Abstract
Cytoplasmic male sterility (CMS) has been widely exploited for hybrid seed production in onions (Allium cepa L.). In contrast to long-day onion cultivars, short-day onion has not yet been investigated for mitochondrial genome structure and DNA rearrangements associated with CMS activity. Here, we report the 3,16,321 bp complete circular mitochondrial genome of tropical onion CMS line (97A). Due to the substantial number of repetitive regions, the assembled mitochondrial genome of maintainer line (97B) remained linear with 15 scaffolds. Additionally, 13 and 20 chloroplast-derived fragments with a size ranging from 143 to 13,984 bp and 153–17,725 bp were identified in the 97A and 97B genomes, respectively. Genome annotation revealed 24 core protein-coding genes along with 24 and 28 tRNA genes in the mitochondrial genomes of 97A and 97B, respectively. Furthermore, comparative genome analysis of the 97A and 97B mitochondrial genomes showed that gene content was almost similar except for the chimeric ORF725 gene which is the extended form of the COX1 gene.
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Data availability
The raw sequencing data are available at Indian Biological Data Centre (IBDC) Accession ID INRP000036 and INSDC Study Accession ID PRJEB57244. The mitochondrial genome assemblies are available at http://45.248.163.59/bic/onion.
References
Allen CA, Van Der Giezen M, Allen JF (2007a) Origin, function, and transmission of mitochondria. In: Martin WF, Müller M (eds) Origin of mitochondria and hydrogenosomes. Springer, Berlin, Heidelberg, pp 39–56
Allen JO, Fauron CM, Minx P, Roark L, Oddiraju S, Guan NL, Meyer L, Sun H, Kim K, Wang C, Du F, Xu D, Gibson M, Cifrese J, Clifton SW, Newton KJ (2007b) Comparisons among two fertile and three male-sterile mitochondrial genomes of maize. Genetics 177(2):1173–1192. https://doi.org/10.1534/GENETICS.107.073312
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(6):1436–1448. https://doi.org/10.1093/molbev/msq029
Archibald JM (2015) Endosymbiosis and eukaryotic cell evolution. Current Biol CB 25(19):R911–R921. https://doi.org/10.1016/J.CUB.2015.07.055
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(5):455. https://doi.org/10.1089/CMB.2012.0021
Bentolila S, Stefanov S (2012) A re-evaluation of rice mitochondrial evolution based on the complete sequence of male-fertile and male-sterile mitochondrial genomes. Plant Physiol 158(2):996–1017. https://doi.org/10.1104/PP.111.190231
Bohra A, Jha UC, Adhimoolam P, Bisht D, Singh NP (2016) Cytoplasmic male sterility (CMS) in hybrid breeding in field crops. Plant Cell Rep 35(5):967–993. https://doi.org/10.1007/S00299-016-1949-3
Chase CD (2007) Cytoplasmic male sterility: a window to the world of plant mitochondrial–nuclear interactions. Trends Genet 23(2):81–90. https://doi.org/10.1016/j.tig.2006.12.004
Chen L, Liu Y-G (2014) Male sterility and fertility restoration in crops. Annu Rev Plant Biol 65(1):579–606. https://doi.org/10.1146/annurev-arplant-050213-040119
Cheng Q, Wang P, Li T, Liu J, Zhang Y, Wang Y, Sun L, Shen H (2021) Complete mitochondrial genome sequence and identification of a candidate gene responsible for cytoplasmic male sterility in celery (Apium graveolens L.). Int J Mol Sci 22(16):8584. https://doi.org/10.3390/IJMS22168584/S1
Chevigny N, Schatz-Daas D, Lotfi F, Gualberto JM (2020) DNA repair and the stability of the plant mitochondrial genome. Int J Mol Sci 21(1):328. https://doi.org/10.3390/IJMS21010328
Conant GC, Wolfe KH (2008) GenomeVx: simple web-based creation of editable circular chromosome maps. Bioinformatics (Oxf, Engl) 24(6):861–862. https://doi.org/10.1093/BIOINFORMATICS/BTM598
Cui X, Wise RP, Schnable PS (1996) The rf2 nuclear restorer gene of male-sterile T-cytoplasm maize. Science (New York, NY) 272(5266):1334–1336. https://doi.org/10.1126/SCIENCE.272.5266.1334
Cui H, Ding Z, Zhu Q, Wu Y, Qiu B, Gao P (2021) Comparative analysis of nuclear, chloroplast, and mitochondrial genomes of watermelon and melon provides evidence of gene transfer. Sci Rep 11(1):1595. https://doi.org/10.1038/s41598-020-80149-9
Finkers R, van Kaauwen M, Ament K, Burger-Meijer K, Egging R, Huits H, Kodde L, Kroon L, Shigyo M, Sato S, Vosman B, van Workum W, Scholten O (2021) Insights from the first genome assembly of Onion (Allium cepa). Genes Genomes Genet. https://doi.org/10.1093/G3JOURNAL/JKAB243
Fujii S, Toriyama K (2009) Suppressed expression of retrograde-regulated male sterility restores pollen fertility in cytoplasmic male sterile rice plants. Proc Natl Acad Sci USA 106(23):9513–9518. https://doi.org/10.1073/PNAS.0901860106
Gaborieau L, Brown GG, Mireau H (2016) The propensity of pentatricopeptide repeat genes to evolve into restorers of cytoplasmic male sterility. Front Plant Sci. https://doi.org/10.3389/FPLS.2016.01816
Gupta A, Singh B (2016) Development of hybrids and hybrid seed production of onion. Principles and production techniques of hybrid seeds in vegetables, pp 101–111
Gurevich A, Saveliev V, Vyahhi N, Tesler G (2013) Genome analysis QUAST: quality assessment tool for genome assemblies. Bioinformatics (Oxf, Engl) 29(8):1072–1075. https://doi.org/10.1093/bioinformatics/btt086
Han J, Thamilarasan SK, Natarajan S, Park JI, Chung MY, Nou IS (2016) De novo assembly and transcriptome analysis of bulb onion (Allium cepa L.) during cold acclimation using contrasting genotypes. PloS One 11(9):e0161987. https://doi.org/10.1371/JOURNAL.PONE.0161987
Handa H (2003) The complete nucleotide sequence and RNA editing content of the mitochondrial genome of rapeseed (Brassica napus L.): comparative analysis of the mitochondrial genomes of rapeseed and Arabidopsis thaliana. Nucleic Acids Res 31(20):5907–5916. https://doi.org/10.1093/NAR/GKG795
Hanson MR, Bentolila S (2004) Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell Online 16(suppl_1):S154–S169. https://doi.org/10.1105/tpc.015966
Havey MJ, Kim S (2021) Molecular marker characterization of commercially used cytoplasmic male sterilities in onion. J Am Soc Horticult Sci 146(5):351–355. https://doi.org/10.21273/JASHS05083-21
He T, Ding X, Zhang H, Li Y, Chen L, Wang T, Yang L, Nie Z, Song Q, Gai J, Yang S (2021) Comparative analysis of mitochondrial genomes of soybean cytoplasmic male-sterile lines and their maintainer lines. Funct Integr Genomics 21(1):43–57. https://doi.org/10.1007/S10142-020-00760-X
Hu J, Wang K, Huang W, Liu G, Gao Y, Wang J, Huang Q, Ji Y, Qin X, Wan L, Zhu R, Li S, Yang D, Zhua Y (2012) The rice pentatricopeptide repeat protein RF5 restores fertility in Hong-Lian cytoplasmic male-sterile lines via a complex with the glycine-rich protein GRP162. Plant Cell 24(1):109–122. https://doi.org/10.1105/TPC.111.093211
Khrustaleva L, Nzeha M, Ermolaev A, Nikitina E, Romanov V (2023) Two-step identification of N-, S-, R- and T-cytoplasm types in onion breeding lines using high-resolution melting (HRM)-based markers. Int J Mol Sci 24(2):1605. https://doi.org/10.3390/IJMS24021605/S1
Kim S, Kim M-S, Kim Y-M, Yeom S-I, Cheong K, Kim K-T, Jeon J, Kim S, Kim D-S, Sohn S-H, Lee Y-H, Choi D (2015) Integrative structural annotation of de novo RNA-Seq provides an accurate reference gene set of the enormous genome of the onion (Allium cepa L.). DNA Res 22(1):19–27. https://doi.org/10.1093/dnares/dsu035
Kim B, Kim K, Yang T-J, Kim S (2016) Completion of the mitochondrial genome sequence of onion (Allium cepa L.) containing the CMS-S male-sterile cytoplasm and identification of an independent event of the ccmF N gene split. Curr Genet 62(4):873–885. https://doi.org/10.1007/s00294-016-0595-1
Kim B, Yang T-J, 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(2):313–322. https://doi.org/10.1007/s00122-018-3218-z
Kitazaki K, Arakawa T, Matsunaga M, Yui-Kurino R, Matsuhira H, Mikami T, Kubo T (2015) Post-translational mechanisms are associated with fertility restoration of cytoplasmic male sterility in sugar beet (Beta vulgaris). Plant J 83(2):290–299. https://doi.org/10.1111/TPJ.12888
Kubo T, Kitazaki K, Matsunaga M, Kagami H, Mikami T (2011) Male sterility-inducing mitochondrial genomes: how do they differ? Crit Rev Plant Sci 30(4):378–400. https://doi.org/10.1080/07352689.2011.587727
Kuhl JC, Cheung F, Yuan Q, Martin W, Zewdie Y, McCallum J, Catanach A, Rutherford P, Sink KC, Jenderek M, Prince JP, Town CD, Havey MJ (2004) A unique set of 11,008 onion expressed sequence tags reveals expressed sequence and genomic differences between the monocot orders Asparagales and Poales. Plant Cell 16(1):114–125. https://doi.org/10.1105/tpc.017202
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(1):1–15. https://doi.org/10.1186/S12864-018-5122-Y/FIGURES/4
Liu H, Cui P, Zhan K, Lin Q, Zhuo G, Guo X, Ding F, Yang W, Liu D, Hu S, Yu J, Zhang A (2011) Comparative analysis of mitochondrial genomes between a wheat K-type cytoplasmic male sterility (CMS) line and its maintainer line. BMC Genomics 12(1):1–14. https://doi.org/10.1186/1471-2164-12-163/FIGURES/6
Lohse M, Drechsel O, Bock R (2007) OrganellarGenomeDRAW (OGDRAW): a tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes. Curr Genet 52(5–6):267–274. https://doi.org/10.1007/S00294-007-0161-Y
Manjunathagowda DC (2021) Perspective and application of molecular markers linked to the cytoplasm types and male-fertility restorer locus in onion (Allium cepa). Plant Breed 140(5):732–744. https://doi.org/10.1111/PBR.12948
Marçais G, Delcher AL, Phillippy AM, Coston R, Salzberg SL, Zimin A (2018) MUMmer4: a fast and versatile genome alignment system. PLoS Comput Biol 14(1):e1005944. https://doi.org/10.1371/JOURNAL.PCBI.1005944
Niu Y, Lu Y, Song W, He X, Liu Z, Zheng C, Wang S, Shi C, Liu J (2022) Assembly and comparative analysis of the complete mitochondrial genome of three Macadamia species (M. integrifolia, M. ternifolia and M. tetraphylla). PLOS ONE 17(5):e0263545. https://doi.org/10.1371/JOURNAL.PONE.0263545
Okazaki M, Kazama T, Murata H, Motomura K, Toriyama K (2013) Whole mitochondrial genome sequencing and transcriptional analysis to uncover an RT102-type cytoplasmic male sterility-associated candidate gene derived from Oryza rufipogon. Plant Cell Physiol 54(9):1560–1568. https://doi.org/10.1093/PCP/PCT102
Park JY, Lee YP, Lee J, Choi BS, Kim S, Yang TJ (2013) Complete mitochondrial genome sequence and identification of a candidate gene responsible for cytoplasmic male sterility in radish (Raphanus sativus L.) containing DCGMS cytoplasm. Theor Appl Genet 126(7):1763–1774. https://doi.org/10.1007/S00122-013-2090-0
Rajkumar H, Ramagoni RK, Anchoju VC, Vankudavath RN, Syed AUZ (2015) De novo transcriptome analysis of Allium cepa L. (onion) bulb to identify allergens and epitopes. PLOS One 10(8):e0135387. https://doi.org/10.1371/journal.pone.0135387
Satoh M, Kubo T, Nishizawa S, Estiati A, Itchoda N, Mikami T (2004) The cytoplasmic male-sterile type and normal type mitochondrial genomes of sugar beet share the same complement of genes of known function but differ in the content of expressed ORFs. Mol Genet Genomics MGG 272(3):247–256. https://doi.org/10.1007/S00438-004-1058-9
Shigyo M, Kik C (2008) Onion. Vegetables II:121–159
Singh P, Sahoo RK, Bulle M, Gupta KJ (2020) An efficient method of mitochondrial DNA isolation from Vigna radiata for genomic studies. Methods Mol Biol 2107:305–315. https://doi.org/10.1007/978-1-0716-0235-5_16/COVER
Skippingtona E, Barkmanb TJ, Ricea DW, Palmera JD (2015) Miniaturized mitogenome of the parasitic plant Viscum scurruloideum is extremely divergent and dynamic and has lost all nad genes. Proc Natl Acad Sci USA 112(27):E3515–E3524. https://doi.org/10.1073/PNAS.1504491112
Sloan DB (2013) One ring to rule them all? Genome sequencing provides new insights into the “master circle” model of plant mitochondrial DNA structure. New Phytol 200(4):978–985. https://doi.org/10.1111/NPH.12395
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(1):1–12. https://doi.org/10.1186/1471-2164-13-352/FIGURES/6
Tillich M, Lehwark P, Pellizzer T, Ulbricht-Jones ES, Fischer A, Bock R, Greiner S (2017) GeSeq—versatile and accurate annotation of organelle genomes. Nucleic Acids Res 45(W1):W6–W11. https://doi.org/10.1093/NAR/GKX391
Tsujimura M, Kaneko T, Sakamoto T, Kimura S, Shigyo M, Yamagishi H, Terachi T (2018) Multichromosomal structure of the onion mitochondrial genome and a transcript analysis. Mitochondrion. https://doi.org/10.1016/J.MITO.2018.05.001
Wang D, Wu YW, Shih ACC, Wu CS, Wang YN, Chaw SM (2007) Transfer of chloroplast genomic DNA to mitochondrial genome occurred at least 300 MYA. Mol Biol Evol 24(9):2040–2048. https://doi.org/10.1093/MOLBEV/MSM133
Wang W, Wu Y, Messing J (2012) The mitochondrial genome of an aquatic plant, Spirodela polyrhiza. PloS One 7(10):e46747. https://doi.org/10.1371/JOURNAL.PONE.0046747
Wang P, Lu Q, Ai Y, Wang Y, Li T, Wu L, Liu J, Cheng Q, Sun L, Shen H (2019) Candidate gene selection for cytoplasmic male sterility in pepper (Capsicum annuum L.) through whole mitochondrial genome sequencing. Int J Mol Sci 20(3):578. https://doi.org/10.3390/IJMS20030578
Wang R, Ba Q, Zhang L, Wang W, Zhang P, Li G (2022) Comparative analysis of mitochondrial genomes provides insights into the mechanisms underlying an S-type cytoplasmic male sterility (CMS) system in wheat (Triticum aestivum L.). Funct Integr Genomics 22(5):951–964. https://doi.org/10.1007/S10142-022-00871-7
Wynn EL, Christensen AC (2019) Repeats of unusual size in plant mitochondrial genomes: identification incidence and evolution. G3 Genes Genomes Genet 9(2):549–559. https://doi.org/10.1534/G3.118.200948
Zheng X, Tang S, Zhu S, Dai Q, Liu T (2016) Identification of an NAC transcription factor family by deep transcriptome sequencing in onion (Allium cepa L.). PLOS ONE 11(6):e0157871. https://doi.org/10.1371/journal.pone.0157871
Zhong X, Yue X, Cui J, Han R, Gao Y, Kang J (2022) Complete mitochondrial genome sequencing and identification of candidate genes responsible for C5-type cytoplasmic male sterility in cabbage (B. oleracea var. capitata). Front Plant Sci. https://doi.org/10.3389/FPLS.2022.1019513
Acknowledgements
The authors are thankful to Science and Engineering Research Board, Department of Science and Technology (DST), India project Grant No. SRG/2019/000632 and Department of Biotechnology, Government of India project Grant No. BT/PR40193/BTIS/137/23/2021 for providing financial assistance.
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RB, RS, and AM optimized the protocol and extracted mitochondrial DNA. OPM and ASD provided the onion samples. DS and RB perform computational analysis of the genome. RB and DS have written the manuscript. ASD and PC gave critical suggestions throughout the study and reviewed the manuscript. The manuscript is seen and approved by all the authors.
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Bishnoi, R., Solanki, R., Singla, D. et al. Comparative mitochondrial genome analysis reveals a candidate ORF for cytoplasmic male sterility in tropical onion. 3 Biotech 14, 6 (2024). https://doi.org/10.1007/s13205-023-03850-2
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DOI: https://doi.org/10.1007/s13205-023-03850-2