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(Allium Cepa L.) and Welsh Onion (A Plant Breed. Biotech. 2019 (June) 7(2):151~160 Online ISSN: 2287-9366 https://doi.org/10.9787/PBB.2019.7.2.151 Print ISSN: 2287-9358 RESEARCH ARTICLE Development of Molecular Markers for Distinguishing Onion (Allium cepa L.) and Welsh Onion (A. fistulosum L.) Based on Polymorphic Mitochondrial Genome Sequences Bongju Kim, Sunggil Kim* Department of Horticulture, Biotechnology Research Institute, Chonnam National University, Gwangju 61186, Korea ABSTRACT During seed production of onion (Allium cepa L.) and Welsh onion (A. fistulosum L.) cultivars, seeds are inadvertently cross-contaminated with each other. However, it is difficult to identify cross-contaminated seeds by visual examination since seed and seedling morphologies of onion and Welsh onion are almost identical. To develop molecular markers for distinguishing onion and Welsh onion at early seedling stages, polymorphic mitochondrial genome sequences between two species were isolated. Using complete mitochondrial genome sequences of onions as references, genome walking was performed to isolate polymorphic Welsh onion sequences. Unlike conserved 3ʹ sequences flanking the atp9 gene, the 5ʹ flanking sequences were completely different between onion and Welsh onion mitochondrial genomes. A simple PCR marker was developed on the basis of polymorphic 5ʹ flanking regions of atp9, and a high resolution melting (HRM) marker was developed based on one of single nucleotide polymorphisms (SNPs) in the 3ʹ flanking regions. A total of 41 onion and 19 Welsh onion cultivars were analyzed using these two molecular markers. Results showed that the onion-specific marker genotype was detected only in onion cultivars, and vice versa. To estimate distribution of onion-specific and Welsh onion-specific organizations of atp9 among Allium species, 14 Allium species related to onion and Welsh onion were analyzed. Results showed that specific organizations were conserved among closely related species of onion and Welsh onion, respectively, implying that there might be no intraspecific variation in the atp9 organizations. Keywords Onion (Allium cepa L.), Welsh onions (Allium fistulosum L.), Molecular marker, High resolution melting (HRM), Seed quality control INTRODUCTION and to protect plant breeders’ rights (Yamashita et al. 2010; Cebeci and Hanci 2016). To produce F1 hybrid seeds of The genus Allium consists of more than 700 species. onions and Welsh onion varieties, cytoplasmic male- Among them, approximately 20 species have been cul- sterility (CMS) has been used for genetic emasculation of tivated for foods and medicinal plants (Friesen and Klaas maternal parents (Colombo and Galmarini 2017). CMS is 1998; van Raamsdonk et al. 2003). Onion (Allium cepa L.) defined as inability to produce viable pollen grains due to is the second most important vegetable in the world aberrant genes in mitochondrial genomes and is widely following tomato (Griffiths et al. 2002). Welsh onion (A. distributed in many plant species (Laser and Lersten 1972). fistulosum L.) is an important vegetable in East Asian Induction of CMS by aberrant mitochondrial genes is re- countries such as Korea, Japan, and China (Brewster 2008). lated with unusual features of plant mitochondrial genomes In the case of onion and Welsh onion, proportions of F1 (Schnable and Wise 1998; Budar et al. 2003; Hanson and hybrid cultivars has been increasing to exploit hybrid vigor Bentolila 2004; Kim and Zhang 2018). Received May 2, 2019; Revised May 18, 2019; Accepted May 18, 2019; Published June 1, 2019 *Corresponding author Sunggil Kim, [email protected], Tel: +82-62-530-2061, Fax: +82-62-530-2069 Copyright ⓒ 2019 by the Korean Society of Breeding Science This is an Open-Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. 152 ∙ Plant Breed. Biotech. 2019 (June) 7(2):151~160 Unlike single and circular chloroplast genomes, in vivo sequences, polymorphic organizations between onion and structures of plant mitochondrial genomes remain contro- Welsh onion mitochondrial genomes were identified in this versial (Backert et al. 1997; Oldenburg and Bendich 2001; study to develop molecular markers for distinguishing Allen et al. 2007; Sloan 2013; Skippington et al. 2015). In onion and Welsh onion at early seedling stages. Since seed particular, multipartite subgenomes are commonly present, and seedling morphologies of onion and Welsh onion are and rearrangements among subgenomes have actively oc- hard to distinguish by visual examination, molecular mark- curred through repeat sequence-mediated recombination ers for distinguishing two species are required to identify (Small et al. 1989; Albert et al. 1998; Kmiec et al. 2006; cross-contaminated seeds of onion or Welsh onion culti- Woloszynska and Trojanowski 2009). As a result, organiz- vars during the quality control process of harvested seeds. ations of plant mitochondrial genomes are highly variable However, no report on development of such molecular among related species and even at the intraspecific level markers for distinction of onion and Welsh onion has been (Sakai and Imamura 1993; Bellaoui et al. 1998; Janska et al. published yet. Cross-contamination of seeds of onion and 1998; Arrieta-Montiel et al. 2001; Kim et al. 2007). Mi- Welsh onion sometimes occurs during harvesting seeds in tochondrial genes responsible for CMS are considered to the fields and cleaning harvested seeds at seed conditioning be created by such dynamic rearrangements of plant facilities. mitochondrial genomes (Hanson and Bentolila 2004; Kim and Zhang 2018). CMS in onions is relatively well characterized compared MATERIALS AND METHODS to Welsh onions. Two kinds of CMS (CMS-S and CMS-T) have been reported in the previous studies (Jones and Plant materials and total genomic DNA extraction Emsweller 1936; Jones and Clarke 1943; Berninger 1965; A male-fertile (2702B) and a male-sterile (2702A) Welsh Schweisguth 1973). Almost complete mitochondrial ge- onion breeding lines were used to identify polymorphic nome sequences of normal, CMS-S, and CMS-T cyto- mitochondrial genome organizations between onions and plasms have recently been reported (Kim et al. 2016, Welsh onions. A cetyl trimethylammonium bromide (CTAB) 2019). A chimeric gene, orf725 was suggested to be a causal method (Doyle and Doyle 1987) was used to extract total gene for CMS in both CMS-S and CMS-T cytoplasms. genomic DNAs from leaf tissues of two breeding lines after Compared with normal male-fertile cytoplasm, CMS-S male-fertility phenotypes had been confirmed. A total of 41 mitochondrial genome was highly variable, and many poly- onion and 19 Welsh onion cultivars were used to validate morphisms have been found (Kim et al. 2016). Meanwhile, reliability of molecular markers developed in this study. there were only three single nucleotide polymorphisms Lists of onion and Welsh onion cultivars analyzed in this (SNPs) between normal and CMS-T mitochondrial geno- study are shown in Supplementary Tables S1 and S2, me sequences, except for orf725 which was detected only respectively. Total genomic DNAs were extracted from in the CMS-T cytoplasm (Kim et al. 2019). seedlings of three-to-four leaf stages using a CTAB met- One type of CMS was discovered from Welsh onion hod. A total of 14 Allium species closely related to onion accessions (Moue and Uehara 1985), but this CMS has not and Welsh onion were used to estimate distribution of been widely used in F1 hybrid breeding due to susceptibility specific atp9 organizations. A list of these Allium species is to several diseases (Yamashita et al. 2010). Another type of shown in Supplementary Table S3. One accession for each CMS has been produced by introduction of cytoplasm of A. Allium species was used. Total genomic DNAs extracted galanthum (Yamashita et al. 1999). However, molecular by a previous study (Kim 2013) were used. genetic information about mitochondrial genome sequen- ces and CMS-inducing genes are very limited in Welsh Identification of conserved mitochondrial genomic onions. regions among three onion cytoplasm types Using well characterized onion mitochondrial genome To identify conserved syntenic blocks among three onion Marker Development for Distinguishing Onion and Welsh Onion ∙ 153 mitochondrial genomes, complete mitochondrial genome dure consisted of an initial denaturation step at 95℃ for 5 sequences produced in the previous studies (Kim et al. minutes; 40 cycles at 95℃ for 30 seconds, 65℃ for 30 2016, 2019) were used. A single circular sequence of CMS-S seconds, and 72℃ for 1 minute, and a final 10 minute (GenBank accession: KU318712) and four scaffold se- extension step at 72℃. PCR products were visualized on quences of normal mitochondrial genome (GenBank ac- 1.5% agarose gels after ethidium bromide staining. cessions MH548362-MH548365) were compared. In the For analysis of an HRM marker, HRM analysis was case of CMS-T whose mitochondrial genome sequences performed in 20-μL reaction mixture containing 0.05 μg were almost identical to those of normal cytoplasm, add- template, 2.0 μL 10× PCR buffer, 1.0 μL forward primer itional organization flanking orf725 depicted by Kim et al. (10 μM), 1.0 μL reverse primer (10 μM), 1.0 μL dNTPs (10 (2019) was used for comparison. mM each), 0.25 U Taq polymerase (Prime Tag DNA polymerase; GeNet Bio), and 1.0 μL 100-fold diluted Genome walking and sequencing of PCR products SYTO®9 green fluorescent nucleic acid stain (Thermo Genome walking was performed to obtain flanking Fisher Scientific, Waltham, MA, USA). Primer sequences sequences of atp9 of both male-fertile and male-sterile are shown in Table 1. Welsh onion breeding lines (2702B and 2702A) using a PCR amplification was carried out with a condition Universal GenomeWalker kit (Clontech, Palo Alto, CA, consisting of an initial denaturation step at 95℃ for 10 USA) according to the manufacturer’s instruction. PCR minutes and 45 cycles at 95℃ for 10 seconds, 60℃ for 5 products of genome walking were visualized on 1.5% seconds, and 72℃ for 5 seconds.
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