Biogenesis of thylakoid networks in angiosperms: knowns and unknowns

Abstract

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.

Regulatory factors for the assembly of thylakoid membrane protein complexes

“…By contrast, the thylakoids in cyanobacteria consist mainly of single layers formed by long lamellae, and extensive stacking of the grana lamellae is not observed [3]. Thus, thylakoid membrane systems evolved in cyanobacteria but became more complex in algae and plants [2], and the ultrastructure and composition differences of the thylakoids in cyanobacteria, algae and plants correspond well with their evolutionary positions [3].…”

“…The most advanced and efficient thylakoids are present in the chloroplasts of land plants, in which they are arranged into extensive, highly interconnected networks of grana stacks connected by stroma lamellae [2]. By contrast, the thylakoids in cyanobacteria consist mainly of single layers formed by long lamellae, and extensive stacking of the grana lamellae is not observed [3].…”

Three-Dimensional Visualization of the Tubular-Lamellar Transformation of the Internal Plastid Membrane Network during Runner Bean Chloroplast Biogenesis

“…In this case, the transfer system for the newly synthesized lipids and proteins into the forming thylakoids can be similar to that occurring during the direct development of a proplastid into a chloroplast (Rast et al, 2015). However, it is still not clear whether the degrading PLB transforms into thylakoids continuously or through the formation of vesicles (Rosinski and Rosen, 1972;Adam et al, 2011;Grzyb et al, 2013;Pribil et al, 2014).…”

“…It involves changes in gene expression together with the transcriptional and translational control of both nuclear and plastid genes. These genes can be regulated by anterograde and retrograde signals, the synthesis of necessary lipids and pigments, the import and routing of the nucleusencoded proteins into plastids, protein-lipid interactions, the insertion of proteins into the plastid membranes, and the assembly into functional complexes (Vothknecht and Westhoff, 2001;Baena-González and Aro, 2002;Kota et al, 2002;Stern et al, 2004;López-Juez, 2007;Waters and Langdale, 2009;Solymosi and Schoefs, 2010;Adam et al, 2011;Pogson and Albrecht, 2011;Ling et al, 2012;Jarvis and López-Juez, 2013;Lyska et al, 2013;Belcher et al, 2015;Börner et al, 2015;Dall'Osto et al, 2015;Ling and Jarvis, 2015;Rast et al, 2015;Sun and Zerges, 2015;Yang et al, 2015). Chloroplast biogenesis is highly integrated with cell and plant development, especially with photomorphogenesis (Pogson et al, 2015), and is controlled by cellular and organismal regulatory mechanisms such as the ubiquitin-proteasome system (Jarvis and López-Juez, 2013).…”

“…The longer wavelength forms are bound to PLBs, while this shorter wavelength form, unbound to LPOR, is mainly found in PTs. In addition to LPOR, PLBs contain enzymes of the chlorophyll and carotenoid biosynthesis pathways, enzymes of the Calvin cycle, and proteins involved in photosynthetic light reactions (subunits of ATP synthase, the oxygen-evolving complex, cytochrome b 6 f, plastocyanin, and ferrodoxin-NADPH oxidoreductase) and other proteins necessary during photomorphogenesis with the exception of the core subunits and the antenna complexes of the two photosystems (von Zychlinski et al, 2005;Kleffmann et al, 2007;Blomqvist et al, 2008;Adam et al, 2011).…”