Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2022 May 20:13:870949.
doi: 10.3389/fpls.2022.870949. eCollection 2022.

Deep Insights Into the Plastome Evolution and Phylogenetic Relationships of the Tribe Urticeae (Family Urticaceae)

Affiliations

Deep Insights Into the Plastome Evolution and Phylogenetic Relationships of the Tribe Urticeae (Family Urticaceae)

Catherine A Ogoma et al. Front Plant Sci. .

Abstract

Urticeae s.l., a tribe of Urticaceae well-known for their stinging trichomes, consists of more than 10 genera and approximately 220 species. Relationships within this tribe remain poorly known due to the limited molecular and taxonomic sampling in previous studies, and chloroplast genome (CP genome/plastome) evolution is still largely unaddressed. To address these concerns, we used genome skimming data-CP genome and nuclear ribosomal DNA (18S-ITS1-5.8S-ITS2-26S); 106 accessions-for the very first time to attempt resolving the recalcitrant relationships and to explore chloroplast structural evolution across the group. Furthermore, we assembled a taxon rich two-locus dataset of trnL-F spacer and ITS sequences across 291 accessions to complement our genome skimming dataset. We found that Urticeae plastomes exhibit the tetrad structure typical of angiosperms, with sizes ranging from 145 to 161 kb and encoding a set of 110-112 unique genes. The studied plastomes have also undergone several structural variations, including inverted repeat (IR) expansions and contractions, inversion of the trnN-GUU gene, losses of the rps19 gene, and the rpl2 intron, and the proliferation of multiple repeat types; 11 hypervariable regions were also identified. Our phylogenomic analyses largely resolved major relationships across tribe Urticeae, supporting the monophyly of the tribe and most of its genera except for Laportea, Urera, and Urtica, which were recovered as polyphyletic with strong support. Our analyses also resolved with strong support several previously contentious branches: (1) Girardinia as a sister to the Dendrocnide-Discocnide-Laportea-Nanocnide-Zhengyia-Urtica-Hesperocnide clade and (2) Poikilospermum as sister to the recently transcribed Urera sensu stricto. Analyses of the taxon-rich, two-locus dataset showed lower support but was largely congruent with results from the CP genome and nuclear ribosomal DNA dataset. Collectively, our study highlights the power of genome skimming data to ameliorate phylogenetic resolution and provides new insights into phylogenetic relationships and chloroplast structural evolution in Urticeae.

Keywords: Urticaceae; Urticaceae s.l.; chloroplast structural evolution; genome skimming; phylogenomic.

PubMed Disclaimer

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
Alternative relationships of Urticeae based on combined loci data from previous analyses. (A) Wu et al. (2013): Maximum likelihood (ML)/Maximum parsimony (MP)/Bayesian inference (BI) analyses based on nuclear, chloroplast, and mitochondrial loci; (B) Kim et al. (2015): MP/BI tree inferred from chloroplast and nuclear DNA data; (C) Wu et al. (2018): ML/MP/BI tree inferred from nuclear, chloroplast, and mitochondrial data; (D) Huang et al. (2019): MP/BI analyses based on chloroplast and nuclear data. Numeric values besides each genus correspond to the total number of accessions sampled per genus and the number below each figure represents the total number (individual/species) of Urticeae samples used in each respective analysis. “*” indicates full support; “–“indicates no support in (A,C), support values of < 75 (MP) and < 0.95 (BI) in (B), and support values of < 50% (MP) and < 0.7 (BI) in (D).
FIGURE 2
FIGURE 2
(A) Gene map of complete chloroplast genome of Girardinia bullosa (a typical representative of gene organization in Urticeae s.l. plastomes); (B) inset map showing the inverted orientation of trnN-GUU in clade 3C except for Discocnide mexicana; (C) inset map of the Urticeae plastome, showing the typical orientation of trnN-GUU. Genes inside and outside the outer circle are transcribed clockwise and counterclockwise, respectively.
FIGURE 3
FIGURE 3
(A) representative map showing expansions and contractions in the IR region; (B) comparison of the IR/SC junctions among 57 Urticeae plastomes. The genes around the borders are shown above or below the main line. LSC, Large Single Copy; SSC, Small Single Copy; IR (a and b), Inverted Repeat a and b.
FIGURE 4
FIGURE 4
(A) Chord diagram showing a connection between species and their corresponding repeat types (Dispersed, Palindromic, Tandem, and SSR). The tick marks beside each repeat type indicate the frequency of the number of repeats detected and their percentages, respectively; (B) frequency of tandem, palindromic, and dispersed repeats; (C) number of the six SSR(simple sequence repeats) nucleotides; (D) the seven most abundant SSR motifs in Urticeae plastomes. The values along the axis represent the abundance values.
FIGURE 5
FIGURE 5
Phylogenetic relationships of Urticeae inferred from maximum likelihood (ML) and Bayesian inference (BI) based on combined complete plastome and nrDNA sequences. Numbers on the branch indicate clade classification (in purple) and ML_BS/BI_PP values (in black)—note that branches with no support values indicate both ML_BS ≥ 90 and BI_PP = 1.00; lastly, “*” indicate incongruence between ML and BI trees and “–” no support values. Representative images of genera within Urticeae s.l. are shown on the right. Photographs: (A–C,E,G,K) by Z.Y. Wu, (D,F) by C.A. Ogoma, (H) by U. Dreschel, (I) by C. Kunath, and (J) photographed by J. Cantley.
FIGURE 6
FIGURE 6
Phylogenetic relationships of Urticeae tribe inferred from maximum likelihood (ML) and Bayesian inference (BI) based on trnL-F intergenic spacer and ITS (trnL-F + ITS) loci sequences. Support values indicated by black circle show ML_BS ≥ 90 and BI_PP ≥ 0.90.

References

    1. Akaike H. (1973). “Information theory as an extension of the maximum likelihood principle,” in Second International Symposium on Information Theory, eds Petrov B. N., Csaki F. (Budapest: Akademiai Kiado; ), 267–281.
    1. Bankevich A., Nurk S., Antipov D., Gurevich A. A., Dvorkin M., Kulikov A. S., et al. (2012). SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19 455–477. 10.1089/cmb.2012.0021 - DOI - PMC - PubMed
    1. Benson G. (1999). Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27 573–580. 10.1093/nar/27.2.573 - DOI - PMC - PubMed
    1. Benvenutti R. C., Dalla Vecchia C. A., Locateli G., Serpa P. Z., Lutinski J. A., Rodrigues Junior S. A., et al. (2020). Gastroprotective activity of hydroalcoholic extract of the leaves of Urera baccifera in rodents. J. Ethnopharmacol. 250:112473. 10.1016/j.jep.2019.112473 - DOI - PubMed
    1. Bodros E., Baley C. (2008). Study of the tensile properties of stinging nettle fibres (Urtica dioica). Mater. Lett. 62 2143–2145. 10.1016/j.matlet.2007.11.034 - DOI