The dynamic history of gymnosperm plastomes: Insights from structural characterization, comparative analysis, phylogenomics, and time divergence

Abstract

Gymnosperms are among the most endangered groups of plant species; they include ginkgo, pines (Conifers I), cupressophytes (Conifers II), cycads, and gnetophytes. The relationships among the five extant gymnosperm groups remain equivocal. We analyzed 167 available gymnosperm plastomes and investigated their diversity and phylogeny. We found that plastome size, structure, and gene order were highly variable in the five gymnosperm groups, of which Parasitaxus usta (Vieill.) de Laub. and Macrozamia mountperriensis F.M.Bailey had the smallest and largest plastomes, respectively. The inverted repeats (IRs) of the five groups were shown to have evolved through distinctive evolutionary scenarios. The IRs have been lost in all conifers but retained in cycads and gnetophytes. A positive association between simple sequence repeat (SSR) abundance and plastome size was observed, and the SSRs with the most variation were found in Pinaceae. Furthermore, the number of repeats was negatively correlated with IR length; thus, the highest number of repeats was detected in Conifers I and II, in which the IRs had been lost. We constructed a phylogeny based on 29 shared genes from 167 plastomes. With the plastome tree and 13 calibrations, we estimated the tree height between present-day angiosperms and gymnosperms to be ∼380 million years ago (mya). The placement of Gnetales in the tree agreed with the Gnetales-other gymnosperms hypothesis. The divergence between Ginkgo and cycads was estimated as ∼284 mya; the crown age of the cycads was 251 mya. Our time-calibrated plastid-based phylogenomic tree provides a framework for comparative studies of gymnosperm evolution.

Comparative plastome genomics, taxonomic delimitation and evolutionary divergences of Tetraena hamiensis var. qatarensis and Tetraena simplex (Zygophyllaceae)

“…The most common reports of small plastomes come from investigations of parasitic plants, such as Taxillus chinensis and Taxillus sutchuenensis in the Loranthaceae family of Santalales 64 Epifagus virginiana in Orobanchaceae family 65 , Cuscuta chinensis and C. japonica in Convolvulaceae family 66 . Some gymnosperms, such as Welwitschia mirabilis in the Welwitschiaceae of the Welwitschiales and Gnetum ula in the Gnetaceae of the Gnetales 67 , 68 , have smaller plastomes. Except for Astragalus membranaceus , which has a plastome of roughly 124 kb owing to the lack of an IR, non-parasitic angiosperms rarely have a plastome less than 130 kb 69 .…”

“…Although infrequent, ndh gene deletion or pseudogenization is expected in the plastomes of photoautotrophic seed plants of many lineages 79 . The phenomena described in which plant plastid ndh genes were specifically deleted, and nuclear-encoded NDH subunits were expressed in Pinaceae 67 , Orchidaceae 80 gametophytes 78 and Geraniales 16 , 81 . Plants that thrive in drought (arid and semi-arid) conditions must adapt to their surroundings more than others.…”

“…The Chloroplast genome (plastome) is an excellent resource for resolving the tree of life and identifying taxa 11 , 13 Numerous studies have demonstrated that the chloroplast genome is a robust and effective method for uncovering plant phylogeny and evolutionary history more accurately 14 , 15 . Unlike the four standard barcodes, due to their significant genetic variety, DNA super-barcode, which employs the entire chloroplast genome sequence, can distinguish between closely related species 11 , 16 , 17 . Despite this, DNA super-barcodes face criticism and challenges in species identification, such as high sequencing costs, lack of a comprehensive cp-genome database, and difficulty tracking species boundaries 18 .…”

“…Plastome has more variation with a significantly higher resolution of phylogenies than the most often used and predicted genus-specific DNA barcodes, which is beneficial for revealing phylogenetic connections between closely related species 21 . Plastome has been widely applied in plant identification 22 , phylogenetic analyses 16 , 22 – 25 and plant population studies 25 . Even with reference genomes or specific fragments, most taxa, such as Zygophyllum and Tetraena, can build a comprehensive database.…”

Plastome sequencing of South American Podocarpus species reveals low rearrangement rates despite ancient gondwanan disjunctions

“…In gymnosperms, the plastome is highly variable in size and organization, and this variation is often used in phylogenetics to identify families, subgenera, and genera [12]. Yet, certain families remain poorly sampled such as only eight of the 187 species within Podocarpaceae have been sequenced so far [13]. Also, the loss of the large IR has been reported in several species, mainly conifers [14][15][16].…”