Comparative Chloroplast Genomics of C3, Kranz type C4 and Single Cell C4 photosynthetic members of Chenopodiaceae

Abstract

Background Chloroplast genome information is critical to understanding taxonomic relationships in the plant kingdom. During the evolutionary process, plants have developed different photosynthetic strategies that are accompanied by complementary biochemical and anatomical features. Members of family Chenopodiaceae have species with C3 photosynthesis and variations of C4 photosynthesis in which photorespiration is reduced by concentrating CO2 around Rubisco through dual coordinated functioning of dimorphic chloroplasts. Among dicots, the family has a large number of C4 species, and greatest structural and biochemical diversity in forms of C4 including the canonical dual-cell Kranz anatomy, and the recently identified single-cell C4 with the presence of dimorphic chloroplasts separated by a vacuole. This is the first comparative analysis of chloroplast genomes in species representative of photosynthetic types in the family. Results High quality and complete chloroplast genomes of eight species representing C3, Kranz type C4, and single-cell C4 (SSC4) photosynthesis were obtained using high throughput sequencing complemented with Sanger sequencing of selected loci. Six of the eight chloroplast genome sequences are new, while two represent corrected versions of previously published chloroplast genomes. Comparative genomic analysis with previously sequenced plastid genomes revealed a similar genome organization, gene order, and content with a few revisions. High-quality complete chloroplast genome sequences resulted in correcting the orientation of the LSC region of the published Bienertia sinuspersici chloroplast genome, identification of stop codons in the rpl23 gene in B. sinuspersici and B. cycloptera, and identifying an instance of IR expansion in the Haloxylon ammodendron inverted repeat sequence. The rare observation of a mitochondria-to-chloroplast inter-organellar gene transfer event was identified in family Chenopodiaceae. Conclusions This study reports complete chloroplast genomes from seven Chenopodiaceae and one Amaranthaceae species. The depth of coverage obtained using high-throughput sequencing complemented with targeted resequencing of certain loci enabled superior resolution of the border junctions, directionality, and repeat region sequences. Therefore, the use of high throughput and Sanger sequencing, in a hybrid method, reaffirms to be rapid, efficient, and reliable for chloroplast genome sequencing.