Abstract
Chloroplast genomes of plants are highly conserved in both gene order and gene content. Analysis of the whole chloroplast genome is known to provide much more informative DNA sites and thus generates high resolution for plant phylogenies. Here, we report the complete chloroplast genomes of three Salix species in family Salicaceae. Phylogeny of Salicaceae inferred from complete chloroplast genomes is generally consistent with previous studies but resolved with higher statistical support. Incongruences of phylogeny, however, are observed in genus Populus, which most likely results from homoplasy. By comparing three Salix chloroplast genomes with the published chloroplast genomes of other Salicaceae species, we demonstrate that the synteny and length of chloroplast genomes in Salicaceae are highly conserved but experienced dynamic evolution among species. We identify seven positively selected chloroplast genes in Salicaceae, which might be related to the adaptive evolution of Salicaceae species. Comparative chloroplast genome analysis within the family also indicates that some chloroplast genes are lost or became pseudogenes, infer that the chloroplast genes horizontally transferred to the nucleus genome. Based on the complete nucleus genome sequences from two Salicaceae species, we remarkably identify that the entire chloroplast genome is indeed transferred and integrated to the nucleus genome in the individual of the reference genome of P. trichocarpa at least once. This observation, along with presence of the large nuclear plastid DNA (NUPTs) and NUPTs-containing multiple chloroplast genes in their original order in the chloroplast genome, favors the DNA-mediated hypothesis of organelle to nucleus DNA transfer. Overall, the phylogenomic analysis using chloroplast complete genomes clearly elucidates the phylogeny of Salicaceae. The identification of positively selected chloroplast genes and dynamic chloroplast-to-nucleus gene transfers in Salicaceae provide resources to better understand the successful adaptation of Salicaceae species.
Highlights
The chloroplast is the photosynthetic organelle that provides energy for plants and algae
The questions that we addressed in this study are: (1) What are potential DNA markers in cp genomes that can be used for phylogenetic analysis of Salicaceae? (2) What is the phylogenetic relation of Salicaceae based on phylogenomic analysis of complete Salicaceae cp genomes? (3) What are the structures and contents of cp genomes in Salicaceae? and (4) What are the evolution and dynamics patterns of cp genomes revealed by examining evolution of cp genes and DNA horizontally transferring events from cp to nucleus?
We amplified and sequenced ∼ 152 kb from all the three Salix species. We compared these sequences directly to the assembled genomes and we observed no nucleotide mismatches or indels/insertions. This result confirmed the reliability of assembled chloroplast genome sequences
Summary
The chloroplast (cp) is the photosynthetic organelle that provides energy for plants and algae. Chloroplast genes are involved in major functions, which include sugar synthesis, starch storage, the production of several amino acids, lipids, vitamins, and pigments. They are involved in key sulfur and nitrogen metabolic pathways. Most cp genomes are composed of circular DNA molecules ranging from 120 to 160 kb in length and have a quadripartite organization consisting of two copies of inverted repeats (IRs) of about 20–28 kb in size. These IRs divide the rest of cp genome into an 80–90 kb Large Single Copy (LSC) region and a 16–27 kb Small Single Copy (SSC) region (Jansen et al, 2005). The gene content and order of cp genomes of angiosperms are generally conserved, which encode four rRNAs, 30 tRNAs, and about 80 unique proteins (Chumley et al, 2006)
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