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Starch Granule Initiation in Arabidopsis Thaliana Chloroplasts

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Starch Granule Initiation in Arabidopsis Thaliana Chloroplasts The Plant Journal (2021) doi: 10.1111/tpj.15359 FOCUSED REVIEW Starch granule initiation in Arabidopsis thaliana chloroplasts Angel Merida 1 and Joerg Fettke2,* 1Institute of Plant Biochemistry and Photosynthesis (IBVF), Consejo Superior de Investigaciones Cientıficas (CSIC), Universidad de Sevilla (US), Avda Americo Vespucio, 49, Sevilla 41092, Spain, and 2Biopolymer Analytics, Institute of Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Str. 24-25, Building 20, Potsdam-Golm 14476, Germany Received 1 April 2021; revised 14 May 2021; accepted 22 May 2021. *For correspondence (e-mail [email protected]). SUMMARY The initiation of starch granule formation and the mechanism controlling the number of granules per plastid have been some of the most elusive aspects of starch metabolism. This review covers the advances made in the study of these processes. The analyses presented herein depict a scenario in which starch synthase isoform 4 (SS4) provides the elongating activity necessary for the initiation of starch granule formation. However, this protein does not act alone; other polypeptides are required for the initiation of an appropriate number of starch granules per chloroplast. The functions of this group of polypeptides include providing suitable substrates (mal- tooligosaccharides) to SS4, the localization of the starch initiation machinery to the thylakoid membranes, and facilitating the correct folding of SS4. The number of starch granules per chloroplast is tightly regulated and depends on the developmental stage of the leaves and their metabolic status. Plastidial phosphorylase (PHS1) and other enzymes play an essential role in this process since they are necessary for the synthesis of the sub- strates used by the initiation machinery. The mechanism of starch granule formation initiation in Arabidopsis seems to be generalizable to other plants and also to the synthesis of long-term storage starch. The latter, how- ever, shows specific features due to the presence of more isoforms, the absence of constantly recurring starch synthesis and degradation, and the metabolic characteristics of the storage sink organs. Keywords: starch granules, starch metabolism, starch granule initiation, starch granule number per chloro- plast, starch morphology, Arabidopsis thaliana. INITIATION OF THE STARCH GRANULE In plants, starch appears in the form of granules in the plas- After cellulose, starch is the most abundant polymer in the tids (mainly in chloroplasts of photosynthetic tissues or amy- biosphere. It plays an essential role in those organisms that loplasts of storage organs such as tubers, endosperm, or accumulate it (photosynthetic eukaryotes and some roots) (Ball and Morell, 2003). The size, number, and morphol- cyanobacteria) (Cenci et al., 2014). Starch is water-insoluble, ogy of these granules vary greatly depending on the species in contrast to glycogen, which is the storage carbohydrate of and even the organ analyzed (Tetlow and Bertoft, 2020). nearly all other organisms. Starch granules are composed of two different polymers: The harvested parts of our staple crop plants are starch- amylose and amylopectin. In both of these glucans, thou- storing organs. Starch is one of the main contributors to the sands of glucosyl residues possessing the a-configuration are human diet in terms of calories, and it is often used as animal linked together. In starch (and in glycogen as well), there are feed. Furthermore, there is also an increasing demand from essentially only two types of glycosidic linkages that intercon- non-food industries for starch as a renewable material (Zee- nect these glucosyl residues: linear chains of a-1,4-linked resi- man et al., 2010). The synthesis and degradation of starch has dues and a-1,6-linked branches. Amylopectin is the main therefore been the subject of much research efforts, all with component of starch, and has a large number of branches the final aim of obtaining more productive crops or modified ordered in clusters that confer a semi-crystalline structure to starches for industrial applications (Zeeman et al., 2010). the granule. In contrast, amylose, the minor component, has a © 2021 The Authors. 1 The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. 2 Angel Merida and Joerg Fettke small number of branches and no known structure (Tetlow et al., 2007). The amylopectin chain-length profiles, reflect- and Bertoft, 2020). The enzymatic activities involved in the for- ing alterations to the inner granule structure, of ss4 mation of starch are relatively simple: ADP-glucose pyrophos- mutants are similar to those of the WT. No changes in the phorylase (AGPase, EC 2.7.7.27) provides ADP-glucose, which activity of the main enzymes involved in the synthesis or is one substrate used by starch synthases (SSs, ADP-Glc:a- degradation of starch were observed, except for an 1,4-glucan a-4-glucosyl transferases, EC 2.4.1.21) to elongate increase in the cytosolic and plastidial phosphorylase activ- the glucan polymer chains. Starch-branching enzyme (SBE, a- ities (see below). It was proposed that SS4 is involved in 1,4-glucan branching enzyme, EC 2.4.1.18) establishes the the priming of starch granule formation (Roldan et al., branches, and starch-debranching enzyme (DBE or isoamy- 2007). lase, EC 3.2.1.68) eliminates excess branches, allowing the SS4 is a GT-B-fold glycosyltransferase classified within crystallization of clusters (Ball et al., 1996; Brust et al., 2013). the GT5 family in the Carbohydrate Active Enzyme (CAZy) This scenario becomes more complex as a consequence of database (Lombard et al., 2013). It has starch catalytic the presence of different isoenzymes for each activity and the (GT5) and glycosyltransferase 1 (GT1) domains in its C- discovery of new proteins involved in the synthesis of the terminal region. These domains are highly conserved granule. These isoenzymes show different substrate affinities, among the SS4 homologs of different species and among and they form different complexes with other enzymes the different isoforms of SSs (Leterrier et al., 2008; Liu involved in starch synthesis and degradation, modulating et al., 2015). In addition, SS4 has a long N-terminal region their activities (Ahmed et al., 2015; Ball et al., 2011; Kotting€ with some features exclusive to this isoform. This region is et al., 2010; Mehrpouyan et al., 2021). Moreover, for some less phylogenetically conserved, although all SS4 analyzed enzymes, for example, plastidial phosphorylase (PHS1, EC have long coiled-coil domains. A domain of approximately 2.4.4.1), their participation in starch synthesis, degradation, or 50 amino acids, highly conserved among all the SS4 both is still a matter of discussion. enzymes analyzed to date, separates the coiled-coil and Overall, the concerted action of all these polypeptides is glycosyltransferase regions (Raynaud et al., 2016). SS4 is necessary to form the starch granule. The initiation of not found soluble throughout the stroma. On the contrary, starch synthesis remains obscure, in contrast to that of localization experiments involving translational fusion with glycogen. For the latter, its synthesis initiation is known to green fluorescence protein (GFP) have indicated SS4 to be depend on a self-glycosylating protein – glycogenin (EC associated with specific areas of the thylakoid membranes 2.4.1.186; Lomako et al., 1988) – that generates short a- known as plastoglobules (Gamez-Arjona et al., 2014). The glucan chains, which are further elongated to form the N-terminal part of the protein is responsible for its localiza- entire glycogen molecule. No functional glycogenin or tion pattern (Raynaud et al., 2016), and the interaction of equivalent has been reported for higher plants. this region with the plastoglobule-associated proteins fib- However, together with advances in the understanding of rillins 1a and 1b has been shown, although the elimination the different steps necessary for the synthesis and degrada- of these fibrillins does not alter the initiation of starch tion of the starch polymers, relevant progress has been made granule formation (Gamez-Arjona et al., 2014). Using trans- in the research on how starch granule formation is initiated. lational fusions of the N-terminal part of SS4 with Agrobac- Most of the available data refer to transitory starch, and this terium glycogen synthase (GS), Lu et al. (2018) showed that focuses on that of the Arabidopsis thaliana leaf starch. There- this region is also somehow involved in altering the shape of fore, the present review will focus on this example. starch granules, which may establish a link between the localization of SS4 and the shape of granules. THE CENTRAL ROLE OF SS4-DEPENDENT INITIATION OF SS4 has an active catalytic site and shows SS activity STARCH GRANULE FORMATION IN ARABIDOPSIS using amylopectin, glycogen, or some maltooligosaccha- CHLOROPLASTS rides (MOS) as substrates when the polypeptide is The chloroplasts of Arabidopsis Columbia-0 usually contain expressed in E. coli (Brust et al., 2013; Szydlowski et al., four to seven starch granules of lenticular shape, although 2009). The active form of SS4 seems to be a homodimer, the granule number per chloroplast varies slightly between and the conserved region localized between the coiled-coil different accessions (Crumpton-Taylor et al., 2012; Malinova and glycosyltransferase regions is necessary for its forma- et al., 2014). In the wild type (WT), the number seems to be tion (Raynaud et al., 2016). correlated to chloroplast volume (Crumpton-Taylor et al., SS4 was the first element described to be involved in 2012). This restricted number seems to be linked to the coor- the initiation of starch granule formation, but this complex dinated initiation of starch granule synthesis and therefore process requires the participation of other players.
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