Evolutionary relationship between organellar DNA inheritance patterns and traits of seed plants

In plants, organellar DNA is predominantly maternally inherited, but biparental and paternal inheritance have also been observed. Specific mechanisms, such as plastid exclusion during pollen mitosis or genome degradation, ensure maternal inheritance. Certain factors, including low temperatures, disrupt cytoskeletal functions, thereby increasing paternal plastid transmission. Despite these findings, the ecological and evolutionary drivers of these inheritance modes remain unclear. We explored the traits associated with biparental and paternal inheritance to reveal the contributing ecological factors.

Plastid inheritance data were compiled for 378 species (302 genera and 112 families) and 12 functional traits obtained from the TRY database were analyzed. Missing values were filled according to Bayesian hierarchical modeling. On the basis of phylogenetic logistic regression, we investigated the relationships between inheritance patterns and plant traits, accounting for evolutionary history.

Our models identified plant height, leaf area, and stem conduit density as traits associated with inheritance modes, with the strongest support for leaf area and limited support for the other traits. Coefficient directions indicated greater plant height, smaller leaves, and higher stem conduit density in species with non-maternal inheritance. Excluding gymnosperms yielded similar tendencies, which suggests that similar ecological factors may be associated with plastid inheritance patterns in both groups.

Functional traits were associated with organelle inheritance patterns, with ecological and evolutionary implications. Similar ecological factors may be associated with the independent occurrence of paternal inheritance across lineages. Future work integrating molecular and ecological data will help elucidate the mechanisms underlying organelle inheritance and their adaptive significance.