Towards the plastome evolution and phylogeny of Cycas L. (Cycadaceae): molecular-morphology discordance and gene tree space analysis

Abstract

Background Plastid genomes (plastomes) present great potential in resolving multiscale phylogenetic relationship but few studies have focused on the influence of genetic characteristics of plastid genes, such as genetic variation and phylogenetic discordance, in resolving the phylogeny within a lineage. Here we examine plastome characteristics of Cycas L., the most diverse genus among extant cycads, and investigate the deep phylogenetic relationships within Cycas by sampling 47 plastomes representing all major clades from six sections. Results All Cycas plastomes shared consistent gene content and structure with only one gene loss detected in Philippine species C. wadei. Three novel plastome regions (psbA-matK, trnN-ndhF, chlL-trnN) were identified as containing the highest nucleotide variability. Molecular evolutionary analysis showed most of the plastid protein-coding genes have been under purifying selection except ndhB. Phylogenomic analyses that alternatively included concatenated and coalescent methods, both identified four clades but with conflicting topologies at shallow nodes. Specifically, we found three species-rich Cycas sections, namely Stangerioides, Indosinenses and Cycas, were not or only weakly supported as monophyly based on plastomic phylogeny. Tree space analyses based on different tree-inference methods both revealed three gene clusters, of which the cluster with moderate genetic properties showed the best congruence with the favored phylogeny. Conclusions Our exploration in plastomic data for Cycas supports the idea that plastid protein-coding genes may exhibit discordance in phylogenetic signals. The incongruence between molecular phylogeny and morphological classification reported here may largely be attributed to the uniparental attribute of plastid, which cannot offer sufficient information to resolve the phylogeny. Contrasting to a previous consensus that genes with longer sequences and a higher proportion of variances are superior for phylogeny reconstruction, our result implies that the most effective phylogenetic signals could come from loci that own moderate variation, GC content, sequence length, and underwent modest selection.

Comparative plastomes of Carya species provide new insights into the plastomes evolution and maternal phylogeny of the genus

“…The plastid, as a key uniparentally inherited organelle in plant cells, carries out not only photosynthesis but also other metabolic processes that mediate the adaptation of the plant to its environment ( Dierckxsens et al., 2016 ). Despite increased interest in phylogenetic and phylogenomic analyses using nuclear genome datasets, plastome-based analyses have also become a powerful solution that have been widely applied to address recalcitrant relationships across the Tree of Life ( Hu et al., 2016 ; Wei et al., 2017 ; Yan et al., 2018 ; Song et al., 2020 ; Wang et al., 2020 ; Tu et al., 2021 ; Dong et al., 2022 ; Liu et al., 2022 ; Ogoma et al., 2022 ). The plastome-based phylogenetic approaches play important roles in plant phylogenetics and evolution, such as revealing ancient and recent introgression or hybridization, tracking seed dispersal in phylogeographic studies, and charactering the structural diversity and evolution of organellar genomes ( Zhao et al, 2018 ; Li et al., 2019 ; Yao et al., 2019 ; Li et al., 2020 ; Yang et al., 2021 and references therein).…”

Analysis of the complete plastomes and nuclear ribosomal DNAs from Euonymus hamiltonianus and its relatives sheds light on their diversity and evolution

“…To investigate sequence divergence of protein-coding genes in the Euonymus plastomes, we estimated the ratio of non-synonymous (dN) to synonymous (dS) substitution rates (dN/dS). Based on dN/dS ratios, no gene was estimated to be under positive selection (>1.0), which was similar to most seed plants [ 52 – 54 ]. However, no variation in coding sequence was identified in nine genes, including seven photosynthesis genes ( psbI , psaI , psbJ , psbF , psbT , psbN , and ycf3 ) and two ribosomal protein genes ( rpl36 and rps7 ).…”

“…Based on dN/dS ratios, no gene was estimated to be under positive selection (>1.0), which was similar to most seed plants [52][53][54]. However, no variation in coding sequence was identified in nine genes, including seven photosynthesis genes (psbI, psaI, psbJ, psbF, psbT, psbN, and ycf3) and two ribosomal protein genes (rpl36 and rps7).…”

“…Relatively higher dS and lower dN have widely been observed in plastid genes from most seed plants, and also in seed-free plants such as lycophytes and ferns [52][53][54]66,67]. Even though most genes would have undergone purifying selection (dN/dS < 1.0), estimating substitution rates of plastid genes in Euonymus is needed to understand the plastome evolution in this genus.…”

Ghost introgression facilitates genomic divergence of a sympatric cryptic lineage in Cycas revoluta

“…The main coastal habitats of C. revoluta are ecologically different from those of its sister species, Cycas panzhihuaensis , from the inland Sichuan basin of China (Liu et al, 2018; Xiao & Moller, 2015), within the area where Cycas originated (Liu et al, 2021). The disjunct distribution of C. revoluta with long phylogenetic branches and morphological autapomorphy imply a high extinction‐to‐speciation rate during the evolution of C. revoluta (Condamine et al, 2015; Liu, Lindstrom, et al, 2022; Walters & Osborne, 2004). The occurrence of multiple extinction events together with frequent hybridization among Cycas (Norstog & Nicholls, 1997) makes it worth studying the influence of ghost introgression on sympatric cryptic lineage evolution in C. revoluta .…”