The Chloroplast Genome Evolution of Venus Slipper (Paphiopedilum): IR Expansion, SSC Contraction, and Highly Rearranged SSC Regions

Abstract

Background: Paphiopedilum is the largest genus of slipper orchids. Previous studies showed that the phylogenetic relationships of this genus are not well resolved, and sparse taxon sampling documented inverted repeat (IR) expansion and small single copy (SSC) contraction of the chloroplast genomes of Paphiopedilum. Here, we sequenced, assembled, and annotated 77 plastomes of Paphiopedilum species. The phylogeny based on the plastome resolved the relationships of the genus except for the phylogenetic position of two unstable species. We used phylogenetic and comparative genomic approaches to elucidate the plastome evolution of Paphiopedilum.Results: The plastomes of Paphiopedilum have conserved genome structure and gene content except in the SSC region. The large single copy/inverted repeat (LSC/IR) boundaries are relatively stable, while the boundaries of inverted repeat/small single copy (IR/SSC) boundaries varied among species. Corresponding to the IR/SSC boundary shifts, the chloroplast genomes of the genus experienced IR expansion and SSC contraction. The IR region incorporated one to six genes of the SSC region. Unexpectedly, great variation in the size, gene order, and gene content of the SSC regions was found, especially in the subg. Parvisepalum. Furthermore, Paphiopedilum provides evidence for the ongoing degradation of the ndh genes in the photoautotrophic plants. The estimated substitution rates of the protein coding genes show accelerated rates of evolution in clpP, psbH, and psbZ. Genes transferred to the IR region due to the boundary shift also have higher substitution rates.Conclusions: We found IR expansion and SSC contraction in the chloroplast genomes of Paphiopedilum with dense sampling, and the genus shows variation in the size, gene order, and gene content of the SSC region. This genus provides an ideal system to investigate the dynamics of plastome evolution.

Complete chloroplast genomes provide insights into evolution and phylogeny of Zingiber (Zingiberaceae)

“…Chloroplast genomes have been used to address the chloroplast genome evolution, patterns and rates of nucleotide substitutions and phylogenetic relationships among land plants [20]. Chloroplast is a kind of vital organelle that can transform light energy into chemical energy in green plants [21,22].…”

Complete chloroplast genome sequencing and comparative analysis of threatened dragon trees Dracaena serrulata and Dracaena cinnabari

“…Inverted repeat regions are considered the most conserved regions. The size variations in cp genomes occur due to expansion/contraction of IRs and single copy regions 76,90,91 . The four junctions (JLA, JLB, JSA, and JSB) between the single copy regions (LSC, SSC) and IRs (IRA, IRB) in cp genomes of D. serrulata, D. cinnabari, and others were comprehensively assessed.…”

Variation in Plastome Sizes Accompanied by Evolutionary History in Monogenomic Triticeae (Poaceae: Triticeae)

“…Inverted repeat expansion and contraction were mostly associated with cp genome size variation ( McCoy et al, 2008 ; Wu et al, 2009 ). Expansion and contraction in IRs of chloroplast genomes have been widely reported in various kinds of plants ( Krause, 2011 ; Weng et al, 2014 ; Schwarz et al, 2015 ; Shrestha et al, 2019 ; He et al, 2020 ; Guo et al, 2021 ). We also found that cp genomes in the 34 Triticeae species exhibited obvious different IR sizes.…”