Skip to main content
SpringerLink
Log in

Polyembryony: A Potential Horticultural Trait, Reveals Complex Mechanism, Role of Molecular Markers and their Application in Fruit Crops

  • Review
  • Published:
The Botanical Review Aims and scope Submit manuscript

Abstract

Rootstocks/scions with potential for commercial growing, either for the industry or fresh market, have been one of the main objectives of the fruit breeding programs. Fruit crop breeding has impediments like polyembryony (PE) which is otherwise desirable for clonal plant propagation. In nature PE exist in some fruit crops like citrus, mango, jamun, rose apple, almond etc. In polyembryonic crops, there is an occurrence of the more than one embryo in seed and subsequently numerous seedlings emerge from that single seed. The mother type seedlings are considered nucellar are often vigorous in nature as compared to zygotic ones. In this review, the classification, genetic basis and mechanism of PE has been discussed. In current review, morphogenetic authentication of seedling from polyembronic seed has been discussed in the light of recent research. Transcriptional pathway along with the inheritance pattern and molecular breeding aspects of PE has also been summarized.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

(Modified from Spillane et al., 2004)

Fig. 2
Fig. 3

Similar content being viewed by others

Data Availability

The authors confirm that the data supporting the findings of this study are available within the article.

References

  • Ahmad, M., Javaid, A., Rahman, H.U., Hussain, S.I., Ramzan, A., Ghafoor, A. 2012. Identification of mandarin x orange hybrids using simple-sequence repeat markers. J. Agric. Res. 50: 225-32.

    Google Scholar 

  • Aleza, P., Juarez, J., Ollitrault, P., Navarro, L. 2010. Polyembryony in non-apomictic citrus genotypes. Ann. Bot. 106:533–545.

    Article  PubMed  PubMed Central  Google Scholar 

  • Aleza, P., Juarez, J., Hernandez, M., Pina, J.A., Ollitrault, P., Navarro, L. 2009. Recovery and characterisation of a Citrus clementina Hort. ex Tan. ‘Clemenules’ haploid plant selected to establish the reference whole citrus genome sequence. BMC Plant Biol.

  • Almeida, L.A., Santana-Vieira, D.D., Santos, N.D., Schuster, I., Filho, WD., Filho, M.A., Gesteira A.D. 2018 Water deficit increases the frequency of hybrid citrus with polyembryonic female parents. Crop Breed. Appl. Biotechnol. 18: 47-54.

    Article  Google Scholar 

  • Anderson, C.M., Castle, W.S., Moore, G.A. 1991. Isozymic identifcation of zygotic seedlings in Swingle citrumelo Citrus paradisi × Poncirus trifoliata nursery and field populations. J. Am. Soc. Hortic. Sci. 116:322-326.

    Article  CAS  Google Scholar 

  • Andrade - Rodriguez, M., Villegas, A., Carrillo, G., Garcia, A. 2004. Polyembryony and identification of Volkamerian lemon zygotic and nucellar seedlings using RAPD. Pesqui. Agropecu. Bras. 39(6):551-559.

    Article  Google Scholar 

  • Andrade - Rodriguez, M., Villegas - Monter, A., Gutierrez, M.A., Carrillo, G., Garcia, A. 2005. Polyembryony and RAPD markers for identification of zygotic and nucellar seedlings in Citrus. Agrocienc. 39:371-383.

    Google Scholar 

  • Aron, Y.C., Zosnek, H., Gazit, S., Degani, C. 1998. Polyembryony in mango (Mangifera indica L.) is controlled by a single dominant gene. Hortscience. 33:1241–1242.

    Article  Google Scholar 

  • Arumuganathan, K., Earle, E.D. 1991. Nuclear DNA content of some important plant species. Plant Mol. Biol. Rep. 9:208–218.

    Article  CAS  Google Scholar 

  • Asins, M.J., Herrero, R., Navarro, L. 1995. Factors affecting citrus tree isozyme-gene expression. Theor. Appl. Genet. 90:892-898.

    Article  CAS  PubMed  Google Scholar 

  • Bally, I.S., Lu, P., Johnson, P.R. 2009. Mango breeding. In Breeding plantation tree crops: tropical species (pp. 51–82). Springer, New York, NY.

  • Barcaccia, G., Albertini, E. 2013. Apomixis in plant reproduction: A novel perspective on an old dilemma. Plant Reprod. 26(3):159-179.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bastianel, M., Schwarz, S.F., Fillho, H.D.C., Lin, L.L., Mochado, M.A., Koller, O.C. 1998. Identification of zygotic and nucellar tangerine seedling (Citrus spp.) using RAPD. Genet. Mol. Biol. 21: 123-127.

    Article  Google Scholar 

  • Batygina, T.B. 1989. New approach to the system of reproduction in flowering plants. Phytomorphology. 39: 311–325.

    Google Scholar 

  • Batygina, T.B. 1998. Morphogenesis of somatic embryos developing in natural conditions. Biologia. 3: 61–64.

    Google Scholar 

  • Batygina, T.B. 2006 Embryoidogeny Embryology of Flowering Plants. Terminology and Concepts, vol. 2. Seed. Enfield: Plymouth Sci. Pub. 403–409.

  • Batygina, T.B., Vinogradova, G.Y. 2007. Phenomenon of polyembryony. Genetic heterogenity of seeds. Russ. J. Dev. Biol. 38: 126–151.

    Article  Google Scholar 

  • Begane, N., Dinesh, M.R., Thokchom, A., Ravishankar, K.V. 2019. Development of Barcodes for Identification of Zygotic and Nucellar Seedlings in Polyembryonic Varieties of Mango (Mangifera indica L.). Int. J. Curr. Microbiol. Appl. Sci. 8(3), 14-19.

    Article  CAS  Google Scholar 

  • Bhojwani, S.S., Bhatnagar, S.P. 1974. The Embryology of Angiosperms, Vikas Publishing House Pvt. Ltd., New Delhi, Pp.357.

  • Bhojwani, S.S., Bhatnagar, S.P. 1999. Polyembryony. In: The Embryology of Angiosperms. Vikas Publishing House Pvt. Ltd., New Delhi, Pp. 236–253.

  • Bhojwani, S.S., Bhatnagar, S.P., Dantu, P.K. 2015. The embryology of angiosperms, 6th Edition. Vikas Publishing house Pp: 263–270.

  • Bisi, R.B., Albrecht, U., Bowman, K. 2020. Seed and seedling nursery characteristics for ten USDA citrus rootstocks. HortScience.doi.org/https://doi.org/10.21273/hortsci14598-19.

    Article  Google Scholar 

  • Bowman, K.D., Gmitter, F.G., Hu, X. 1995. Relationships of seed size and shape with polyembryony and the zygotic or nucellar origin of Citrus spp. seedlings. HortScience. 30(6):1270-1282.

    Article  Google Scholar 

  • Cameron, J.W., Johnston J.C. 1949. Nucellar Seedlings may permit development of disease-free citrus varieties. California Agriculture 3(1):9-12.

    Google Scholar 

  • Cameron, J.W., Soost, R.K. 1979. Sexual and nucellar embryony in F1 hybrid and advanced crosses in Citrus with Poncirus. J. Am. Soc. Hortic. Sci. 104(3): 408–410.

    Article  Google Scholar 

  • Cameron, J.W., Soost, R.K. 1980. Leaf types of F1 hybrids and backcrosses involving unifoliate Citrus and trifoliate Poncirus. J. Am. Soc. Hortic. Sci. 105:517-519.

    Article  Google Scholar 

  • Carrillo-Medrano, S.H., Gutierrez-Espinosa, M.A., Robles-Gonzalez, M.M., Cruz-Izquierdo, S. 2018. Identification of Mexican lime hybrids by SSR molecular markers. Revista Mexicana de Ciencias Agrícolas 1: 11-23

    Google Scholar 

  • Caruso, M., Distefano, G., Paolo, D.P., Malfa, S.L., Russo, G., Gentile. A. 2014. High resolution melting analysis for early identification of citrus hybrids: A reliable tool to overcome the limitations of morphological markers and assist rootstock breeding. Sci. Hortic. 180:199-206.

    Article  CAS  Google Scholar 

  • Catalano, C., Las Casas, G., Giuffrida, A., Ferlito, F., Di Guardo, M., Continella, A., Bennici, S., La Malfa, S., Gentile, A. and Distefano, G. 2022. Reproductive biology factors hampering lemon [Citrus limon (L.) Burm. f.] genetic improvement. Agriculture, 12:2020.

    Article  CAS  Google Scholar 

  • Cordeiro, M.C.R., Pinto, A.C.Q., Ramos, V.H.V., Faleiro, F.G., Fraga, L.M.S. 2006. Identification of plantlet genetic origin in polyembryonic mango. Brazilian Magazine of Fruit Culture 28(3): 454-457.

    Google Scholar 

  • Crete, P. 1944. Polyembryony in Actinidia chinensis. Bulletin de la Societe Botanique de France 91: 89–92.

    Article  Google Scholar 

  • Darlan-Ramos, J., Neto, S.E.A., Castro, N.E.A., Martis, P.C.C., Correia, M.G. 2006. Poliembrionia e caracterizaçao de frutos de citrumelo ‘Swingle’ e de Poncirus trifoliata. Ciência e Agrotecnologia 30(1):88-91.

    Article  Google Scholar 

  • Das, A., Mandal, B., Sarkar, J., Chaudhuri, S. 2007. Occurrence of zygotic twins seedlings in mandarin orange plants of north eastern Himalayan region. Curr. Sci. 92(11): 1488-1489

    Google Scholar 

  • Degani, C., El-Batsri, R., Gazit, S. 1990. Enzyme polymorphism in mango. J. Am. Soc. Hortic. Sci. 32:1105-1108.

    Google Scholar 

  • Denagi, C., Cohen, M., Reuveni, O., El-Batsri, R., Gazit, S. 1993. Frequency and characteristics of zygotic seedlings from polyembryonic mango cultivars, determined using isoenzymes as genetic markers. Acta Hortic. 341(1): 7885.

    Google Scholar 

  • Dewi, P.S., Wakana, A., Tanimoto, Y., Fujiwara, Y., Sakai, K. and Kajiwara, K. 2013. Morphology of sterile anthers and inheritance of cytoplasmic-genetic male sterility in zygotic seedlings of polyembryonic acid citrus. J. Jpn. Soc. Hortic. Sci. 82:203-214.

    Article  Google Scholar 

  • Dhineshbabu, K. 2005. Histological and biochemical characterisation of polyembryony in Muvandan and Vellaikolumban mangoes. Ph.D. thesis, KAU.

  • Dillon, N.L., Innes, D.J., Bally, I.S., Wright, C.L., Devitt, L.C., Dietzgen, R.G. 2014. Expressed sequence tag-simple sequence repeat (EST-SSR) marker resources for diversity analysis of mango (Mangifera indica L.). Diversity, 6(1), 72-87.

    Article  Google Scholar 

  • Duarte, F.E.V., d O, Barros, D.D.R., Girari, E.A., Soares-Filho, W.D.A., Passos, O.S. 2013. Poliembrionia e atributos morfológicos de sementes de porta-enxertos de citros. Rev. Bras. Frutic. 35(1):246-254.

    Article  Google Scholar 

  • Durzan, D.J. 2008. Monozygotic cleavage polyembryogenesis and conifer tree improvement. Cytol. Genet. 42: 159–173.

    Article  Google Scholar 

  • Duval, M. F., Bunel, J., Sitbon, C., Risterucci, A.M. 2005. Development of microsatellite markers for mango (Mangifera indica L.). Mol. Ecol. Notes 5:824–826.

    Article  CAS  Google Scholar 

  • Esen, A., Soost, R.K. 1974. Inheritance of browning of young-shoot extracts of citrus. J. Hered. 65:97-100.

    Article  Google Scholar 

  • Fiaz, S., Xiukang, W., Younas, A., Alharthi, B., Riaz, A., Ali, H. 2021. Apomixis and strategies to induce apomixis to preserve hybrid vigor for multiple generations. GM Crops Food 12:57-70.

    Article  PubMed  Google Scholar 

  • Frost, H.B., Soost, R.K. 1968. Seed Reproduction: Development of Gametes and embryos, In: the citrus industry, Volumen 2. Reuther, W., I. D. Batchelor, H. J. Webber (eds.). Division of Agriculture and Science, University of California Press. Berkeley, Cal., USA pp. 290–324.

  • Furr, J.R., Reece, P.C., Hornciar, G. 1946. Identification of hybrid and nucellar citrus seedlings by a modification of the rootstock color test. In Proceedings of American Society for Horticultural Science 48:141-146.

    Google Scholar 

  • Gaikwad, P.N., Sharma, V., Singh, J., Sidhu, G.S., Singh, H., and Omar, A.A. 2023. Biotechnological advancements in Phytophthora disease diagnosis, interaction and management in citrus. Sci. Hortic. 310:111739.

    Article  CAS  Google Scholar 

  • Gaikwad, P.N., Singh, J. and Sidhu, G.S. 2024. Identification and diversity analysis of interspecific citrus rootstock hybrids with combination of morphological traits and microsatellite markers. Hortic. Environ. Biotechnol.

  • Galan - Sauco, V. 2009. El cultivo Del mango. 2. ed. rev. ampl. Tenerife: Mundi-Prensa, Galvez - Lopez, D., Salvador - Figueroa, M., Becerra - Leor, E.N., Gonzalez - Paz, M, 340p.

  • Galvez - Lopez, D., Salvador - Figueroa, M., Becerra - Leor, E.N., Gonzalez - Paz, M., HernandezDelgado, S., Mayek - Perez, N. 2010. Molecular diversity and genetic relationships of mango germplasm from Chiapas, Mexico. Agrociencia. 44:07-915.

    Google Scholar 

  • Ganeshaiah, K.N., Shanker, R.U., Joshi, N.Y. 1991. Evolution of polyembryony: Consequences to the fitness of mother and offspring. J. Genet. 70: 103-27.

    Article  Google Scholar 

  • Garcia, R., Asins, M.J., Forner, J., Carbonell, E.A. 1999. Genetic analysis of apomixis in Citrus and Poncirus by molecular markers. Theor. Appl. Genet. 99:511–518.

    Article  CAS  PubMed  Google Scholar 

  • Ge, X.X., Chai, L.J., Liu, Z., Wu, X.M., Deng, X.X., Guo, W.W. 2012. Transcriptional profiling of genes involved in embryogenic, non-embryogenic calluses and somatic embryogenesis of Valencia sweet orange by SSH based microarray. Planta. 236:1107– 1124.

    Article  CAS  PubMed  Google Scholar 

  • Golein, B., Fifaei, R., Ghasemi, M. 2011. Identification of zygotic and nucellar seedlings in citrus interspecific crosses by inter simple sequence repeats (ISSR) markers. Afr. J. Biotechnol. 10:18965-18970.

    CAS  Google Scholar 

  • Grossniklaus, U., Nogler, G.A., Van Dijk, P.J. 2001. How to avoid sex: The genetic control of gametophytic apomixis. The Plant Cell. 13:149-1497.

    Google Scholar 

  • Haberlandt, G. 1921. Ober experimentelle Erzeugung von Adventivembryonen bei Genathera lamarckiana. Sit.,h. Frellssisch. A had. Wiss. Berlin 40: 695-725.

    Google Scholar 

  • Hand, M.L., Koltunow, A.M. 2014. The genetic control of apomixes: Asexual seed formation. Genet. 197(2):441-450.

    Article  CAS  Google Scholar 

  • Hearn, C.J. 1977. Recognition of zygotic seedlings in certain orange crosses by vegetative characters. Proceedings of International Society for Citriculture 2: 611-614.

    Google Scholar 

  • Hong, Q.B., Xiang, S.Q., Chen, K.L., Chen, L.G. 2001. Two complementary dominant genes controlling apomixis in genus Citrus and Poncirus. Acta Genetica Sinica. 28:1062–1067.

    CAS  PubMed  Google Scholar 

  • Iwamasa, M., Ueno, I., Nishiura, M. 1967. Inheritance of nucellar embryony in Citrus. Bull Fruit Tree Research Station E 2:9–24.

    Google Scholar 

  • Jeong, S., Palmer, T.M., Lukowitz, W. 2011. The RWP-RK factor GROUNDED promotes embryonic polarity by facilitating YODA MAP kinase signalling. Curr. Biol. 21, 1268–1276.

    Article  CAS  PubMed  Google Scholar 

  • Jia, H.H., Xu, Y.T., Yin, Z.P., Wu, X.M., Qing, M., Fan, Y.J., Song, X., Xie, K.D., Xie, Z.Z., Xu, Q. and Deng, X.X. 2021. Transcriptomes and DNA methylomes in apomictic cells delineate nucellar embryogenesis initiation in citrus. DNA Res. 28 :14.

    Article  Google Scholar 

  • Kashyap, K., Banu, S., Shrivastava, M.N., Ramchiary, N. 2018. Study of polyembryony and development of molecular markers for identification of zygotic and nucellar seedlings in Khasi mandarin (Citrus reticulata Blanco). Int. j. environ. agric. biotech. 3(2), p.239076.

    Google Scholar 

  • Kepiro, J.L., Roose, M.L. 2010. AFLP markers closely linked to a major gene essential for nucellar embryony (apomixis) in Citrus maxima x Poncirus trifoliata. Tree Genet. Genomes. 6: 1–11.

    Article  Google Scholar 

  • Khan, I.A., Roose, M.L. 1988. Frequency and characteristics of nucellar and zygotic seedlings in three cultivars of trifoliate orange. J. Am. Soc. Hortic. Sci. 113: 105–10.

    Article  Google Scholar 

  • Kim, M., Kim, S.H., Kim, H.B., Park, Y.C., Song, K.J. 2020. Some factors affecting the efficiency of hybrid embryo rescue in the ‘Shiranuhi’ Mandarin. Hortic. Sci. Tech. 38(2):271- 281.

    CAS  Google Scholar 

  • Kishore, K. 2015. Polyembryony in Horticulture and its significance.

  • Kobayashi, S., Ikeda, I., Nakatani, M. 1978. Studies on the nucellar embryogenesis in Citrus. I. Formation of nucellar embryo and development of ovule. Kaju Shikenjo hokoku. Bulletin of the Fruit Tree Research Station. Series E. Akitsu.

  • Koltunow, A.M. 1993. Apomixis: embryo sacs and embryos formed without meiosis or fertilization in ovules. Plant Cell. 5:1425– 1437.

    Article  PubMed  PubMed Central  Google Scholar 

  • Koltunow, A.M., Soltys, K., Nito, N., McClure, S. 1995. Anther, ovule, seed, and nucellar embryo development in Citrus sinensis cv. Valencia. Can. J. Plant Sci. 73:1567–82.

    Google Scholar 

  • Koltunow, A.M., Scott, N.S., Chaudhury, A.M. 2001. The use of apomixis in cloning horticultural plants. Current applications and molecular prospects. Acta Hortic. 560:333-343.

    Article  CAS  Google Scholar 

  • Kuhn, D.N., Bally, I.S.E., Dillon, N.L., Innes, D., Groh, A.M., Rahaman, J., Ophir, R., Cohen, Y., Sherman, A. 2017. Genetic map of Mango: A tool for Mango breeding. Front. Plant Sci. 8:577.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kumar, K., Rani, U. 2013. Techniques to differentiate zygotic and nucellar seedlings in polyembryonic fruit crops. Int. j. agric. environ. biotechnol. 6(3): 344-350.

    Google Scholar 

  • Kumar, V., Malik, S.K., Pal, D., Srinivasan, R., Bhat, S.R. 2014. Comparative transcriptome analysis of ovules reveals stress related genes associated with nucellar polyembryony in citrus. Tree Genet. Genomes. 10:449-464.

    Article  Google Scholar 

  • Kumar, K., Srivastav, M., Singh, S.K., Singh, A. and Sharma, N. 2018. Studies on extent of polyembryony in salt tolerant mango rootstocks. Indian J. Hortic. 75:139-140.

    Article  Google Scholar 

  • Lebegue, A. 1952. Polyembryony in angiosperm. Bulletin de la Société Botanique de France 99: 329–69.

    Article  Google Scholar 

  • Long, J.M., Liu, Z., Wu, X.M., Fang, Y.N., Jia, H.H., Xie, Z.Z., Deng, X.X., Guo, W.W. 2016. Genome-scale mRNA and small RNA transcriptomic insights into initiation of citrus apomixis. J. Exp. Bot. 67(19), pp.5743-5756.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lopez-Valenzuela, J.A., Martinez, O., Paredes-Lopez, O. 1997. Geographic differentiation and embryo type identification in Mangifera indica L. cultivars using RAPD markers. HortScience. 32(6): 105-1108.

    Article  Google Scholar 

  • Luo, C., He, X.H., Chen, H., Ou, S.J., Gao, M.P., Brown, J.S., Schnell, R.J. 2011. Genetic diversity of mango cultivars estimated using SCoT and ISSR markers. Biochem. Syst. Ecol. 39(4-6), 676-684.

    Article  CAS  Google Scholar 

  • Maheshwari, P. 1950. An introduction to the embryology of angiosperms. Tata Mc-Graw-Hill Publishing Co. Ltd., New York, pp.453.

    Book  Google Scholar 

  • Mannen, H., Tsuji, S., Mukai, F., Goto, N., Ohtagaki, S. 1993. Genetic similarity using DNA fingerprinting in cattle to determine relationship coefficient. J. Hered. 84(3):166-169.

    Article  CAS  PubMed  Google Scholar 

  • Marcial C, J., Monter, A.V., Mancera, H.A.Z. and Izquierdo, S.I.C. 2021. Identification of zygotic and nucellar seedlings, originated by the largest embryo in mango seeds cv Ataulfo, using simple-sequence repeat (SSR). Afr. J. Agric. Res. 17:794-801.

    Article  Google Scholar 

  • Martinez - Ochoa, E.D.C., Villegas - Velazquez, I., Alarcon - Zuniga, B., Gonzalez - Hernandez, V.A., Villegas - Monter, A. 2021. Polyembryony in citrus: Does the largest embryo in the seed develop a nucellar seedling? Sci. Agric. 79(6): e20200060.

    Article  Google Scholar 

  • Martínez, O.E.C., Andrade, R.M., Rocandio, R.M., Villegas, M.A. 2012. Identification of zygotic and nucellar seedlings in polyembryonic mango cultivars. Pesqui. Agropecu. Bras. 47:1629- 1636.

    Article  Google Scholar 

  • Moore, G.A., Castle, W.S. 1988. Morphological and isozymic analysis of open-pollinated citrus rootstock populations. J. Hered. 79: 59-63.

    Article  Google Scholar 

  • Mukherjee, S.K. 1950. Mango: its allopolyploid nature. Nature 166, 196–197.

    Article  CAS  PubMed  Google Scholar 

  • Nakano, M., Shimada, T., Endo, T., Fujii, H., Nesumi, H., Kita, M., Ebina, M., Shimizu, T., Omura, M. 2012. Characterization of genomic sequence showing strong association with polyembryony among diverse Citrus species and cultivars, and its synteny with Vitis and Populus. Plant Sci. 183:131–142.

    Article  CAS  PubMed  Google Scholar 

  • Nakano, M., Kigoshi, K., Shimizu, T., Endo, T., Shimada, T., Fujii, H. 2013. Characterization of genes associated with polyembryony and in vitro somatic embryogenesis in Citrus. Tree Genet. Genomes. 9: 795–803.

    Article  Google Scholar 

  • Narayanaswami, S., Roy, S.K. 1960. Embryo sac development and polyembryony in Syzygium cumini (Linn.) Skeels. Bot. not. 113(3):273-84.

    Google Scholar 

  • Ngo, B.X., Kim, J.H., Wakana, A., Isshiki, S. and Mori, T. 2011. Estimation of self-incompatibility genotypes of Citrus cultivars with Got-3 allozyme markers. J. Jpn. Soc. Hortic. Sci. 80:284-294.

    Article  Google Scholar 

  • Nicolosi, E. 2007. Origin and taxonomy. Citrus genetics, breeding and biotechnology, pp.19–43.

  • Ochoa, E.D.C.M., Andrade-Rodríguez, M., Rodríguez, M.R., Monter, A.V. 2012. Identification of zygotic and nucellar seedlings in polyembryonic mango cultivars. Pesqui. Agropecu. Bras. 47(11), 1629-1636.

    Article  Google Scholar 

  • Oliveira, A.C.D., Garcia, A.N., Cristofani, M., Machado, M.A. 2002. Identification of citrus hybrids through the combination of leaf apex morphology and SSR markers. Euphytica. 128:397–403

    Article  Google Scholar 

  • Parameswaran, N.K., Babu, K. 2015. Polyembryony and its Precalence in Horticultural Crops. Basics of Horticulture. Revised edition by Peter KV NIPA, New Delhi.

    Google Scholar 

  • Parlevliet, J.E., Cameron, J.W. 1959. Evidence on the inheritance of nucellar embryony in Citrus. Proceedings of American Society of Horticultural Sciences 74:252–260.

    Google Scholar 

  • Pieringer, A.P., Edwards, G.J. 1965. Identification of nucellar and zygotic citrus seedlings by infrared spectroscopy. J. Am. Soc. Hortic. 86:226-234.

    CAS  Google Scholar 

  • Pullaiah, T., Lakshminarayan, K., HanumanthRao, B. 2001. Polyembryony. In: Textbook of Embryology of Angiosperm. Regency Publication, New Delhi, pp. 164–77.

  • Raga, V., Bernet, G.P., Carbonell, E.A., Asins, M.J. 2012. Segregation and linkage analyses in two complex populations derived from the citrus rootstock Cleopatra mandarin. Inheritance of seed reproductive traits. Tree Genet. Genomes. 8:1061–107.

    Article  Google Scholar 

  • Rao, M.N., Jaya, R.S., Chunxian, C., Shu, H., Fred, G.G. 2008. Characterization of zygotic and nucellar seedlings from sour orange-like citrus rootstock candidates using RAPD and EST-SSR markers. Tree Genet. Genomes. 4: 113–124.

    Article  Google Scholar 

  • Ravishankar, K.V., Anand, L., Dinesh, M.R. 2000. Assessment of genetic relatedness among mango cultivars of India using RAPD markers. J. Hortic. Sci. 75(2), 198-201.

    CAS  Google Scholar 

  • Rocha, A., Salomão, T.M.F., Siqueira, D.L.D., Cruz, C.D., Salomão, L.C.C. 2014. Identification of 'Uba' mango tree zygotic and nucellar seedlings using ISSR markers. Rev. Ceres. 61(5), 597-604.

    Article  Google Scholar 

  • Rodriguez, M., Monter, A., Castaneda, C.G., Velazquez, A. 2004. Polyembryony and identification of Volkameriana lemon zygotic and nucellar seedlings using RAPD. Pesqui. Agropecu. Bras. 39: 551-559.

    Article  Google Scholar 

  • Rodriguez, M., Monter, A., Espinosa, A., Castaneda, C.G., Velazquez, A. 2005. Polyembryony and RAPD markers for identification of zygotic and nucellar seedlings in Citrus. Agrocienc. 39: 371-383.

    Google Scholar 

  • Ruiz, C., Breto, M.P., Asins, M.J. 2000. A quick methodology to identify sexual seedlings in citrus breeding programs using SSR markers. Euphytica 112: 89-94.

    Article  CAS  Google Scholar 

  • Sabrinho, S.J., Gurgel, J.T.A. 1953. Polyembrionia e embrionia adventicia em Citrus, Mangefira e Myrtaceae frutiferas, Dusenia 4:421-428.

  • Sachar, R.C., Chopra, R.N. 1957. A study of endosperm and embryo in Mangifera. Indian J. Agric. Sci. 27:219-238.

    Google Scholar 

  • Sánchez-Damas, J.J., Avitia, E.G., Castillo, G.A.M., Villegas, A.M., Corona, T.T. 2006. Estudio anatómico de la poliembrionía en tres portainjertos de cítricos. Rev Chapingo Ser Hortic. 12(2):145-152.

    Article  Google Scholar 

  • Sane, A., Dinesh, M.R., Ravishankar, K.V., Ravishankar, H., Vasugi, C. 2011. Implications of polyembryony on the growth performance in mango cultivars. In Global Conference on Augmenting Production and Utilization of Mango: Biotic and Abiotic Stresses 1066 (pp. 47–54).

  • Schmidt, A. 2020. Controlling apomixis: Shared features and distinct characteristics of gene regulation. Genes. 11:329.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmidt, A., Schmid, M.W., Klostermeier, U.C., Qi, W., Guthorl, D., Sailer, C., Waller, M., Rosenstiel, P., Grossniklaus, U. 2014. Apomictic and sexual germline development differ with respect to cell cycle, transcriptional, hormonal and epigenetic regulation. PLoS Genet. 10(7), p.e1004476.

    Article  PubMed  PubMed Central  Google Scholar 

  • Schnell, R.J., Knight, R.J. 1992. Frequency of zygotic seedlings from five polyembryonic mango rootstocks. HortScience. 27(2), 174-176.

    Article  Google Scholar 

  • Schnell, R.J., Olano, C.T., Quintanilla, W.E., Meerow, A.W. 2005. Isolation and characterization of 15 microsatellite loci from mango (Mangifera indica L.) and cross-species amplification in closely related taxa. Mol. Ecol. Notes. 5: 625–627.

    Article  CAS  Google Scholar 

  • Schnell, R.J., Brown, J.S., Olano, C.T., Meerow, A.W., Campbell, R.J., Kuhn, D.N. 2006. Mango genetic diversity analysis and pedigree inferences for Florida cultivars using microsatellite markers. J. Am. Soc. Hortic. Sci. 131: 214–224.

    Article  CAS  Google Scholar 

  • Sherman, A., Rubinstein, M., Eshed, R., Benita, M., Ish-Shalom, M., Sharabi-Schwager, M., Ophir, R. 2015. Mango (Mangifera indica L.) germplasm diversity based on single nucleotide polymorphisms derived from the transcriptome. BMC plant boil. 15(1), 277.

    Article  Google Scholar 

  • Shimada, T., Endo, T., Fujii, H., Nakano, M., Sugiyama, A., Daido, G. 2018. MITE insertion-dependent expression of CitRKD1 with an RWP-RK domain regulates somatic embryogenesis in citrus nucellar tissues. BMC Plant Biol. 18:166.

    Article  PubMed  PubMed Central  Google Scholar 

  • Shudo, A., Tarora, K., Makishi, Y., Ichi, R., Takahashi Matsumura, M., Shimabuku, S., Matsuda, N., Nakasone, S., Urasaki, N. 2013. Development of CAPS markers and their application in breeding for mango, Mangifera indica L. Euphytica 190(3):345–355.

    Article  CAS  Google Scholar 

  • Sidhu, G.S., Dhaliwal, H.S. and Gaikwad, P.N., 2024. Polyembryony and morpho-genetic characterisation of zygotic seedlings through microsatellite markers in ten polyembryonic citrus rootstocks. Seed Sci. Technol. 52:85-107.

    Article  Google Scholar 

  • Singh, H. 2014. Morphological and molecular characterization of nucellar and zygotic seedlings in citrus rootstocks. M.Sc. Thesis, Punjab Agricultural University, Ludhiana, Punjab, India.

  • Singh, G., Aulakh, P.S., Sarao, N.K., Sidhu, G.S., Rattanpal, H.S. 2015. Identification of zygotic seedlings using SSRs markers in intra-specific hybridization in mandarin (C. reticulata Blanco). Proceedings of national symposium on “Precision citriculture for food safety and nutritional security under changing climate” held at ICAR Central Citrus Research Institute, Nagpur, Maharashtra. November 27–29, p 7.

  • Singh, G., Aulakh, P.S., Sarao, N.K., Rattanpal, H.S., Sidhu, G.S. 2018. Molecular verification of putative zygotic seedlings in different intra-specific crosses in Mandarins (Citrus reticulata) by SSR markers. Agric. Res. 8:21-26.

    Article  Google Scholar 

  • Singh, J., Dhaliwal, H.S., Thakur, A., Sidhu, G.S., Chhuneja, P., Gmitter, F.G. Jr. 2020. Optimizing recovery of hybrid embryos from interspecific citrus crosses of polyembryonic rough lemon (Citrus jambhiri Lush.). Agron. 10:1940.

    Article  CAS  Google Scholar 

  • Singh, J., Sharma, A., Sharma, V., Gaikwad, P.N., Sidhu, G.S., Kaur, G., Kaur, N., Jindal, T., Chhuneja, P. and Rattanpal, H.S. 2023. Comprehensive genome-wide identification and transferability of chromosomespecific highly variable microsatellite markers from citrus species. Sci. Rep. 13:10919.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soares, F.W.S., Lee, L.M., Cunha Sobrinho, A.P. 1995. Influence of pollinators on polyembryony in citrus. Acta Hortic. 403: 256–265.

    Article  Google Scholar 

  • Soares-Filho, W.D.S., Moreira, C.S., Da Cunha, M.A.P., Da Cunha-Sobrinho, A.P., Passos, O.S. 2000. Poliembrionia e freqüência de híbridos em Citrus spp. Pesqui. Agropecu. Bras. (35):857-864.

    Article  Google Scholar 

  • Soost, R.K., Roose, M.L. 1996. Citrus, chapter 6. In: Janick J, Moore JN, editors. Fruit Breeding Vol I: Tree and Tropical Fruits. Wiley: New York pp. 257-323.

    Google Scholar 

  • Souza, I.G.B., Valente, S.E.S., Britto, F.B., de Souza, V.A.B., Lima, P.D.C. 2011. RAPD analysis of the genetic diversity of mango (Mangifera indica L.) germplasm in Brazil. Embrapa Meio-Norte-Artigo em periódico indexado (ALICE).

  • Spiegel-Roy, P., Bardi, A., Shani, A. 1977. Peroxidase isozymes as a tool for early separation of nucellar and zygotic citrus seedlings. Second Meeting of the International Society of Citriculture. Proceeding of the International Society of Citriculture. Vol. 2. Florida, USA pp. 619–624.

  • Sturrock, D. 1962. A Progress Report on Some Mango Hybrids. Proceedings of the Florida State Horticultural Society 75: 384-387.

    Google Scholar 

  • Sturrock, T.T. 1968. Genetics of mango polyembryony. Proceedings of the Florida State Horticultural Society 81:311–314.

    Google Scholar 

  • Swamy, B.G.L. 1943. Gametogenesis and embryogeny of Eulophia epidendraea Fischer. In Proc. Nat. Inst. Sci. India. 9:59-65.

    Google Scholar 

  • Sykes, S.R. 2011. Characterization of citrus rootstock germplasm introduced as seeds to Australia from the People’s Republic of China. Sci. Hortic. 127:298-304.

    Article  Google Scholar 

  • Tatum, J.H., Berry, R.E., Hearn, C.J. 1974. Characterization of Citrus cultivars and separation of nucellar and zygotic seedlings by thin layer chromatography. Proceedings Florida State Horticulture Society 87:75-81.

    CAS  Google Scholar 

  • Thakur, D.R., Bojwa, B.S. 1971. Extent of polyembryony in some species and varieties of Citrus. Indian J. Hortic. 28(1):25-28.

    Google Scholar 

  • Torres, A.M., Soost, R., Mau-Lastovicka, T. 1982. Citrus isozymes. Journal of Heredity 73: 335-339.

    Article  CAS  Google Scholar 

  • Toyama T.K. (1974) Haploidy in peach. HortScience. 9: 187–8.

    Article  Google Scholar 

  • Tupke, A.H., Akhare, A.A., Gahukar, S.J., Bahatkar, B.P., Zadokar, A.R., Gaikwad, P.N. and Katkade, R.R. 2021. DNA fingerprinting: a novel technique for identification of important species of citrus. Ann. Phytomed. 10:202-207.

    Article  CAS  Google Scholar 

  • Tusa, N., Abbate, L., Ferrante, S., Lucretti, S., Scarano, M.T. 2002. Identification of zygotic and nucellar seedlings in citrus interploidy crosses by means of isozymes, flow cytometry and ISSR-PCR. Cell. Mol. Biol. Lett. 7: 703-708.

    CAS  PubMed  Google Scholar 

  • Villegas-Monter, A., Matinez-Ochoa, E.D.C., Andrade-Rodriguez, M. and Villegas-Velazquez, I., 2022. Citrus Polyembryony. In Advances in Citrus Production and Research. IntechOpen.

  • Viruel, M.A., Escribano, P., Barbieri, M., Ferri, M., Hormaza, J.I. 2005. Fingerprinting, embryo type and geographic differentiation in mango (Mangifera indica L.) with microsatellites. Mol. Breed. 15: 383–393.

    Article  CAS  Google Scholar 

  • Wakana, A., Uemoto, S. 1987a. Adventive embryogenesis in Citrus I. The occurrence of adventive embryos without pollination or fertilization. Am. J. Bot. 74:517–530.

    Article  Google Scholar 

  • Wakana, A., Uemoto, S. 1987b. Adventive embryogenesis in Citrus (Rutaceae) II Post Fertilization Development. Am. J. Bot. 75: 1033-47.

    Article  Google Scholar 

  • Waki, T., Hiki, T., Watanabe, R., Hashimoto, T., Nakajima, K. 2011. The Arabidopsis RWP-RK protein RKD4 triggers gene expression and pattern formation in early embryogenesis. Curr. Biol. 21, 1277–1281.

    Article  CAS  PubMed  Google Scholar 

  • Wang, X., Xu, Y., Zhang, S., Cao, L., Huang, Y., Cheng, J., Wu, G., Tian, S., Chen, C., Liu, Y. and Yu, H. 2017. Genomic analyses of primitive, wild and cultivated citrus provide insights into asexual reproduction. Nat. Genet. 49:765-772.

    Article  CAS  PubMed  Google Scholar 

  • Wang, N., Song, X., Ye, J., Zhang, S., Cao, Z., Zhu, C., Hu, J., Zhou, Y., Huang, Y., Cao, S. and Liu, Z. 2022. Structural variation and parallel evolution of apomixis in citrus during domestication and diversification. Natl. Sci. Rev. 9:114.

    Article  Google Scholar 

  • Weinbaum, S.A., Cohen, E., Spiegel, R.P. 1982. Rapid screening of ‘Satsuma’ mandarin progeny to distinguish nucellar and zygotic seedlings. HortScience. 17: 239-240.

    Article  Google Scholar 

  • Wilms, H.J., Van Went, J.L., Cresti, M., Ciampolni, F. 1983. Adventive Embryogenesis in Citrus. Caryologia. 36:65-78.

    Article  Google Scholar 

  • Woo, J.K., Park, Y.C., Lee, J.W., Yun, S.H., Kim, M., Park, S., Lee, Y., Song, K.J., Kim, H.B. 2019. Evaluation of polyembryony for genetic resources and efficacy of simple sequence repeat markers for the identification of nucellar and zygotic embryo-derived individuals in citrus. Appl. Biol. Chem. 62, pp.1-11.

    Article  CAS  Google Scholar 

  • Wu, G.A., Sugimoto, C., Kinjo, H., Azama, C., Mitsube, F., Talon, M., Gmitter Jr, F.G. and Rokhsar, D.S. 2021. Diversification of mandarin citrus by hybrid speciation and apomixis. Nat. commun. 12:4377.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiang, C., Roose, M.L. 1988. Frequency and characteristics of nucellar and zygotic seedlings in 12 citrus rootstocks. Sci. Hortic. 37:47–59.

    Article  Google Scholar 

  • Xu, Y., Jia, H., Wu, X., Koltunow, A.M., Deng, X. and Xu, Q., 2021. Regulation of nucellar embryony, a mode of sporophytic apomixis in Citrus resembling somatic embryogenesis. Curr. Opin. Plant Biol. 101984.

  • Xu, Y., Jia, H., Tan, C., Wu, X., Deng, X. and Xu, Q. 2022. Apomixis: genetic basis and controlling genes. Horticul. Res. 9:150.

    Article  Google Scholar 

  • Yadav, C.B., Rozen, A., Eshed, R., Ish-Shalom, M., Faigenboim, A., Dillon, N., Bally, I., Webb, M., Kuhn, D., Ophir, R. and Cohen, Y. 2023. Promoter insertion leads to polyembryony in mango-a case of convergent evolution with citrus. Hortic. Res. 10:227.

    Article  Google Scholar 

  • Yakovlev, M.S. 1967. Polyembryony in higher plants and principles of its classification. Phytomorphology. 17:278-282.

    Google Scholar 

  • Yamaoka, S., Nishihama, R., Yoshitake, Y., Ishida, S., Inoue, K., Saito, M., Okahashi, K., Bao, H., Nishida, H., Yamaguchi, K. and Shigenobu, S. 2018. Generative cell specification requires transcription factors evolutionarily conserved in land plants. Curr. Biol. 28:479-486.

    Article  CAS  PubMed  Google Scholar 

  • Yildiz, E., Kaplankiran, M., Demirkeser, T.H., Uzun, Y., Toplu, C. 2013. Identification of zygotic and nucellar individuals produced from several citrus crosses using SSRs markers. Not. Bot. Horti Agrobot. 41(2):478-484.

    Article  CAS  Google Scholar 

  • Yun, S.H., Moon, Y.S., Jin, S.B., Kang, I., Lee, D.H. 2011. Early identification of putative zygotic seedlings in citrus crosses between ‘Morita unshiu’ (Citrus Unshiu Marc.) and ‘Ponkan’ (C. reticulata Blanco) using RAPD and SRAP. J. Life Sci. 21:502-08.

    Article  Google Scholar 

  • Zhang, S., Liang, M., Wang, N., Xu, Q., Deng, X., Chai, L. 2018. Reproduction in woody perennial citrus: an update on nucellar embryony and self-incompatibility. Plant Reprod. 31:43-57.

    Article  PubMed  Google Scholar 

  • Zhu, S., Wu, B., Ma, Y., Chen, J., Zhong, G. 2013. Obtaining citrus hybrids by in vitro culture of embryos from mature seeds and early identification of hybrid seedlings by allele-specific PCR. Sci. Hortic. 161:300-305.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to Dr. Gurdev Singh Khush Laboratories, School of Agricultural Biotechnology, Punjab Agricultural University. Ludhiana, India and Chhatrapati Shahu Maharaj Research, Training and Human Development Institute (SARTHI), Pune, India.

Funding

This review received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Author information

Authors and Affiliations

  1. School of Agricultural Biotechnology, Punjab Agricultural University, Ludhiana, 141004, India

    Gurupkar Singh Sidhu, Prashant Mohanpuria, Popat Nanaso Gaikwad, Gurpreet Kaur & Harmanpreet Kaur

Authors
  1. Gurupkar Singh Sidhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Prashant Mohanpuria
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Popat Nanaso Gaikwad
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gurpreet Kaur
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Harmanpreet Kaur
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization, GSS, PM; review collected, GSS, PNG, PM; writing and original draft preparation: GSS, PNG, PM, GK, HK; review and editing: GSS, PNG, PM. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Gurupkar Singh Sidhu.

Ethics declarations

Conflict of Interest

The authors state that the publishing of this review does not create a conflict of interest for them.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sidhu, G.S., Mohanpuria, P., Gaikwad, P.N. et al. Polyembryony: A Potential Horticultural Trait, Reveals Complex Mechanism, Role of Molecular Markers and their Application in Fruit Crops. Bot. Rev. (2024). https://doi.org/10.1007/s12229-024-09300-9

Download citation

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12229-024-09300-9

Keywords

Search

Navigation