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Diplospory and obligate apomixis in Miconia albicans (Miconieae, Melastomataceae) and an embryological comparison with its sexual congener M. chamissois

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Abstract

Apomixis, or asexual reproduction through seeds, has been reported for species of the tribe Miconieae, Melastomataceae, but details of the process have yet to be described. We analyzed and compared sporogenesis and gametogenesis in the apomictic Miconia albicans and the sexual M. chamissois. The results point to some differences between species, which were related to the apomictic process. In M. albicans microsporogenesis, problems during meiosis and degeneration of its products led to total pollen sterility, while M. chamissois presented normal bicellular pollen grains in the mature anther. The absence or abnormality of meiosis in M. albicans megasporogenesis led to the formation of an unreduced embryo sac and also to egg cell parthenogenesis, which gave rise to the apomictic embryo. Embryo and endosperm development were autonomous, resulting in seeds and fruits independent of pollination and fertilization. Thus, in this species, apomixis can be classified as diplosporic and obligate. In contrast, meiosis was as expected in the sexual M. chamissois, and led to the development of a reduced embryo sac. Despite the divergent pathways, many embryological characteristics were similar between the studied species and other Melastomataceae and they seem to be conservative character states for the family.

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References

  • Allem AC (2004) Optimization theory in plant evolution: an overview of long-term evolutionary prospects in the angiosperms. Bot Rev 69:225–251

    Article  Google Scholar 

  • Asker SE (1979) Progress in apomixis research. Hereditas 91:231–240

    Article  Google Scholar 

  • Asker SE, Jerling L (1992) Apomixis in plants. CRC Press, Boca Raton

    Google Scholar 

  • Baumgratz JFA, Souza MLDR, Woodgyer EM, NicLughada EM (1996) Polysporangiate anthers: described for the first time in Melastomataceae. Kew Bull 51:133–144

    Article  Google Scholar 

  • Baumgratz JFA, Bernardo KFR, Chiavegatto B, Goldenberg R, Guimarães PJF, Kriebel R, Martins AB, Michelangeli FA, Reginato M, Romero R, Souza MLDR, Woodgyer E (2010) Melastomataceae. In: Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro (http://floradobrasil.jbrj.gov.br/2010/FB000161)

  • Bicknell RA, Koltunow AM (2004) Understanding apomixis: recent advances and remaining conundrums. Plant Cell 16:229–245

    Article  Google Scholar 

  • Borges HBN (1991) Biologia reprodutiva de quatro espécies de Melastomataceae. Dissertation, Universidade Estadual de Campinas

  • Caetano APS (2010) Apomixia e reprodução sexuada em espécies de Miconia Ruiz & Pavón, Melastomataceae. Dissertation, Universidade Estadual de Campinas

  • Caetano APS, Teixeira SP, Forni-Martins ER, Carmello-Guerreiro SM (2013) Pollen insights into apomictic and sexual Miconia (Miconieae, Melastomataceae). Int J Plant Sci 174(5)

  • Carman JG (1997) Asynchronous expression of duplicate genes in angiosperm may cause apomixis, bispory, tetraspory, and polyembryony. Biol J Linn Soc 61:51–94

    Article  Google Scholar 

  • Clausing G, Renner SS (2001) Molecular phylogenetics of Melastomataceae and Memecylaceae: implications for character evolution. Am J Bot 88:486–498

    Article  PubMed  CAS  Google Scholar 

  • Cooper DC, Brink RA (1949) The endosperm-embryo relationship in an autonomous apomict, Taraxacum officinale. Bot Gaz 111:139–153

    Article  Google Scholar 

  • Cortez PA, Carmello-Guerreiro SM (2008) Ontogeny and structure of the pericarp and the seed coat of Miconia albicans (Sw.) Triana (Melastomataceae) from “cerrado”, Brazil. Rev Bras Bot 31:71–79

    Article  Google Scholar 

  • Cortez PA, Carmello-Guerreiro SM, Teixeira SP (2012) Understanding male sterility in Miconia species (Melastomataceae)—a morphological approach. Aust J Bot 60:506–516

    Article  Google Scholar 

  • Davis GL (1966) Systematic embryology of the angiosperms. John Wiley, New York

    Google Scholar 

  • den Nijs HCM, Menken SBJ (1996) Relations between breeding system, ploidy level, and taxonomy in some advanced sections of Taraxacum. In: Hind HDN, Beentje HJ (eds) Advances in Compositae systematics. Royal Botanic Gardens, Kew, pp 665–677

    Google Scholar 

  • Feder N, O’Brien TP (1968) Plant microtechnique: some principles and new methods. Am J Bot 55:123–142

    Article  Google Scholar 

  • Gerrits PO, Smid L (1983) A new, less toxic polymerization system for the embedding of soft tissues in glycol methacrylate and subsequent preparing of serial sections. J Microsc 132:81–85

    Article  PubMed  CAS  Google Scholar 

  • Goldenberg R, Shepherd GJ (1998) Studies on the reproductive biology of Melastomataceae in “cerrado” vegetation. Plant Syst Evol 211:13–29

    Article  Google Scholar 

  • Goldenberg R, Varassin IG (2001) Sistemas reprodutivos de espécies de Melastomataceae da Serra do Japi, Jundiaí, São Paulo, Brasil. Braz J Bot 24:283–288

    Google Scholar 

  • Hãkansson A, Levan A (1957) Endo-duplicational meiosis in Allium odorum. Hereditas 43:179–200

    Article  Google Scholar 

  • Hörandl E (2010) The evolution of self-fertility in apomictic plants. Sex Plant Reprod 23:73–86

    Article  PubMed  Google Scholar 

  • Johansen DA (1940) Plant microtechnique. McGraw-Hill Book Company, New York

    Google Scholar 

  • Johri BM, Ambegaokar KB, Srivastava PS (1992) Comparative embryology of angiosperms. Springer, Berlin

    Book  Google Scholar 

  • Kapil RN, Tiwari SC (1978) Plant embryological investigations and fluorescence microscopy: as assessment of integration. Int Rev Cytol 53:291–331

    Article  CAS  Google Scholar 

  • Klink CA, Machado RB (2005) Conservation of the Brazilian cerrado. Conserv Biol 19:707–713

    Article  Google Scholar 

  • Koltunow AM (1993) Apomixis: embryo sacs and embryo formed without meiosis or fertilization in ovules. Plant Cell 5:1425–1437

    PubMed  Google Scholar 

  • Koltunow AM, Grossniklaus U (2003) Apomixis: a developmental perspective. Annu Rev Plant Biol 54:547–574

    Article  PubMed  CAS  Google Scholar 

  • Koltunow AM, Johnson SD, Bicknell RA (1998) Sexual and apomictic development in Hieracium. Sex Plant Reprod 11:213–230

    Article  Google Scholar 

  • Lersten NR, Curtis JD (1988) Secretory reservoirs (ducts) of two kinds in giant ragweed (Ambrosia trifida; Asteraceae). Am J Bot 75:1313–1323

    Article  Google Scholar 

  • Medeiros JD, Morretes BL (1996) The embryology of Miconia cabucu (Melastomataceae). Cytologia 61:83–91

    Article  Google Scholar 

  • Medeiros JD, Roos AL (1996) Aspectos do microsporângio, da microsporogênese e do gametófito masculino de Tibouchina cerastifolia (Naud.) Cogn. (Melastomataceae). Biotemas 9:5–14

    Google Scholar 

  • Meirmans PG, Den Nijs JCM, van Tienderen PH (2006) Male sterility in triploid dandelions: asexual females vs asexual hermaphrodites. Heredity 96:45–52

    PubMed  CAS  Google Scholar 

  • Melo GF, Machado IC, Luceño M (1999) Reproducción de tres especies de Clidemia (Melastomataceae) en Brasil. Rev Biol Trop 47:359–363

    Google Scholar 

  • Mendes-Rodrigues C, Carmo-Oliveira R, Tavalera S, Aista M, Ortiz PL, Oliveira PE (2005) Polyembryony and apomixis in Eriotheca pubescens (Malvaceae-Bombacoideae). Plant Biol 7:533–540

    Article  PubMed  CAS  Google Scholar 

  • Mogie M (1992) The evolution of asexual reproduction in plants. Chapman & Hall, London

    Google Scholar 

  • Mogie M, Britton NF, Stewart-Cox JA (2007) Asexuality, polyploidy and the male function. In: Hörandl E, Grossniklaus U, van Dijk PJ, Sharbel T (eds) Apomixis: evolution, mechanisms and perspectives. Gantner Verlag, Ruggell, pp 195–214

    Google Scholar 

  • Nogler GA (1984) Gametophytic apomixis. In: Johri BM (ed) Embryology of angiosperms. Springer, Berlin, pp 475–518

    Chapter  Google Scholar 

  • Ozias-akins P, van Dijk PJ (2007) Mendelian genetics of apomixis in plants. Annu Rev Genet 41:509–537

    Article  PubMed  CAS  Google Scholar 

  • Pagliarini SP (2000) Meiotic behavior of economically important plant species: the relationship between fertility and male sterility. Genet Mol Biol 23:997–1002

    Article  Google Scholar 

  • Renner SS (1993) Phylogeny and classification of the Melastomataceae and Memecylaceae. Nord J Bot 13:519–540

    Article  Google Scholar 

  • Richards AJ (1997) Plant breeding systems. Chapman & Hall, London

    Google Scholar 

  • Risso-Pascotto C, Pagliarini MS, Valle CB (2006) Microsporogenesis in Brachiaria dictyoneura Stapf (Poaceae: Paniceae). Genet Mol Res 5:837–845

    PubMed  CAS  Google Scholar 

  • Rutishauser A (1982) Introducción a la embriología y biología de la reproducción de las Angiospermas. Editorial HemisferioSur, Buenos Aires

    Google Scholar 

  • Santos APM, Fracasso CM, Santos ML, Romero R, Sazima M, Oliveira PE (2012) Reproductive biology and species geographical distribution in the Melastomataceae: a survey based on New World taxa. Ann Bot 110:667–679

    Article  PubMed  Google Scholar 

  • Savidan Y (2007) Apomixis in higher plants. In: Hörandl E, Grossniklaus U, van Dijk PJ, Sharbel T (eds) Apomixis: evolution, mechanisms and perspectives. Gantner Verlag, Ruggell, pp 15–22

    Google Scholar 

  • Solt ML, Wurdack JJ (1980) Chromosome numbers in the Melastomataceae. Phytologia 47:199–220

    Google Scholar 

  • Stebbins GL (1950) Variation and evolution in plants. Columbia Univ. Press, New York

    Google Scholar 

  • Subramanyam K (1942) Gametogenesis and embryogeny in a few members of Melastomataceae. J Indian Bot Soc 21:69–85

    Google Scholar 

  • Subramanyam K (1944) A contribution to the life-history of Sonerila wallachii Benn. P Indian Acad Sci 19:115–120

    Google Scholar 

  • Subramanyam K (1948) An embryological study of Melastoma malabathricum L. J Indian Bot Soc 27:11–19

    Google Scholar 

  • Subramanyam K (1951) Embryology of Oxyspora paniculata. Phytomorphology 1:205–212

    Google Scholar 

  • Thompson SL, Choe G, Ritland K, Whitton J (2008) Cryptic sex within male-sterile polyploid populations of the Easter daisy, Townsendia hookeri. Int J Plant Sci 169:183–193

    Article  Google Scholar 

  • Tobe H, Raven PH (1983) An embryological analysis of Myrtales, its definition and characteristics. Ann Mo Bot Gard 70:71–94

    Article  Google Scholar 

  • Van Baarlen P, De Jong JH, van Dijk PJ (2002) Comparative cyto-embryological investigations of sexual and apomictic dandelions (Taraxacum) and their apomictic hybrids. Sex Plant Reprod 15:31–38

    Article  Google Scholar 

  • Venkatesh CS (1955) The structure and dehiscence of the anther in Memecylon and Mouriria. Phytomorphology 5:435–440

    Google Scholar 

Download references

Acknowledgments

The research was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). We thank Diana Sampaio, Simone Pádua Texeira, and Clesnan Mendes Rodrigues for critical reading of different versions of this manuscript. We thank the Clube Caça e Pesca Itororó for the permission to collect in their protected area.

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Correspondence to Paulo Eugênio Oliveira.

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Caetano, A.P.S., Simão, D.G., Carmo-Oliveira, R. et al. Diplospory and obligate apomixis in Miconia albicans (Miconieae, Melastomataceae) and an embryological comparison with its sexual congener M. chamissois . Plant Syst Evol 299, 1253–1262 (2013). https://doi.org/10.1007/s00606-013-0793-y

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