Comparative Analyses of 3,654 Plastid Genomes Unravel Insights Into Evolutionary Dynamics and Phylogenetic Discordance of Green Plants

Abstract

The plastid organelle is essential for many vital cellular processes and the growth and development of plants. The availability of a large number of complete plastid genomes could be effectively utilized to understand the evolution of the plastid genomes and phylogenetic relationships among plants. We comprehensively analyzed the plastid genomes of Viridiplantae comprising 3,654 taxa from 298 families and 111 orders and compared the genomic organizations in their plastid genomic DNA among major clades, which include gene gain/loss, gene copy number, GC content, and gene blocks. We discovered that some important genes that exhibit similar functions likely formed gene blocks, such as the psb family presumably showing co-occurrence and forming gene blocks in Viridiplantae. The inverted repeats (IRs) in plastid genomes have doubled in size across land plants, and their GC content is substantially higher than non-IR genes. By employing three different data sets [all nucleotide positions (nt123), only the first and second codon positions (nt12), and amino acids (AA)], our phylogenomic analyses revealed Chlorokybales + Mesostigmatales as the earliest-branching lineage of streptophytes. Hornworts, mosses, and liverworts forming a monophylum were identified as the sister lineage of tracheophytes. Based on nt12 and AA data sets, monocots, Chloranthales and magnoliids are successive sister lineages to the eudicots + Ceratophyllales clade. The comprehensive taxon sampling and analysis of different data sets from plastid genomes recovered well-supported relationships of green plants, thereby contributing to resolving some long-standing uncertainties in the plant phylogeny.

Characterizing conflict and congruence of molecular evolution across organellar genome sequences for phylogenetics in land plants

“…Knowledge of the land plant tree of life has been clarified significantly by major recent sequencing efforts, such as the One Thousand Transcriptomes (1Kp) project ( Ruhfel et al., 2014 ; Gitzendanner et al., 2018 ; One Thousand Plant Transcriptomes Initiative, 2019 ; Yang et al., 2022 ) and the Plant and Fungal Tree of Life (PAFTOL) project ( Baker et al., 2022 ), as well as by numerous earlier studies employing datasets from Sanger sequencing (e.g., Chase et al., 1993 ; Chaw et al., 2000 ; Nickrent et al., 2000 ; Qiu et al., 2007 ; Soltis et al., 2011 ) or earlier methods of plastome sequencing (e.g., Moore et al., 2007 ; Moore et al., 2010 ). As sequencing depth continues to increase, obtaining complete plastome and even mitochondrial genomes from short-read data is becoming easier, even when these sequences are not the primary target of study ( Weitemier et al., 2014 ; Morales-Briones et al., 2021 ).…”

Genome-Wide Analysis of the MADS-Box Gene Family in Holoparasitic Plants (Balanophora subcupularis and Balanophora fungosa var. globosa)

“…Redundant genes generally have a genetic compensation function (i.e., the loss of one gene can be compensated by another with overlapping functions and expression patterns), and probably establish a genetically robust system for adaption ( Wagner, 2000 ; Dean et al, 2008 ; Rutter et al, 2017 ; Yang et al, 2022 ). Studies have indicated that the reduction of gene expression after replication promotes the long-term maintenance of duplicate genes and functional redundancy ( Qian et al, 2010 ).…”

Revealing the rise of a living fossil menagerie

“…With recent advances in phylogenetics and genomics, Ginkgo has helped bridge knowledge gaps between ferns and angiosperms (Liu et al, 2021). Despite some conflicting nuclear and plastome gene data and results among coalescent-based, species tree and supermatrix analyses, studies have begun to identify more robust evolutionary and functional patterns among plant genomes (Leebens-Mack et al, 2019;Yang et al, 2022). More living fossil attributes of Ginkgo are important to problems in biogeography (Berry, 1924;Lidgard and Love, 2018), paleoecology and habitat tracking (Zhao et al, 2016;Hohmann et al, 2018), adaptation to climate shifts (Huang et al, 2015;Zhao et al, 2019), and the global carbon cycle (Beerling and Royer, 2002;Steinthorsdottir et al, 2022).…”