Large-Scale Comparative Analysis Reveals the Mechanisms Driving Plastomic Compaction, Reduction, and Inversions in Conifers II (Cupressophytes).

Abstract

Conifers II (cupressophytes), comprising about 400 tree species in five families, are the most diverse group of living gymnosperms. Their plastid genomes (plastomes) are highly variable in size and organization, but such variation has never been systematically studied. In this study, we assessed the potential mechanisms underlying the evolution of cupressophyte plastomes. We analyzed the plastomes of 24 representative genera in all of the five cupressophyte families, focusing on their variation in size, noncoding DNA content, and nucleotide substitution rates. Using a tree-based method, we further inferred the ancestral plastomic organizations of internal nodes and evaluated the inversions across the evolutionary history of cupressophytes. Our data showed that variation in plastome size is statistically associated with the dynamics of noncoding DNA content, which results in different degrees of plastomic compactness among the cupressophyte families. The degrees of plastomic inversions also vary among the families, with the number of inversions per genus ranging from 0 in Araucariaceae to 1.27 in Cupressaceae. In addition, we demonstrated that synonymous substitution rates are significantly correlated with plastome size as well as degree of inversions. These data suggest that in cupressophytes, mutation rates play a critical role in driving the evolution of plastomic size while plastomic inversions evolve in a neutral manner.