Is Doubled Haploid Production in Sorghum Impossible?
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Published:
Dec 25, 2017
Keywords:
Haploid Anther culture Chromosome doubling Plant breeding Sorghum
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Abstract
Doubled Haploid (DH) is an efficient tool in plant breeding programs. This method reduces time to homozygosity. DH production has been developed and routinely used in several species but not sorghum. The objective of this review is to provide an overview of DH production and the barriers in DH production of sorghum from previous studies on three potential methods for haploid induction; androgenesis, gynogenesis, and wide hybridization. The information could be valuable in the development of DH protocol in sorghum which may be employed in genetics and molecular studies.
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How to Cite
Teingtham, K., & Borde, N. D. L. (2017). Is Doubled Haploid Production in Sorghum Impossible?. Applied Science and Engineering Progress, 10(4). Retrieved from https://ph02.tci-thaijo.org/index.php/ijast/article/view/184001
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References
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[3] W. L. Rooney, J. Blumenthal, B. Bean, and J. E. Mullet, “Designing sorghum as a dedicated bioenergy feedstock,” Biofuels, Bioproducts and Biorefining, vol. 1, pp. 147–157, 2007.
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[5] M. Wędzony, B. P. Forster, I. Żur, E. Golemiec, M. Szechyńska-Hebda, E. Dubas, G. Gotębiowska, and M. Wędzony, “Progress in doubled haploid technology in higher plants,” in Advances in Haploid Production in Higher Plants, Netherlands: Springer Netherlands, 2009, pp. 1–33.
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[9] V. K. Mishra and R. Gowswami, “Haploid production in higher plant,” International Journal of Chemical and Biological Sciences, vol. 1, pp. 26–45, 2014.
[10] A. Castillo, L. Cistue, M. Valles, J. Sanz, I. Romagosa, and J. L. Molina-Cano, “Efficient production of androgenic doubled-haploid mutants in barley by the application of sodium azide to anther and microspore cultures,” Plant Cell Reports, vol. 20, pp. 105–111, 2001.
[11] G. S. Khush and S. S. Virmani, “Haploids in plant breeding,” in In Vitro Haploid Production in Higher Plants, Dordrecht: Springer, 1996, pp. 11–33.
[12] M. Rahman and M. Michalak de Jiménez, “Behind the scenes of microspore-based double haploid development in Brassica napus: A review,” Journal of Plant Science and Molecular Breeding, vol. 5, pp. 1, 2016.
[13] A. F. Blaskeslee and J. Belling, “Chromosomal mutations in the Jimson weed, Datura stramonium,” Journal of Heredity, vol. 15, pp. 195–206, 1924.
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[16] M. A. Germana, “Anther culture for haploid and doubled haploid production,” Plant Cell Tissue and Organ Culture, vol. 104, pp. 283–300, Mar. 2011.
[17] M. Maluszynski, K. Kasha, B. P. Forster, and I. Szarejko, Doubled Haploid Production in Crop Plants: A Manual, Springer Science & Business Media, 2003.
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[19] N. Naik, P. Rout, N. Umakanta, R. L. Verma, J. L. Katara, K. K. Sahoo, O. N. Singh, and S. Samantaray, “Development of doubled haploids from an elite indica rice hybrid (BS6444G) using anther culture,” Plant Cell, Tissue and Organ Culture, vol. 128, pp. 679–689, 2017.
[20] A. Ismaili and P. P. Mohammadi, “Effect of genotype, induction medium, carbohydrate source, and polyethylene glycol on embryogenesis in maize (Zea mays L.) anther culture,” Acta Physiologiae Plantarum, vol. 38, pp. 74, 2016.
[21] S. Sriskandarajah, M. Sameri, E. Lerceteau-Köhler, and A. Westerbergh, “Increased recovery of green doubled haploid plants from barley anther culture,” Crop Science, vol. 55, pp. 2806–2812, 2015.
[22] L. Zhao, L. Liu, J. Wang, H. Guo, J. Gu, S. Zhao, J. Li, and Y. Xie, “Development of a new wheat germplasm with high anther culture ability by using a combination of gamma-ray irradiation and anther culture,” Journal of the Science of Food and Agriculture, vol. 95, pp. 120–125, 2015.
[23] G. H. Liang, X. Gu, G. Yue, Z. Shi, and K. Kofoid, “Haploidy in sorghum,” in In Vitro Haploid Production in Higher Plants, Springer, 1997, pp. 149–161.
[24] N. Kumaravadivel and S. R. Sree Rangasamy, “Plant regeneration from sorghum anther cultures and field evaluation of progeny,” Plant Cell Reports, vol. 13, pp. 286–290, Feb. 1994.
[25] R. V. Sairam and N. Seetharama, “Androgenic response of cultured anthers and microspores of sorghum,” International Sorghum and Millets Newsletter, vol. 37, pp. 69–71, 1996.
[26] S. Dora, S. Polumahanthi, and N. S. Mani, “Efficient callus induction protocol for Sorghum bicolor,” Asian Journal of Plant Science and Research, vol. 4, pp. 14–21, 2014.
[27] D. C. Nguyen, S. Nakamura, A. D. H. Totok, and T. Yoshida, “Effects of physiological status of parent plants and culture medium composition on the anther culture of sorghum,” Plant Production Science, vol. 1, pp. 211–215, 1998.
[28] N. Kumaravadivel and S. R. S. Rangasamy, “Plant regeneration from sorghum anther cultures and field evaluation of progeny,” Plant Cell Reports, vol. 13, pp. 286–290, 1994.
[29] I. Arulselvi and S. Krishnaveni, “Effect of hormones, explants and genotypes in vitro culturing of sorghum,” Journal of Biochemical Technology, vol. 1, pp. 96–103, 2009.
[30] A. Bidmeshkipour, R. Thengane, M. Bahagvat, S. Ghaffari, and V. Rau, “Production of haploid wheat via maize pollination,” Journal of Sciences, Islamic Republic of Iran, vol. 18, pp. 5–11, 2007.
[31] S. Sato, T. Clemente, and I. Dweikat, “Identification of an elite sorghum genotype with high in vitro performance capacity,” In Vitro Cellular & Developmental Biology-Plant, vol. 40, pp. 57–60, 2004.
[32] A. Raghuwanshi and R. G. Birch, “Genetic transformation of sweet sorghum,” Plant Cell Reports, vol. 29, pp. 997–1005, 2010.
[33] W. Powell, “The influence of genotype and temperature pre-treatment on anther culture response in barley (Hordeum vulgare L.),” Plant Cell, Tissue and Organ Culture, vol. 12, pp. 291–297, 1988.
[34] R. Siddique, “Impact of different media and genotypes in improving anther culture response in rice (Oryza sativa) in Bangladesh,” European Scientific Journal, vol. 11, 2015.
[35] T. D. Silva, “Microspore embryogenesis” in Embryogenesis, Croatia, EU: InTech, 2012.
[36] G. Q. Liu, E. K. Gilding, and I. D. Godwin, “A robust tissue culture system for sorghum Sorghum bicolor (L.) Moench,” South African Journal of Botany, vol. 98, pp. 157–160, May 2015.
[37] L. Elkonin and N. Pakhomova, “Influence of nitrogen and phosphorus on induction embryogenic callus of sorghum,” Plant Cell, Tissue and Organ Culture, vol. 61, pp. 115–123, 2000.
[38] E. R. J. Keller and L. Korzun, “Ovary and ovule culture for haploid production,” in In Vitro Haploid Production in Higher Plants: Volume 1: Fundamental Aspects and Methods. Dordrecht: Springer, 1996, pp. 217–235.
[39] B. Bohanec, Doubled Haploids via Gynogenesis. Dordrecht: Springer, 2009, pp. 35–46.
[40] I. W. Paulson, “Embryogeny and caryopsis development of Sorghum bicolor (L.) Moench,” Crop Science, vol. 9, no. 1, pp. 97–102, 1969.
[41] M. Mdarhri-Alaoui, N. Saidi, A. Chlyah, and H. Chlyah, “Green haploid plant formation in durum wheat through in vitro gynogenesis,” Comptes Rendus de l’Academie des Sciences Series III Sciences de la Vie, vol. 321, pp. 25–30, 1998.
[42] L. S. Bates and C. W. Deyoe, “Wide Hybridization and Cereal Improvement,” Economic Botany, vol. 27, pp. 401–412, 1973.
[43] M. Inagaki, “Wheat haploids through the bulbosum technique,” in Wheat, Heidelberg, Berlin: Springer, 1990, pp. 448–459.
[44] P. Hayes, A. Corey, and J. DeNoma, “Doubled haploid production in barley using the Hordeum bulbosum (L.) technique,” in Doubled Haploid Production in Crop Plants, Dordrecht: Springer, 2003, pp. 5–14.
[45] H. W. Rines, “Oat haploids from wide hybridization,” in Doubled Haploid Production in Crop Plants, Netherlands: Springer, 2003, pp. 155–159.
[46] B. Duara and G. Stebbins Jr, “A polyhaploid obtained from a hybrid derivative of Sorghum halepense x S. vulgare var. sudanense,” Genetics, vol. 37, pp. 369–374, 1952.
[47] D. A. Laurie and M. D. Bennett, “Cytological evidence for fertilization in hexaploid wheat × sorghum crosses,” Plant Breeding, vol. 100, pp. 73–82, 1988.
[48] M. Inagaki and A. Mujeeb-Kazi, “Comparison of polyhaploid production frequencies in crosses of hexaploid wheat with maize, pearl millet and sorghum,” Japanese Journal of Breeding, vol. 45, pp. 157–161, 1995.
[49] C. D. Palmer and W. Keller, “Challenges and limitations to the use of haploidy in crop improvement,” in Haploids in Crop Improvement II, Heidelberg, Berlin: Springer, 2005, pp. 295–303.
[50] J. Maluszynska, “Cytogenetic tests for ploidy level analyses—chromosome counting,” in Doubled Haploid Production in Crop Plants, Dordrecht: Springer, 2003, pp. 391–395.
[51] L. Leus, K. Van Laere, A. Dewitte, and J. Van Huylenbroeck, “Flow cytometry for plant breeding,” in XXIII International Eucarpia Symposium, Section Ornamentals: Colourful Breeding and Genetics, Belgium: International Society for Horticultural Science (ISHS), 2009, pp. 221–226.
[52] S. J. Ochatt, “Flow cytometry in plant breeding,” Cytometry part A, vol. 73, pp. 581–598, 2008.
[53] B. Bohanec, Ploidy Determination Using Flow Cytometry. Dordrecht: Springer, 2003, pp. 397–403.
[54] J. S. Johnston, M. D. Bennett, A. L. Rayburn, D. W. Galbraith, and H. J. Price, “Reference standards for determination of DNA content of plant nuclei,” American Journal of Botany, vol. 86, pp. 609–613, 1999.
[55] J. M. Beaulieu, I. J. Leitch, S. Patel, A. Pendharkar, and C. A. Knight, “Genome size is a strong predictor of cell size and stomatal density in angiosperms,” New Phytologist, vol. 179, pp. 975–986, 2008.
[56] H. Vandenhout, R. Ortiz, D. Vuylsteke, R. Swennen, and K. Bai, “Effect of ploidy on stomatal and other quantitative traits in plantain and banana hybrids,” Euphytica, vol. 83, pp. 117–122, 1995.
[57] K. J. Kasha, “Chromosome doubling and recovery of doubled haploid plants,” in Haploids in Crop Improvement II, Heidelberg, Berlin: Springer, 2005, pp. 123–152.
[58] S. Antoine-Michard and M. Beckert, “Spontaneous versus colchicine-induced chromosome doubling in maize anther culture,” Plant Cell, Tissue and Organ Culture, vol. 48, no. 3, pp. 203–207, 1997.
[59] Y.-D. Guo and S. Pulli, “An efficient androgenic embryogenesis and plant regeneration method through isolated microspore culture in timothy (Phleum pratense L.),” Plant Cell Reports, vol. 19, pp. 761–767, 2000.
[60] Y. Y. Leung, L. L. Y. Hui, and V. B. Kraus, “Colchicine -- update on mechanisms of action and therapeutic uses,” Seminars in Arthritis and Rheumatism, vol. 45, no. 3, pp. 341–350, Dec. 2015.
[61] A. Nowakowska, E. Skrzypek, I. Marcińska, I. Czyczyło-Mysza, K. Dziurka, K. Juzoń, T. Warzecha, A. Sutkowska, Z. Nita, and K. Werwińska, “Application of chosen factors in the wide crossing method for the production of oat doubled haploids,” Open Life Sciences, vol. 10, pp. 99–105, 2015.
[62] Y. Finkelstein, S. E. Aks, J. R. Hutson, D. N. Juurlink, P. Nguyen, G. Dubnov-Raz, U. Pollak, G. Koren, and Y. Bentur, “Colchicine poisoning: The dark side of an ancient drug,” Clinical Toxicology, vol. 48, pp. 407–414, 2010.
[63] A. E. Melchinger, W. S. Molenaar, V. Mirdita, and W. Schipprack, “Colchicine alternatives for chromosome doubling in maize haploids for doubled-haploid production,” Crop Science, vol. 56, pp. 559–569, 2016.
[64] A. L. Hansen, A. Gertz, M. Joersbo, and S. B. Andersen, “Antimicrotubule herbicides for in vitro chromosome doubling in Beta vulgaris L. ovule culture,” Euphytica, vol. 101, pp. 231–237, 1998.
[2] S. Rao, B. V. Reddy, N. Nagaraj, and H. D. Upadhyaya, “Sorghum production for diversified uses,” in Genetics, Genomics and Breeding of Sorghum, Florida: CRC Press, 2014, pp. 1–27.
[3] W. L. Rooney, J. Blumenthal, B. Bean, and J. E. Mullet, “Designing sorghum as a dedicated bioenergy feedstock,” Biofuels, Bioproducts and Biorefining, vol. 1, pp. 147–157, 2007.
[4] W. Zegada-Lizarazu and A. Monti, “Are we ready to cultivate sweet sorghum as a bioenergy feedstock? A review on field management practices,” Biomass and Bioenergy, vol. 40, pp. 1–12, 2012.
[5] M. Wędzony, B. P. Forster, I. Żur, E. Golemiec, M. Szechyńska-Hebda, E. Dubas, G. Gotębiowska, and M. Wędzony, “Progress in doubled haploid technology in higher plants,” in Advances in Haploid Production in Higher Plants, Netherlands: Springer Netherlands, 2009, pp. 1–33.
[6] R. Fritsche-Neto, D. D. Garbuglio, and A. Borém, “Double haploids,” in Biotechnology and Plant Breeding, San Diego: Academic Press, 2014, pp. 201–224.
[7] G. N. De La Fuente, U. K. Frei, and T. Lübberstedt, “Accelerating plant breeding,” Trends in Plant Science, vol. 18, pp. 667–672, 2013.
[8] B. Hussain, M. A. Khan, Q. Ali, and S. Shaukat, “Why double haploid production is the best method for genetic improvement and genetic studies of wheat?,” International Journal for Agro Veterinary and Medical Sciences, vol. 6, pp. 216–228, 2012.
[9] V. K. Mishra and R. Gowswami, “Haploid production in higher plant,” International Journal of Chemical and Biological Sciences, vol. 1, pp. 26–45, 2014.
[10] A. Castillo, L. Cistue, M. Valles, J. Sanz, I. Romagosa, and J. L. Molina-Cano, “Efficient production of androgenic doubled-haploid mutants in barley by the application of sodium azide to anther and microspore cultures,” Plant Cell Reports, vol. 20, pp. 105–111, 2001.
[11] G. S. Khush and S. S. Virmani, “Haploids in plant breeding,” in In Vitro Haploid Production in Higher Plants, Dordrecht: Springer, 1996, pp. 11–33.
[12] M. Rahman and M. Michalak de Jiménez, “Behind the scenes of microspore-based double haploid development in Brassica napus: A review,” Journal of Plant Science and Molecular Breeding, vol. 5, pp. 1, 2016.
[13] A. F. Blaskeslee and J. Belling, “Chromosomal mutations in the Jimson weed, Datura stramonium,” Journal of Heredity, vol. 15, pp. 195–206, 1924.
[14] C. D. Palmer and W. A. Keller, “Overview of haploidy,” in Haploids in Crop Improvement II, Springer, 2005, pp. 3–9.
[15] J. M. Dunwell, “Haploids in flowering plants: Origins and exploitation,” Plant Biotechnology Journal, vol. 8, pp. 377–424, 2010.
[16] M. A. Germana, “Anther culture for haploid and doubled haploid production,” Plant Cell Tissue and Organ Culture, vol. 104, pp. 283–300, Mar. 2011.
[17] M. Maluszynski, K. Kasha, B. P. Forster, and I. Szarejko, Doubled Haploid Production in Crop Plants: A Manual, Springer Science & Business Media, 2003.
[18] P. S. Rao and P. Suprasanna, “Methods to double haploid chromosome numbers,” in In Vitro Haploid Production in Higher Plants, Springer Netherlands, 1996, pp. 317–339.
[19] N. Naik, P. Rout, N. Umakanta, R. L. Verma, J. L. Katara, K. K. Sahoo, O. N. Singh, and S. Samantaray, “Development of doubled haploids from an elite indica rice hybrid (BS6444G) using anther culture,” Plant Cell, Tissue and Organ Culture, vol. 128, pp. 679–689, 2017.
[20] A. Ismaili and P. P. Mohammadi, “Effect of genotype, induction medium, carbohydrate source, and polyethylene glycol on embryogenesis in maize (Zea mays L.) anther culture,” Acta Physiologiae Plantarum, vol. 38, pp. 74, 2016.
[21] S. Sriskandarajah, M. Sameri, E. Lerceteau-Köhler, and A. Westerbergh, “Increased recovery of green doubled haploid plants from barley anther culture,” Crop Science, vol. 55, pp. 2806–2812, 2015.
[22] L. Zhao, L. Liu, J. Wang, H. Guo, J. Gu, S. Zhao, J. Li, and Y. Xie, “Development of a new wheat germplasm with high anther culture ability by using a combination of gamma-ray irradiation and anther culture,” Journal of the Science of Food and Agriculture, vol. 95, pp. 120–125, 2015.
[23] G. H. Liang, X. Gu, G. Yue, Z. Shi, and K. Kofoid, “Haploidy in sorghum,” in In Vitro Haploid Production in Higher Plants, Springer, 1997, pp. 149–161.
[24] N. Kumaravadivel and S. R. Sree Rangasamy, “Plant regeneration from sorghum anther cultures and field evaluation of progeny,” Plant Cell Reports, vol. 13, pp. 286–290, Feb. 1994.
[25] R. V. Sairam and N. Seetharama, “Androgenic response of cultured anthers and microspores of sorghum,” International Sorghum and Millets Newsletter, vol. 37, pp. 69–71, 1996.
[26] S. Dora, S. Polumahanthi, and N. S. Mani, “Efficient callus induction protocol for Sorghum bicolor,” Asian Journal of Plant Science and Research, vol. 4, pp. 14–21, 2014.
[27] D. C. Nguyen, S. Nakamura, A. D. H. Totok, and T. Yoshida, “Effects of physiological status of parent plants and culture medium composition on the anther culture of sorghum,” Plant Production Science, vol. 1, pp. 211–215, 1998.
[28] N. Kumaravadivel and S. R. S. Rangasamy, “Plant regeneration from sorghum anther cultures and field evaluation of progeny,” Plant Cell Reports, vol. 13, pp. 286–290, 1994.
[29] I. Arulselvi and S. Krishnaveni, “Effect of hormones, explants and genotypes in vitro culturing of sorghum,” Journal of Biochemical Technology, vol. 1, pp. 96–103, 2009.
[30] A. Bidmeshkipour, R. Thengane, M. Bahagvat, S. Ghaffari, and V. Rau, “Production of haploid wheat via maize pollination,” Journal of Sciences, Islamic Republic of Iran, vol. 18, pp. 5–11, 2007.
[31] S. Sato, T. Clemente, and I. Dweikat, “Identification of an elite sorghum genotype with high in vitro performance capacity,” In Vitro Cellular & Developmental Biology-Plant, vol. 40, pp. 57–60, 2004.
[32] A. Raghuwanshi and R. G. Birch, “Genetic transformation of sweet sorghum,” Plant Cell Reports, vol. 29, pp. 997–1005, 2010.
[33] W. Powell, “The influence of genotype and temperature pre-treatment on anther culture response in barley (Hordeum vulgare L.),” Plant Cell, Tissue and Organ Culture, vol. 12, pp. 291–297, 1988.
[34] R. Siddique, “Impact of different media and genotypes in improving anther culture response in rice (Oryza sativa) in Bangladesh,” European Scientific Journal, vol. 11, 2015.
[35] T. D. Silva, “Microspore embryogenesis” in Embryogenesis, Croatia, EU: InTech, 2012.
[36] G. Q. Liu, E. K. Gilding, and I. D. Godwin, “A robust tissue culture system for sorghum Sorghum bicolor (L.) Moench,” South African Journal of Botany, vol. 98, pp. 157–160, May 2015.
[37] L. Elkonin and N. Pakhomova, “Influence of nitrogen and phosphorus on induction embryogenic callus of sorghum,” Plant Cell, Tissue and Organ Culture, vol. 61, pp. 115–123, 2000.
[38] E. R. J. Keller and L. Korzun, “Ovary and ovule culture for haploid production,” in In Vitro Haploid Production in Higher Plants: Volume 1: Fundamental Aspects and Methods. Dordrecht: Springer, 1996, pp. 217–235.
[39] B. Bohanec, Doubled Haploids via Gynogenesis. Dordrecht: Springer, 2009, pp. 35–46.
[40] I. W. Paulson, “Embryogeny and caryopsis development of Sorghum bicolor (L.) Moench,” Crop Science, vol. 9, no. 1, pp. 97–102, 1969.
[41] M. Mdarhri-Alaoui, N. Saidi, A. Chlyah, and H. Chlyah, “Green haploid plant formation in durum wheat through in vitro gynogenesis,” Comptes Rendus de l’Academie des Sciences Series III Sciences de la Vie, vol. 321, pp. 25–30, 1998.
[42] L. S. Bates and C. W. Deyoe, “Wide Hybridization and Cereal Improvement,” Economic Botany, vol. 27, pp. 401–412, 1973.
[43] M. Inagaki, “Wheat haploids through the bulbosum technique,” in Wheat, Heidelberg, Berlin: Springer, 1990, pp. 448–459.
[44] P. Hayes, A. Corey, and J. DeNoma, “Doubled haploid production in barley using the Hordeum bulbosum (L.) technique,” in Doubled Haploid Production in Crop Plants, Dordrecht: Springer, 2003, pp. 5–14.
[45] H. W. Rines, “Oat haploids from wide hybridization,” in Doubled Haploid Production in Crop Plants, Netherlands: Springer, 2003, pp. 155–159.
[46] B. Duara and G. Stebbins Jr, “A polyhaploid obtained from a hybrid derivative of Sorghum halepense x S. vulgare var. sudanense,” Genetics, vol. 37, pp. 369–374, 1952.
[47] D. A. Laurie and M. D. Bennett, “Cytological evidence for fertilization in hexaploid wheat × sorghum crosses,” Plant Breeding, vol. 100, pp. 73–82, 1988.
[48] M. Inagaki and A. Mujeeb-Kazi, “Comparison of polyhaploid production frequencies in crosses of hexaploid wheat with maize, pearl millet and sorghum,” Japanese Journal of Breeding, vol. 45, pp. 157–161, 1995.
[49] C. D. Palmer and W. Keller, “Challenges and limitations to the use of haploidy in crop improvement,” in Haploids in Crop Improvement II, Heidelberg, Berlin: Springer, 2005, pp. 295–303.
[50] J. Maluszynska, “Cytogenetic tests for ploidy level analyses—chromosome counting,” in Doubled Haploid Production in Crop Plants, Dordrecht: Springer, 2003, pp. 391–395.
[51] L. Leus, K. Van Laere, A. Dewitte, and J. Van Huylenbroeck, “Flow cytometry for plant breeding,” in XXIII International Eucarpia Symposium, Section Ornamentals: Colourful Breeding and Genetics, Belgium: International Society for Horticultural Science (ISHS), 2009, pp. 221–226.
[52] S. J. Ochatt, “Flow cytometry in plant breeding,” Cytometry part A, vol. 73, pp. 581–598, 2008.
[53] B. Bohanec, Ploidy Determination Using Flow Cytometry. Dordrecht: Springer, 2003, pp. 397–403.
[54] J. S. Johnston, M. D. Bennett, A. L. Rayburn, D. W. Galbraith, and H. J. Price, “Reference standards for determination of DNA content of plant nuclei,” American Journal of Botany, vol. 86, pp. 609–613, 1999.
[55] J. M. Beaulieu, I. J. Leitch, S. Patel, A. Pendharkar, and C. A. Knight, “Genome size is a strong predictor of cell size and stomatal density in angiosperms,” New Phytologist, vol. 179, pp. 975–986, 2008.
[56] H. Vandenhout, R. Ortiz, D. Vuylsteke, R. Swennen, and K. Bai, “Effect of ploidy on stomatal and other quantitative traits in plantain and banana hybrids,” Euphytica, vol. 83, pp. 117–122, 1995.
[57] K. J. Kasha, “Chromosome doubling and recovery of doubled haploid plants,” in Haploids in Crop Improvement II, Heidelberg, Berlin: Springer, 2005, pp. 123–152.
[58] S. Antoine-Michard and M. Beckert, “Spontaneous versus colchicine-induced chromosome doubling in maize anther culture,” Plant Cell, Tissue and Organ Culture, vol. 48, no. 3, pp. 203–207, 1997.
[59] Y.-D. Guo and S. Pulli, “An efficient androgenic embryogenesis and plant regeneration method through isolated microspore culture in timothy (Phleum pratense L.),” Plant Cell Reports, vol. 19, pp. 761–767, 2000.
[60] Y. Y. Leung, L. L. Y. Hui, and V. B. Kraus, “Colchicine -- update on mechanisms of action and therapeutic uses,” Seminars in Arthritis and Rheumatism, vol. 45, no. 3, pp. 341–350, Dec. 2015.
[61] A. Nowakowska, E. Skrzypek, I. Marcińska, I. Czyczyło-Mysza, K. Dziurka, K. Juzoń, T. Warzecha, A. Sutkowska, Z. Nita, and K. Werwińska, “Application of chosen factors in the wide crossing method for the production of oat doubled haploids,” Open Life Sciences, vol. 10, pp. 99–105, 2015.
[62] Y. Finkelstein, S. E. Aks, J. R. Hutson, D. N. Juurlink, P. Nguyen, G. Dubnov-Raz, U. Pollak, G. Koren, and Y. Bentur, “Colchicine poisoning: The dark side of an ancient drug,” Clinical Toxicology, vol. 48, pp. 407–414, 2010.
[63] A. E. Melchinger, W. S. Molenaar, V. Mirdita, and W. Schipprack, “Colchicine alternatives for chromosome doubling in maize haploids for doubled-haploid production,” Crop Science, vol. 56, pp. 559–569, 2016.
[64] A. L. Hansen, A. Gertz, M. Joersbo, and S. B. Andersen, “Antimicrotubule herbicides for in vitro chromosome doubling in Beta vulgaris L. ovule culture,” Euphytica, vol. 101, pp. 231–237, 1998.