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Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Patterns of polyembryony and frequency of surviving multiple embryos of the Brazilian pine Araucaria angustifolia

Sarah Zanon Agapito-Tenfen A C , Neusa Steiner B , Miguel Pedro Guerra A and Rubens Onofre Nodari A
+ Author Affiliations
- Author Affiliations

A Plant Developmental Physiology and Genetics Laboratory, CropScience Department, Federal University of Santa Catarina; Rod. Admar Gonzaga 1346, 88034-001, Florianópolis – Brazil.

B Rural Sciences Department, Federal University of Santa Catarina; Rod. Ulisses Gaboardi, Km 3, 89520-000, Curitibanos – Brazil.

C Corresponding author. Email: sarahagro@gmail.com

Australian Journal of Botany 59(8) 749-755 https://doi.org/10.1071/BT11195
Submitted: 26 July 2011  Accepted: 24 November 2011   Published: 23 January 2012

Abstract

The development of polyembryony is a common reproductive strategy in conifers. Multiple embryos are observed during early seed developmental stages. However, upon seed maturation, only the dominant embryo survives, with few exceptions. Although programmed cell death has been reported as the major mechanism responsible for elimination of subordinate embryos, the genetics of surviving embryos and the probabilities of survival remain unclear. The aim of this study is to determine patterns of polyembryony and survival frequency in Araucaria angustifolia (Bert) O. Ktze. Thus, we investigate the morphogenetic parameters that might be related to embryo survival using nuclear microsatellite markers and morphological characteristics of immature embryos and seedlings. Our novel approach couples genotype frequency analysis with the number of surviving embryos, presence of embryo dominance and number of cotyledons present within a single seed. Polyembryonic seedling frequency was low (0.022%) and 91% of surviving embryos were monozygotic. From all monozygotic embryos, 98% showed differences in growth rate (height) in relation to each other. Concrescent tissues were common in the monozygotic polyembryony patterns observed (80%) but not for those with polyzygotic polyembryony. We demonstrate that the survival of multiple embryos is a rare event in A. angustifolia seeds. To the best of our knowledge this study represents the first evidence of cleavage polyembryony in immature embryos and seedlings from A. angustifolia. Our novel approach using a combined set of morphological parameters and microsatellite markers was successful in investigating polyembryony patterns and survival.


References

Bozhkov P (2005) Regulation of programmed cell death in plant embryogenesis. BMC Plant Biology 5, S6
Regulation of programmed cell death in plant embryogenesis.Crossref | GoogleScholarGoogle Scholar |

Burdon RD, Zabkiewicz JA (1973) Identical and non-identical seedlings twins in Pinus radiata. Canadian Journal of Botany 51, 2001–2004.
Identical and non-identical seedlings twins in Pinus radiata.Crossref | GoogleScholarGoogle Scholar |

Creste S, Tulmann Neto A, Figueira A (2001) Detection of single sequence repeat polymorphisms in denaturing polyacrylamide sequencing gels by silver staining. Plant Molecular Biology Reporter 19, 299–306.
Detection of single sequence repeat polymorphisms in denaturing polyacrylamide sequencing gels by silver staining.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhslSlt78%3D&md5=91ac9ec2e0d2817d20a9a51a056f1bc6CAS |

Dogra PD (1978) Morphology, development and nomenclature of conifer embryo. Phytomorphology 28, 307–322.

Doyle J (1957) Aspects and problems of conifer embryology. The Advanced Science Journal 14, 120–130.

Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure from small quantities of fresh leaf tissues. Phytochemical Bulletin 19, 11–15.

Durzan DJ (2008) Monozygotic cleavage polyembryogenesis and conifer tree improvement. Cytology and Genetics 42, 159–173.
Monozygotic cleavage polyembryogenesis and conifer tree improvement.Crossref | GoogleScholarGoogle Scholar |

Erdelska O, Vidovencova Z (1994) Cleavage polyembryony in vivo and in vitro. Biologia Plantarum 36, 329–334.
Cleavage polyembryony in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar |

Filonova L, von Arnold S, Daniels J, Bozhkov P (2002) Programmed cell death eliminates all but one embryo in polyembryonic plant seed. Cell Death and Differentiation 9, 1057–1062.
Programmed cell death eliminates all but one embryo in polyembryonic plant seed.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38vntVGrtA%3D%3D&md5=2338d4cad8c7ca121c1c1e4bee49a38cCAS |

Gupta PK, Pullman GS (1991) Method for reproducing coniferous plants by somatic embryogenesis using abscisic acid and osmotic potential variation. US Patent 5036007.

Haines RJ, Prakash N (1980) Proembryo development and suspensor elongation in Araucaria Juss. Australian Journal of Botany 28, 511–522.
Proembryo development and suspensor elongation in Araucaria Juss.Crossref | GoogleScholarGoogle Scholar |

Henderson ST, Petes TD (1992) Instability of simple sequence DNA in Saccharomyces cerevisiae. Molecular and Cellular Biology 12, 2749–2757.

Johansen DA (1950) ‘Plant embryology.’ (Chronica Botanica Co.: Waltham, MA)

Krutovskii KV, Politov DV (1995) Allozyme evidence for polyzygotic polyembryony in Siberian stone pine (Pinus sibirica Du Tour). Theoretical and Applied Genetics 90, 811–818.
Allozyme evidence for polyzygotic polyembryony in Siberian stone pine (Pinus sibirica Du Tour).Crossref | GoogleScholarGoogle Scholar |

Maheshwari P, Singh H (1967) The female gametophyte of gymnosperms. Biological Reviews of the Cambridge Philosophical Society 42, 88–129.
The female gametophyte of gymnosperms.Crossref | GoogleScholarGoogle Scholar |

Mantovani A, Morellato PC, Dos Reis MS (2004) Fenologia reprodutiva e produção de sementes em Araucaria angustifolia (Bert.) O. Kuntze. Revista Brasileira de Botânica 27, 787–796.

Orr-Ewing A (1957) A cytological study of the effects of self-pollination on Pseudotsuga menziesii (Mirb.) Franco. Silvae Genetica 6, 179–185.

Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. The Journal of Heredity 86, 248–249.

Rousset F (2008) Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Molecular Ecology Resources 8, 103–106.
Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux.Crossref | GoogleScholarGoogle Scholar |

Sambrook J, Fritsch EF, Maniatis T (1989) ‘Molecular cloning: a laboratory manual.’ 2nd edn. (Cold Spring Harbor Laboratory Press: New York)

Schmidt AB, Ciampi AY, Guerra MP, Nodari RO (2007) Isolation and characterization of microsatellite markers for Araucaria angustifolia (Araucariaceae). Molecular Ecology Notes 7, 340–342.
Isolation and characterization of microsatellite markers for Araucaria angustifolia (Araucariaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkvVKqsbw%3D&md5=ec9c9d5ffdfe64caa7ef705190ef7eeeCAS |

Steiner N, Vieira FN, Maldonado S, Guerra MP (2005) Effect of carbon source on morphology and histodifferentiation of Araucaria angustifolia embryogenic cultures. Brazilian Archives of Biology and Technology 48, 895–903.
Effect of carbon source on morphology and histodifferentiation of Araucaria angustifolia embryogenic cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XitF2htb4%3D&md5=613f66c3d7ac5e700ea8369325f1f153CAS |

Strand M, Prolla TA, Liskay RM, Petes TD (1993) Destabilization of tract of simple repetitive DNA in yeast by mutations affecting DNA mismatch repair. Nature 365, 274–276.
Destabilization of tract of simple repetitive DNA in yeast by mutations affecting DNA mismatch repair.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXms1equr0%3D&md5=18674c07eed206fa4c8529d85f1525d5CAS |

Von Arnold S, Sabala I, Bozkov P, Dyachok J, Filonova L (2002) Developmental pathways of somatic embryogenesis. Plant Cell, Tissue and Organ Culture 69, 233–249.
Developmental pathways of somatic embryogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltlSrtbo%3D&md5=44863356a0ac9410a76b238dff445cc5CAS |

Vuosku J, Sutela S, Tillman-Sutela E, Kauppi A, Jokela A, Sarjala T, Häggman H (2009a) Pine embryogenesis: many licences to kill for a new life. Plant Signaling & Behavior 4, 928–932.
Pine embryogenesis: many licences to kill for a new life.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXms1ajtbc%3D&md5=290094008988cb34d39b0d30049958ebCAS |

Vuosku J, Sarjala T, Jokela A, Sutela S, Sääskilahti L, Suorsa M, Läärä M, Häggman H (2009b) One tissue, two fates: different roles of megagametophyte cells during Scots pine embryogenesis. Journal of Experimental Botany 60, 1375–1386.
One tissue, two fates: different roles of megagametophyte cells during Scots pine embryogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsFShsL8%3D&md5=b08695d48b890178f531763c831bf49eCAS |

Wendt dos Santos AL, Steiner N, Guerra MP, Zoglauer K, Moerschbacher MB (2008) Somatic embryogenesis in Araucaria angustifolia. Biologia Plantarum 52, 195–199.
Somatic embryogenesis in Araucaria angustifolia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnt1eht7g%3D&md5=320c6e1147ca9521395afca9362f281eCAS |

Williams CG (2007) Re-thinking the embryo lethal system within the Pinaceae. Canadian Journal of Botany 85, 667–677.
Re-thinking the embryo lethal system within the Pinaceae.Crossref | GoogleScholarGoogle Scholar |

Williams CG (2008) Selfed embryo death in Pinus taeda: a phenotypic profile. New Phytologist 178, 210–222.
Selfed embryo death in Pinus taeda: a phenotypic profile.Crossref | GoogleScholarGoogle Scholar |

Williams CG (2009) ‘Conifer reproductive biology.’ (Springer: New York)10.1007/978-1-4020-9602-0

Wright S (1949) The genetical structure of populations. Annals of Eugenics 15, 323–354.
The genetical structure of populations.Crossref | GoogleScholarGoogle Scholar |