Comparative Analysis of Mitochondrial Genomes of Stemona Tuberosa Lour. Reveals Heterogeneity in Structure, Synteny, Intercellular Gene Transfer, and RNA Editing

Overview

Journal BMC Plant Biol

Publisher Biomed Central

Specialty Biology

Date 2025 Jan 6

PMID 39762746

Authors

De Xu

Tao Wang

Juan Huang

Qiang Wang

Zhide Wang

Zhou Xie

Dequan Zeng

Xue Liu

Liang Fu

Affiliations

Soon will be listed here.

Abstract

Background: Stemona tuberosa, a vital species in traditional Chinese medicine, has been extensively cultivated and utilized within its natural distribution over the past decades. While the chloroplast genome of S. tuberosa has been characterized, its mitochondrial genome (mitogenome) remains unexplored.

Results: This paper details the assembly of the complete S. tuberosa mitogenome, achieved through the integration of Illumina and Nanopore sequencing technologies. The assembled mitogenome is 605,873 bp in size with a GC content of 45.63%. It comprises 66 genes, including 38 protein-coding genes, 25 tRNA genes, and 3 rRNA genes. Our analysis delved into codon usage, sequence repeats, and RNA editing within the mitogenome. Additionally, we conducted a phylogenetic analysis involving S. tuberosa and 17 other taxa to clarify its evolutionary and taxonomic status. This study provides a crucial genetic resource for evolutionary research within the genus Stemona and other related genera in the Stemonaceae family.

Conclusion: Our study provides the inaugural comprehensive analysis of the mitochondrial genome of S. tuberosa, revealing its unique multi-branched structure. Through our investigation of codon usage, sequence repeats, and RNA editing within the mitogenome, coupled with a phylogenetic analysis involving S. tuberosa and 17 other taxa, we have elucidated its evolutionary and taxonomic status. These investigations provide a crucial genetic resource for evolutionary research within the genus Stemona and other related genera in the Stemonaceae family.

References

Wang Y, Tang H, DeBarry J, Tan X, Li J, Wang X . MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 2012; 40(7):e49. PMC: 3326336. DOI: 10.1093/nar/gkr1293. View

Ni Y, Li J, Chen H, Yue J, Chen P, Liu C . Comparative analysis of the chloroplast and mitochondrial genomes of Saposhnikovia divaricata revealed the possible transfer of plastome repeat regions into the mitogenome. BMC Genomics. 2022; 23(1):570. PMC: 9364500. DOI: 10.1186/s12864-022-08821-0. View

Benson G . Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 1998; 27(2):573-80. PMC: 148217. DOI: 10.1093/nar/27.2.573. View

Xiao S, Xu P, Deng Y, Dai X, Zhao L, Heider B . Comparative analysis of chloroplast genomes of cultivars and wild species of sweetpotato (Ipomoea batatas [L.] Lam). BMC Genomics. 2021; 22(1):262. PMC: 8042981. DOI: 10.1186/s12864-021-07544-y. View

Wicke S, Schneeweiss G, dePamphilis C, Muller K, Quandt D . The evolution of the plastid chromosome in land plants: gene content, gene order, gene function. Plant Mol Biol. 2011; 76(3-5):273-97. PMC: 3104136. DOI: 10.1007/s11103-011-9762-4. View

Sloan D, Wu Z, Sharbrough J . Correction of Persistent Errors in Arabidopsis Reference Mitochondrial Genomes. Plant Cell. 2018; 30(3):525-527. PMC: 5894837. DOI: 10.1105/tpc.18.00024. View

Sloan D, Alverson A, Chuckalovcak J, Wu M, McCauley D, Palmer J . Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biol. 2012; 10(1):e1001241. PMC: 3260318. DOI: 10.1371/journal.pbio.1001241. View

Wang Y, Chen S, Chen J, Chen C, Lin X, Peng H . Characterization and phylogenetic analysis of the complete mitochondrial genome sequence of Photinia serratifolia. Sci Rep. 2023; 13(1):770. PMC: 9840629. DOI: 10.1038/s41598-022-24327-x. View

Tillich M, Lehwark P, Pellizzer T, Ulbricht-Jones E, Fischer A, Bock R . GeSeq - versatile and accurate annotation of organelle genomes. Nucleic Acids Res. 2017; 45(W1):W6-W11. PMC: 5570176. DOI: 10.1093/nar/gkx391. View

10.

Wick R, Schultz M, Zobel J, Holt K . Bandage: interactive visualization of de novo genome assemblies. Bioinformatics. 2015; 31(20):3350-2. PMC: 4595904. DOI: 10.1093/bioinformatics/btv383. View

11.

Li H, Durbin R . Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009; 25(14):1754-60. PMC: 2705234. DOI: 10.1093/bioinformatics/btp324. View

12.

Huang S, Kong F, Ma Q, Guo Z, Zhou L, Wang Q . Nematicidal Stemona Alkaloids from Stemona parviflora. J Nat Prod. 2016; 79(10):2599-2605. DOI: 10.1021/acs.jnatprod.6b00528. View

13.

Xie Y, Liu W, Guo L, Zhang X . Mitochondrial genome complexity in : nanopore sequencing reveals chloroplast gene transfer and DNA rearrangements. Front Genet. 2024; 15:1395805. PMC: 11188483. DOI: 10.3389/fgene.2024.1395805. View

14.

Ma Q, Wang Y, Li S, Wen J, Zhu L, Yan K . Assembly and comparative analysis of the first complete mitochondrial genome of Acer truncatum Bunge: a woody oil-tree species producing nervonic acid. BMC Plant Biol. 2022; 22(1):29. PMC: 8756732. DOI: 10.1186/s12870-021-03416-5. View

15.

Katoh K, Misawa K, Kuma K, Miyata T . MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002; 30(14):3059-66. PMC: 135756. DOI: 10.1093/nar/gkf436. View

16.

Alverson A, Rice D, Dickinson S, Barry K, Palmer J . Origins and recombination of the bacterial-sized multichromosomal mitochondrial genome of cucumber. Plant Cell. 2011; 23(7):2499-513. PMC: 3226218. DOI: 10.1105/tpc.111.087189. View

17.

Wang L, Liu X, Xu Y, Zhang Z, Wei Y, Hu Y . Assembly and comparative analysis of the first complete mitochondrial genome of a traditional Chinese medicine Angelica biserrata (Shan et Yuan) Yuan et Shan. Int J Biol Macromol. 2023; 257(Pt 1):128571. DOI: 10.1016/j.ijbiomac.2023.128571. View

18.

Torre S, Sebastiani F, Burbui G, Pecori F, Pepori A, Passeri I . Novel Insights Into Refugia at the Southern Margin of the Distribution Range of the Endangered Species . Front Plant Sci. 2022; 13:826158. PMC: 8886209. DOI: 10.3389/fpls.2022.826158. View

19.

Jin J, Yu W, Yang J, Song Y, dePamphilis C, Yi T . GetOrganelle: a fast and versatile toolkit for accurate de novo assembly of organelle genomes. Genome Biol. 2020; 21(1):241. PMC: 7488116. DOI: 10.1186/s13059-020-02154-5. View

20.

Yang H, Chen H, Ni Y, Li J, Cai Y, Ma B . Hybrid Assembly of the Mitochondrial Genome Provides the First Evidence of the Multi-Chromosomal Mitochondrial DNA Structure of Species. Int J Mol Sci. 2022; 23(22). PMC: 9694629. DOI: 10.3390/ijms232214267. View