Clade-Specific Plastid Inheritance Patterns Including Frequent Biparental Inheritance in Passiflora Interspecific Crosses

Plastid inheritance in angiosperms is presumed to be largely maternal, with the potential to inherit plastids biparentally estimated for about 20% of species. In Passiflora, maternal, paternal and biparental inheritance has been reported; however, these studies were limited in the number of crosses and progeny examined. To improve the understanding of plastid transmission in Passiflora, the progeny of 45 interspecific crosses were analyzed in the three subgenera: Passiflora, Decaloba and Astrophea. Plastid types were assessed following restriction digestion of PCR amplified plastid DNA in hybrid embryos, cotyledons and leaves at different developmental stages. Clade-specific patterns of inheritance were detected such that hybrid progeny from subgenera Passiflora and Astrophea predominantly inherited paternal plastids with occasional incidences of maternal inheritance, whereas subgenus Decaloba showed predominantly maternal and biparental inheritance. Biparental plastid inheritance was also detected in some hybrids from subgenus Passiflora. Heteroplasmy due to biparental inheritance was restricted to hybrid cotyledons and first leaves with a single parental plastid type detectable in mature plants. This indicates that in Passiflora, plastid retention at later stages of plant development may not reflect the plastid inheritance patterns in embryos. Passiflora exhibits diverse patterns of plastid inheritance, providing an excellent system to investigate underlying mechanisms in angiosperms.

Interspecific Hybrids Between Pelargonium × hortorum and Species From P. Section Ciconium Reveal Biparental Plastid Inheritance and Multi-Locus Cyto-Nuclear Incompatibility

The genetics underlying Cyto-Nuclear Incompatibility (CNI) was studied in Pelargonium interspecific hybrids. We created hybrids of 12 closely related crop wild relatives (CWR) with the ornamental P. × hortorum. Ten of the resulting 12 (F1) interspecific hybrids segregate for chlorosis suggesting biparental plastid inheritance. The segregation ratios of the interspecific F2 populations show nuclear interactions of one, two, or three nuclear genes regulating plastid function dependent on the parents. We further validated that biparental inheritance of plastids is common in section Ciconium, using diagnostic PCR primers. Our results pave the way for using the diverse species from section Ciconium, each with its own set of characteristics, as novel sources of desired breeding traits for P. × hortorum cultivars.

Intra-individual heteroplasmy in the Gentiana tongolensis plastid genome (Gentianaceae)

Chloroplasts are typically inherited from the female parent and are haploid in most angiosperms, but rare intra-individual heteroplasmy in plastid genomes has been reported in plants. Here, we report an example of plastome heteroplasmy and its characteristics in Gentiana tongolensis (Gentianaceae). The plastid genome of G. tongolensis is 145,757 bp in size and is missing parts of petD gene when compared with other Gentiana species. A total of 112 single nucleotide polymorphisms (SNPs) and 31 indels with frequencies of more than 2% were detected in the plastid genome, and most were located in protein coding regions. Most sites with SNP frequencies of more than 10% were located in six genes in the LSC region. After verification via cloning and Sanger sequencing at three loci, heteroplasmy was identified in different individuals. The cause of heteroplasmy at the nucleotide level in plastome of G. tongolensis is unclear from the present data, although biparental plastid inheritance and transfer of plastid DNA seem to be most likely. This study implies that botanists should reconsider the heredity and evolution of chloroplasts and be cautious with using chloroplasts as genetic markers, especially in Gentiana.

Interspecific plastome recombination reflects ancient reticulate evolution in Picea (Pinaceae)

Plastid sequences are a cornerstone in plant systematic studies and key aspects of their evolution, such as uniparental inheritance and absent recombination, are often treated as axioms. While exceptions to these assumptions can profoundly influence evolutionary inference, detecting them can require extensive sampling, abundant sequence data, and detailed testing. Using advancements in high-throughput sequencing, we analyzed the whole plastomes of 65 accessions of Picea, a genus of ~35 coniferous forest tree species, to test for deviations from canonical plastome evolution. Using complementary hypothesis and data-driven tests, we found evidence for chimeric plastomes generated by interspecific hybridization and recombination in the clade comprising Norway spruce (P. abies) and ten other species. Support for interspecific recombination remained after controlling for sequence saturation, positive selection, and potential alignment artifacts. These results reconcile previous conflicting plastid-based phylogenies and strengthen the mounting evidence of reticulate evolution in Picea. Given the relatively high frequency of hybridization and biparental plastid inheritance in plants, we suggest interspecific plastome recombination may be more widespread than currently appreciated and could underlie reported cases of discordant plastid phylogenies.