Comparative Chloroplast Genomes of Nicotiana Species (Solanaceae): Insights Into the Genetic Variation, Phylogenetic Relationship, and Polyploid Speciation

Abstract

Nicotiana L. is a genus rich in polyploidy, which represents an ideal natural system for investigating speciation, biodiversity, and phytogeography. Despite a wealth of phylogenetic work on this genus, a robust evolutionary framework with a dated molecular phylogeny for the genus is still lacking. In this study, the 19 complete chloroplast genomes of Nicotiana species were assembled, and five published chloroplast genomes of Nicotiana were retrieved for comparative analyses. The results showed that the 24 chloroplast genomes of Nicotiana, ranging from 155,327 bp (N. paniculata) to 156,142 bp (N. heterantha) in size, exhibited typical quadripartite structure. The chloroplast genomes were rather conserved in genome structure, GC content, RNA editing sites, and gene content and order. The higher GC content observed in the IR regions could be a result of the presence of abundant rRNA and tRNA genes, which contained a relatively higher GC content. A total of seven hypervariable regions, as new molecular markers for phylogenetic analysis, were uncovered. Based on 78 protein-coding genes, we constructed a well-supported phylogenetic tree, which was largely in agreement with previous studies, except for a slight conflict in several sections. Chloroplast phylogenetic results indicated that the progenitors of diploid N. sylvestris, N. knightiana, and the common ancestor of N. sylvestris and N. glauca might have donated the maternal genomes of allopolyploid N. tabacum, N. rustica, and section Repandae, respectively. Meanwhile, the diploid section Noctiflorae lineages (N. glauca) acted as the most likely maternal progenitor of section Suaveolentes. Molecular dating results show that the polyploid events range considerably in ~0.12 million (section Nicotiana) to ~5.77 million (section Repandae) years ago. The younger polyploids (N. tabacum and N. rustica) were estimated to have arisen ~0.120 and ~0.186 Mya, respectively. The older polyploids (section Repandae and Suaveolentes) were considered to have originated from a single polyploid event at ~5.77 and ~4.49 Mya, respectively. In summary, the comparative analysis of chloroplast genomes of Nicotiana species has not only revealed a series of new insights into the genetic variation and phylogenetic relationships in Nicotiana but also provided rich genetic resources for speciation and biodiversity research in the future.

Phylotranscriptomics supports numerous polyploidization events and phylogenetic relationships in Nicotiana

“…Our nuclear analyses revealed two major clades, which were not indicated by previous molecular or morphological analyses (McCarthy et al, 2016;Clarkson et al, 2017). The plastid phylogenetic tree in this study showed a consistent placement with our previous result based on the whole plastid genomes (Wang et al, 2022). Furthermore, the availability of genome-scale data allowed us to examine the consistency of phylogenetic signals in the nuclear and plastid genomes for the first time, and several incongruent have been identified between nuclear and plastid phylogeny, especially for section Petunioides and Sylvestres (Figure 1).…”

“…However, these phylogeny relationships in the genus Nicotiana were inferred from several nuclear or plastid makers, which lack enough support and reliable results. Our recent analysis of whole plastid genomes provided a well-supported phylogenetic relationship of 11 sections in Nicotiana (Wang et al, 2022), which supported the section Tomentosae as the base clade of all others, and the section Petunioides was sister to the section Trigonophyllae.…”

“…Based on the comparative nuclear genome analysis, Sierro et al (2018) found that the tetraploid species N. rustica inherited about 41% of its genome from its paternal progenitor, N. undulata, and 59% from its maternal progenitor, the common ancestor of N. paniculata and N. knightiana. Whereas, the pieces of evidence from comparative plastid genes and genome analysis revealed that the maternal parent of the tetraploid N. rustica was from the species of section Paniculatae, and the diploid N. knightiana was genetically closer than N. paniculata to N. rustica (Clarkson et al, 2004;Mehmood et al, 2020;Wang et al, 2022). The result from sequence similarity analysis support that both N. knightiana and N. paniculata might have donated the maternal genome of N. rustica (Figure 3B).…”

“…And the deep relationships of Nicotiana have usually neither been resolved nor well-supported. Recent analyses using the complete chloroplast genomes of Nicotiana in 11 sections have recovered a nearly fully resolved phylogenetic relationship and deduced a potential maternal progenitor of polyploid species (Wang et al, 2022). However, evidence of phylogenetic relationships and diploid progenitors of polyploid species from the nuclear are still lacking.…”

The Chloroplast Genome of a V. amygdalina Specie Isolated from Awka, Nigeria: Comparative and Phylogenetic Analysis

“…No variation occurred in the IR loci, indicating that the IR region of V. amygdalina is conserved. This conservation of the IR genome within species has been observed in pangenomic studies of cucumber [11], yam [12], and tobacco [13] chloroplast genomes.…”