in cpSar1 knock-outs. Although grana stacks are disorganized and vesicles accumulate , FZL is believed to play a more prominent role later in thylakoid development (Gao et al., 2006; Adam et al., 2011). The THF1 (THylakoid Formation1) protein is also assumed to be involved in vesicular trafficking because in thf1 mutants white/yellow patches appear that completely lack grana stacks or any form of thylakoid membrane but accumulate membrane vesicles (Wang et al., 2004). "
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    ABSTRACT: Thylakoids of land plants have a bipartite structure, consisting of cylindrical grana stacks, made of membranous discs piled one on top of the other, and stroma lamellae which are helically wound around the cylinders. Protein complexes predominantly located in the stroma lamellae and grana end membranes are either bulky [photosystem I (PSI) and the chloroplast ATP synthase (cpATPase)] or are involved in cyclic electron flow [the NAD(P)H dehydrogenase (NDH) and PGRL1-PGR5 heterodimers], whereas photosystem II (PSII) and its light-harvesting complex (LHCII) are found in the appressed membranes of the granum. Stacking of grana is thought to be due to adhesion between Lhcb proteins (LHCII or CP26) located in opposed thylakoid membranes. The grana margins contain oligomers of CURT1 proteins, which appear to control the size and number of grana discs in a dosage- and phosphorylation-dependent manner. Depending on light conditions, thylakoid membranes undergo dynamic structural changes that involve alterations in granum diameter and height, vertical unstacking of grana, and swelling of the thylakoid lumen. This plasticity is realized predominantly by reorganization of the supramolecular structure of protein complexes within grana stacks and by changes in multiprotein complex composition between appressed and non-appressed membrane domains. Reversible phosphorylation of LHC proteins (LHCPs) and PSII components appears to initiate most of the underlying regulatory mechanisms. An update on the roles of lipids, proteins, and protein complexes, as well as possible trafficking mechanisms, during thylakoid biogenesis and the de-etiolation process complements this review.
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