Pepper (Capsicum annuum L.) anther culture: fundamentalresearch and practical applications

Pepper (Capsicum annuum L.) anther culture: fundamentalresearch and practical applications

To create new varieties resistant to biotic and abiotic stress factors that possess high productivity and improved fruit quality, breeders require modern breeding methods and techniques. Double haploid (DH) lines are an invaluable breeding element due to their guaranteed, completely homozygous nature. One of the fastest methods for obtaining DH lines is anther culture. Microspore embryogenesis provides considerable opportunities in the areas of breeding and biotechnology and represents a model system for fundamental biological research. The effectiveness of pepper anther culture is still low, which affects the application of DH lines in breeding programs. A detailed study of the anther culture process will produce a deeper understanding of the mechanisms that underlie the switch from gametophyte to sporophyte during embryo development. In this respect, the genes expressed during microspore embryogenesis and those that control the cellular response to stress have a key role. This review provides information about the control of embryo formation together with the features of practical application of pepper anther culture.

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  • Conclusion The significant advantage of in vitro androgenesis as a breeding tool is that it speeds up both processes: achieving homozygosity and increasing selection efficiency. Pepper belongs to androgenesis-recalcitrant plants, characterized by a low frequency of embryo induction from anthers and a low rate of plant regeneration. Therefore, it is necessary to investigate the changes, cytological and biochemical, that occur in cells during the switch from gametophyte to sporophyte pathways of microspore development in vitro. Clarifying the genetic control of different stages of embryo transformation is a milestone for improvement of the pepper androgenetic process. Research work with pepper in this vein is still at an early stage, and extensive experimental work is required to identify the genes responsible for microspore embryogenesis and their expression in different embryo transformation stages. Such knowledge could lead to more efficient protocols for embryo induction and regeneration from pepper anthers and microspores. This, in turn, will increase the number of researchers who can apply anther culture as their method of choice in future projects related to pepper breeding. References Abak K, Pochard E, Dumas de Vaulx R (1982). Transmission of resistance to Phytophthora capsici on roots and stems of pepper plants: study of doubled haploid lines issued from the cross “PM 217” x “Yolo Wonder” through anther culture. Capsicum Newsl 1: 62-64. Alremi F, Taşkın H, Sönmez K, Büyükalaca S, Ellialtıoğlu Ş (2014). Effect of genotype and nutrient medium on anther culture of pepper ( Capsicum annuum L.). Turk J Agric Natur Sci 1: 108- 116 (article in Turkish with an abstract in English). Arı E, Bedir H, Yıldırım S, Yıldırım T (2016). Androgenic responses of 64 ornamental pepper ( Capsicum annuum L.) genotypes to shed-microspore culture in autumn season. Turk J Biol 40: 706 − 717. 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Successful development of new sweet (hot) pepper cultivars by anther culture. Acta Hortic 402: 442- 444. Djian-Caporalino C, Fazari A, Arguel MJ,·Vernie T, VandeCasteele C, Faure I, Brunoud G, Pijarowski L, Palloix A, Lefebvre V, Abad P (2007). Root-knot nematode ( Meloidogyne spp.) Me resistance genes in pepper ( Capsicum annuum L.) are clustered on the P9 chromosome. Theor Appl Genet 114: 473-486. Dumas de Vaulx R, Chambonnet D, Pochard E (1981). In vitro anther culture in red pepper ( Capsicum annuum L.): improvement of the rate of plant production in different genotypes by treatments at 35 °C. Agronomie 1: 859-864. Dunwell JM (2010). Haploids in flowering plants: origins and exploitation. Plant Biotechnol J 8: 377-424. Ercan N, Sensoy FA, Sensoy AS (2006). Influence of growing season and donor plant age on anther culture response of some pepper cultivars ( Capsicum annuum L.). Sci Hortic- Amsterdam 110: 16-20. Ercan N, Şensoy FA (2011). Androgenic responses of different ( Capsicum annuum L.) cultivars. Biyoloji Bilimleri Arastirma Dergisi 4: 59-61. Forster BP, Heberle-Bors E, Kasha KJ, Touraev A (2007). The resurgence of haploids in higher plants. Trends Plant Sci 12: 368-375. Gémesné JA, Gyulai G, Petus M, Venczel G, Ségi Z, Zatyko L (2000). DH-breeding of sweet pepper ( Capsicum annuum L.). In: Biotechnological Approaches for Utilization of Gametic Cells, COST 824, final meeting, Bled, Slovenia, pp. 157-159. Gémesné Juhász A, Petus M, Venczel G, Zatykó L, Gyulai G, Cséplö M (2001). Genetic variability of anther donor versus spontaneous doubled haploid descendants and colchicines induced doubled haploid sweet pepper ( Capsicum annuum L.) lines. Acta Hortic 560: 149-152. Gémes Juhász A, Kristóf Z, Vági P, Lantos C, Pauk J (2009). In vitro anther and isolated microspore culture as tools in sweet and spice pepper breeding. Acta Hortic 829: 61-64. George L, Narayanaswamy S (1973). Haploid Capsicum through experimental androgenesis. Protoplasma 78: 467-480. Germanà MA (2011). Anther culture for haploid and doubled haploid production. Plant Cell Tiss Org 104: 283-300. González-Melendi P, Testillano PS, Ahmadian P, Fadón B, Vicente O, Risueño MC (1995). In situ characterization of the late vacuolate microspore as a convenient stage to induce embryogenesis in Capsicum. Protoplasma 187: 60-71. Grozeva S, Rodeva V, Todorova V, Pundeva R (2009). Obtaining of pepper plants via anther culture. Genet Breed 38: 25-31. Grozeva S, Todorova V, Cholakov T, Rodeva V (2013). Effect of temperature and growth period of donor plants on pepper anther culture. In: 3rd International Conference— Research People and Actual Tasks on Multidisciplinary Sciences. Lozenec, Bulgaria, pp. 60-64. Gyulai G, Gémesné JA, Sági Z, Venczel G, Pintér P, Kristóf Z, Törjék O, Heszky L, Bottka S, Kiss J et al. (2000). Doubled haploid development and PCR-analysis of F1 hybrid derived DH-R2 paprika ( Capsicum annuum L.) lines. J Plant Physiol 156: 168- 174. Gyulai G, Gémesné JA, Sági Z, Zatykó L, Heszhy L, Venczel G (1999). PCR analysis of F 1 hybrid derived DH pepper lines. Capsicum & Eggplant Newsl 18: 40-43. Hwang JK, Paek KY, Cho DH (1998). Breeding of resistant pepper lines ( Capsicum annuum L.) to bacterial spot ( Xanthomonas campestris pv. vesicatoria) through anther culture. Acta Hortic 461: 301-310. Irikova T, Denev I (2008). Identification of two embryogenesis- related genes in sweet pepper ( Capsicum annuum L.) genome. CR Acad Bulg Sci 61: 761-770. Irikova T, Grozeva S, Denev I (2012). Identification of BABY BOOM and LEAFY COTYLEDON genes in sweet pepper ( Capsicum annuum L.) genome by their partial gene sequences. Plant Growth Regul 67: 191-198. Irikova T, Grozeva S, Popov P, Rodeva V, Todorovska E (2011b). In vitro response of pepper anther culture ( Capsicum annuum L.) depending on genotype, culture medium and duration of cultivation. Biotechnol Biotech Eq 25: 2604-2609. Irikova T, Grozeva S, Rodeva V (2011a). Anther culture in pepper ( Capsicum annuum L.) in vitro. Acta Physiol Plant 33: 1559- 1570. Janzac B, Fabre MF, Palloix A, Moury B (2009). Phenotype and spectrum of action of the Pvr4 resistance in pepper against potyviruses, and selection for virulent variants. Plant Pathology 58: 443-449. Kaplan DR, Cooke TJ (1997). Fundamental concepts in the embryogenesis of dicotyledons: a morphological interpretation of embryo mutants. Plant Cell 9: 1903-1919. Kim M, Jang IC, Kim JA, Park EJ, Yoon M, Lee Y (2008). Embryogenesis and plant regeneration of hot pepper (Capsicum annuum L.) through isolated microspore culture. Plant Cell Rep 27: 425-434. Kim M, Park EJ, Lee Y (2013). High-quality embryo production and plant regeneration using a two-step culture system in isolated microspore cultures of hot pepper ( Capsicum annuum L.). Plant Cell Tiss Org Cult 112: 191-201. Kisia ł a A, Olszewska D, Niklas-Nowak A, Nowaczyk P (2011). Biometrical characteristics of R 2 generation of anther-derived pepper ( Capsicum spp.) plants. Acta Agrobot 64: 53-58. Koleva-Gudeva L, Gulaboski R, Janevik-Ivanovska E, Trajkova F, Maksimova V (2013). Capsaicin—inhibitory factor for somatic embryogenesis in pepper anther culture. Electron J Biol 9: 29-36. Koleva-Gudeva L, Spasenoski M, Trajkova F (2007). Somatic embryogenesis in pepper anther culture: the effect of incubation treatments and different media. Sci Hortic 111: 114-119. Koleva-Gudeva L, Trajkova F (2012). Anther culture of pepper: morphological characteristics of fruits of androgenetic pepper lines ( Capsicum annuum L.). J Res Agric 1: 136-145. Krasteva L, Pandeva R, Rodeva R, Todorova V, Neykov S, Uzundzhalieva K, Velcheva N, Cvikić D, Tome E, Ilieva V (2012). Pepper as a target object of SEE-ERA.NET PROJECT. Acta Hortic 960: 151-158. Kuo JS, Wang YY, Chien NF, Ku SJ, Kung ML, Hsu HC (1973). Investigations on the anther culture in vitro of Nicotiana tabacum and Capsicum annuum . Acta Bot Sin 15: 36-52. Lantos C, Juhász AG, Somogyi G, Ötvös K, Vági P, Mihály R, Kristóf Z, Somogyi N, Pauk J (2009). Improvement of isolated microspore culture of pepper ( Capsicum annuum L.) via co- culture with ovary of pepper or wheat. Plant Cell Tiss Org Cult 97: 285-293. POPOVA IRIKOVA et al. / Turk J Biol 725 Lantos C, Juhász AG, Somogyi G, Vági P, Mihály R, Kristóf Z, Pauk J (2012). Androgenesis induction in microspore culture of sweet pepper ( Capsicum annuum L.). Plant Biotechnol Rep 6: 123- 132. Lee Y, Chae K, Ha J, Lee JS, Jang IC, Jeong S, Kim M, Yoon M (2009). A novel stress-related gene in developing pepper anthers. Russ J Plant Physiol 56: 654-662. Liu WY, Yang HB, Jo YD, Jeong HJ, Kang BC (2013). Classical genetics and traditional breeding in pepper. In: Kang BC, Kole C, editors. Genetics, Genomics and Breeding of Pepper and Eggplants. Boca Raton, FL, USA: CRC Press, Taylor & Francis Group, pp. 16-39. Luitel B, Adhikari P, Shrestha S, Kang W (2012). Morphological characterization of anther derived plants in minipaprika ( Capsicum annuum L.). Kor J Breed Sci 44: 450-461. Luitel B, Kang W (2013a). In vitro androgenic response of minipaprika ( Capsicum annuum L.) genotypes in different culture media. Hort Environ Biotechnol 54: 162-171. Luitel B, Kang W (2013b). Assessment of fruit quality variation in doubled haploids of minipaprika ( Capsicum annuum L.). Hortic Environ Biotechnol 54: 257-265. Madhusudhana R (2015). Linkage mapping. In: Madhusudhana R, Rajendrakumar P, Patil JV, editors. Sorghum Molecular Breeding. India: Springer, pp. 47-70. Magnard JL, Le Deunff E, Domenech J, Rogowsky PM, Testillano PS, Rougier M, Risueño MC, Vergne P, Dumas C (2000). Genes normally expressed in the endosperm are expressed at early stages of microspore embryogenesis in maize. Plant Mol Biol 44: 559-574. Malik M, Wang F, Dirpaul J, Zhou N, Polowick P, Ferrie A, Krochko J (2007). Transcript profiling and identification of molecular markers for early microspore embryogenesis in Brassica napus . Plant Physiol 144: 134-154. Malik MR, Krochko JE (2009). Gene expression profiling of microspore embryogenesis in Brassica napus . In: Touraev A, Forster BP, Jain SM, editors. Advances in Haploid Production in Higher Plants. The Netherlands: Springer, pp. 115-125. Mannerlof M, Tenning P (1997). Screening of transgenic plants by multiplex PCR. Plant Mol Biol Rep 15: 38-45. Maraschin SF, de Priester W, Spaink HP, Wang M (2005). Androgenic switch: an example of plant embryogenesis from the male gametophyte perspective. J Exp Bot 56: 1711-1726. Mimura Y, Inoue T, Minamiyama Y, Kubo N (2012). An SSR-based genetic map of pepper ( Capsicum annuum L.) serves as an anchor for the alignment of major pepper maps. Breed Sci 62: 93-98. Minamiyama Y, Tsuro M, Hirai M (2006). An SSR-based linkage map of Capsicum annuum . Mol Breed 18: 157-169. Mitykó J, Gémes Juhász A (2006). Improvement in the haploid technique routinely used for breeding sweet and spice peppers in Hungary. Acta Agron Hung 54: 203-219. Mitsushashi W, Yamashita T, Toyomasu T, Kashiwagi Y, Konnai T (2004). Sequential development of cysteine proteinase activities and gene expression during somatic embryogenesis in carrot. Biosci Biotechnol Biochem 68: 705-713. Mordhorst AP, Toonen MAJ, de Vries SC (1997). Plant embryogenesis. Crit Rev Plant Sci 16: 535-576. Murovec J, Bohanec B (2013). Haploids and doubled haploids in plant breeding. In: Abdurakhmonov I, editor. Plant Breeding. In Tech, pp. 87-105. Nervo G, Azzimonti MT, Bonelli A, Tamietti G (2007). 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Effect of 2,4-dichlorophenoxyacetic acid pretreatment of Capsicum spp. donor plants on the anther culture efficiency of lines selected by capsaicinoid content. BTa JBCBB 96: 179-183. Ochoa-Alejo N, Ramirez-Malagon R (2001). In vitro chili pepper biotechnology. In Vitro Cell Dev Biol Plant 37: 701-729. Olszewska D, Kisiała A, Niklas-Nowak A, Nowaczyk P (2014). Study of in vitro anther culture in selected genotypes of genus Capsicum . Turk J Biol 38: 118-124. Olszewska D, Kisia ł a A, Nowaczyk P (2011). The assessment of doubled haploid lines obtained in pepper ( Capsicum annuum L.) anther culture. Folia Hort 23: 93-99. Olszewska D, Niklas-Nowak A, Nowaczyk P (2010). Variation in the quantitative characters of androgenic pepper lines derived from hybrid Capsicum frutescens x Capsicum chinense jacq. Veget Crops Research Bul 73: 5-11. Özkum D, Tıpırdamaz R (2007). Effects of silver nitrate, activated charcoal and cold treatment on the in vitro androgenesis of pepper ( Capsicum annuum L.). Acta Hortic 729: 133-136. Parra-Vega V, González-García B, Seguí-Simarro JM (2013a). Morphological markers to correlate bud and anther development with microsporogenesis and microgametogenesis in pepper ( Capsicum annuum L.). Acta Physiol Plant 35: 627- 633. Dunwell JM (2010). Haploids in flowering plants: origins and exploitation. Plant Biotechnol J 8: 377-424. Ercan N, Sensoy FA, Sensoy AS (2006). Influence of growing season and donor plant age on anther culture response of some pepper cultivars ( Capsicum annuum L.). Sci Hortic- Amsterdam 110: 16-20. Ercan N, Şensoy FA (2011). Androgenic responses of different ( Capsicum annuum L.) cultivars. Biyoloji Bilimleri Arastirma Dergisi 4: 59-61. Forster BP, Heberle-Bors E, Kasha KJ, Touraev A (2007). The resurgence of haploids in higher plants. Trends Plant Sci 12: 368-375. Gémesné JA, Gyulai G, Petus M, Venczel G, Ségi Z, Zatyko L (2000). DH-breeding of sweet pepper ( Capsicum annuum L.). In: Biotechnological Approaches for Utilization of Gametic Cells, COST 824, final meeting, Bled, Slovenia, pp. 157-159. Gémesné Juhász A, Petus M, Venczel G, Zatykó L, Gyulai G, Cséplö M (2001). Genetic variability of anther donor versus spontaneous doubled haploid descendants and colchicines induced doubled haploid sweet pepper ( Capsicum annuum L.) lines. Acta Hortic 560: 149-152. Gémes Juhász A, Kristóf Z, Vági P, Lantos C, Pauk J (2009). In vitro anther and isolated microspore culture as tools in sweet and spice pepper breeding. Acta Hortic 829: 61-64. George L, Narayanaswamy S (1973). Haploid Capsicum through experimental androgenesis. Protoplasma 78: 467-480. Germanà MA (2011). Anther culture for haploid and doubled haploid production. Plant Cell Tiss Org 104: 283-300. González-Melendi P, Testillano PS, Ahmadian P, Fadón B, Vicente O, Risueño MC (1995). In situ characterization of the late vacuolate microspore as a convenient stage to induce embryogenesis in Capsicum. Protoplasma 187: 60-71. Grozeva S, Rodeva V, Todorova V, Pundeva R (2009). Obtaining of pepper plants via anther culture. Genet Breed 38: 25-31. Grozeva S, Todorova V, Cholakov T, Rodeva V (2013). Effect of temperature and growth period of donor plants on pepper anther culture. In: 3rd International Conference— Research People and Actual Tasks on Multidisciplinary Sciences. Lozenec, Bulgaria, pp. 60-64. Gyulai G, Gémesné JA, Sági Z, Venczel G, Pintér P, Kristóf Z, Törjék O, Heszky L, Bottka S, Kiss J et al. (2000). Doubled haploid development and PCR-analysis of F1 hybrid derived DH-R2 paprika ( Capsicum annuum L.) lines. J Plant Physiol 156: 168- 174. Gyulai G, Gémesné JA, Sági Z, Zatykó L, Heszhy L, Venczel G (1999). PCR analysis of F 1 hybrid derived DH pepper lines. Capsicum & Eggplant Newsl 18: 40-43. Hwang JK, Paek KY, Cho DH (1998). Breeding of resistant pepper lines ( Capsicum annuum L.) to bacterial spot ( Xanthomonas campestris pv. vesicatoria) through anther culture. Acta Hortic 461: 301-310. Irikova T, Denev I (2008). Identification of two embryogenesis- related genes in sweet pepper ( Capsicum annuum L.) genome. CR Acad Bulg Sci 61: 761-770. Irikova T, Grozeva S, Denev I (2012). Identification of BABY BOOM and LEAFY COTYLEDON genes in sweet pepper ( Capsicum annuum L.) genome by their partial gene sequences. Plant Growth Regul 67: 191-198. Irikova T, Grozeva S, Popov P, Rodeva V, Todorovska E (2011b). In vitro response of pepper anther culture ( Capsicum annuum L.) depending on genotype, culture medium and duration of cultivation. Biotechnol Biotech Eq 25: 2604-2609. Irikova T, Grozeva S, Rodeva V (2011a). Anther culture in pepper ( Capsicum annuum L.) in vitro. Acta Physiol Plant 33: 1559- 1570. Janzac B, Fabre MF, Palloix A, Moury B (2009). Phenotype and spectrum of action of the Pvr4 resistance in pepper against potyviruses, and selection for virulent variants. Plant Pathology 58: 443-449. Kaplan DR, Cooke TJ (1997). Fundamental concepts in the embryogenesis of dicotyledons: a morphological interpretation of embryo mutants. Plant Cell 9: 1903-1919. Kim M, Jang IC, Kim JA, Park EJ, Yoon M, Lee Y (2008). Embryogenesis and plant regeneration of hot pepper (Capsicum annuum L.) through isolated microspore culture. Plant Cell Rep 27: 425-434. Kim M, Park EJ, Lee Y (2013). High-quality embryo production and plant regeneration using a two-step culture system in isolated microspore cultures of hot pepper ( Capsicum annuum L.). Plant Cell Tiss Org Cult 112: 191-201. Kisia ł a A, Olszewska D, Niklas-Nowak A, Nowaczyk P (2011). Biometrical characteristics of R 2 generation of anther-derived pepper ( Capsicum spp.) plants. Acta Agrobot 64: 53-58. Koleva-Gudeva L, Gulaboski R, Janevik-Ivanovska E, Trajkova F, Maksimova V (2013). Capsaicin—inhibitory factor for somatic embryogenesis in pepper anther culture. Electron J Biol 9: 29-36. Koleva-Gudeva L, Spasenoski M, Trajkova F (2007). Somatic embryogenesis in pepper anther culture: the effect of incubation treatments and different media. Sci Hortic 111: 114-119. Koleva-Gudeva L, Trajkova F (2012). Anther culture of pepper: morphological characteristics of fruits of androgenetic pepper lines ( Capsicum annuum L.). J Res Agric 1: 136-145. Krasteva L, Pandeva R, Rodeva R, Todorova V, Neykov S, Uzundzhalieva K, Velcheva N, Cvikić D, Tome E, Ilieva V (2012). Pepper as a target object of SEE-ERA.NET PROJECT. Acta Hortic 960: 151-158. Kuo JS, Wang YY, Chien NF, Ku SJ, Kung ML, Hsu HC (1973). Investigations on the anther culture in vitro of Nicotiana tabacum and Capsicum annuum . Acta Bot Sin 15: 36-52. Lantos C, Juhász AG, Somogyi G, Ötvös K, Vági P, Mihály R, Kristóf Z, Somogyi N, Pauk J (2009). Improvement of isolated microspore culture of pepper ( Capsicum annuum L.) via co- culture with ovary of pepper or wheat. Plant Cell Tiss Org Cult 97: 285-293. POPOVA IRIKOVA et al. / Turk J Biol 725 Lantos C, Juhász AG, Somogyi G, Vági P, Mihály R, Kristóf Z, Pauk J (2012). Androgenesis induction in microspore culture of sweet pepper ( Capsicum annuum L.). Plant Biotechnol Rep 6: 123- 132. Lee Y, Chae K, Ha J, Lee JS, Jang IC, Jeong S, Kim M, Yoon M (2009). A novel stress-related gene in developing pepper anthers. Russ J Plant Physiol 56: 654-662. Liu WY, Yang HB, Jo YD, Jeong HJ, Kang BC (2013). Classical genetics and traditional breeding in pepper. In: Kang BC, Kole C, editors. Genetics, Genomics and Breeding of Pepper and Eggplants. Boca Raton, FL, USA: CRC Press, Taylor & Francis Group, pp. 16-39. Luitel B, Adhikari P, Shrestha S, Kang W (2012). Morphological characterization of anther derived plants in minipaprika ( Capsicum annuum L.). Kor J Breed Sci 44: 450-461. Luitel B, Kang W (2013a). In vitro androgenic response of minipaprika ( Capsicum annuum L.) genotypes in different culture media. Hort Environ Biotechnol 54: 162-171. Luitel B, Kang W (2013b). Assessment of fruit quality variation in doubled haploids of minipaprika ( Capsicum annuum L.). Hortic Environ Biotechnol 54: 257-265. Madhusudhana R (2015). Linkage mapping. In: Madhusudhana R, Rajendrakumar P, Patil JV, editors. Sorghum Molecular Breeding. India: Springer, pp. 47-70. Magnard JL, Le Deunff E, Domenech J, Rogowsky PM, Testillano PS, Rougier M, Risueño MC, Vergne P, Dumas C (2000). Genes normally expressed in the endosperm are expressed at early stages of microspore embryogenesis in maize. Plant Mol Biol 44: 559-574. Malik M, Wang F, Dirpaul J, Zhou N, Polowick P, Ferrie A, Krochko J (2007). Transcript profiling and identification of molecular markers for early microspore embryogenesis in Brassica napus . Plant Physiol 144: 134-154. Malik MR, Krochko JE (2009). Gene expression profiling of microspore embryogenesis in Brassica napus . In: Touraev A, Forster BP, Jain SM, editors. Advances in Haploid Production in Higher Plants. The Netherlands: Springer, pp. 115-125. Mannerlof M, Tenning P (1997). Screening of transgenic plants by multiplex PCR. Plant Mol Biol Rep 15: 38-45. Maraschin SF, de Priester W, Spaink HP, Wang M (2005). Androgenic switch: an example of plant embryogenesis from the male gametophyte perspective. J Exp Bot 56: 1711-1726. Mimura Y, Inoue T, Minamiyama Y, Kubo N (2012). An SSR-based genetic map of pepper ( Capsicum annuum L.) serves as an anchor for the alignment of major pepper maps. Breed Sci 62: 93-98. Minamiyama Y, Tsuro M, Hirai M (2006). An SSR-based linkage map of Capsicum annuum . Mol Breed 18: 157-169. Mitykó J, Gémes Juhász A (2006). Improvement in the haploid technique routinely used for breeding sweet and spice peppers in Hungary. Acta Agron Hung 54: 203-219. Mitsushashi W, Yamashita T, Toyomasu T, Kashiwagi Y, Konnai T (2004). Sequential development of cysteine proteinase activities and gene expression during somatic embryogenesis in carrot. Biosci Biotechnol Biochem 68: 705-713. Mordhorst AP, Toonen MAJ, de Vries SC (1997). Plant embryogenesis. Crit Rev Plant Sci 16: 535-576. Murovec J, Bohanec B (2013). Haploids and doubled haploids in plant breeding. In: Abdurakhmonov I, editor. Plant Breeding. In Tech, pp. 87-105. Nervo G, Azzimonti MT, Bonelli A, Tamietti G (2007). Application of in vitro anther culture methods to a pepper breeding program for disease resistance. In: Proceedings of the 51st Italian Society of Agricultural Genetics Annual Congress, Riva del Granda, Italy, Poster Abstract S 2.03. Niklas-Nowak A, Olszewska D, Kisiała A, Nowaczyk P (2012). Study of individual plant responsiveness in anther cultures of selected pepper ( Capsicum spp.) genotypes. Folia Hort 24: 141-146. Novak F (1974). Induction of a haploid callus in anther cultures of Capsicum sp. Z Pflanzenzücht 72: 46-54. Nowaczyk L, Banach-Szott M, Olszewska D, Nowaczyk P (2014). 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Turkish Journal of Biology-Cover
  • ISSN: 1300-0152
  • Yayın Aralığı: Yılda 6 Sayı
  • Yayıncı: TÜBİTAK
Sayıdaki Diğer Makaleler

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