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Doubled haploid production in onion (Allium cepa L.): from gynogenesis to chromosome doubling

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Abstract

Bulb onion (Allium cepa L.) is an allogamous diploid (2n = 16) important for its culinary uses, nutritional value, and medicinal benefits. Despite its economic importance, onion yields and bulb quality are declining, emphasizing the need for new and improved strategies for maintaining and enhancing overall crop quality. Development of inbred lines in onion through traditional breeding is often difficult due to its biennial life cycle, inbreeding depression, and comparatively high heterozygosities. Moreover, genetic research in onion has been hampered by large nuclear genome size. In this regard, gynogenic doubled haploids promise several advantages over inbred lines in support of onion breeding programs and genetic studies. These include complete homozygosity in doubled haploid lines, reduced DNA methylation, elimination of deleterious alleles, and amenability to genetic analysis. This review focuses on the application of in vitro gynogenesis for producing doubled haploids in onion. Factors influencing haploid induction, methods for inducing chromosome doubling and ploidy assessment, evaluation of haploid progenies and doubled haploid lines, and features of doubled haploids potentially useful in crop improvement and genetic studies, are discussed. We identify four major limitations to the success and efficiency of in vitro gynogenesis in onion and discuss strategies for mitigating the negative impacts they pose. This review may be useful to research programs producing doubled haploids in onion or other Allium species using in vitro gynogenesis.

Key Message

In onion, doubled haploids (DHs) were generated by gynogenesis using in vitro culturing of unfertilized ovules, ovaries or whole flowers. Genotype, geographical origin, photoperiodicity and genetic structure all affect gynogenic efficiency in onion. Despite higher doubling efficiencies, there are several disadvantages with induced chromosome doubling inlcuding low survival rates of explants, cytotoxicity, vitrification and polyploidization.

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References

  • Abdelrahman M, Sawada Y, Nakabayashi R, Sato S, Hirakawa H, El-Sayed M, Hirai MY, Saito K, Yamauchi N, Shigyo M (2015) Integrating transcriptome and target metabolome variability in doubled haploids of Allium cepa for abiotic stress protection. Mol Breed 35:195. https://doi.org/10.1007/s111032-015-0378-2

    Article  Google Scholar 

  • Abraham A, Mathew PM (1963) Cytology of coconut endosperm. Ann Bot 27:505–512

    Article  Google Scholar 

  • Ahmadi B, Ebrahimzadeh H (2020) In vitro androgenesis: spontaneous vs. artificial genome doubling and characterization of regenerants. Plant Cell Rep. https://doi.org/10.1007/s00299-020-02509-z

    Article  PubMed  Google Scholar 

  • Ahmadi B, Shariatpanahi ME, Ojaghkandi MA, Hydari AA (2014) Improved microspore induction and plantlet regeneration using putrescine, cefotaxime and vancomycin in Brassica napus L. Plant Cell Tissue Organ Cult 118:495–505

    Article  CAS  Google Scholar 

  • Ahmadi B, Ahmadi M, Teixiera da Silva JA (2018) Microspore embryogenesis in Brassica: calcium signaling, epigenetic modification, and programmed cell death. Planta 248:1339–1350

    Article  CAS  PubMed  Google Scholar 

  • Alan AR, Mutschler MA, Brants A, Cobb E, Earle ED (2003) Production of gynogenic plants from hybrids of Allium cepa L. and A. roylei Stearn. Plant Sci 165:1201–1211

    Article  CAS  Google Scholar 

  • Alan AR, Brants A, Cobb E, Goldschmied PA, Mutschler MA, Earle ED (2004) Fecund gynogenic lines from onion (Allium cepa L.) breeding materials. Plant Sci 167:1055–1066

    Article  CAS  Google Scholar 

  • Alan AR, Lim W, Mutschler MA, Earle ED (2007) Complementary strategies for ploidy manipulations in gynogenic onion (Allium cepa L.). Plant Sci 173:25–31

    Article  CAS  Google Scholar 

  • Alan AR, Toprak FC, Kaska A (2016) Production and evaluation of gynogenic leek (Allium ampeloprasum L.) plants. Plant Cell Tissue Organ Cult 125:249–259

    Article  CAS  Google Scholar 

  • Alifar M, Ebadi A, Fatahi Maghadam MR (2015) Effect of putrescine and chloremquat pre-flowering treatment on embryo rescue technique such in diallele crosses of grape cultivars Flame seedless, Perlette and Yaghooh. Iran J Hortic Sci 46:179–192

    Google Scholar 

  • Anandhan S, Ashwini CA, Gopal J, Sanjay MR, Poonam SV, Kisan LE (2014) Variation in gynogenic potential for haploid induction in Indian short-day onions. Ind J Genet Plant Breed 74:526–528

    Article  Google Scholar 

  • Arshad MS, Sohaib M, Nadeem M, Saeed F, Imran A, Javed A, Amjad Z, Batool SM (2017) Status and trends of nutraceuticals from onion and onion by-products: a critical review. Cogent Food Agric 3:1280254

    Google Scholar 

  • Asif M (2013) Progress and opportunities of doubled haploid production. Springer, Basel

    Book  Google Scholar 

  • Aubry CJ, De Buyser J, Hartmann C, Henry Y, Rode A (1989) Changes in molecular organization of the mitochondrial genome in albino tissue cultures derived from wheat pollen embryos and in plants regenerated from theses cultures. Plant Sci 65:103–110

    Article  CAS  Google Scholar 

  • Azpeitia A, Chan JL, Saenz L, Oropeza C (2003) Effect of 22(S),23(S)-homobrassinolide on somatic embryogenesis in plumule explants of Cocos nucifera (L.) cultured in vitro. J Hortic Sci Biotechnol 78:591–596

    Article  CAS  Google Scholar 

  • Bah AA, Wang ZD, Wang XQ, Yan MM, Um YC, Xu Z, Guo DP (2012) In vitro plant regeneration from unpollinated ovaries of Allium chinense. Sci Hortic 147:105–110

    Article  CAS  Google Scholar 

  • Baldwin S, Pither-Joyce M, Wright K, Chen L, McCallum J (2012) Development of robust genomic simple sequence repeat markers for estimation of genetic diversity within and among bulb onion (Allium cepa L.) populations. Mol Breed 30:1401–1411

    Article  CAS  Google Scholar 

  • Bang H, Kim S, Park SO, Yoo K, Patil BS (2013) Development of a codominant CAPS marker linked to the Ms locus controlling fertility restoration in onion (Allium cepa L.). Sci Hortic 153:42–49

    Article  CAS  Google Scholar 

  • Bohance B (1998) Gynogenic haploid induction in plant breeding. In: Hansen M (ed) Gametic embryogenesis. COST 824 report of activities 1995–1997. European Commission, Luxembourg, pp 253–255

    Google Scholar 

  • Bohanec B (2002) Doubled haploid onions. In: Rabinowitch HD, Currah L (eds) Allium crop science: recent advances. CABI Publishing House, Wallingford, pp 145–158

    Chapter  Google Scholar 

  • Bohanec B (2009) Doubled haploids via gynogenesis. In: Touraev A, Forster BP, Jain SM (eds) Advances in haploid production in higher plants. Springer, Dordrecht, pp 35–46

    Chapter  Google Scholar 

  • Bohanec B, Jakše M (1999) Variations in gynogenic response among long-day onion (Allium cepa L.) accessions. Plant Cell Rep 18:737–742

    Article  CAS  Google Scholar 

  • Bohanec B, Jakše M, Ihan A, Javornik B (1995) Studies of gynogenesis in onion (Allium cepa L.) induction procedures and genetic analysis of regenerants. Plant Sci 104:215–224

    Article  CAS  Google Scholar 

  • Bohanec B, Jakše M, Havey MJ (2003) Genetic analyses of gynogenetic haploid production in onion. J Am Soc Hortic Sci 128:571–574

    Article  Google Scholar 

  • Campion B, Alloni C (1990) Induction of haploid plants in onion (Allium cepa L.) by in vitro culture of unpollinated ovules. Plant Cell Tissue Organ Cult 20:1–6

    Article  CAS  Google Scholar 

  • Campion B, Azzimonti MT, Vicini E, Schiavi M, Falavigna A (1992) Advances in haploid plant induction in onion (Allium cepa L.) through in vitro gynogenesis. Plant Sci 86:97–104

    Article  Google Scholar 

  • Campion B, Bohanec B, Javornik B (1995a) Gynogenic lines of onion (Allium cepa L.): evidence of their homozygosity. Theor Appl Genet 91:598–602

    Article  CAS  PubMed  Google Scholar 

  • Campion B, Perri E, Azzimonti MT, Vicini E, Schiavi M (1995b) Spontaneous and induced chromosome doubling in gynogenic lines of onion (Allium cepa L.). Plant Breed 114:243–246

    Article  Google Scholar 

  • Castillo AM, Cistue L, Valles MP, Soriano M (2008) Chromosome doubling in monocots. In: Touraev A, Forster BP, Jain SM (eds) Advances in haploid production in higher plants. Springer, Dordrecht, pp 329–338

    Google Scholar 

  • Chen JF, Cui L, Malik AA, Mbira KG (2011) In vitro haploid and dihaploid production via unfertilized ovule culture. Plant Cell Tissue Organ Cult 104:311–319

    Article  Google Scholar 

  • Chiancone B, Tassoni A, Bagni N, Germanà MA (2006) Effect of polyamines on in vitro anther culture of Citrus clementina Hort ex Tan. Plant Cell Tissue Organ Cult 87:145–153

    Article  CAS  Google Scholar 

  • Chiancone B, Karasawa MMG, Gianguzzi V, Abdelgalel AM, Barany I, Testillano PS, Marinoni DT, Botta R, Germanà MA (2015) Early embryo achievement through isolated microspore culture in Citrus clementina Hort. ex Tan., cvs. ‘Monreal Rosso’ and ‘Nules’. Front Plant Sci 6:413

    Article  PubMed  PubMed Central  Google Scholar 

  • Chiavarino AM, Rosato M, Manzanero S, Jimenez G, Gonzalez-Sanchez M, Puretas MJ (2000) Chromosome nondisjunction and instabilities in tapetal cells are affected by B chromosomes in maize. Genetics 155:889–897

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chugh KN, Batt AR, Pratt MR (2016) Chemical methods for encoding and decoding of posttranslational modifications. Cell Chem Biol. https://doi.org/10.1016/j.chembiol.2015.11.006

    Article  Google Scholar 

  • Currah L (2002) Onions in the tropics and subtropics: cultivars and country reports. In: Rabinowitch HD, Currah L (eds) Allium crop science. CABI Publishing House, Wallingford, pp 379–408

    Chapter  Google Scholar 

  • D’Amato F (1984) Role of polyploidy in reproductive organs and tissues. In: Johri BM (ed) Embryology of Angiosperms. Springer, New York, pp 519–566

    Chapter  Google Scholar 

  • da Silva Dias JC (2003) Protocol for broccoli microspore culture. In: Maluszynski M, Kasha KJ, Forster BP, Szarejko I (eds) Doubled haploid production in crop plants. Springer, Dordrecht, pp 195–204

    Chapter  Google Scholar 

  • Dane F, Meric C (2005) Cytological and embryological studies of anther in rice (Oryza sativa) cv. ‘Rocca’. Acta Bot Hung 47:257–272

    Article  Google Scholar 

  • de Klerk GJ, Pramanik D (2017) Trichloroacetate, an inhibitor of wax biosynthesis, prevents the development of hyperhydricity in Arabidopsis seedlings. Plant Cell Tissue Organ Cult 131:89–195. https://doi.org/10.1007/s11240-017-1264-x

    Article  CAS  Google Scholar 

  • Dhooghe E, Van Laere K, Eeckhaut T, Lueus L, Van Huylenbroeck J (2011) Mitotic chromosome doubling of plant tissues in vitro. Plant Cell Tissue Organ Cult 104:359–373. https://doi.org/10.1007/s11240-010-9786-5

    Article  Google Scholar 

  • Dong YQ, Zhao WX, Li XU, Liu XC, Gao NN, Huang JH, Wang WY, Xu XL, Tang ZH (2016) Androgenesis, gynogenesis and parthenogenesis haploids in cucurbit species. Plant Cell Rep 35:1991–2019

    Article  CAS  PubMed  Google Scholar 

  • Duangjit J, Bohanec B, Chan AP, Town CD, Havey MJ (2013) Transcriptome sequencing to produce SNP-based genetic maps of onion. Theor Appl Genet 126:2093–2101

    Article  CAS  PubMed  Google Scholar 

  • Duangjit J, Welsh K, Wise ML, Bohanec B, Havey MJ (2014) Genetic analyses of anthocyanin concentrations and intensity of red bulb color among segregating haploid progenies of onion. Mol Breed 34:75–85

    Article  CAS  Google Scholar 

  • Dunstan DI, Short KC (1977) Improved growth of tissue cultures of onion, Allium cepa. Physiol Plant 41:70–72

    Article  Google Scholar 

  • Dunwell JM (2010) Haploids in flowering plants: origins and exploitation. Plant Biotechnol J 8:377–424

    Article  CAS  PubMed  Google Scholar 

  • Dwivedi SL, Britt AB, Tripathi L, Sharma S, Upadhyaya HD, Ortiz R (2015) Haploids: constraints and opportunities in plant breeding. Biotechnol Adv. https://doi.org/10.1016/j.biotechadv.2015.07.001

    Article  PubMed  Google Scholar 

  • Ebrahimi R, Zamani Z (2009) Effect of Polyamines on in vitro gynogenesis of onion (Allium cepa L.). Am Eurasian J Sustain Agric 3:71–74

    Google Scholar 

  • Ebrahimzadeh H, Shariatpanahi ME, Ahmadi B, Soltanloo H, Lotfi M, Zarafi E (2018a) Efficient parthenogenesis induction and in vitro haploid plant regeneration in cucumber (Cucumis sativus L.) using putrescine, spermidine and cycocel. J Plant Growth Regul. https://doi.org/10.1007/s000344-018-9803-1

    Article  Google Scholar 

  • Ebrahimzadeh H, Soltanloo H, Shariatpanahi ME, Eskandari A, Ramezanpour SS (2018b) Improved chromosome doubling of parthenogenetic haploid plants of cucumber (Cucumis sativus L.) using colchicine, trifluralin, and oryzalin. Plant Cell Tissue Organ Cult 135:407–417. https://doi.org/10.1007/s11240-018-1473-y

    Article  CAS  Google Scholar 

  • Evans DA, Sharp WR, Medina-Filho HP (1984) Somaclonal and gametoclonal variation. Am J Bot 71:759–774. https://doi.org/10.1002/j.1537-2197.1984.tb14141.x

    Article  Google Scholar 

  • FAOSTAT (2017) Food and Agriculture Organization of the United Nations. FAO statistical database. FAOSTAT, Rome

    Google Scholar 

  • Fayos O, Valles MP, Garces-Claver A, Mallor C, Castillo AM (2015) Doubled haploid production from Spanish onion (Allium cepa L.) germplasm: embryogenesis induction, plant regeneration and chromosome doubling. Front Plant Sci. https://doi.org/10.3389/fpls.2015.00384

    Article  PubMed  PubMed Central  Google Scholar 

  • Ferrie AMR (2017) Doubled haploid production in higher plants. In: Thomas BG, Murray BG, Murphy DJ (eds) Encyclopedia of applied plant sciences, vol 2. Academic Press, Waltham, pp 147–151

    Chapter  Google Scholar 

  • Forodi BR, Hassandokht M, Kashi A, Sepahvand N (2009) Influence of spermidine on haploid plant production in Iranian onion (Allium cepa L.) populations through in vitro culture. Hortic Environ Biotechnol 50:461–466

    CAS  Google Scholar 

  • Forster BP, Heberle-Bors E, Kasha KJ, Touraev A (2007) The resurgence of haploids in higher plants. Trends Plant Sci 12:368–375. https://doi.org/10.1016/j.tplants.2007.06.007

    Article  CAS  PubMed  Google Scholar 

  • Foschi ML, Martinez LE, Ponce MT, Galmarini CR, Bohanec B (2013) Effect of colchicines and amiprophos-methyl on the production of in vitro doubled haploid onion plants and correlation assessment between ploidy level and stomatal size. Revolut FCA UNCUYO 45:155–164

    Google Scholar 

  • Fukui K, Nakayama S (1996) Plant chromosomes: laboratory methods. CRC Press, Tokyo

    Google Scholar 

  • Gamborg OL, Miller RA, Ojima K (1968) Nutrients requirements of suspension cultures of soybean root cells. Exp Cell Res 50:151–158

    Article  CAS  PubMed  Google Scholar 

  • Geoffriau E, Kahane R, Rancillac M (1997a) Variation of gynogenesis ability in onion (Allium cepa L.). Euphytica 94:37–44

    Article  Google Scholar 

  • Geoffriau E et al (1997b) Ploidy stability and in vitro chromosome doubling in gynogenic clones of onion (Allium cepa L.). Plant Sci 122:201–208

    Article  CAS  Google Scholar 

  • Geoffriau E, Kahane R, Martin-Tanguy J (2006) Polyamines are involved in the gynogenesis process in onion. Physiol Plant 127:119–129. https://doi.org/10.1111/j.1399-3054.2005.00597.x

    Article  CAS  Google Scholar 

  • Germanà MA (2006) Doubled haploid production in fruit crops. Plant Cell Tissue Organ Cult 86:131–146

    Article  Google Scholar 

  • Germanà MA (2011a) Gametic embryogenesis and haploid technology as valuable support to plant breeding. Plant Cell Rep 30:839–857

    Article  PubMed  CAS  Google Scholar 

  • Germanà MA (2011b) Anther culture for haploid and doubled haploid production. Plant Cell Tissue Organ Cult 104:283–300

    Article  Google Scholar 

  • Grzebelus E, Adamus A (2004) Effect of anti-mitotic agents on development and genome doubling of gynogenic onion (Allium cepa L.) embryos. Plant Sci 167:569–574

    Article  CAS  Google Scholar 

  • Gurel E, Gurel S, Lemaux PG (2008) Biotechnology applications for sugar beet. Crit Rev Plant Sci 27:108–140

    Article  CAS  Google Scholar 

  • Hanna AB (1994) Genetic evaluation of some economic characters in onion (Allium cepa). Dissertation, Banha Branch, Zagazig University

  • Hassandokht MR, Campion B (2002) Low temperature, medium and genotype effect on the gynogenic ability of onion (Allium cepa L.) flowers cultured in vitro. Adv Hortic Sci 16:72–78

    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, Bohanec B (2007) Onion inbred line ‘B8667 A&B’ and synthetic populations ‘Sapporo-Ki-1 A&B’ and ‘Onion Haploid-1’. Hortic Sci 42:1731–1732

    Google Scholar 

  • Higashiyama T, Yang WC (2017) Gametophytic pollen tube guidance: attractant peptides, gametic controls, and receptors. Plant Physiol 173:112–121

    Article  CAS  PubMed  Google Scholar 

  • Hyde PT, Earle ED, Mutschler MA (2012) Doubled haploid onion (Allium cepa L.) lines and their impact on hybrid performance. Hortic Sci 47:1690–1695

    Google Scholar 

  • Ibrahim AM, Kayat FB, Susanto D, Kashiani P, Arifullah M (2016) Haploid induction in spring onion (Allium fistulosum L.) via gynogenesis. Biotechnol 15:10–16

    Article  CAS  Google Scholar 

  • Jakše M, Bohanec B (2000) Studies of alternative approaches for genome doubling in onion. In: Bohanec B (ed) Biotechnological approaches for utilization of gametic cells. Proc COST final meet, 1–5 July 2000, Bled, Slovenia, pp 101–104

  • Jakše M, Bohanec B, Ihan A (1996) Effect of media components on the gynogenic regeneration of onion (Allium cepa L.) cultivars and analysis of regenerants. Plant Cell Rep 15:934–938

    Article  PubMed  Google Scholar 

  • Jakše M, Havey MJ, Bohanec B (2003) Chromosome doubling procedures of onion (Allium cepa L.) gynogenic embryos. Plant Cell Rep 21:905–910

    Article  PubMed  CAS  Google Scholar 

  • Jakše M, Hirschegger P, Bohanec B (2010) Evaluation of gynogenic responsiveness and pollen viability of selfed doubled haploid onion lines and chromosome doubling via somatic regeneration. J Am Soc Hortic Sci 135:67–73

    Article  Google Scholar 

  • Javornik B, Bohanec B, Campion B (1998) Second cycle gynogenesis in onion, Allium cepa L., and genetic analysis of the plants. Plant Breed 117:275–278

    Article  Google Scholar 

  • Jensen CJ (1974) Chromosome doubling techniques in haploids. In: Kasha KL (ed) Haploids in higher plants advances and potential. University of Guelph, Guelph, pp 153–190

    Google Scholar 

  • Joshi H, Tandon J (1976) Heterosis for yield and its genetic basis in the onion. Ind J Agric Sci 46:88–92

    Google Scholar 

  • Kasha KJ (2005) Chromosome doubling and recovery of doubled haploid plants. In: Palmer CE, Keller WA, Kasha KJ (eds) Biotechnology in agriculture and forestry. Haploids in crop improvement II, Springer, Berlin, pp 123–152

    Google Scholar 

  • Kaska A, Toprak FC, Alan AR (2013) Gynogenesis induction in leek (Allium ampeloprasum L.) breeding materials. Curr Opin Biotechnol 24S:S42–S47

    Article  Google Scholar 

  • Keller J (1990) Culture of unpollinated ovules, ovaries, and flower buds in some species of the genus Allium and haploid induction via gynogenesis in onion (Allium cepa L.). Euphytica 47:241–247

    Google Scholar 

  • Keller ERJ, Korzun L (1996) Haploidy in onion (Allium cepa L.) and other Allium species. In: Jain SM, Sopory SK, Veilleux RE (eds) In vitro haploid production in higher plants, vol 3. Kluwer, Dordrecht, pp 51–71

    Chapter  Google Scholar 

  • Kelliher T, Starr D, Wang W, McCuiston J, Zhong H, Nuccio ML, Martin B (2016) Maternal haploids are preferentially induced by CENH3-tailswap transgenic complementation in maize. Front Plant Sci 7:414. https://doi.org/10.3389/fpls.2016.00414

    Article  PubMed  PubMed Central  Google Scholar 

  • Khar A, Kumar A, Islam S, Kumar A, Agarwal A (2018) Genotypic response towards haploid induction in short day tropical Indian onion (Allium cepa L.). Ind J Agric Sci 88:709–713

    CAS  Google Scholar 

  • Khar A, Islam S, Kalia P, Bhatia R, Kumar A (2019) Present status of haploidy research in onion (Allium cepa)—a review. Ind J Agric Sci 89:396–405

    CAS  Google Scholar 

  • Khosa JS, McCallum J, Dhatt AS, Macknight RC (2016a) Enhancing onion breeding using molecular tools. Plant Breed 135:9–20. https://doi.org/10.1111/pbr.12330

    Article  Google Scholar 

  • Khosa JS, Lee R, Brauning S, Lord J, Pither-Joyce M, McCallum J, Macknight RC (2016b) Doubled haploid ‘CUDH2107’ as a reference for bulb onion (Allium cepa L.) research: development of a transcriptome catalogue and identification of transcripts associated with male fertility. PLoS ONE. https://doi.org/10.1371/journal.pone.0166568

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim S, Kim CW, Park M, Choi D (2015) Identification of candidate genes associated with fertility restoration of cytoplasmic male-sterility in onion (Allium cepa L.) using a combination of bulked segregant analysis and RNA-seq. Theor Appl Genet 128:2289–2299. https://doi.org/10.1007/s00122-015-2584-z

    Article  CAS  PubMed  Google Scholar 

  • Kiszczak W, Krzyzanowska D, Strycharczuk K, Kowalska U, Wolko B, Górecka K (2011) Determination of ploidy and homozygosity of carrot plants obtained from anther cultures. Acta Physiol Plant 33:401–407

    Article  Google Scholar 

  • Klutschewski S (2012) Methodical improvements in microspore culture of Brassica napus L. Dissertation, University of Gottingen

  • Lee JH, Natarajan S, Biswas MK, Shirasawa K, Isobe S, Kim HT, Park JI, Seong CN, Nou IS (2018) SNP discovery of Korean short day onion inbred lines using double digest restriction site-associated DNA sequencing. PLoS ONE 13:e0201229. https://doi.org/10.1371/journal.pone.0201229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li JW, Si SW, Cheng JY, Li JX, Liu JQ (2013) Thidiazuron and sliver nitrate enhanced gynogenesis of unfertilized ovule cultures of Cucumis sativus. Biol Plant 57:164–168

    Article  CAS  Google Scholar 

  • Lora J, Hormaza JI (2018) Pollen wall development in mango (Mangifera indica L., Anacardiaceae). Plant Rep. https://doi.org/10.1007/s00497-018-0342-5

    Article  Google Scholar 

  • Malik MR, Wang F, Dirpaul J, Zhou N, Hammerlindl J, Keller W, Abrams SR, Ferrie AM, Krochko JE (2008) Isolation of an embryogenic line from non-embryogenic Brassica napus cv. Westar through microspore embryogenesis. J Exp Bot 59:2857–2873

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maluszynski M, Kasha KJ, Forster BP, Szarejko I (2003) Doubled haploid production in crop plants: a manual. Springer, Dordrecht

    Book  Google Scholar 

  • Martinez LE, Aguero CB, Lopez ME, Galmarini CR (2000) Improvement of in vitro gynogenesis induction in onion (Allium cepa L.) using polyamines. Plant Sci 156:221–226

    Article  CAS  PubMed  Google Scholar 

  • Mathapati GB, Kalia P, Islam S, Saini N, Kumar A, Khar A (2018) Influence of culture media and their compositions on haploid induction in Indian short day onion. Proc Natl Acad Sci B. https://doi.org/10.1007/s40011-018-0990-0

    Article  Google Scholar 

  • McCallum J, Baldwin S, Macknight R, Khosa J, Shaw M (2018) Molecular mapping of genes and QTL: progress to date and development of new population resources for NGS genetics. In: Shigyo M, Khar A, Abdelrahman M (eds) The allium genomes. Compendium of plant genomes. Springer, Cham, pp 181–196

    Google Scholar 

  • Michalik B, Adamus A, Nowak E (2000a) Gynogenesis in polish onion cultivars. J Plant Physiol 156:211–216

    Article  CAS  Google Scholar 

  • Michalik B, Adamus A, Samek L, Nowak E (2000b) Gynogenesis in Polish onion cultivars: effect of temperature during donor plant growth. In: Bohanec B (ed) Biotechnological approaches for utilization of gametic Cells. Proc COST final meeting, 1–5 July 2000, Bled, Slovenia, pp 91–94.

  • Mishra V, Chaturvedi R (2014) An overview on haploid production in tree. In: Ramavat KG, Merillon JM, Ahuja MR (eds) Tree biotechnology. CRC Press, Boca Raton, pp 151–186

    Google Scholar 

  • Molenaar WS, Schipprack W, Melchinger AE (2018) Nitrous oxide induced chromosome doubling of maize haploids. Crop Sci 58:650–659. https://doi.org/10.2135/cropsci2017.07.0412

    Article  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Muren RC (1989) Haploid plant induction from unpollinated ovaries in onion. Hortic Sci 24:833–834

    Google Scholar 

  • Murovec J, Bohanec B (2012) Haploids and doubled haploids in plant breeding. In: Abdurakhmonov IY (ed) Plant breeding. Intech Open, London. https://doi.org/10.5772/29982

  • Musial K, Bohanec B, Przywara L (2001) Embryological study on gynogenesis in onion (Allium cepa L.). Sex Plant Rep 13:335–341

    Article  Google Scholar 

  • Nair AS, Seo BB (1993) Plantlet regeneration from callus initiated from flower buds in the wild species Allium senescens var. Minor Plant Cell Tissue Organ Cult 34:205–207

    Article  CAS  Google Scholar 

  • Nunes RLC, Oliveira ABD, Dutra AS (2014) Agronomic performance of onion hybrids in Barauna, in the semi-arid region of Brazil. Revistaia Cienc Agron 45:606–611. https://doi.org/10.1590/S1806-66902014000300023

    Article  Google Scholar 

  • Ochatt SJ, Patat-Ochatt EM, Moessner A (2011) Ploidy level determination within the context of in vitro breeding. Plant Cell Tissue Organ Cult 104:329–341. https://doi.org/10.1007/s11240-011-9918-6

    Article  Google Scholar 

  • Oono K (1981) In vitro methods applied to rice. In: Thorpe TA (ed) Plant tissue culture. Academic Press, New York, pp 273–298

    Chapter  Google Scholar 

  • Padoan D, Mossad A, Chiancone B, Germanà MA, Sha Valli Khan PS (2013) Ploidy levels in Citrus clementine affects leaf morphology, stomatal density and water content. Theor Exp Plant Physiol 25:283–290

    Article  Google Scholar 

  • Ponce M, Martinez L, Galmarini C (2006) Influence of CCC, putrescine and gellam gum concentration on gynogenic embryo induction in Allium cepa. Biol Plant 50:425–428

    Article  CAS  Google Scholar 

  • Puddephat IJ, Robinson HT, Smith BM, Lynn J (1999) Influence of stock plant pre-treatment on gynogenic embryo induction from flower buds of onion. Plant Cell Tissue Organ Cult 57:145–148

    Article  Google Scholar 

  • Ravi M, Chan SWL (2010) Haploid plants produced by centromere-mediated genome elimination. Nature 464:615–618

    Article  CAS  PubMed  Google Scholar 

  • Ren J, Wu P, Trampe B, Tian X, Chen S, Lubberstedt T (2017) Novel technologies in doubled haploid line development. Plant Biotechnol J 15:1361–1370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ribeiro CB, Pereira FDC, Filho LDN, Braz GT, Ruy MC, Silva MB, Cenzi G, Techio VH, Souza JCD (2018) Haploid identification using tropicalized haploid inducer progenies in maize. Crop Breed Appl Biotechnol 18:16–23. https://doi.org/10.1590/1984-70332018v18n1a3

    Article  CAS  Google Scholar 

  • Robarts DW, Wolfe AD (2014) Sequence-related amplified polymorphism (SRAP) markers: a potential resource for studies in plant molecular biology. Appl Plant Sci 2:1–13

    Article  Google Scholar 

  • San Noeum LH (1976) Haploides d'Hordeum vulgare L. par culture in vitro d'ovaires non fecondes. Ann Amelior Plantes 26:751–754

    Google Scholar 

  • Segui-Simarro JM (2010) Androgenesis revisited. Bot Rev 76:377–404

    Article  Google Scholar 

  • Segui-Simarro JM (2015) Editorial: doubled haploidy in model and recalcitrant species. Front Plant Sci 6:1175. https://doi.org/10.3389/fpls.2015.01175

    Article  PubMed  PubMed Central  Google Scholar 

  • Segui-Simarro JM, Corral-Martinez P, Parra-Vega V, Gonzalez-Garcia B (2011) Androgenesis in recalcitrant Solanaceous crops. Plant Cell Rep 30:765–778. https://doi.org/10.1007/s00299-010-0984-8

    Article  CAS  PubMed  Google Scholar 

  • Seguí-Simarro JM, Nuez F (2008) Pathways to doubled haploidy: chromosome doubling during androgenesis. Cytogenet Genome Res 120:358–369. https://doi.org/10.1159/000121085

    Article  PubMed  Google Scholar 

  • Sha Valli Khan PS, Prakash E, Rao KR (2002) Callus induction and plantlet regeneration in Bixa orellana L., an annatto-yielding tree. Vitro Cell Dev Biol-Plant 38:186–190

    Article  CAS  Google Scholar 

  • Sha Valli Khan PS, Kozai T, Nguyen QT, Dhawan V (2003) Growth and water relations of Paulownia fortunei under photomixotrophic and photoautotrophic conditions. Biol Plant 46:161–166

    Article  Google Scholar 

  • Singh BD, Singh AK (2015) Marker-assisted plant breeding: principles and practices. Springer, New Delhi

    Book  Google Scholar 

  • Solorzano-Cascante P, Sanchez-Chiang N, Jimenez VM (2018) Explant type, culture system, 6-benzyladenine, meta-toplin and encapsulation affect indirect somatic embryogenesis and regeneration in Carica papaya L. Front Plant Sci 9:1769. https://doi.org/10.3389/fpls.2018.01769

    Article  PubMed  PubMed Central  Google Scholar 

  • Sulistyaningish E, Yamashita K, Tashiro Y (2002) Haploid induction from F1 hybrids between CM shallot with Allium galanthum cytoplasm and common onion by unpollinated flower culture. Euphytica 125:139–144

    Article  Google Scholar 

  • Sulistyaningsih E, Aoyagi Y, Tashiro Y (2006) Flower bud culture of shallot (Allium cepa L. Aggregatum group) with cytogenetic analysis of resulting gynogenic plants and somaclones. Plant Cell Tissue Organ Cult 86:249–255. https://doi.org/10.1007/s11240-006-9114-2

    Article  Google Scholar 

  • Susek A, Javornik B, Bohanec B (2002) Factors affecting direct organogenesis from flower explants of Allium giganteum. Plant Cell Tissue Organ Cult 68:27–33

    Article  CAS  Google Scholar 

  • Tavan M, Mirjalili MH, Karimzadeh G (2015) In vitro polyploidy induction: changes in morphological anatomical and phytochemical characteristics of Thymus persicus (Lamiaceae). Plant Cell Tissue Organ Cult 122:573–583

    Article  CAS  Google Scholar 

  • Testillano P, Georgiev S, Mogensen HL, Coronado MJ, Dumas C, Risueno MC, Matthys-Rochon E (2004) Spontaneous chromosome doubling results from nuclear fusion during in vitro maize induced microspore embryogenesis. Chromosoma 112:342–349. https://doi.org/10.1007/s00414-004-0279-3

    Article  CAS  PubMed  Google Scholar 

  • Tiburcio A, Altabella J, Bitrian M, Akazar R (2014) The roles of polyamines during the life span of plants: from development to stress. Planta 240:1–18

    Article  CAS  PubMed  Google Scholar 

  • Umehara M, Sueyoshi T, Shimomura K, Nakahara T (2006) Production of interspecific hybrids between Allium fistulosum and Allium macrosternon Bunge through ovary culture. Plant Cell Tissue Organ Cult 87:297–304

    Article  CAS  Google Scholar 

  • van den Dries N, Giannì S, Czerednik A, Krens FA, de Klerk GJM (2013) Flooding of the apoplast is the key factor in the development of hyperhydricity. J Exp Bot 64:5221–5230. https://doi.org/10.1093/jxb/ert315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vieira MLC, Santini L, Diniz AL, de Freitas MC (2016) Microsatellite markers: what they mean and why they are so useful. Genet Mol Biol 39:312–328

    Article  PubMed  PubMed Central  Google Scholar 

  • Vinogradov AE (1994) Measurement by flow cytometry of genomic AT/GC ratio and genome size. Cytometry 16:34–40

    Article  CAS  PubMed  Google Scholar 

  • Warchol M, Czyzylo-Mysza IM, Marcinska I, Dziurka K, Noga A, Skrzypek E (2018) The effect of genotype, media composition, pH and sugar concentrations on oat (Avena sativa L.) doubled haploid production through oat × maize crosses. Acta Physiol Plant. https://doi.org/10.1007/s11738-018-2669-9

    Article  Google Scholar 

  • Yarali F, Arpaci BB (2018) Cold/heat shock pre-treatment for gynogenic haploid embryo induction in Amaryllidaceae and Cucurbitaceae: a review. Sci Bull F 22:11–14

    Google Scholar 

  • Yarali F, Yanmaz R (2016) The effects of media composition on in vitro gynogenic embryo induction in Allium tuncelianum (Kollaman) Ozhatay, Matthew, Siraneci). Int J Agric Sci 8:3247–3251

    Google Scholar 

  • Yarali F, Yanmaz R (2017) The effects of plant growth regulators on in vitro gynogenic embryo formation in onion (Allium cepa L.). Afr J Biotechnol 16:1977–1983

    Article  CAS  Google Scholar 

  • Yarali Karkan F (2019) Influence of cold pre-treatments on callus and embryo induction in onion (Allium cepa L.) via flower bud culture. Fresenius Environ Bull 28:8070–8075

    Google Scholar 

  • Ye YM, Tong J, Shi XP, Yuan W, Li GR (2010) Morphological and cytological studies of diploid and colchicine-induced tetraploid lines of crape myrtle (Lagerstroemia indica L.). Sci Hortic 124:95–101

    Article  Google Scholar 

  • Yuan S, Su Y, Liu Y, Li Z, Fang Z, Yang L, Zhuang M, Zhang Y, Lv H, Sun P (2015) Chromosome doubling of microspore-derived plants from cabbage (Brassica oleracea var. capitata L.) and broccoli (Brassica oleracea var italica L.). Front Plant Sci 6:1118. https://doi.org/10.3389/fpls.2015.01118

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang L, Zhang L, Luo J, Chen W, Hao M, Liu B, Yan Z, Zhang B, Zhang H, Zheng Y, Liu D, Yen Y (2011) Synthesizing double haploid hexaploid wheat populations based on a spontaneous alloploidization process. J Genet Genomics 38:89–94

    Article  PubMed  Google Scholar 

  • Zhao H, Wang XX, Du YC, Zhu DW, Guo YM, Gao JC, Li F, Snyder JC (2014) Haploid induction via in vitro gynogenesis in tomato (Solanum lycopersicum L.). J Integr Agric 13:2122–2131

    Article  Google Scholar 

  • Zhou K, Fleet P, Nevo E, Zhang X, Sun G (2017) Transcriptome analysis reveals plant response to colchicine treatment during on chromosome doubling. Sci Rep 7:1–11. https://doi.org/10.1038/s41598-017-08391-2

    Article  CAS  Google Scholar 

  • Zobayed SMA, Armstrong J, Armstrong W (1999) Cauliflower shoot culture: effects of different types of ventilation on growth and physiology. Plant Sci 141:209–217

    Article  Google Scholar 

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Acknowledgements

Ms. G. Vijayalakshmi, express thanks to the Department of Science and Technology, New Delhi, for awarding INSPIRE research fellowship [0824-2013].

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Authors and Affiliations

  1. Department of Botany, Yogi Vemana University, Vemanapuram, Kadapa, Andhra Pradesh, 516005, India

    Patan Shaik Sha Valli Khan, Gujjula Vijayalakshmi, Mondem Muni Raja & Mude Lakshmipathi Naik

  2. Dipartimento di Scienze Agrarie, Alimentari e Forestali, Universita Degli Studi di Palermo, Viale Delle Scienze, 11, Ed. 4, 90128, Palermo, Italy

    Maria Antonietta Germanà

  3. Biology Department, Lamar University, Beaumont, TX, USA

    Randal G. Terry

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  1. Patan Shaik Sha Valli Khan
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Contributions

PSSVK participated in the review design, data collection, and analysis, writing and revision of the manuscript. GV, MM, and MLN conceived and designed the manuscript. Both MAG and RGT helped in the editing and revision of the manuscript. All authors have read and approved the final manuscript and declare no conflict of interest.

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Correspondence to Patan Shaik Sha Valli Khan.

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Khan, P.S.S.V., Vijayalakshmi, G., Raja, M.M. et al. Doubled haploid production in onion (Allium cepa L.): from gynogenesis to chromosome doubling. Plant Cell Tiss Organ Cult 142, 1–22 (2020). https://doi.org/10.1007/s11240-020-01831-4

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