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 chlorophyll-containing light-harvesting complex antennae by playing a protective role within the chloroplast.