Early Gene Duplication Within Chloroplastida and Its Correspondence With Relocation of Starch Metabolism to Chloroplasts

Abstract

The endosymbiosis event resulting in the plastid of photosynthetic eukaryotes was accompanied by the appearance of a novel form of storage polysaccharide in Rhodophyceae, Glaucophyta, and Chloroplastida. Previous analyses indicated that starch synthesis resulted from the merging of the cyanobacterial and the eukaryotic storage polysaccharide metabolism pathways. We performed a comparative bioinformatic analysis of six algal genome sequences to investigate this merger. Specifically, we analyzed two Chlorophyceae, Chlamydomonas reinhardtii and Volvox carterii, and four Prasinophytae, two Ostreococcus strains and two Micromonas pusilla strains. Our analyses revealed a complex metabolic pathway whose intricacies and function seem conserved throughout the green lineage. Comparison of this pathway to that recently proposed for the Rhodophyceae suggests that the complexity that we observed is unique to the green lineage and was generated when the latter diverged from the red algae. This finding corresponds well with the plastidial location of starch metabolism in Chloroplastidae. In contrast, Rhodophyceae and Glaucophyta produce and store starch in the cytoplasm and have a lower complexity pathway. Cytoplasmic starch synthesis is currently hypothesized to represent the ancestral state of storage polysaccharide metabolism in Archaeplastida. The retargeting of components of the cytoplasmic pathway to plastids likely required a complex stepwise process involving several rounds of gene duplications. We propose that this relocation of glucan synthesis to the plastid facilitated evolution of chlorophyllcontaining light-harvesting complex antennae by playing a protective role within the chloroplast. BOTH glycogen and starch are made of glucose chains (glucans) linked at the a-1,4 position and branched at a-1,6. While glycogen is a homogeneous hydrosoluble polymer with uniformly distributed branches, starch is known to be composed of two types of polysaccharides: a minor amylose fraction with very few branches (,1% a-1,6 linkages) and a major moderately branched (5% a-1,6 linkages) amylopectin fraction. Unlike glycogen, amylopectin displays an asymmetric distribution of branches, which regularly alternates poorly branched with highly branched regions. This generates clusters of chains and forms the backbone of the insoluble and semicrystalline starch granule (for a review of starch structure, see Buléon et al. 1997).Glycogen is by far the most widespread form of storage polysaccharide. It is found in archaea, bacteria, and many heterotrophic eukaryotes. Interestingly, the distribution of starch metabolism within the tree of life is restricted to Archaeplastida and some eukaryotic lineages derived from the Archaeplastida by secondary endosymbiosis (alveolates, cryptophytes). Archaeplastida themselves can be traced back to a single endosymbiotic event involving an ancestor of present-day cyanobacteria and a heterotrophic eukaryotic host (Rodríguez-Ezpelata et al. 2005). This event introduced the organelle now known as th...

A Putative Phosphatase, LSF1, Is Required for Normal Starch Turnover in Arabidopsis Leaves

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Functional Interactions between Starch Synthase III and Isoamylase-Type Starch-Debranching Enzyme in Maize Endosperm

“…Starch biosynthetic enzymes in chloroplast-containing organisms include five conserved classes of starch synthase (SS), which elongate linear glucans at the nonreducing end using ADP-Glc as the monosaccharide donor, and two or three starch branching enzymes (SBEs), which generate branch linkages by cleaving an a(1/4) bond and transferring the released linear segment to a 6-hydroxyl group elsewhere in the molecule Deschamps et al, 2008). Four a (1/6)-glucosidases, referred to as starch debranching enzymes (DBEs), are also conserved in the green algae and land plants.…”

Plant Biotechnology for the Development of Design Starches

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