Skip to main content
Log in

Assembly of Satsuma mandarin mitochondrial genome and identification of cytoplasmic male sterility–specific ORFs in a somatic cybrid of pummelo

  • Original Article
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

Cytoplasmic male sterility (CMS) and seedlessness are highly desirable traits for citrus. However, a high-quality reference mitochondrial genome of citrus is unavailable, and the mechanisms of CMS remain to be elucidated in citrus. We previously generated a male sterile somatic cybrid of pummelo (G1+HBP) by fusing protoplasts from CMS ‘Guoqing No. 1’ Satsuma mandarin (G1) and fertile ‘Hirado Buntan’ pummelo (HBP). Here, we sequenced and assembled the mitochondrial genome of G1, G1+HBP, and HBP into circular molecules of 521.6 kb, 538.4 kb, and 518.3 kb, respectively. Mitochondrial genome of citrus encodes 35–36 proteins, three ribosomal RNAs, and 21 tRNAs. Comparative analysis indicated that nuclear genome and chloroplast genome of the cybrid are from HBP, whereas the mitochondrial genome sequences of the cybrid and G1 have 96.9% synteny, and that the cybrid has an extra recombinant mitochondrial DNA fragment of only 16.8 kb. Compared with the fertile HBP mitochondrial genome, 21 and 20 CMS-specific mitotype-specific sequences (MSSs), and 89 and 70 CMS-specific ORFs were identified in the cybrid and G1 mitochondrial genomes, respectively. Among them, 57 ORFs that co-transcribed with the same mitochondrial genes in the cybrid and G1 were identified as the CMS-specific ORFs. The assembly of mitochondrial genomes and the identification of the CMS-specific ORFs provide basis for determination of the CMS-associated gene and elucidation of CMS mechanisms in citrus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aleza P, Garcialor A, Juarez J, Navarro L (2016) Recovery of citrus cybrid plants with diverse mitochondrial and chloroplastic genome combinations by protoplast fusion followed by in vitro shoot, root, or embryo micro grafting. Plant Cell Tiss Org 126:205–217

    Article  CAS  Google Scholar 

  • Alverson AJ, Wei X, Rice DW, Stern DB, Barry K, Palmer JD (2010) Insights into the evolution of mitochondrial genome size from complete sequences of Citrullus lanatus and Cucurbita pepo (Cucurbitaceae). Mol Biol Evol 27:1436–1448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bausher MG, Singh ND, Lee SB, Jansen RK, Daniell H (2006) The complete chloroplast genome sequence of Citrus sinensis (L.) Osbeck var ‘Ridge Pineapple’: organization and phylogenetic relationships to other angiosperms. BMC Plant Biol 6:21

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cai XD, Fu J, Deng XX, Guo WW (2007) Production and molecular characterization of potential seedless cybrid plants between pollen sterile Satsuma mandarin and two seedy Citrus cultivars. Plant Cell Tissue Organ Cult 90:275–283

    Article  Google Scholar 

  • Chen LT, Liu YG (2014) Male sterility and fertility restoration in crops. Annu Rev Plant Biol 65:579–606

    Article  CAS  PubMed  Google Scholar 

  • Chen Z, Zhao N, Li S, Grover CE, Nie H, Wendel JF, Hua J (2017) Plant mitochondrial genome evolution and cytoplasmic male sterility. Crit Rev Plant Sci 36:55–69

    Article  Google Scholar 

  • Cheng YJ, Yi HL, Pang XM, Guo WW, Deng XX (2001) An efficient method for genomic DNA extraction from woody fruit plants. J Huazhong Agric Univ 20:481–483

    CAS  Google Scholar 

  • Cingolani P, Platts A, Wang LL, Coon M, Nguyen T, Wang L, Land SJ, Lu X, Ruden DM (2012) A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 6:80–92

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cole LW, Guo W, Mower JP, Palmer JD (2018) High and variable rates of repeat-mediated mitochondrial genome rearrangement in a genus of plants. Mol Biol Evol 35:2773–2785

    CAS  PubMed  Google Scholar 

  • Dambier D, Benyahia H, PensabeneBellavia G, AkaKacar Y, Froelicher Y, Belfalah Z, Beniken L, Handaji N, Printz B, Morillon R, Yesiloglu T, Navarro L, Ollitrault P (2011) Somatic hybridization for citrus rootstock breeding: an effective tool to solve important issues of the Mediterranean citrus industry. Plant Cell Rep 30:883–900

    Article  CAS  PubMed  Google Scholar 

  • Donoso JM, Eduardo I, Picanol R, Batlle I, Howad W, Aranzana MJ, Arus P (2015) High-density mapping suggests cytoplasmic male sterility with two restorer genes in almond × peach progenies. Hortic Res 2:15016

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fang YN, Qiu WM, Wang Y, Wu XM, Xu Q, Guo WW (2014) High-throughput sequencing and degradome analysis reveal altered expression of miRNAs and their targets in a male-sterile cybrid pummelo (Citrus grandis). BMC Genomics 17:591

    Article  CAS  Google Scholar 

  • Fang YN, Zheng BB, Wang L, Yang W, Wu XM, Xu Q, Guo WW (2016) Identification of differentially expressed microRNAs from a male sterile Ponkan mandarin (Citrus reticulata Blanco) and its fertile wild type by small RNA and degradome sequencing. Tree Genet Genomes 10:1567–1581

    Article  Google Scholar 

  • Forde BG, Oliver RJ, Leaver CJ (1978) Variation in mitochondrial translation products associated with male-sterile cytoplasms in maize. Proc Natl Acad Sci 75:3841–3845

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujii S, Toda T, Kikuchi S, Suzuki R, Yokoyama K, Tsuchida H, Yano K, Toriyama K (2011) Transcriptome map of plant mitochondria reveals islands of unexpected transcribed regions. BMC Genomics 12:279

    Article  PubMed  PubMed Central  Google Scholar 

  • Garcia LE, Zubko MK, Zubko EI, Sanchezpuerta MV (2019) Elucidating genomic patterns and recombination events in plant cybrid mitochondria. Plant Mol Biol 100:433–450

    Article  CAS  PubMed  Google Scholar 

  • Goremykin VV, Salamini F, Velasco R, Viola R (2009) Mitochondrial DNA of Vitis vinifera and the issue of rampant horizontal gene transfer. Mol Biol Evol 26:99–110

    Article  CAS  PubMed  Google Scholar 

  • Goremykin VV, Lockhart PJ, Viola R, Velasco R (2012) The mitochondrial genome of Malus domestica and the import-driven hypothesis of mitochondrial genome expansion in seed plants. Plant J 71:615–626

    Article  CAS  PubMed  Google Scholar 

  • Goto S, Yoshioka T, Ohta S, Kita M, Hamada H, Shimizu T (2016) Segregation and heritability of male sterility in populations derived from progeny of Satsuma mandarin. PLoS One 11:e0162408

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Goto S, Yoshioka T, Ohta S, Kita M, Hamada H, Shimizu T (2018) QTL mapping of male sterility and transmission pattern in progeny of Satsuma mandarin. PLoS One 13:e0200844

    Article  PubMed  PubMed Central  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, LindbladToh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grosser JW, Ollitrault P, Olivaresfuster O (2000) Somatic hybridization in citrus: an effective tool to facilitate variety improvement. In Vitro Cell Dev-Pl 36:434–449

    Article  Google Scholar 

  • Gualberto JM, Newton KJ (2017) Plant mitochondrial genomes: dynamics and mechanisms of mutation. Annu Rev Plant Biol 68:225–252

    Article  CAS  PubMed  Google Scholar 

  • Guo WW, Cheng YJ, Deng XX (2002) Regeneration and molecular characterization of intergeneric somatic hybrids between Citrus reticulata and Poncirus trifoliata. Plant Cell Rep 20:829–834

    Article  CAS  Google Scholar 

  • Guo WW, Prasad D, Cheng YJ, Serrano P, Deng XX, Grosser JW (2004) Targeted cybridization in citrus: transfer of Satsuma cytoplasm to seedy cultivars for potential seedlessness. Plant Cell Rep 22:752–758

    Article  CAS  PubMed  Google Scholar 

  • Guo WW, Xiao SX, Deng XX (2013) Somatic cybrid production via protoplast fusion for citrus improvement. Sci Hortic 163:20–26

    Article  Google Scholar 

  • Haas BJ, Delcher AL, Mount SM, Wortman JR, Smith RK Jr, Hannick LI, Maiti R, Ronning CM, Rusch DB, Town CD, Salzberg SL, White O (2003) Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Res 31:5654–5666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hanson MR, Bentolila S (2004) Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16:S154–S169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harris RS (2007) Improved pairwise alignment of genomic DNA. Ph.D. Thesis, The Pennsylvania State University

  • Hu ZY, Tong Z, Wei J, Yi HL, Deng XX (2006) Mitochondrial gene expression in stamens is differentially regulated during male gametogenesis in Citrus unshiu. J Hortic Sci Biotechnol 81:565–569

    Article  CAS  Google Scholar 

  • Jing B, Heng SP, Tong D, Wan ZJ, Fu TD, Tu JX, Ma CZ, Yi B, Wen J, Shen JX (2012) A male sterility-associated cytotoxic protein ORF288 in Brassica juncea causes aborted pollen development. J Exp Bot 63:1285–1295

    Article  CAS  PubMed  Google Scholar 

  • Kim B, Yang T, Kim S (2019) Identification of a gene responsible for cytoplasmic male-sterility in onions (Allium cepa L.) using comparative analysis of mitochondrial genome sequences of two recently diverged cytoplasms. Theor Appl Genet 132:313–322

    Article  CAS  PubMed  Google Scholar 

  • Kim YJ, Zhang D (2018) Molecular control of male fertility for crop hybrid breeding. Trends Plant Sci 23:53–65

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi S, Ohgawara T, Fujiwara K, Oiyama I (1991) Analysis of cytoplasmic genomes in somatic hybrids between navel orange (Citrus sinensis Osb.) and ‘Murcott’ tangor. Theor Appl Genet 82:6–10

    Article  CAS  PubMed  Google Scholar 

  • Kubo T, Newton KJ (2008) Angiosperm mitochondrial genomes and mutations. Mitochondrion 8:5–14

    Article  CAS  PubMed  Google Scholar 

  • Li H (2013) Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv preprint 1303:3997

    Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li S, Chen Z, Zhao N, Wang Y, Nie H, Hua J (2018) The comparison of four mitochondrial genomes reveals cytoplasmic male sterility candidate genes in cotton. BMC Genomics 19:775

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lilly JW, Harvey MJ (2001) Small, repetitive DNAs contribute significantly to the expanded mitochondrial genome of cucumber. Genetics 159:317–328

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu YZ, Liu Q, Tao NG, Deng XX (2006) Efficient isolation of RNA from fruit peel and pulp of ripening navel orange (Citrus sinensis Osbeck). J Huazhong Agric Univ 25:300–304 (in Chinese with English abstract)

    CAS  Google Scholar 

  • Lohse M, Drechsel O, Kahlau S, Bock R (2013) OrganellarGenomeDRAW—a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets. Nucleic Acids Res 41:W575–W581

    Article  PubMed  PubMed Central  Google Scholar 

  • Luo D, Xu H, Liu Z, Guo J, Li H, Chen L, Fang C, Zhang Q, Bai M, Yao N, Wu H, Wu H, Ji C, Zheng H, Chen Y, Shan Y, Li X, Zhao X, Li R, Liu YG (2013) A detrimental mitochondrial-nuclear interaction causes cytoplasmic male sterility in rice. Nat Genet 45:573–577

    Article  CAS  PubMed  Google Scholar 

  • Murashige T, Tucker DPH (1969) Growth factor requirement of citrus tissue cultures. In: Proceedings of the First International Citrus Symposium. University of California, Riverside, pp 1155–1161

    Google Scholar 

  • Ngangkham U, Parida SK, De S, Kumar KA, Singh AK, Singh NK, Mohapatra T (2010) Genic markers for wild abortive (WA) cytoplasm based male sterility and its fertility restoration in rice. Mol Breed 26:275–292

    Article  CAS  Google Scholar 

  • Okonechnikov K, Golosova O, Fursov M, the UGENE team (2012) Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics 28:1166–1167

    Article  CAS  PubMed  Google Scholar 

  • Omura M, Shimada T (2016) Citrus breeding, genetics and genomics in Japan. Breed Sci 66:3–17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pertea M, Kim D, Pertea G, Leek JT, Salzberg SL (2016) Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat Protoc 11:1650–1667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richardson AO, Palmer JD (2007) Horizontal gene transfer in plants. J Exp Bot 58:1–9

    Article  CAS  PubMed  Google Scholar 

  • Sanchezpuerta MV, Zubko MK, Palmer JD (2015) Homologous recombination and retention of a single form of most genes shape the highly chimeric mitochondrial genome of a cybrid plant. New Phytol 206:381–396

    Article  CAS  Google Scholar 

  • Tanaka Y, Tsuda M, Yasumoto K, Yamagishi H, Terachi T (2012) A complete mitochondrial genome sequence of Ogura-type male-sterile cytoplasm and its comparative analysis with that of normal cytoplasm in radish (Raphanus sativus L.). BMC Genomics 13:352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang H, Zheng X, Li C, Xie X, Chen Y, Chen L, Zhao X, Zheng H, Zhou J, Ye S, Guo J, Liu YG (2017) Multi-step formation, evolution, and functionalization of new cytoplasmic male sterility genes in the plant mitochondrial genomes. Cell Res 27:130–146

    Article  CAS  PubMed  Google Scholar 

  • Unseld M, Marienfeld J, Brandt P, Brennicke A (1997) The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat Genet 15:57–61

    Article  CAS  PubMed  Google Scholar 

  • Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, Cuomo CA, Zeng Q, Wortman J, Young SK, Earl AM (2014) Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 9:e112963

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang J, Jiang J, Li X, Li A, Zhang Y, Guan R, Wang Y (2012) Complete sequence of heterogenous-composition mitochondrial genome (Brassica napus) and its exogenous source. BMC Genomics 13:675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L, Pan ZY, Guo WW (2010) Proteomic analysis of leaves from a diploid cybrid produced by protoplast fusion between Satsuma mandarin and pummelo. Plant Cell Tissue Organ Cult 103:165–174

    Article  CAS  Google Scholar 

  • Wang R, Fang YN, Wu XM, Qing M, Li CC, Xie KD, Deng XX, Guo WW (2020) The miR399- CsUBC24 module regulates reproductive development and male fertility in citrus. Plant Physiol 183:1681–1695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Xu YT, Zhang SQ, Cao L, Huang Y, Cheng JF, Wu GZ, Tian SL, Chen CL, Liu Y, Yu HW, Yang XM, Lan H, Wang N, Wang L, Xu JD, Jiang XL, Xie ZZ, Tan ML, Larkin RM, Chen LL, Ma BG, Ruan YJ, Deng XX, Xu Q (2017) Genomic analyses of primitive, wild and cultivated citrus provide insights into asexual reproduction. Nat Genet 49:765–772

    Article  CAS  PubMed  Google Scholar 

  • Xiao SX, Biswas MK, Li M, Deng XX, Xu Q, Guo WW (2014) Production and molecular characterization of diploid and tetraploid somatic cybrid plants between male sterile Satsuma mandarin and seedy sweet orange cultivars. Plant Cell Tissue Organ Cult 116:81–88

    Article  CAS  Google Scholar 

  • Xie H, Wang J, Qian M, Li N, Zhu Y, Li S (2014) Mitotype-specific sequences related to cytoplasmic male sterility in Oryza species. Mol Breed 33:803–811

    Article  Google Scholar 

  • Xie H, Peng X, Qian M, Cai Y, Ding X, Chen Q, Cai Q, Zhu Y, Yan L, Cai Y (2018) The chimeric mitochondrial gene orf182 causes non-pollen-type abortion in Dongxiang cytoplasmic male-sterile rice. Plant J 95:715–726

    Article  CAS  Google Scholar 

  • Xu Q, Chen LL, Ruan X, Chen DJ, Zhu AD, Chen CL, Bertrand D, Jiao WB, Hao BH, Lyon MP, Chen JJ, Gao S, Xing F, Lan H, Chang JW, Ge XH, Lei Y, Hu Q, Miao Y, Wang L, Xiao SX, Biswas MK, Zeng WF, Guo F, Cao HB, Yang XM, Xu XW, Cheng YJ, Xu J, Liu JH, Luo OJ, Tang ZH, Guo WW, Kuang HH, Zhang HY, Roose ML, Nagarajan N, Deng XX, Ruan YJ (2013) The draft genome of sweet orange (Citrus sinensis). Nat Genet 45:59–66

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto M, Matsumoto R, Yamada Y (1995) Relationship between sterility and seedlessness in citrus. J Japan Soc Hort Sci 64:23–29

    Article  Google Scholar 

  • Yamamoto M, Matsumoto R, Okudai N, Yamada Y (1997) Aborted anthers of citrus result from gene-cytoplasmic male sterility. Sci Hortic 70:9–14

    Article  Google Scholar 

  • Yu F, Bi C, Wang X, Qian X, Ye N (2018) The complete mitochondrial genome of Citrus sinensis. Mitochondrial DNA Part B 3:592–593

    Article  PubMed  PubMed Central  Google Scholar 

  • Zerbino DR, Birney E (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821–829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang S, Shi Q, Albrecht U, Shatters RG, Stange R, Mccollum G, Zhang S, Fan C, Stover E (2017) Comparative transcriptome analysis during early fruit development between three seedy citrus genotypes and their seedless mutants. Hortic Res 4:17041

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao N, Wang Y, Hua J (2018) The roles of mitochondrion in intergenomic gene transfer in plants: a source and a pool. Int J Mol Sci 19:547

    Article  PubMed Central  CAS  Google Scholar 

  • Zheng BB, Wu XM, Ge XX, Deng XX, Grosser JW, Guo WW (2012) Comparative transcript profiling of a male sterile cybrid pummelo and its fertile type revealed altered gene expression related to flower development. PLoS One 7:e43758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng BB, Fang YN, Pan ZY, Sun L, Deng XX, Grosser JW, Guo WW (2014) iTRAQ-based quantitative proteomics analysis revealed alterations of carbohydrate metabolism pathways and mitochondrial proteins in a male sterile cybrid pummelo. J Proteome Res 13:2998–3015

    Article  CAS  PubMed  Google Scholar 

  • Zhu A, Guo W, Gupta S, Fan W, Mower JP (2016) Evolutionary dynamics of the plastid inverted repeat: the effects of expansion, contraction, and loss on substitution rates. New Phytol 209:1747–1756

    Article  CAS  PubMed  Google Scholar 

  • Zhu CQ, Zheng XJ, Huang Y, Ye JL, Chen P, Zhang CL, Zhao F, Xie ZZ, Zhang SQ, Wang N, Li H, Wang L, Tang XM, Chai LJ, Xu Q, Deng XX (2019) Genome sequencing and CRISPR/Cas9 gene editing of an early flowering mini citrus (Fortunella hindsii). Plant Biotechnol J 17:2199–2210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The authors thank Drs. Yi-Fei Liu and Shuai-Bin Wang from the South China Botanical Garden (CAS), Dr. An-Dan Zhu from the Kunming Institute of Botany, Chinese Academy of Sciences for bioinformatic support, and our colleague Prof. Robert M. Larkin for critical reading of the manuscript.

Data Archiving Statement

The assembled mitochondrial genome sequences can be retrieved from NCBI GenBank using accession numbers It2304200, It2304217, and It2304225. The raw data of Illumina and PacBio Sequel-based sequencing of mitochondrial DNA, total DNA, and lncRNA can be retrieved from the NCBI SRA database using accession numbers SRR10821402 to SRR10821405 (G1), SRR10828042 to SRR10828045 (HBP), and SRR10841900 to SRR10841903 (G1+HBP).

Funding

This research was financially supported by the Ministry of Science and Technology of China (no. 2018YFD1000106), the National Natural Science Foundation of China (nos. 31530065, 31820103011), and the Fundamental Research Funds for Central Universities (nos. 2662018PY007).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Xiao-Meng Wu or Wen-Wu Guo.

Additional information

Communicated by C. Chen

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

ESM 1

(DOCX 1886 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, S., Yin, ZP., Wu, XM. et al. Assembly of Satsuma mandarin mitochondrial genome and identification of cytoplasmic male sterility–specific ORFs in a somatic cybrid of pummelo. Tree Genetics & Genomes 16, 84 (2020). https://doi.org/10.1007/s11295-020-01480-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11295-020-01480-w

Keywords

Navigation