Characterization of Rheum palmatum mitochondrial genome and comparative analysis among Caryophyllales species

Longlong Gao, Lijun Hao, Wenjie Xu, Tianyi Xin, Chi Song, Yulin Lin, Lingping Zhu, Jingyuan Song

PDF(1520 KB)
PDF(1520 KB)
Acupuncture and Herbal Medicine ›› 2023, Vol. 3 ›› Issue (4) : 323-332. DOI: 10.1097/HM9.0000000000000078
Original Articles
research-article

Characterization of Rheum palmatum mitochondrial genome and comparative analysis among Caryophyllales species

Author information +
History +

Abstract

Objective:This work aimed to report the first complete mitochondrial genome (mitogenome) of Rheum palmatum, summarize the features of Caryophyllales mitogenomes, and to reveal the potential of utilizing the mitogenomes of R. palmatum and other Caryophyllales species for inferring phylogenetic relationships and species identification.

Methods: Both Illumina short reads and PacBio HiFi reads were utilized to obtain a complete mitogenome of R. palmatum. A variety of bioinformatics tools were employed to characterize the R. palmatum mitogenome, compare the reported mitogenomes in Caryophyllales and conduct phylogenetic analysis.

Results: The mitogenome of R. palmatum was assembled into a single master circle of 302,993 bp, encoding 35 known protein-coding genes, 18 transfer RNA genes, and three ribosome RNA genes. A total of 249 long repeats and 49 simple sequence repeats were identified in this mitogenome. The sizes of mitogenomes in Caryophyllales varied from 253 kb to 11.3 Mb. Among them, 23 mitogenomes were circular molecules, one was linear, and one consisted of relaxed circles, linear molecules, and supercoiled DNA. Out of the total mitogenomes, 11 were single-chromosome structure, whereas the remaining 14 were multi-chromosomal organizations. The phylogenetic analysis is consistent with both the Engler system (1964) and the Angiosperm Phylogeny Group III system.

Conclusions: We obtained the first mitogenome of R. palmatum, which consists of a master circle. Mitogenomes in Caryophyllales have variable genome sizes and structures even within the same species. Circular molecules are still the dominant pattern in Caryophyllales. Single-chromosome mitogenomes account for nearly a half of all the mitogenomes in Caryophyllales, in contrast to previous studies. It is feasible to utilize mitochondrial genomes for inferring phylogenetic relationships and conducting species identification.

Keywords

Caryophyllales / Mitochondrial genome / Molecular identification / Phylogenetic analysis / Rheum palmatum

Cite this article

Download citation ▾
Longlong Gao, Lijun Hao, Wenjie Xu, Tianyi Xin, Chi Song, Yulin Lin, Lingping Zhu, Jingyuan Song. Characterization of Rheum palmatum mitochondrial genome and comparative analysis among Caryophyllales species. Acupuncture and Herbal Medicine, 2023, 3(4): 323‒332 https://doi.org/10.1097/HM9.0000000000000078

References

[[1]]
Wang XM, Hou XQ, Zhang YQ, et al.Distribution pattern of genuine species of rhubarb as traditional Chinese medicine. J Med Plant Res. 2010;4(18):1865-1876.
[[2]]
Chen D, Wang Y, Shi W, et al.Analysis of endophyte diversity of Rheum palmatum among different tissues and ages. Arch Microbiol. 2022;205(1):14.
[[3]]
Feng TS, Yuan ZY, Yang RQ, et al.Purgative components in rhubarbs: adrenergic receptor inhibitors linked with glucose carriers. Fitoterapia. 2013;91:236-246.
[[4]]
Xin T, Li R, Lou Q, et al.Application of DNA barcoding to the entire traditional Chinese medicine industrial chain: a case study of Rhei Radix etRhizoma. Phytomedicine. 2022;105:154375.
[[5]]
Chang SJ, Huang SH, Lin YJ, et al.Antiviral activity of Rheum palmatum methanol extract and chrysophanol against Japanese encephalitis virus. Arch Pharm Res. 2014;37(9):1117-1123.
[[6]]
Wen Q, Miao J, Lau N, et al.Rhein attenuates lipopolysaccharide-primed inflammation through NF-κB inhibition in RAW264.7 cells: targeting the PPAR-γ signal pathway. Can J Physiol Pharmacol. 2020;98(6):357-365.
[[7]]
Shang X, Dai L, He J, et al.A high-value-added application of the stems of Rheum palmatum L. as a healthy food: the nutritional value, chemical composition, and anti-inflammatory and antioxidant activities. Food Funct. 2022;13(9):4901-4913.
[[8]]
Nguyen LTH, Ahn SH, Shin HM, et al.Anti-psoriatic effect of Rheum palmatum L. and its underlying molecular mechanisms. Int J Mol Sci. 2022;23(24):16000.
[[9]]
Chen Y, Zhu J.Anti-HBV effect of individual traditional Chinese herbal medicine in vitro and in vivo: an analytic review. J Viral Hepat. 2013;20(7):445-452.
[[10]]
Manimaran A, Manoharan S.Tumor preventive efficacy of emodin in 7,12-dimethylbenz[a]anthracene-induced oral carcinogenesis: a histopathological and biochemical approach. Pathol Oncol Res. 2018;24(1):19-29.
[[11]]
Rezapour Kalkhoran M, Kazerouni F, Omrani MD, et al.Cytotoxic effect of emodin on growth of SKBR3 breast cancer cells. Research Article. Int J Cancer Manag. 2017;10(4):e8094.
[[12]]
El-Saied MA, Sobeh M, Abdo W, et al.Rheum palmatum root extract inhibits hepatocellular carcinoma in rats treated with diethylnitrosamine. J Pharm Pharmacol. 2018;70(6):821-829.
[[13]]
Smith SA, Brown JW, Yang Y, et al.Disparity, diversity, and duplications in theCaryophyllales. New Phytol. 2018;217(2):836-854.
[[14]]
Yang Y, Moore MJ, Brockington SF, et al.Dissecting molecular evolution in the highly diverse plant clade Caryophyllales using transcriptome sequencing. Mol Biol Evol. 2015;32(8):2001-2014.
[[15]]
Pfanner N, Warscheid B, Wiedemann N.Mitochondrial proteins: from biogenesis to functional networks. Nat Rev Mol Cell Biol. 2019;20(5):267-284.
[[16]]
Møller IM, Rasmusson AG, Van Aken O.Plant mitochondria—past, present and future. Plant J. 2021;108(4):912-959.
[[17]]
Li J, Li J, Ma Y, et al.The complete mitochondrial genome of okra(Abelmoschus esculentus): using nanopore long reads to investigate gene transfer from chloroplast genomes and rearrangements of mitochondrial DNA molecules. BMC Genomics. 2022;23(1):481.
[[18]]
Li J, Xu Y, Shan Y, et al.Assembly of the complete mitochondrial genome of an endemic plant, Scutellaria tsinyunensis, revealed the existence of two conformations generated by a repeat-mediated recombination. Planta. 2021;254(2):36.
[[19]]
Hong Z, Liao X, Ye Y, et al.A complete mitochondrial genome for fragrant Chinese rosewood(Dalbergia odorifera, Fabaceae) with comparative analyses of genome structure and intergenomic sequence transfers. BMC Genomics. 2021;22(1):672.
[[20]]
Gao L, Xu W, Xin T, et al.Application of third-generation sequencing to herbal genomics. Front Plant Sci. 2023;14:1124536.
[[21]]
Kozik A, Rowan BA, Lavelle D, et al.The alternative reality of plant mitochondrial DNA: one ring does not rule them all. PLoS Genet. 2019;15(8):e1008373.
[[22]]
Smith DR, Keeling PJ.Mitochondrial and plastid genome architecture: reoccurring themes, but significant differences at the extremes. Proc Natl Acad Sci U S A. 2015;112(33):10177-10184.
[[23]]
Dong S, Chen L, Liu Y, et al.The draft mitochondrial genome of Magnolia biondii and mitochondrial phylogenomics of angiosperms. PLoS One. 2020;15(4):e0231020.
[[24]]
Qu XJ, Zhang XJ, Cao DL, et al.Plastid and mitochondrial phylogenomics reveal correlated substitution rate variation in Koenigia(Polygonoideae, Polygonaceae) and a reduced plastome for Koenigia delicatula including loss of all NDH genes. Mol Phylogenet Evol. 2022;174:107544.
[[25]]
Ślipiko M, Myszczyński K, Buczkowska K, et al.Super-mitobarcoding in plant species identification? It can work! The case of leafy liverworts belonging to the genus Calypogeia. Int J Mol Sci. 2022;23(24):15570.
[[26]]
Kojoma M, Kurihara K, Yamada K, et al.Genetic identification of cinnamon(Cinnamomum spp.) based on the trnL-trnF chloroplast DNA. Planta Med. 2002;68(1):94-96.
[[27]]
Li YX, Gong XH, Li Y, et al.The influence of Aconitum carmichaelii Debx. on the pharmacokinetic characteristics of main components in Rheum palmatum L. Phytother Res. 2015;29(8):1259-1264.
[[28]]
Arseneau JR, Steeves R, Laflamme M.Modified low-salt CTAB extraction of high-quality DNA from contaminant-rich tissues. Mol Ecol Resour. 2017;17(4):686-693.
[[29]]
Jin JJ, Yu WB, Yang JB, et al.GetOrganelle: a fast and versatile toolkit for accurate de novo assembly of organelle genomes. Genome Biol. 2020;21(1):241.
[[30]]
Altschul SF, Gish W, Miller W, et al.Basic local alignment search tool. J Mol Biol. 1990;215(3):403-410.
[[31]]
Chaisson MJ, Tesler G.Mapping single molecule sequencing reads using basic local alignment with successive refinement (BLASR): application and theory. BMC Bioinform. 2012;13:238.
[[32]]
Koren S, Walenz BP, Berlin K, et al.Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res. 2017;27(5):722-736.
[[33]]
Li H, Durbin R.Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25(14):1754-1760.
[[34]]
Walker BJ, Abeel T, Shea T, et al.Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One. 2014;9(11):e112963.
[[35]]
Kurtz S, Phillippy A, Delcher AL, et al.Versatile and open software for comparing large genomes. Genome Biol. 2004;5(2):R12.
[[36]]
Tillich M, Lehwark P, Pellizzer T, et al.GeSeq—versatile and accurate annotation of organelle genomes. Nucleic Acids Res. 2017;45(W1):W6-W11.
[[37]]
Greiner S, Lehwark P, Bock R.OrganellarGenomeDRAW (OGDRAW) version 1.3.1: expanded toolkit for the graphical visualization of organellar genomes. Nucleic Acids Res. 2019;47(W1):W59-W64.
[[38]]
Rice P, Longden I, Bleasby A.EMBOSS: theEuropean Molecular Biology Open Software Suite. Trends Genet. 2000;16(6):276-277.
[[39]]
Zhang D, Gao F, Jakovlić I, et al.PhyloSuite: an integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Mol Ecol Resour. 2020;20(1):348-355.
[[40]]
Rozewicki J, Li S, Amada KM, et al.MAFFT-DASH: integrated protein sequence and structural alignment. Nucleic Acids Res. 2019;47(W1):W5-W10.
[[41]]
Kalyaanamoorthy S, Minh BQ, Wong TKF, et al.ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14(6):587-589.
[[42]]
Ronquist F, Teslenko M, van der Mark P, et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61(3):539-542.
[[43]]
Gualberto JM, Newton KJ.Plant mitochondrial genomes: dynamics and mechanisms of mutation. Annu Rev Plant Biol. 2017;68:225-252.
[[44]]
Kim CK, Kim YK.The multipartite mitochondrial genome of Fallopia multiflora(Caryophyllales: Polygonaceae). Mitochondrial DNA B Resour. 2018;3(1):155-156.
[[45]]
Logacheva MD, Schelkunov MI, Fesenko AN, et al.Mitochondrial genome of Fagopyrum esculentum and the genetic diversity of extranuclear genomes in buckwheat. Plants (Basel). 2020;9(5):618.
[[46]]
Sloan DB, Alverson AJ, Storchová H, et al.Extensive loss of translational genes in the structurally dynamic mitochondrial genome of the angiosperm Silene latifolia. BMC Evol Biol. 2010;10:274.
[[47]]
Sloan DB, Alverson AJ, Chuckalovcak JP, et al.Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biol. 2012;10(1):e1001241.
[[48]]
Krüger M, Juříček OAJ, Abeyawardana M, et al. Variation in plastid genomes in the gynodioecious species Silene vulgaris. BMC Plant Biol. 2019;19(1):568.
[[49]]
Štorchová H, Stone JD, Sloan DB, et al.Homologous recombination changes the context of Cytochrome b transcription in the mitochondrial genome of Silene vulgarisKRA. BMC Genomics. 2018;19(1):874.
[[50]]
Sloan DB, Müller K, McCauley DE, et al. Intraspecific variation in mitochondrial genome sequence, structure, and gene content in Silene vulgaris, an angiosperm with pervasive cytoplasmic male sterility. New Phytol. 2012;196(4):1228-1239.
[[51]]
Sloan DB, Alverson AJ, Wu M, et al.Recent acceleration of plastid sequence and structural evolution coincides with extreme mitochondrial divergence in the angiosperm genus Silene. Genome Biol Evol. 2012;4(3):294-306.
[[52]]
GROUP TAP.An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc. 2009;161(2):105-121.
[[53]]
Skippington E, Barkman TJ, Rice DW, et al.Miniaturized mitogenome of the parasitic plant Viscum scurruloideum is extremely divergent and dynamic and has lost all NAD genes. Proc Natl Acad Sci U S A. 2015;112(27):E3515-E3524.
[[54]]
Shi Y, Liu Y, Zhang S, et al.Assembly and comparative analysis of the complete mitochondrial genome sequence of Sophora japonica “JinhuaiJ2”. PLoS One. 2018;13(8):e0202485.
[[55]]
Li RJ, W L, Xin TY, et al. Analysis of chloroplast genomes and development of specific DNA barcodes for identifying the original species of Rhei Radix etRhizoma. Acta Pharmaceutica Sinica. 2022;57(5):1495-1505.
[[56]]
Wolfe KH, Li WH, Sharp PM.Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclearDNAs. Proc Natl Acad Sci USA. 1987;84(24):9054-9058.
[[57]]
Drouin G, Daoud H, Xia J.Relative rates of synonymous substitutions in the mitochondrial, chloroplast and nuclear genomes of seed plants. Mol Phylogenet Evol. 2008;49(3):827-831.

RIGHTS & PERMISSIONS

2023 Acupuncture and Herbal Medicine
PDF(1520 KB)

Accesses

Citations

Detail

Sections
Recommended

/