Comparative analysis of mitochondrial genomes of Schisandra repanda and Kadsura japonica

The family Schisandraceae is a basal angiosperm plant group distributed in East and Southeast Asia and includes many medicinal plant species such as Schisandra chinensis. In this study, mitochondrial genomes (mitogenomes) of two species, Schisandra repanda and Kadsura japonica, in the family were characterized through de novo assembly using sequencing data obtained with Oxford Nanopore and Illumina sequencing technologies. The mitogenomes of S. repanda were assembled into one circular contig (571,107 bp) and four linear contigs (10,898–607,430 bp), with a total of 60 genes: 38 protein-coding genes (PCGs), 19 tRNA genes, and 3 rRNA genes. The mitogenomes of K. japonica were assembled into five circular contigs (211,474–973,503 bp) and three linear contigs (8,010–72,712 bp), with a total of 66 genes: 44 PCGs, 19 tRNA genes, and 3 rRNA genes. The mitogenomes of the two species had complex structural features with high repeat numbers and chloroplast-derived sequences, as observed in other plant mitogenomes. Phylogenetic analysis based on PCGs revealed the taxonomical relationships of S. repanda and K. japonica with other species from Schisandraceae. Finally, molecular markers were developed to distinguish between S. repanda, K. japonica, and S. chinensis on the basis of InDel polymorphisms present in the mitogenomes. The mitogenomes of S. repanda and K. japonica will be valuable resources for molecular and taxonomic studies of plant species that belong to the family Schisandraceae.

[1]  Yicun Chen,et al.  Assembly and comparative analysis of the complete mitochondrial genome of Salix wilsonii using PacBio HiFi sequencing , 2022, Frontiers in Plant Science.

[2]  Shihai Yang,et al.  Analysis of Floral Organ Development and Sex Determination in Schisandra chinensis by Scanning Electron Microscopy and RNA-Sequencing , 2022, Life.

[3]  Yingjuan Su,et al.  The Complete Mitochondrial Genome of Ophioglossum vulgatum L. Is with Highly Repetitive Sequences: Intergenomic Fragment Transfer and Phylogenetic Analysis , 2022, Genes.

[4]  Xiangdong Yang,et al.  Complete mitochondrial genome sequence and comparative analysis of the cultivated yellow nutsedge , 2022, The plant genome.

[5]  Guo Chen,et al.  De novo assembly of the complete mitochondrial genome of sweet potato (Ipomoea batatas [L.] Lam) revealed the existence of homologous conformations generated by the repeat-mediated recombination , 2022, BMC Plant Biology.

[6]  Y. Ni,et al.  De novo assembly of the complete mitochondrial genome of sweet potato (Ipomoea batatas [L.] Lam) revealed the existence of homologous conformations generated by the repeat-mediated recombination , 2022, BMC Plant Biology.

[7]  Haiyan Li,et al.  Integration of full-length transcriptomes and anthocyanin metabolite analysis for understanding fruit coloration mechanism in Schisandra chinensis , 2022, Physiology and Molecular Biology of Plants.

[8]  Masanori Arita,et al.  Mitochondrial genome of Garcinia mangostana L. variety Mesta , 2022, Scientific Reports.

[9]  C. P. Hong,et al.  Long-read transcriptome sequencing provides insight into lignan biosynthesis during fruit development in Schisandra chinensis , 2022, BMC Genomics.

[10]  Guoxiang Liu,et al.  RNA Editing and Its Roles in Plant Organelles , 2021, Frontiers in Genetics.

[11]  Yuxiao Wang,et al.  Assembly and comparative analysis of the first complete mitochondrial genome of Acer truncatum Bunge: a woody oil-tree species producing nervonic acid , 2021, BMC Plant Biology.

[12]  C. P. Hong,et al.  Development of Chloroplast-based InDel Markers for the Discrimination of Schisandraceae Plant Species , 2021 .

[13]  P. Gao,et al.  Comparative analysis of nuclear, chloroplast, and mitochondrial genomes of watermelon and melon provides evidence of gene transfer , 2021, Scientific Reports.

[14]  Lihui Men,et al.  Pharmacodynamic effects and molecular mechanisms of lignans from Schisandra chinensis Turcz. (Baill.), a current review. , 2020, European journal of pharmacology.

[15]  Yuan Qin,et al.  Assembly and comparative analysis of the complete mitochondrial genome of Suaeda glauca , 2020, BMC Genomics.

[16]  Ju sung Kim,et al.  A Study on the Native Environment and Cutting Propagation for the Black-berry Magnolia Vine [Schisandra repanda (Siebold & Zucc.) Radlk] in Halla Mountain , 2020 .

[17]  Yan Yan,et al.  Candidate genes involved in the biosynthesis of lignan in Schisandra chinensis fruit based on transcriptome and metabolomes analysis. , 2020, Chinese journal of natural medicines.

[18]  Liang Xu,et al.  Comparative Analysis of the Mitochondrial Genome Sequences of two Medicinal Plants: Arctium Lappa and A. Tomentosum , 2020 .

[19]  E. H. Honorio Coronado,et al.  Nuclear and plastidial SNP and INDEL markers for genetic tracking studies of Jacaranda copaia , 2019, Conservation Genetics Resources.

[20]  Soo-Jin Kwon,et al.  The complete mitochondrial genome sequence of Schisandra chinensis (Austrobaileyales: Schisandraceae) , 2019, Mitochondrial DNA. Part B, Resources.

[21]  M. Chu,et al.  Genetic diversity estimation of Yunnan indigenous goat breeds using microsatellite markers , 2019, Ecology and evolution.

[22]  Dawei Li,et al.  Evolution and Diversification of Kiwifruit Mitogenomes through Extensive Whole-Genome Rearrangement and Mosaic Loss of Intergenic Sequences in a Highly Variable Region , 2019, Genome biology and evolution.

[23]  R. Michelmore,et al.  The alternative reality of plant mitochondrial DNA: One ring does not rule them all , 2019, bioRxiv.

[24]  Wei Tang,et al.  Molecular and Functional Diversity of RNA Editing in Plant Mitochondria , 2018, Molecular Biotechnology.

[25]  S. Dong,et al.  The complete mitochondrial genome of the early flowering plant Nymphaea colorata is highly repetitive with low recombination , 2018, BMC Genomics.

[26]  A. Christensen,et al.  Repeats of Unusual Size in Plant Mitochondrial Genomes: Identification, Incidence and Evolution , 2018, G3: Genes, Genomes, Genetics.

[27]  V. Knoop,et al.  Plant organelle RNA editing and its specificity factors: enhancements of analyses and new database features in PREPACT 3.0 , 2018, BMC Bioinformatics.

[28]  Changwei Bi,et al.  The complete mitochondrial genome sequence of an alpine plant Arabis alpina , 2018, Mitochondrial DNA. Part B, Resources.

[29]  Fei Liu,et al.  A review of polysaccharides from Schisandra chinensis and Schisandra sphenanthera: Properties, functions and applications. , 2018, Carbohydrate polymers.

[30]  Nan Zhao,et al.  The Roles of Mitochondrion in Intergenomic Gene Transfer in Plants: A Source and a Pool , 2018, International journal of molecular sciences.

[31]  Kazutaka Katoh,et al.  MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization , 2017, Briefings Bioinform..

[32]  Yul-Ho Kim,et al.  Chromosome Reshuffling Patterns of Korean Soybean Cultivars using Genome-wide 202 InDel Markers , 2017 .

[33]  Jerrold I. Davis,et al.  Mitochondrial genome evolution in Alismatales: Size reduction and extensive loss of ribosomal protein genes , 2017, PloS one.

[34]  Axel Fischer,et al.  GeSeq – versatile and accurate annotation of organelle genomes , 2017, Nucleic Acids Res..

[35]  A. Simpson,et al.  Mitochondrial Genome Evolution and a Novel RNA Editing System in Deep-Branching Heteroloboseids , 2017, Genome biology and evolution.

[36]  J. Gualberto,et al.  Plant Mitochondrial Genomes: Dynamics and Mechanisms of Mutation. , 2017, Annual review of plant biology.

[37]  Uwe Scholz,et al.  MISA-web: a web server for microsatellite prediction , 2017, Bioinform..

[38]  M. Sanchez-Puerta,et al.  Foreign Plastid Sequences in Plant Mitochondria are Frequently Acquired Via Mitochondrion-to-Mitochondrion Horizontal Transfer , 2017, Scientific Reports.

[39]  A. Paterson,et al.  Analysis of the Complete Mitochondrial Genome Sequence of the Diploid Cotton Gossypium raimondii by Comparative Genomics Approaches , 2016, BioMed research international.

[40]  Yi Ding,et al.  The mitochondrial genome map of Nelumbo nucifera reveals ancient evolutionary features , 2016, Scientific Reports.

[41]  Wei Guo,et al.  Extraction and Separation of Active Ingredients in Schisandra chinensis (Turcz.) Baill and the Study of their Antifungal Effects , 2016, PloS one.

[42]  Maureen R. Hanson,et al.  RNA Recognition Motif-Containing Protein ORRM4 Broadly Affects Mitochondrial RNA Editing and Impacts Plant Development and Flowering1[OPEN] , 2015, Plant Physiology.

[43]  Sang-Choon Lee,et al.  Complete chloroplast and ribosomal sequences for 30 accessions elucidate evolution of Oryza AA genome species , 2015, Scientific Reports.

[44]  J. Palmer,et al.  Miniaturized mitogenome of the parasitic plant Viscum scurruloideum is extremely divergent and dynamic and has lost all nad genes , 2015, Proceedings of the National Academy of Sciences.

[45]  K. Gao,et al.  New lignans from the roots of Schisandra sphenanthera. , 2015, Fitoterapia.

[46]  Hwan-Hee Jang,et al.  Changes in Antioxidant and Antimicrobial Activities of Schizandra chinensis Baillon under Different Solvent Extraction , 2014 .

[47]  Daniel B. Sloan,et al.  History of Plastid DNA Insertions Reveals Weak Deletion and AT Mutation Biases in Angiosperm Mitochondrial Genomes , 2014, Genome biology and evolution.

[48]  P. Pinton,et al.  The Mitochondrial Permeability Transition Pore and Cancer: Molecular Mechanisms Involved in Cell Death , 2014, Front. Oncol..

[49]  P. Xiao,et al.  Genus Kadsura, a good source with considerable characteristic chemical constituents and potential bioactivities. , 2014, Phytomedicine : international journal of phytotherapy and phytopharmacology.

[50]  C. Park,et al.  Cuttings for Mass Propagation Affecting the Impact of Increasing Reproductive Efficiency of Schisandra chinensis , 2014 .

[51]  J. Gualberto,et al.  The plant mitochondrial genome: dynamics and maintenance. , 2014, Biochimie.

[52]  Chunyi Zhang,et al.  The Arabidopsis thaliana RNA editing factor SLO2, which affects the mitochondrial electron transport chain, participates in multiple stress and hormone responses. , 2014, Molecular plant.

[53]  Alexandros Stamatakis,et al.  RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies , 2014, Bioinform..

[54]  Andrew J. Alverson,et al.  Horizontal Transfer of Entire Genomes via Mitochondrial Fusion in the Angiosperm Amborella , 2013, Science.

[55]  Axel Brennicke,et al.  RNA editing in plants and its evolution. , 2013, Annual review of genetics.

[56]  B. Moon,et al.  Development of RAPD-Derived SCAR Markers and Multiplex-PCR for Authentication of the Schisandrae Fructus , 2013 .

[57]  Andrew J. Alverson,et al.  The “fossilized” mitochondrial genome of Liriodendron tulipifera: ancestral gene content and order, ancestral editing sites, and extraordinarily low mutation rate , 2013, BMC Biology.

[58]  K. Katoh,et al.  MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability , 2013, Molecular biology and evolution.

[59]  Henning Lenz,et al.  PREPACT 2.0: Predicting C-to-U and U-to-C RNA Editing in Organelle Genome Sequences with Multiple References and Curated RNA Editing Annotation , 2013, Bioinformatics and biology insights.

[60]  B. Faircloth,et al.  Primer3—new capabilities and interfaces , 2012, Nucleic acids research.

[61]  Joo-Hwan Kim,et al.  Molecular identification of Schisandra chinensis and its allied species using multiplex PCR based on SNPs , 2012, Genes & Genomics.

[62]  Haiyan Zhang,et al.  ParaAT: a parallel tool for constructing multiple protein-coding DNA alignments. , 2012, Biochemical and biophysical research communications.

[63]  M. Rousseau-Gueutin,et al.  Plastid sequences contribute to some plant mitochondrial genes. , 2012, Molecular biology and evolution.

[64]  Andrew J. Alverson,et al.  Rapid Evolution of Enormous, Multichromosomal Genomes in Flowering Plant Mitochondria with Exceptionally High Mutation Rates , 2012, PLoS biology.

[65]  Matthew Berriman,et al.  Artemis: an integrated platform for visualization and analysis of high-throughput sequence-based experimental data , 2011, Bioinform..

[66]  Andrew J. Alverson,et al.  Origins and Recombination of the Bacterial-Sized Multichromosomal Mitochondrial Genome of Cucumber[C][W] , 2011, Plant Cell.

[67]  C. Kim,et al.  Simultaneous determination of nine lignans using pressurized liquid extraction and HPLC-DAD in the fruits of Schisandra chinensis , 2010 .

[68]  Andrew J. Alverson,et al.  Insights into the evolution of mitochondrial genome size from complete sequences of Citrullus lanatus and Cucurbita pepo (Cucurbitaceae). , 2010, Molecular biology and evolution.

[69]  Henning Lenz,et al.  Introducing the plant RNA editing prediction and analysis computer tool PREPACT and an update on RNA editing site nomenclature , 2010, Current Genetics.

[70]  D. Severson,et al.  Genome-based polymorphic microsatellite development and validation in the mosquito Aedes aegypti and application to population genetics in Haiti , 2009, BMC Genomics.

[71]  A. Christensen,et al.  Diversity of the Arabidopsis Mitochondrial Genome Occurs via Nuclear-Controlled Recombination Activity , 2009, Genetics.

[72]  J. Palmer,et al.  Fine-scale mergers of chloroplast and mitochondrial genes create functional, transcompartmentally chimeric mitochondrial genes , 2009, Proceedings of the National Academy of Sciences.

[73]  G. Drouin,et al.  Relative rates of synonymous substitutions in the mitochondrial, chloroplast and nuclear genomes of seed plants. , 2008, Molecular phylogenetics and evolution.

[74]  Yu-Wei Wu,et al.  The mitochondrial genome of the gymnosperm Cycas taitungensis contains a novel family of short interspersed elements, Bpu sequences, and abundant RNA editing sites. , 2008, Molecular biology and evolution.

[75]  Ralph Bock,et al.  OrganellarGenomeDRAW (OGDRAW): a tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes , 2007, Current Genetics.

[76]  Yu-Wei Wu,et al.  Transfer of chloroplast genomic DNA to mitochondrial genome occurred at least 300 MYA. , 2007, Molecular biology and evolution.

[77]  C. Lemieux,et al.  An unexpectedly large and loosely packed mitochondrial genome in the charophycean green alga Chlorokybus atmophyticus , 2007, BMC Genomics.

[78]  Jun Li,et al.  KaKs_Calculator: Calculating Ka and Ks Through Model Selection and Model Averaging , 2007, Genom. Proteom. Bioinform..

[79]  M. Whiting,et al.  A mitochondrial genome phylogeny of Diptera: whole genome sequence data accurately resolve relationships over broad timescales with high precision , 2007 .

[80]  Justin C. Fay,et al.  Sequence divergence, functional constraint, and selection in protein evolution. , 2003, Annual review of genomics and human genetics.

[81]  M. W. Gray,et al.  Diversity and Evolution of Mitochondrial RNA Editing Systems , 2003, IUBMB life.

[82]  Y. Notsu,et al.  The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants , 2002, Molecular Genetics and Genomics.

[83]  I. Leitch,et al.  DNA C-values in seven families fill phylogenetic gaps in the basal angiosperms , 2002 .

[84]  P. Vandenabeele,et al.  The role of mitochondrial factors in apoptosis: a Russian roulette with more than one bullet , 2002, Cell Death and Differentiation.

[85]  L. Hurst The Ka/Ks ratio: diagnosing the form of sequence evolution. , 2002, Trends in genetics : TIG.

[86]  J. Palmer,et al.  Inaugural Article: Punctuated evolution of mitochondrial gene content: High and variable rates of mitochondrial gene loss and transfer to the nucleus during angiosperm evolution , 2002 .

[87]  M. Morgante,et al.  Microsatellites are preferentially associated with nonrepetitive DNA in plant genomes , 2002, Nature Genetics.

[88]  J. Stoye,et al.  REPuter: the manifold applications of repeat analysis on a genomic scale. , 2001, Nucleic acids research.

[89]  J. Palmer,et al.  Multiple losses and transfers to the nucleus of two mitochondrial succinate dehydrogenase genes during angiosperm evolution. , 2001, Genetics.

[90]  Yangrae Cho,et al.  Dynamic evolution of plant mitochondrial genomes: mobile genes and introns and highly variable mutation rates. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[91]  Guido Kroemer,et al.  Mitochondrial control of cell death , 2000, Nature Medicine.

[92]  Wei Qian,et al.  Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. , 2000, Molecular biology and evolution.

[93]  Mark W. Chase,et al.  The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes , 1999, Nature.

[94]  M. Nakazono,et al.  Transcription of plastid-derived tRNA genes in rice mitochondria , 1998, Current Genetics.

[95]  M. Hasegawa,et al.  Gene transfer to the nucleus and the evolution of chloroplasts , 1998, Nature.

[96]  S. Backert,et al.  The mystery of the rings: structure and replication of mitochondrial genomes from higher plants , 1997 .

[97]  N. Tsutsumi,et al.  A chloroplast-derived sequence is utilized as a source of promoter sequences for the gene for subunit 9 of NADH dehydrogenase (nad9) in rice mitochondria , 1996, Molecular and General Genetics MGG.

[98]  Michele Morgante,et al.  The comparison of RFLP, RAPD, AFLP and SSR (microsatellite) markers for germplasm analysis , 1996, Molecular Breeding.

[99]  K. Oda,et al.  Gene clusters for ribosomal proteins in the mitochondrial genome of a liverwort, Marchantia polymorpha. , 1992, Nucleic acids research.

[100]  G. Igloi,et al.  Editing of a chloroplast mRNA by creation of an initiation codon , 1991, Nature.

[101]  Michael W. Gray,et al.  RNA editing in plant mitochondria , 1989, Nature.

[102]  C. Epstein,et al.  Familial mitochondrial encephalomyopathy (MERRF): Genetic, pathophysiological, and biochemical characterization of a mitochondrial DNA disease , 1988, Cell.

[103]  Yul-Ho Kim,et al.  Genetic Identification and Phylogenic Analysis of New Varieties and 149 Korean Cultivars using 27 InDel Markers Selected from Dense Variation Blocks in Soybean (Glycine max (L.) Merrill) , 2019 .

[104]  Jeffrey P. Mower,et al.  Complete mitochondrial genomes from the ferns Ophioglossum californicum and Psilotum nudum are highly repetitive with the largest organellar introns. , 2017, The New phytologist.

[105]  Jeffrey P. Mower,et al.  Plant Mitochondrial Genome Diversity: The Genomics Revolution , 2012 .

[106]  S. Renner,et al.  Horizontal Gene Transfer in Eukaryotes: Fungi-to-Plant and Plant-to-Plant Transfers of Organellar DNA , 2012 .

[107]  G. Benson,et al.  Tandem repeats finder: a program to analyze DNA sequences. , 1999, Nucleic acids research.

[108]  B F Lang,et al.  Mitochondrial genome evolution and the origin of eukaryotes. , 1999, Annual review of genetics.

[109]  A. Brennicke,et al.  The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides , 1997, Nature Genetics.

[110]  K. Newton Plant Mitochondrial Genomes: Organization, Expression and Variation , 1988 .