Characterization and Dynamics of Intracellular Gene Transfer in Plastid Genomes of Viola (Violaceae) and Order Malpighiales

Functional gene transfer from organelles to the nucleus, known as intracellular gene transfer (IGT), is an ongoing process in flowering plants. The complete plastid genomes (plastomes) of two Ulleung island endemic violets, Viola ulleungdoensis and V. woosanensis, were characterized, revealing a lack of the plastid-encoded infA, rpl32, and rps16 genes. In addition, functional replacement of the three plastid-encoded genes in the nucleus was confirmed within the genus Viola and the order Malpighiales. Three strategies for the acquisition of a novel transit peptide for successful IGT were identified in the genus Viola. Nuclear INFA acquired a novel transit peptide with very low identity between these proteins, whereas the nuclear RPL32 gene acquired an existing transit peptide via fusion with the nuclear-encoded plastid-targeted SOD gene (Cu-Zn superoxide dismutase superfamily) as one exon, and translated both proteins in the cytosol using alternative mRNA splicing. Nuclear RPS16 contains an internal transit peptide without an N-terminal extension. Gene loss or pseudogenization of the plastid-borne rpl32 and rps16 loci was inferred to occur in the common ancestor of the genus Viola based on an infrageneric phylogenetic framework in Korea. Although infA was lost in the common ancestor of the order Malpighiales, the rpl32 and rps16 genes were lost multiple times independently within the order. Our current study sheds additional light on plastid genome composition and IGT mechanisms in the violet genus and in the order Malpighiales.

Complete Plastid and Mitochondrial Genomes of Aeginetia indica Reveal Intracellular Gene Transfer (IGT), Horizontal Gene Transfer (HGT), and Cytoplasmic Male Sterility (CMS)

Orobanchaceae have become a model group for studies on the evolution of parasitic flowering plants, and Aeginetia indica, a holoparasitic plant, is a member of this family. In this study, we assembled the complete chloroplast and mitochondrial genomes of A. indica. The chloroplast and mitochondrial genomes were 56,381 bp and 401,628 bp long, respectively. The chloroplast genome of A. indica shows massive plastid genes and the loss of one IR (inverted repeat). A comparison of the A. indica chloroplast genome sequence with that of a previous study demonstrated that the two chloroplast genomes encode a similar number of proteins (except atpH) but differ greatly in length. The A. indica mitochondrial genome has 53 genes, including 35 protein-coding genes (34 native mitochondrial genes and one chloroplast gene), 15 tRNA (11 native mitochondrial genes and four chloroplast genes) genes, and three rRNA genes. Evidence for intracellular gene transfer (IGT) and horizontal gene transfer (HGT) was obtained for plastid and mitochondrial genomes. ψndhB and ψcemA in the A. indica mitogenome were transferred from the plastid genome of A. indica. The atpH gene in the plastid of A. indica was transferred from another plastid angiosperm plastid and the atpI gene in mitogenome A. indica was transferred from a host plant like Miscanthus siensis. Cox2 (orf43) encodes proteins containing a membrane domain, making ORF (Open Reading Frame) the most likely candidate gene for CMS development in A. indica.