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Triparental origin of triploid onion, Allium × cornutum (Clementi ex Visiani, 1842), as evidenced by molecular, phylogenetic and cytogenetic analyses

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Reconstruction of the parental origins of cultivated plants from wild relatives, especially after long periods of domestication, is not a trivial task. However, recent advances in molecular phylogenetics, among other approaches, have proved to be very informative in analyses of the origin and evolution of polyploid genomes. An established minor garden crop, triploid onion Allium x cornutum (Clementi ex Visiani, 1842) (2n = 3x = 24), is widespread in southeastern Asia and Europe. Our previous cytogenetic analyses confirmed its highly heterozygous karyotype and indicated its possible complex triparental genome origin. Allium cepa L. and Allium roylei Stearn were suggested as two putative parental species of A. x cornutum, whereas the third parental species remained hitherto unknown. Here we report the phylogenetic analyses of the internal transcribed spacers ITS1-5.8S-ITS2 of 35S rDNA and the non-transcribed spacer (NTS) region of 5S rDNA of A. x cornutum and its relatives of the section Cepa. Both ITS and NTS sequence data revealed intra-individual variation in triploid onion, and these data clustered into the three main clades, each with high sequence homology to one of three other species of section Cepa: A. cepa, A. roylei, and unexpectedly, the wild Asian species Allium pskemense B. Fedtsh. Allium pskemense is therefore inferred to be the third, so far unknown, putative parental species of triploid onion Allium x cornutum. The 35S and 5S rRNA genes were found to be localised on somatic chromosomes of A. x cornutum and its putative parental species by double fluorescent in situ hybridisation (FISH). The localisation of 35S and 5S rDNA in A. x cornutum chromosomes corresponded to their respective positions in the three putative parental species, A. cepa, A. pskemense, and A. roylei. GISH (genomic in situ hybridisation) using DNA of the three putative parental diploids corroborated the results of the phylogenetic study. The combined molecular, phylogenetic and cytogenetic data obtained in this study provided evidence for a unique triparental origin of triploid onion A. x cornutum with three putative parental species, A. cepa, A. pskemense, and A. roylei.
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... Further due to its hybrid origin, its name was changed to A. x cornutum. However, a study undertaken by Fredotović et al. (2014) suggested the grouping of this taxon with the Indian clone 'Pran' (Allium x proliferum). ...
... Cepa and the wild Asian species Allium pskemense B. Fedtsh., A. pskemense is therefore inferred to be the third, so far unknown, putative parental species of triploid onion Allium x cornutum. GISH (genomic in situ hybridisation) using DNA of the three putative parental diploids corroborated the results of the phylogenetic study (Fredotović et al., 2014). This taxon has been reported in the adjoining parts of India, in Pakistan and Bhutan (Pradheep et al., 2014). ...
... The spotting of the fraternity of interspecific hybridization event had acknowledged, it might have naturally occurred in antiquity surpassed by inadvertent introgression into the onion population (Little et al. 1944;Davis 1957) . The male-sterile cytoplasm had originated through series of possible inter-specific hybridization could lead to natural triploid Pran, it is an intermediate evolutionary species between Allium 9 cornutum Clement ex Visiani or Allium 9 proliferum (Moench) Schra presented in Fig. 2. The alien cytoplasm of 'Pran' transferred into 'onion' (Fredotovic et al. 2014;Maab 1997;Havey 1993;Koul and Gohil 1971). The event had supported by the southern blotting of S-cytoplasm; the restriction fragment length polymorphism (RFLP) of cpDNA and mtDNA in S-cytoplasm differed from T-and N-cytoplasm(s). ...
... The polymorphism of cpDNA-41 identical to S-cytoplasmic plants and 'Pran'. 'Pran' is a viviparous triploid onion (Allium 9 cornutum Clement ex Visiani, or Allium 9 proliferum (Moench) Schra) natural interspecific hybrid taught to be tri-parental origin between Allium cepa L., Allium pskemense B. Fedtsh and Allium roylei Stearn revealed and presented in Fig. 2 (Fredotovic et al. 2014;Havey 1991a;b, c, 1992a, b;Singh et al. 1967;Koul and Gohil 1971). ...
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Onion (Allium cepa L.) is the most diversified crop of the family Alliaceae; it is in cultivation since from ancient era for its edible bulbs and verdant foliage due to the immense nutritional and medicinal properties. The increased social acceptance of bulb onion in daily diet could lead to an increase in cultivable area with a similar bulb production. However, the output per unit area had limited due to the lack of exploitation of heterosis for bulb yield. The only possibility to increase the onion productivity is to increase the volume of the individual bulb, and it can achieve by exploiting heterosis for earliness, biotic and abiotic stress resistance, bulb weight, and size by the development of hybrid with the use of male sterility mechanisms like cytoplasmic-genic male sterility or cytoplasmic male sterility system in onion. The male sterility trait is precious in heterosis breeding due to its potential advantages in the development of onion hybrids. In these perspectives, the present review reveals the origin, evolution, maintenance, and prevalence of male sterility systems of onion and the technique of identification of the male sterility systems. The polymorphisms between male-sterile and male-fertile phenotypes difference with morphological-molecular markers with the marker-phenotype linkage of onion.
... The third shallot species, A. × cornutum Clementi ex Vis. (2n = 3x = 24), is of a unique triparental origin: A. cepa, A. pskemense, and A. roylei [5,6,20]. Landraces of A. × cornutum are grown mainly in the Mediterranean part of Croatia [5], whereas landraces from the A. cepa Aggregatum group are mostly distributed in the mainland. ...
... In this study, A. × cornutum accessions are distinctive in several bulb traits, including ovate bulb shape (BQL 1 {7}), no bulblets offsets (BQL 3 {0}), thick bulb skin, and light brown color (BQL 5 {7}, BQL 4 {4}, respectively), green/white bulb flesh color (BQL 6 {3}) and have the smallest bulb diameter compared with the two other species. Fredotović et al. [20] and Puizina [5] reported on the elongated pear-shaped bulbs in A. × cornutum, and our earlier study by Major et al. [21] supports the finding that the A. × cornutum has the narrowest bulb diameter compared to other shallot species from Croatia, which contributes to the further identification of A. × cornutum and its specific features compared to other shallot species and types later assessed and later examined in this study. ...
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... Allium × cornutum (2n = 3x = 24) is an established small garden crop widely distributed in southeastern Asia and Europe. Combined molecular, phylogenetic and cytogenetic analysis provided evidence for its unique genetic structure and triploid genomic origin with three putative parent species of section Cepa: A. cepa, A. roylei and the wild Asian species Allium pskemense B. Fedtsh [1]. These onions are edible species and have been used in human nutrition for years. ...
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Onions are one of the most widely grown vegetable crops. As production increases, so does the generation of waste from various parts of the onion, raising the need for efficient ecological disposal and use of such waste products. However, onion waste products are a rich source of antioxidants with a range of biological properties, therefore, they could potentially be used in food and pharmaceutical industries. In the present study, we identified the main flavonols and anthocyanins in peel extracts of Allium × cornutum Clement ex Visiani, 1842, and two varieties of Allium cepa L. and tested their antioxidant, antimicrobial and antiproliferative properties. Quercetin 3,4′-diglucolside, quercetin 4′-monoglucoside and quercetin are the most abundant flavonols in all onion extracts detected by high-performance liquid chromatography (HPLC) method. The composition of anthocyanins varied in all extracts. 2,2′-diphenyl-1-picrylhydrazyl (DPPH) and oxygen radical absorbance capacity (ORAC) assays showed that the triploid onion A. × cornutum had the highest antioxidant power. Evaluation of antimicrobial activity by broth microdilution assay also showed that A. × cornutum had higher antimicrobial activity compared to the red and yellow onion varieties. Comparable antiproliferative activity was confirmed for all onion extracts tested on three cancer cell lines: Hela (cervical cancer cell line), HCT116 (human colon cancer cell line) and U2OS (human osteosarcoma cell line). The most abundant onion flavonols (quercetin 3,4′-diglucoside and quercetin 4′-monoglucoside) showed weaker antimicrobial as well as antiproliferative properties compared to the extracts, leading to the conclusion that other phytochemicals besides flavonols contribute to the biological activity of onion peel extracts. The results demonstrate the antioxidant and antimicrobial properties of onion peels, which have promising potential as cancer cell proliferation inhibitors.
... cepa, A. pskemense B. Fedt. and A. roylei Stearn), traditionally cultivated in costal Croatia under the name 'Ljutika' (shallot) [15]. Due to its tasty bulbs and leaves it is widely used as a spice and similarly cultivated in other parts of the world such as South-East Asia and Europe. ...
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... For example, natural trigenomic taxa are known in Epilobium (Epilobium ciliatum × E. hirsutum × E. parviflorum, [27]), Potamogeton (Potamogeton perfoliatus × P. gramineus × P. lucens, [23]) and Cardamine (Cardamine rivularis × C. amara × C. pratensis, [71]). Artificially produced triparental hybrids were published from the genera Melilotus [39], Rosa [19], Triticum [70], Allium [16] and Brassica [40]. They almost all belong to herbaceous plants. ...
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... To summarize, we infer that the visual inspection of rDNA cluster graph topologies coupled with calculation of graph parameters is highly informative for the assessment of rDNA genomic organization, number of rRNA gene families, and loci. The method may provide clues for testable hypotheses about evolutionary histories of interspecific hybrids and allopolyploids, especially in biological systems with unknown or not well defined genome donors (Mahelka et al., 2011;Kaplan et al., 2013;Fredotovic et al., 2014;Belyayev et al., 2018). It is necessary to stress that a robust evaluation of hybridization and polyploidy cannot be solely based on read clustering, but should involve a combination of various cytogenetic, molecular and genomic methods. ...
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... Allium cornutum is a minor garden onion crop traditionally cultivated in Asia, Europe, and North America, under different local names [22,23]. It is characterized by an unusual genetic structure and triploid karyotype (2n = 3x = 24), a result of a spontaneous hybridization between the three different Allium species [24,25]. Since the composition of headspace-volatile sulfur compounds and free amino-acids of triploid onion A. cornutum has not been studied so far, we aimed to identify those two groups of phytonutrients and compare them with the corresponding components of common onion. ...
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Triploid viviparous onions [Allium x cornutum Clementi ex Visiani 1842, syn Allium cepa L. var. viviparum Metzg. (ALEF.), auct.] (2n = 3x = 24), are known in some countries only as rare relict crops. In other parts of the world they are still traditionally or even commercially cultivated. In previous cytogenetic studies of the Croatian triploid viviparous onion Ljutika, Giemsa C-banding, chromosome pairing analysis during meiosis, and genomic hybridization in situ indicated a complex hybrid with highly heterozygous karyotype structure, with possible triparental genome organization. This study continues an analysis of the karyotype structure of Ljutika. Staining with fluorochromes CMA(3) (Chromomycin A(3)) and DAPI (4,6-diamidino-2-phenylindole) confirmed previous results from Giemsa C-banding and revealed GC-rich heterochromatic regions associated mainly with chromosome ends and nucleolus organizing regions (NORs), and only a few interstitial bands. FISH mapping of the ribosomal 18S-5.8S-26S genes revealed two major rDNA signals on the short arms of two subtelocentric satellite chromosomes in almost all metaphase plates of Ljutika. The largest subtelocentric chromosome lacked rDNA signals. A significantly smaller rDNA signal was occasionally located on one small submetacentric chromosome. These results are in agreement with previously published results from identification of NORs by silver-staining technique, which confirmed a maximum three nucleoli in interphase nuclei. We discuss the molecular mechanisms underlying rearrangements and activity of ribosomal genes in the triploid karyotype.
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