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.

Plastome Evolution in Dolomiaea (Asteraceae, Cardueae) Using Phylogenomic and Comparative Analyses

“…Due to the lack of recombination, usually uniparental inheritance and high copy numbers per cells (Wicke et al, 2011;Ruhlman and Jansen, 2014), whole plastome sequences have been extensively used in reconstructing the plant Tree of Life (e.g., Jansen et al, 2007;Moore et al, 2007;Ruhfel et al, 2014;Gitzendanner et al, 2018;Li et al, 2019). Comparative plastome studies provide the opportunity to explore sequence variation and the molecular evolutionary patterns associated with genome rearrangements (e.g., Knox, 2014;Weng et al, 2014;Rabah et al, 2019;Shrestha et al, 2019) as well as gene loss, duplication, and transfer events (e.g., Downie and Jansen, 2015;Wu and Chaw, 2016;Sun et al, 2017), while also detecting signatures of positive selection in plastid genes facilitating our understanding of plants adapting to extreme environments (e.g., alpine areas) (Bock et al, 2014;Jiang et al, 2018;Liu et al, 2018). Highly divergent regions and simple sequence repeats (SSRs) obtained from whole plastome sequence hold promise as efficient molecular markers implemented in species delimitation and population genetics Cui et al, 2019).…”

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“…Positive correlations of dN and dS with both indels and rearrangements have been reported for legumes [26] and similar observations have been made in unrelated angiosperm lineages [27,69]. Both dN and dS have been positively correlated to inversions in cupressophytes [50] and in Cephalotaxus total substitutions were correlated to both indels and repeats. The strongest correlation was between repeats and substitutions, and repeats were also correlated with indels [70].…”

Comparative Genomic Analysis Reveals the Mechanism Driving the Diversification of Plastomic Structure in Taxaceae Species

“…Dealing with the rearrangements of two specific inverted fragments, our study provides novel insights into the structural diversification of Taxaceae plastomes. Phylogeny of the Taxaceae genera has been controversial for many years (Lu et al, 2014;Wu and Chaw, 2016;Zhang et al, 2019). In this study, 73 shared protein-coding genes were used to determine the relationships among the four genera.…”

“…The plastomes of Amentotaxus and Torreya species were larger than 130 kb and harbored more genes (Table 1). However, the plastome of Pseudotaxus chienii was smaller and contained only three rRNA genes (rrn4.5, rrn5, and rrn23), suggesting that it might have evolved toward reduced size Wu and Chaw, 2016).…”