Abstract

Chloroplasts are unique organelles within the plant cells and are responsible for sustaining life forms on the earth due to their ability to conduct photosynthesis. Multiple functional genes within the chloroplast are responsible for a variety of metabolic processes that occur in the chloroplast. Considering its fundamental role in sustaining life on the earth, it is important to identify the level of diversity present in the chloroplast genome, what genes and genomic content have been lost, what genes have been transferred to the nuclear genome, duplication events, and the overall origin and evolution of the chloroplast genome. Our analysis of 2511 chloroplast genomes indicated that the genome size and number of coding DNA sequences (CDS) in the chloroplasts genome of algae are higher relative to other lineages. Approximately 10.31% of the examined species have lost the inverted repeats (IR) in the chloroplast genome that span across all the lineages. Genome-wide analyses revealed the loss of the Rbcl gene in parasitic and heterotrophic plants occurred approximately 56 Ma ago. PsaM, Psb30, ChlB, ChlL, ChlN, and Rpl21 were found to be characteristic signature genes of the chloroplast genome of algae, bryophytes, pteridophytes, and gymnosperms; however, none of these genes were found in the angiosperm or magnoliid lineage which appeared to have lost them approximately 203–156 Ma ago. A variety of chloroplast-encoded genes were lost across different species lineages throughout the evolutionary process. The Rpl20 gene, however, was found to be the most stable and intact gene in the chloroplast genome and was not lost in any of the analyzed species, suggesting that it is a signature gene of the plastome. Our evolutionary analysis indicated that chloroplast genomes evolved from multiple common ancestors ~1293 Ma ago and have undergone vivid recombination events across different taxonomic lineages.

Highlights

  • Photosynthesis is a process by which autotrophic plants utilize chlorophyll to transform solar energy into chemical energy [1]

  • Principal component analysis (PCA) of the chloroplast genome size of algae, bryophytes, eudicots, gymnosperms, magnoliids, monocots, Nymphaeales, protists, and pteridophytes reveals a clear distinction between the different plant groups (Figure 2)

  • The larger genome size (0.177 Mb) of the chloroplast genome in algae with deleted inverted repeats (IR) regions, and the higher number of coding sequences (CDS) (172.16 per genome) in IR-deleted taxa of algae indicates that the loss of IR regions in algae led to a genetic rearrangement and an enlargement in the chloroplast genome

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Summary

Introduction

Photosynthesis is a process by which autotrophic plants utilize chlorophyll to transform solar energy into chemical energy [1]. This essential process occurs inside a semiautonomous organelle, commonly known as a plastid or chloroplast [4]. A subsequent split into gymnosperms and angiosperms occurred approximately 290 to 320 million years ago and the divergence of monocots and eudicots within the angiosperm lineage occurred approximately 90 to 130 million years ago [6] Throughout this evolutionary time scale, the endosymbiont retained its existence inside the cell and its dominant function of photosynthesis without undergoing any basic evolutionary changes (photosynthesis) [7,8,9,10]. All of the protein synthesis and photosynthetic machinery used by the plastid is encoded by its own genome, commonly referred to as the plastome, that is arranged in a quadripartite structure [17,18,19,20]. The majority of genes in the chloroplast genome have been either functionally transferred to the nuclear genome or lost during evolution [31,32]

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