Plastid genome evolution and inheritance in Passiflora

Plastid genomes (plastomes) of photosynthetic angiosperms are for the most part highly conserved in their organization, mode of inheritance and rates of nucleotide substitution. A small number of distantly related lineages including Passiflora share a syndrome of features that deviate from this general pattern, including extensive genomic rearrangements, accelerated rates of nucleotide substitution, biparental inheritance and plastome-genome incompatibility. Plastome evolution studies in Passiflora are limited in taxon sampling; hence the phylogenetic extent of the rearrangements is unknown. To gain better understanding in plastome evolution in Passiflora, plastomes from 31 taxa and transcriptomes from 6 species were sequenced and assembled. In addition, interspecific crosses within two largest subgenera, Passiflora and Decaloba, were greatly expanded to understand mode of plastid inheritance in the genus. Phylogenomic analyses with 68 protein-coding genes generated a fully resolved, strongly supported tree that is congruent with the comprehensive phylogenies based on a few plastid and nuclear loci. Extensive rearrangements were detected including several gene/intron losses, inverted repeat expansion/contraction and inversions, some of which occurred in parallel. Nucleotide substitution rate analyses of 68 protein-coding genes across the genus showed lineage- and locus-specific acceleration. Comparative transcriptome analyses identified missing or divergent plastid genes in Passiflora that have followed three distinct evolutionary paths: transfer to the nucleus, substitution by the nuclear genes and highly divergent gene that likely remain functional. Plastid-encoded rps7 was transferred into the intron of a nuclear-encoded plastid-targeted thioredoxin m-type gene, acquiring its plastid transit peptide. Plastid rpl20 likely experienced a novel substitution by a duplicated, nuclear-encoded mitochondrial-targeted rpl20 that has a similar gene structure. Interspecific hybrids in Passiflora exhibit diverse modes of plastid inheritance including a clade-specific paternal or maternal pattern along with frequent transmission of biparental plastids. Furthermore, heteroplasmy due to biparental inheritance was restricted to early developmental stage in hybrids and plastid types from either parent were excluded in older plants resulting plastid homogeneity. These results of unusual plastome dynamics and inheritance identified in Passiflora presents the genus as an exciting system to study plastome evolution in angiosperms