Abstract
Plastome downsizing is rare in photosynthetic seed plants. However, a large-scale study of five cupressophyte families (conifers II) indicated that the plastomes of some Cupressaceous genera are notably reduced and compact. Here, we enriched taxon sampling in Cupressaceae by adding plastomes of ten previously unreported genera to determine the origin, evolution, and consequences of plastome reduction in this family. We discovered that plastome downsizing is specific to Callitroideae (a Southern Hemispheric subfamily). Their plastomes are the smallest, encode the fewest plastid genes, and contain the fewest GC-end codons among Cupressaceae. We show that repeated tRNA losses and shrinkage of intergenic spacers together contributed to the plastome downsizing in Callitroideae. Moreover, our absolute nucleotide substitution rate analyses suggest relaxed functional constraints in translation-related plastid genes (clpP, infA, rpl, and rps), but not in photosynthesis- or transcription-related ones, of Callitris (the most diverse genus in Callitroideae). We hypothesize that the small and low-GC plastomes of Callitroideae emerged ca. 112–75 million years ago as an adaptation to increased competition with angiosperms on the Gondwana supercontinent. Our findings highlight Callitroideae as another case of plastome downsizing in photosynthetic seed plant lineages.
Highlights
Cupressaceae is the most widely distributed family in cupressophytes, comprising 30–32 genera and ca. 133 species
Topologies of maximum likelihood (ML) and Bayesian inference (BI) trees inferred from 79 concatenated protein-coding genes have 100% bootstrap support (BS) and 1.0 posterior probability (PP) at almost all nodes (Figure 1)
The branch leading to Callitroideae is remarkably long and contains a signature of positive selection, suggesting that positive selection resulted in accelerated rates of plastid nucleotide substitutions before the diversification of Callitroideae
Summary
Cupressaceae (cypress family) is the most widely distributed family in cupressophytes (conifers II), comprising 30–32 genera and ca. 133 species. Bald cypress (Taxodium), China fir (Cunninghamia), cordilleran cypress (Austrocedrus), and cypress pine (Callitris) are important sources of timber, furniture, and ornamentals (Farjon, 2005). They are distributed across all continents except Antarctica (Farjon, 2005; Brodribb et al, 2012). Cypress genera have been classified into seven (or six) subfamilies (Mao et al, 2012; Yang et al, 2012). Two of the seven subfamilies, Athrotaxidoideae and Callitroideae, are mainly restricted to the Southern Hemisphere, while the other five (Cupressoideae, Cunninghamioideae, Sequoioideae, Taiwanioideae, and Taxodioideae) are mostly distributed in the Northern Hemisphere (Gadek et al, 2000; Farjon and Filer, 2013)
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