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The triparental triploid onion Allium × cornutum Clementi ex Visiani, 1842, possesses a sterile S-type of cytoplasm

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Abstract

Triploid onion, Allium × cornutum Clementi ex Visiani, 1842 (2n = 3x = 24), a vegetatively reproduced garden crop, possess a complex triparental genome organization with three putative parental species, A. cepa L., A. pskemense B. Fedtsch., and A. roylei Stearn. Two of its most studied clones are the Croatian ‘Ljutika’ and the Indian ‘Pran’, which are genetically highly similar. Earlier studies have shown that ‘Pran’ possesses some molecular markers in the chloroplast DNA (cpDNA) identical to those of the unique male-sterile (S) cytoplasm, used for onion breeding. To find out whether ‘Ljutika’ also possesses a S-type of cytoplasm, we analyzed several cpDNA and mitochondrial (mtDNA) molecular markers. The PCR amplification and RFLP analysis of the chloroplast genes accD, atpF, petB and the mitochondrial gene cob, as well as the sequence analysis of the chloroplast matK and atpB-rbcL regions showed that ‘Ljutika’ possesses the male-sterile S-type of cytoplasm. The phylogenetic analysis of the matK and atpB-rbcL sequences of A. × cornutum, its parental species and other Allium species of the section Cepa showed that none of the analyzed species had the identical type of cpDNA as A. × cornutum. Results also suggested that A. pskemense can be excluded as a donor of the S-cytoplasm and a female parent, whereas cpDNA of A. roylei, although not identical to S-cytoplasm, possessed many polymorphisms of S-type. Fluorescent in situ hybridization, using fluorescently labelled parental genomic DNAs as probes in combination with fluorescently labelled 5S and 35S rDNAs enabled simultaneous visualization of the three genomes during meiosis and confirmed their homeologus intergenomic pairing.

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References

  • Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723

    Article  Google Scholar 

  • Berninger E (1965) Contribution a l’etude de la sterilite male de l’oignon (Allium cepa L.). Ann Amelior Plant 15:183–199

    Google Scholar 

  • Cho KS, Yang TJ, Hong SY, Kwon YS, Woo JG, Park HG (2006) Determination of cytoplasmic male sterile factors in onion plants (Allium cepa L.) using PCR-RFLP and SNP markers. Mol Cells 21(3):411–417

    CAS  PubMed  Google Scholar 

  • Engelke T, Terefe D, Tatlioglu T (2003) A PCR-based marker system monitoring CMS-(S), CMS-(T) and (N)-cytoplasm in the onion (Allium cepa L.). Theor Appl Genet 107:162–167

    Article  CAS  PubMed  Google Scholar 

  • Fonseca JP, Levy A, Henriques R, Costa JC, Neto C, Robalo J (2016) Phylogenenetic approach of the section D.C. of based on cpDNA. A case of taxonomic inflation? Plant Biosyst Int J Deal Asp Plant Biol 150(4):787–798

    Google Scholar 

  • Fredotović Ž, Šamanić I, Weiss-Schneeweiss H, Kamenjarin J, Jang TS, Puizina J (2014) Triparental origin of triploid onion, Allium × cornutum (Clementi ex Visiani, 1842), as evidenced by molecular, phylogenetic and cytogenetic analysis. BMC Plant Biol 14:24

    Article  PubMed  PubMed Central  Google Scholar 

  • Friesen N, Klaas M (1998) Origin of some minor vegetatively propagated Allium crops studied with RAPD and GISH. Genet Resour Crop Evol 45:511–523

    Article  Google Scholar 

  • Gurushidze M, Mashayekhi S, Blattner FR, Friesen N, Fritsch RM (2007) Phylogenetic relationship of wild and cultivated species of Allium section Cepa inferred by nuclear rDNA ITS sequence analysis. Plant Syst Evol 269:259–269

    Article  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Havey MJ (1991) Phylogenic relationships among cultivated Allium species from restriction enzyme analysis of the chloroplast genome. Theor Appl Genet 81:752–757

    Article  CAS  PubMed  Google Scholar 

  • Havey MJ (1992) Restriction enzyme analysis of the nuclear 45 s ribosomal DNA of six cultivated Alliums (Alliaceae). Plant Syst Evol 181:45–55

    Article  CAS  Google Scholar 

  • Havey MJ (1993) A putative donor of S-cytoplasm and its distribution among open-pollinated populations of onion. Theor Appl Genet 86:128–134

    Article  CAS  PubMed  Google Scholar 

  • Havey MJ (1995) Identification of cytoplasm using the polymerase chain reaction to aid in the extraction of maintainer lines from open-pollinated populations of onion. Theor Appl Genet 90(2):263–268

    Article  CAS  PubMed  Google Scholar 

  • Havey MJ (1999) Seed yield, floral morphology, and lack of male-fertility restoration of male-sterile onion (Allium cepa) populations possessing the cytoplasm of Allium galanthum. J Am Soc Hortic Sci 124(6):626–629

    Google Scholar 

  • Higgins DG, Thompson JD, Gibson TJ (1996) Using CLUSTAL for multiple sequence alignments. Methods Enzymol 266:383–402

    Article  CAS  PubMed  Google Scholar 

  • Jones H, Clarke A (1943) Inheritance of male sterility in the onion and the production of hybrid seed. Proc Am Soc Hortic Sci 43:189–194

    Google Scholar 

  • Jones H, Emsweller SL (1936) A male-sterile onion. Proc Am Soc Hortic Sci 34:582–585

    Google Scholar 

  • Khar A, Saini N (2016) Limitations of PCR-based molecular markers to identify male-sterile and maintainer plants from Indian onion (Allium cepa L.) populations. Plant Breed 135:519–524

    Article  CAS  Google Scholar 

  • Kim S, Lee E, Cho DY, Han T, Bang H, Patil BS (2009) Identification of a novel chimeric gene, orf725, and its use in development of a molecular marker for distinguishing three cytoplasm types in onion (Allium cepa L.). Theor Appl Genet 118:433–441

    Article  CAS  PubMed  Google Scholar 

  • Kim S, Park JY, Yang T (2015) Comparative analysis of the complete chloroplast genome sequences of a normal male-fertile cytoplasm and two different cytoplasms conferring cytoplasmic male sterility in onion (Allium cepa L.). J Hortic Sci Biotechnol 90(4):459–468

    Article  CAS  Google Scholar 

  • Klaas M, Friesen N (2001) Molecular markers in Allium. In: Rabinowitch HD, Currah L (eds) Allium crop science: recent advances. CABI Publishing, Wallingford, pp 159–187

    Google Scholar 

  • Koul AK, Gohil RN (1971) Further studies on natural triploidy in viviparous onions. Cytology 36:253–261

    Article  Google Scholar 

  • Lepen I, Puizina J (2011) Fish mapping of 18S-5.8S-26S rRNA genes and fluorochrome banding in the triploid viviparous onion Allium × cornutum Clementi ex Visiani, 1842. Acta Biol Crac Ser Bot 53(1):111–116

    Google Scholar 

  • Lilly JW, Havey MJ (2001) Sequence anaysis of a chloroplast intergenic spacer for phylogenetic estimates in Allium section Cepa and a PCR-based polymorphism detecting mixtures of male-fertile and male-sterile cytoplasmic onion. Theor Appl Genet 102(1):78–82

    Article  CAS  Google Scholar 

  • Maaß HI (1997) Studies on triploid viviparous onions and their origin. Genet Resour Crop Evol 44:95–99

    Article  Google Scholar 

  • Noguchi J, De-yuan H (2004) Multiple origins of the Japanese nocturnal Hemerocallis citrina var. vespertina (Asparagales: Hemerocallidaceae): evidence from noncoding chloroplast DNA sequences and morphology. Int J Plant Sci 165(1):219–230

    Article  Google Scholar 

  • Pich U, Fuchs J, Schubert I (1996) How do Alliaceae stabilize their chromosome ends in the absence of TTTAGGG sequences? Chromosome Res 4(3):207–213

    Article  CAS  PubMed  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  CAS  PubMed  Google Scholar 

  • Puizina J (2013) Shallots in Croatia—genetics, morphology and nomenclature. Acta Bot Croat 72:387–398

    Google Scholar 

  • Puizina J, Papeš D (1996) Cytogenetical evidence for hybrid structure and origin of diploid and triploid shallots (Allium cepa var. viviparum, Lilliaceae) from Dalmatia (Croatia). Plant Syst Evol 199:203–215

    Article  Google Scholar 

  • Puizina J, Papeš D (1997) Further cytogenetic analyses of the Croatian triploid shallot “Ljutika” (Allium cepa var. viviparum, Alliaceae) and its comparison with the Indian triploid “Pran”. Plant Syst Evol 208:11–23

    Article  Google Scholar 

  • Puizina J, Javornik B, Bohanec B, Schweizer D, Maluszynska J, Papeš D (1999) Random amplified polymorphic DNA analysis, genome size, and genomic in situ hybridization of triploid viviparous onions. Genome 42:1208–1216

    Article  CAS  PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Rønsted N, SymondsM RE, Birkholm T, Christensen S, Meerow AW, Molander M, Mølgaard P, Petersen G, Rasmussen N, van Staden J, Stafford GI, Jäger AK (2012) Can phylogeny predict chemical diversity and potential medicinal activity of plants? A case study of Amaryllidaceae. BMC Evol Biol 12(1):182

    Article  PubMed  PubMed Central  Google Scholar 

  • Saghai Maroof MA, Soliman KM, Jorgensen RA, Allard RW (1984) Ribosomal DNA spacer length polymorphism in barley: Mendelian inheritance, chromosomal location and population dynamics. Proc Natl Acad Sci USA 81:8014–8018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saini N, Hedau NK, Khar A, Yadav S, Bhatt J, Agrawal PK (2015) Successful deployment of marker assisted selection (MAS) for inbred and hybrid development in long-day onion (Allium cepa L.). Indian J Genet Plant Breed 75(1):93–98

    Article  Google Scholar 

  • Sato Y (1998) PCR amplification of CMS-specific mitochondrial nucleotide sequences to identify cytoplasmic genotypes of onion (Allium cepa L.). Theor Appl Genet 96:367–370

    Article  CAS  PubMed  Google Scholar 

  • Senda M, Mikami T, Kinoshita T (1993) The sugar beet mitochondrial gene for the ATP-ase alpha-subunit: sequence, transcription and rearrangements in cytoplasmic male-sterile plants. Curr Genet 24:164–170

    Article  CAS  PubMed  Google Scholar 

  • Singh F, Ved Brat S, Khoshoo TN (1967) Natural triploidy in viviparous onions. Cytologia 32:403–407

    Article  Google Scholar 

  • Son JH, Park KC, Park YJ, Kong JH, Kim NS (2010) Sequence diversification of 45S rRNA ITS, trnH-psbA spacer, and matK genic regions in several Allium species. Genes Genomics 32:165–172

    Article  CAS  Google Scholar 

  • Steele PR, Hertweck KL, Mayfield D, McKain MR, Leebens-Mack J, Pires JC (2012) Quality and quantity of data recovered from massively parallel sequencing: examples in Asparagales and Poaceae. Am J Bot 99:330–348

    Article  CAS  PubMed  Google Scholar 

  • Swofford DL (2001) PAUP*: Phylogenetic analysis using parsimony (*and other methods), Version 4.0b.10 for 32-Bit Microsoft Windows. Sunderland, MA, USA, Sinauer Associates

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • von Kohn C, Kiełkowska A, Havey MJ (2013) Sequencing and annotation of the chloroplast DNAs and identification of polymorphisms distinguishing normal male-fertile and male-sterile cytoplasm of onion. Genome 56:737–742

    Article  Google Scholar 

  • Vu HQ, Iwata M, Yamauchi N, Shigyo M (2011) Production of novel alloplasmic male sterile lines in Allium cepa harbouring the cytoplasm from Allium roylei. Plant Breed 130(4):469–475

    Article  Google Scholar 

  • Yamashita K, Tashiro T (1999a) Possibility of developing male sterile line of shallot (Allium cepa L. Aggregatum group) with cytoplasm from A. galanthum Kar. et Mr. I. Japan. Soc Hortic Sci 68:256–262

    Article  CAS  Google Scholar 

  • Yamashita K, Tashiro T (1999b) Possibility of developing male sterile line of shallot (Allium cepa L. Aggregatum group) with cytoplasm from A. galanthum Kar. et Mr. J. Japan. Soc Hortic Sci 68:256–262

    Article  CAS  Google Scholar 

  • Yamashita K, Arita H, Tashiro Y (1999) Cytoplasm of a wild species Allium galanthum Kar. et Kir. is useful for developing male sterile line of A. fistulosum L. J. Japan. Soc Hortic Sci 68:788–797

    Article  Google Scholar 

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Acknowledgements

We thank the Centre for Genetic Resources (CGN, Netherlands) for providing specimens of A. pskemense and A. roylei used in this study. This work received funding from the Croatian Ministry of Science, Education and Sport through a grant to Jasna Puizina (No. 177-11911196-0829).

Author’s contribution

The experimental design was conceived by JP. The material was sampled and taxonomically identified by JK. Experiments were performed by ZF, IS, JK. Contributing reagents/consumables/tools by JP. Data were analyzed by JP with assistance from ZF and IS. This paper was written by JP and ZF. All authors read and approved the final manuscript.

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Correspondence to Jasna Puizina.

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Fredotović, Ž., Šamanić, I., Kamenjarin, J. et al. The triparental triploid onion Allium × cornutum Clementi ex Visiani, 1842, possesses a sterile S-type of cytoplasm. Genet Resour Crop Evol 64, 1971–1983 (2017). https://doi.org/10.1007/s10722-017-0489-1

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