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

Understanding male sterility in Miconia species (Melastomataceae): a morphological approach

Priscila Andressa Cortez A , Sandra Maria Carmello-Guerreiro A and Simone Pádua Teixeira B C
+ Author Affiliations
- Author Affiliations

A Departamento de Biologia Vegetal, Instituto de Biologia, Universidade Estadual de Campinas, Caixa Postal 6109, Campinas, SP, 13083-970, Brazil.

B Departamento de Ciências Farmacêuticas, Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, Avenida do Café, s/n, Ribeirão Preto, SP, 14040-903, Brazil.

C Corresponding author. Email: spadua@fcfrp.usp.br

Australian Journal of Botany 60(6) 506-516 https://doi.org/10.1071/BT12076
Submitted: 31 March 2012  Accepted: 14 June 2012   Published: 12 September 2012

Abstract

Pollen abortion occurs in virtually all species and often does not prejudice reproductive success. However, large numbers of abnormal pollen grains are characteristic of some groups. Among them is Miconia, in which partial and complete male sterility is often related to apomixis. In this study, we compared the morphology of pollen grains over several developmental stages in Miconia species with different rates of male sterility. Our aim was to improve the knowledge of mechanisms that lead to male sterility in this ecologically important tropical group. Routine techniques for microscopy were used to examine anthers in several developmental stages collected from the apomictic species Miconia albicans and M. stenostachya. Both species are completely male sterile since even the pollen grains with apparently normal cytoplasm were not able to develop a pollen tube. Meiosis is a rare event in M. albicans anthers and happens in an irregular way in M. stenostachya, leading to the pollen abortion. M. albicans has more severe abnormalities than M. stenostachya since even the microspores and pollen grain walls were affected. Moreover, in M. stenostachya, most mitosis occurring during microgametogenesis was also abnormal, leading to the formation of bicellular pollen grains with two similar cells, in addition to the formation of pollen grains of different sizes. Notably, abnormalities in both species did not reach the production of Übisch bodies, suggesting little or no tapetum involvement in male sterility in these two species.


References

Alves-Ferreira M, Wellmer F, Banhara A, Kumar V, Riechmann JL, Meyerowitz EM (2007) Global expression profiling applied to the analysis of Arabidopsis stamen development. Plant Physiology 145, 747–762.
Global expression profiling applied to the analysis of Arabidopsis stamen development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlemsrnM&md5=c2628ab9203c2f920060fbd7395d85afCAS |

Ariizumi T, Hatakeyama K, Hinata K, Sato S, Kato T, Tabata S, Toriyami K (2003) A novel male-sterile mutant of Arabidopsis thaliana, faceless pollen-1, produces pollen with a smooth surface and an acetolysis-sensitive exine. Plant Molecular Biology 53, 107–116.
A novel male-sterile mutant of Arabidopsis thaliana, faceless pollen-1, produces pollen with a smooth surface and an acetolysis-sensitive exine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpvVGgtLc%3D&md5=81e053452b39b9bdf2a48e12a545b7a1CAS |

Ariizumi T, Hatakeyama K, Hinata K, Sato S, Kato T, Tabata S, Toriyami K (2005) The HKM gene, which is identical to the MS1 gene of Arabidopsis thaliana, is essential for primexine formation and exine pattern formation. Sexual Plant Reproduction 18, 1–7.
The HKM gene, which is identical to the MS1 gene of Arabidopsis thaliana, is essential for primexine formation and exine pattern formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXkvFSrtbY%3D&md5=9733813768a26a9e4ba0df04398fad8bCAS |

Ariizumi T, Kawanabe T, Hatakeyama K, Sato S, Kato T, Tabata S, Toriyami K (2008) Ultrastructural characterization of exine development of the transient defective exine 1 mutant suggests the existence of a factor involved in constructing reticulate exine architecture from sporopollenin aggregates. Plant & Cell Physiology 49, 58–67.
Ultrastructural characterization of exine development of the transient defective exine 1 mutant suggests the existence of a factor involved in constructing reticulate exine architecture from sporopollenin aggregates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitVSgtbw%3D&md5=ac368d2456b5cecb2a10666d5153f7adCAS |

Asker S (1979) Progress in apomixis research. Hereditas 91, 231–240.
Progress in apomixis research.Crossref | GoogleScholarGoogle Scholar |

Bertasso-Borges MS, Coleman JR (2005) Cytogenetics and embryology of Eupatorium laevigatum (Compositae). Genetics and Molecular Biology 28, 123–128.
Cytogenetics and embryology of Eupatorium laevigatum (Compositae).Crossref | GoogleScholarGoogle Scholar |

Biasi R, Falasca G, Speranza A, De Stradis A, Scoccianti V, Franceschetti M, Bagni N, Altamura MM (2001) Biochemical and ultrastructural features related to male sterility in the dioecious species Actinidia deliciosa. Plant Physiology and Biochemistry 39, 395–406.
Biochemical and ultrastructural features related to male sterility in the dioecious species Actinidia deliciosa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXktlSit7w%3D&md5=5b1d808cda328341a18a14381b95ae7cCAS |

Bohdanowicz J, Szczuka E, Swierczynska J, Sobieska J, Koscinska-Pajak M (2005) Distribution of microtubules during regular and disturbed microsporogenesis and pollen grain development in Gagea lutea (L.) Ker.-Gaw. Acta Biologica Cracoviensia. Series; Botanica 47, 89–96.

Budar F, Pelletier G (2001) Male sterility in plants: occurrence, determinism, significance and use. Comptes Rendus de L’Académie des Sciences III 324, 543–550.
Male sterility in plants: occurrence, determinism, significance and use.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvgsFWrtA%3D%3D&md5=92ad65a2d030d8dc34fac89e9d52e96dCAS |

Byzova MV, Franken J, Aarts MGM, Almeida-Engler J, Engler G, Mariani C, Van Lookeren Campagne MM, Angenent GC (1999) Arabidopsis STERILE APETALA, a multifunctional gene regulating inflorescence, flower, and ovule development. Genes & Development 13, 1002–1014.
Arabidopsis STERILE APETALA, a multifunctional gene regulating inflorescence, flower, and ovule development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXivFGkurk%3D&md5=673b67da9f306783882ca775f96537feCAS |

Calisto V, Fuzinatto VA, Message HJ, Mendes-Bonato AB, Boldrini KR, Pagliarini MS, Borges do Valle C (2008) Desynapsis and precocious cytokinesis in Brachiaria humidicola (Poaceae) compromise meiotic division. Journal of Genetics 87, 27–31.
Desynapsis and precocious cytokinesis in Brachiaria humidicola (Poaceae) compromise meiotic division.Crossref | GoogleScholarGoogle Scholar |

Cardoso MB, Kaltchuk-Santos E, Mundstock EC, Bodanese-Zanettini MH (2004) Initial segmentation patterns of microspores and pollen viability in soybean cultured anthers: indication of chromosome doubling. Brazilian Archives of Biology and Technology 47, 703–712.
Initial segmentation patterns of microspores and pollen viability in soybean cultured anthers: indication of chromosome doubling.Crossref | GoogleScholarGoogle Scholar |

Consiglio F, Conicella C, Monti L, Carputo D (2003) Highlights of meiotic genes in Arabidopsis thaliana. African Journal of Biotechnology 2, 516–520.

Couteau F, Belzile F, Horlow C, Grandjean O, Vezon D, Doutriaux MP (1999) Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmc1 mutant of Arabidopsis. The Plant Cell 11, 1623–1634.
Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmc1 mutant of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXms1aiu70%3D&md5=71e86ef91b398f763bc7f6fa0bbfcc54CAS |

Dawe RK (1998) Meiotic chromosome organization and segregation in plants. Annual Review of Plant Physiology and Plant Molecular Biology 49, 371–395.
Meiotic chromosome organization and segregation in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjvVShur0%3D&md5=cf0254ba30b8b984366455a08a29d0eeCAS |

de Jong AJ, Schmidt ED, de Vries SC (1993) Early events in higher-plant embryogenesis. Plant Molecular Biology 22, 367–377.
Early events in higher-plant embryogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXltFegsrg%3D&md5=05c786ceb3404d43821b8f5ba9d251ecCAS |

Goldberg RB, Beals TP, Sanders PM (1993) Anther development: basic principles and practical applications. The Plant Cell 5, 1217–1229.
Anther development: basic principles and practical applications.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c7gvValsg%3D%3D&md5=48e42ff8d16187a49fdc27c1008e3288CAS |

Goldenberg R, Shepherd GJ (1998) Studies on the reproductive biology of Melastomataceae in ‘cerrado’ vegetation. Plant Systematics and Evolution 211, 13–29.
Studies on the reproductive biology of Melastomataceae in ‘cerrado’ vegetation.Crossref | GoogleScholarGoogle Scholar |

Grelon M, Vezon D, Gendrot G, Pelletier G (2001) AtSPO11–1 is necessary for efficient meiotic recombination in plants. European Molecular Biology Organization Journal 20, 589–600.
AtSPO11–1 is necessary for efficient meiotic recombination in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXitFGqtLw%3D&md5=251c1c61ca3f91e166f03581da4c22ebCAS |

Hulskamp M, Nikesh SP, Grini P, Schneitz K, Zimmermann I, Lolle SJ, Pruitt RE (1997) The STUD gene is required for male-specific cytokinesis after telophase II of meiosis in Arabidopsis thaliana. Developmental Biology 187, 114–124.
The STUD gene is required for male-specific cytokinesis after telophase II of meiosis in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2szmsl2isA%3D%3D&md5=89f3ed3b157e1e2a077c045f8d5fdf25CAS |

Jiang H, Wang F, Wu Y, Zhou X, Huang X, Zhu J, Gao J-F, Dong R-B, Cao K-M, Yang Z-N (2009) MULTIPOLAR SPINDLE 1 (MPS1), a novel coiled-coil protein of Arabidopsis thaliana, is required for meiotic spindle organization. The Plant Journal 59, 1001–1010.
MULTIPOLAR SPINDLE 1 (MPS1), a novel coiled-coil protein of Arabidopsis thaliana, is required for meiotic spindle organization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1yrsrnP&md5=53ea571d673f01ea821452568886a18aCAS |

Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. The Journal of Cell Biology 27, 137A–138A.

Kaul MLH, Murphy TGK (1985) Mutant genes affecting higher plant meiosis. Theoretical and Applied Genetics 70, 449–466.
Mutant genes affecting higher plant meiosis.Crossref | GoogleScholarGoogle Scholar |

Koltunow AM, Bicknell RA, Chaudhury AM (1995) Apomixis: molecular strategies for the generation of genetically identical seeds without fertilization. Plant Physiology 108, 1345–1352.
Apomixis: molecular strategies for the generation of genetically identical seeds without fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnsVags7w%3D&md5=b901d5f98e105bf657fd7b378ac1ef38CAS |

Laser KD, Lersten NR (1972) Anatomy and cytology of microsporogenesis in cytoplasmic male sterile angiosperms. Botanical Review 38, 425–454.
Anatomy and cytology of microsporogenesis in cytoplasmic male sterile angiosperms.Crossref | GoogleScholarGoogle Scholar |

Lersten NR (2004) ‘Flowering plant embryology – with emphasis on economic species.’ (Blackwell Publishing: Ames, Iowa) 10.1002/9780470752685.ch1

Otto SP, Whitton J (2000) Polyploid incidence and evolution. Annual Review of Genetics 34, 401–437.
Polyploid incidence and evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlvFOjsg%3D%3D&md5=542f4aa7d3a8fa019004ad296efad026CAS |

Owen HA, Makaroff CA (1995) Ultrastructure of microsporogenesis and microgametogenesis in Arabidopsis thaliana (L.) Heynh. ecotype Wassilewskija (Brassicaceae). Protoplasma 185, 7–21.
Ultrastructure of microsporogenesis and microgametogenesis in Arabidopsis thaliana (L.) Heynh. ecotype Wassilewskija (Brassicaceae).Crossref | GoogleScholarGoogle Scholar |

Pijnacker LP, Ferwerda MA, Mattheij WM (1992) Microsporogenesis in three tetraploid somatic hybrids of potato and their di(ha)ploid fusion partners. Theoretical and Applied Genetics 85, 269–273.
Microsporogenesis in three tetraploid somatic hybrids of potato and their di(ha)ploid fusion partners.Crossref | GoogleScholarGoogle Scholar |

Risso-Pascotto C, Pagliarini MS, Valle CB, Jank L (2005) Symmetric pollen mitosis I and suppression of pollen mitosis II prevent pollen development in Brachiaria jubata (Gramineae). Brazilian Journal of Medical and Biological Research 38, 1603–1608.
Symmetric pollen mitosis I and suppression of pollen mitosis II prevent pollen development in Brachiaria jubata (Gramineae).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MrnvVensw%3D%3D&md5=1f0a672ad935eb222cb8f8f0aaf0ba66CAS |

Roeder GS (1997) Meiotic chromosomes: it takes two to tango. Genes & Development 11, 2600–2621.
Meiotic chromosomes: it takes two to tango.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2svnslelug%3D%3D&md5=4e7aa73b681da81eb34e3eb4b49b56f9CAS |

Santos RP, Mariath JEA (1997) A simple method for fixing, dehydrating and embedding pollen tubes cultivated in vitro for optical and transmission electron microscopy. Biotechnic & Histochemistry 72, 315–319.
A simple method for fixing, dehydrating and embedding pollen tubes cultivated in vitro for optical and transmission electron microscopy.Crossref | GoogleScholarGoogle Scholar |

Scott RJ (1994) Pollen exine: the sporopollenin enigma and the physics of pattern. In ‘Molecular and cellular aspects of plant reproduction’. (Eds RJ Scott, MA Stead) pp. 49–81. (University Press: Cambridge) 10.1017/CBO9780511752339.006

Siddiqi I, Ganesh G, Grossniklaus U, Subbiah V (2000) The DYAD gene is required for progression through female meiosis in Arabidopsis. Development 127, 197–207.

Soltis DE, Soltis PS, Tate JA (2004) Advances in the study of polyploidy since plant speciation. New Phytologist 161, 173–191.
Advances in the study of polyploidy since plant speciation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmsVWluw%3D%3D&md5=c9c5e958f44c6aabebc69693c411e883CAS |

Soltis DE, Soltis PS, Schemske DW, Hancock JF, Thompson JN, Husband BC, Judd WS (2007) Autopolyploidy in angiosperms: have we grossly underestimated the number of species? Taxon 56, 13–30.
Autopolyploidy in angiosperms: have we grossly underestimated the number of species?Crossref | GoogleScholarGoogle Scholar |

Soltis DE, Albert VA, Leebens-Mack J, Bell CD, Paterson AH, Zheng C, Sankoff D, dePamphilis CW, Kerr Wall P, Soltis PS (2009) Polyploidy and angiosperm diversification. American Journal of Botany 96, 336–348.
Polyploidy and angiosperm diversification.Crossref | GoogleScholarGoogle Scholar |

Spillane C, Steimer A, Grossniklaus U (2001) Apomixis in agriculture: the quest for clonal seeds. Sexual Plant Reproduction 14, 179–187.
Apomixis in agriculture: the quest for clonal seeds.Crossref | GoogleScholarGoogle Scholar |

Taylor PE, Glover JA, Lavithis M, Craig S, Singh MB, Knox RB, Dennis ES, Chaudhury AM (1998) Genetic control of male fertility in Arabidopsis thaliana: structural analyses of postmeiotic developmental mutants. Planta 205, 492–505.
Genetic control of male fertility in Arabidopsis thaliana: structural analyses of postmeiotic developmental mutants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXksFGmsrw%3D&md5=1126c16a535312eefa61684d2ac9b335CAS |

Tsuchiya T, Toriyama K, Yoshikawa M, Ejiri S, Hinata K (1995) Tapetum-specific expression of the gene for an endo-b-1,3-glucanase causes male sterility in transgenic tobacco. Plant & Cell Physiology 36, 487–494.

Worall D, Hird DL, Hodge R, Paul W, Draper J, Scott R (1992) Premature dissolution of the microsporocyte callose wall causes male sterility in transgenic tobacco. The Plant Cell 4, 759–771.
Premature dissolution of the microsporocyte callose wall causes male sterility in transgenic tobacco.Crossref | GoogleScholarGoogle Scholar |

Yang M, Hu Y, Lodhi M, McCombie WR, Ma H (1999) The Arabidopsis SKP1-LIKE1 gene is essential for male meiosis and may control homologue separation. Proceedings of the National Academy of Sciences of the United States of America 96, 11416–11421.
The Arabidopsis SKP1-LIKE1 gene is essential for male meiosis and may control homologue separation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmvVCmsbc%3D&md5=456fe9c1d9358391adde5514be346c5cCAS |

Zhu Y, Dun X, Zhou Z, Xia S, Yi B, Wen J, Shen J, Ma C, Tu J, Fu T (2010) A separation defect of tapetum cells and microspore mother cells results in male sterility in Brassica napus: the role of abscisic acid in early anther development. Plant Molecular Biology 72, 111–123.
A separation defect of tapetum cells and microspore mother cells results in male sterility in Brassica napus: the role of abscisic acid in early anther development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsV2mtb7F&md5=14d49339d073a59f537e87fb8952500eCAS |