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Interaction of lipid bodies with other cell organelles in the maturing pollen of Magnolia × soulangeana (Magnoliaceae)

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Abstract

The pollen grain maturation in Magnolia × soulangeana was studied ultrastructurally and cytochemically using both the light and transmission electron microscope. Emphasis was given on the storage lipid bodies of the vegetative cell (VC) and their interaction with other cell organelles. Stereological analysis of electron micrographs was performed to evaluate the variation in volume density (VV), surface density, and surface-to-volume ratio (S/V) of various cell organelles during pollen maturation. The size and numerical density of the lipid bodies, and their frequency of association with other cell organelles, were also determined. It was noted that during pollen ontogeny and maturation, the lipid bodies changed their pattern of distribution in the VC cytoplasm, which may be a good marker for the succeeding stages of pollen development. Also, the size, osmiophily, and VV of the lipid bodies were progressively reduced during pollen maturation whereas the S/V was significantly increased. This seems to indicate that the lipid bodies are mobilized in part during this period of pollen maturation. In particular, the intermediate and mature pollen showed a high percentage of lipid bodies establishing a physical contact with either glyoxysomes, either protein storage vacuoles, or small vesicles presumably originated from dictyosomes. This physical contact was found in both the chemically fixed and rapid freeze-fixed pollen indicating that it is neither artifactual nor casual. On the basis of this intimate association with other cell organelles and the morphometric analysis performed, we suggest that the mobilization of lipid bodies is likely mediated not only by glyoxysomes but also by other catabolic pathways involving the interaction of lipid bodies with either protein storage vacuoles or small Golgi vesicles.

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References

  • Abreu I, Oliveira M (2003) Lipid and polysaccharide variations in Actinidia deliciosa during pollen ontogeny and germination. Acta Hort 610:473–477

    CAS  Google Scholar 

  • Binns D, Januszewski T, Chen Y, Hill J, Markin V, Zhao Y, Gilpin C, Chapman K, Anderson R, Goodman J (2006) An intimate collaboration between peroxisomes and lipid bodies. J Cell Biol 173:719–731

    Article  PubMed  CAS  Google Scholar 

  • Bronner R (1975) Simultaneous demonstration of lipids and starch in plant tissues. Stain Technol 50:1–4

    PubMed  CAS  Google Scholar 

  • Caiola MG, Brandizzi F, Canini A (2000) Hermodactylus tuberosus L. (Iridaceae) pollen organisation before and after anther dehiscence. Plant Biosystems 134:353–364

    Article  Google Scholar 

  • Chapman K, Trelease R (1991) Acquisition of membrane lipids by differentiating glyoxysomes: role of lipid bodies. J Cell Biol 115:995–1007

    Article  PubMed  CAS  Google Scholar 

  • Charzynska M, Murgia M, Cresti M (1989) Ultrastructure of the vegetative cell of Brassica napus pollen with particular reference to microbodies. Protoplasma 152:22–28

    Article  Google Scholar 

  • Cheung AY, Wu H-M (2007) Structural and functional compartmentalization in pollen tubes. J Exp Bot 58:75–82

    Article  PubMed  CAS  Google Scholar 

  • Crane PR (1998) The phylogenetic position and fossil history of the Magnoliaceae. In: Hunt D (ed) Magnolias and their allies. International Dendrology Society and the Magnolia Society, United Kingdom, pp 21–36

    Google Scholar 

  • Cresti M, Ciampolini F, Sarfatti G (1983) Ultrastructural features of Malus communis L. mature pollen. In: Mulcahy DL, Ottaviano E (eds) Pollen: biology and implications for plant breeding. Elsevier, New York, pp 165–172

    Google Scholar 

  • Cresti M, Blackmore S, Van Went JL (1992) Atlas of sexual reproduction in flowering plants. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Cresti M, El-Ghazaly G, Milanesi C, Walles B (1999) Ultrastructural characteristics of Betula pendula tapetum and pollen grains after rapid freezing and freeze-substitution. Grana 38:194–202

    Article  Google Scholar 

  • Dinis AM (1997) Estudo ultrastrutural e citoquímico da microsporogénese em Magnolia × soulangeana Soul.-Bod. (Magnoliaceae). Ph.D. thesis, Faculty of Sciences and Technology, University of Coimbra, Coimbra, Portugal

  • Dinis AM, Mesquita JF (1994) Ultrastructural and cytochemical evidence for the presence of peroxisomes in the generative cell of Magnolia × soulangeana pollen grain. Ann Bot 73:83–90

    Article  Google Scholar 

  • Dinis AM, Mesquita JF (1999) Ultrastructural study of the relationship between generative and vegetative cells in Magnolia × soulangeana Soul.-Bod. pollen grains. Protoplasma 206:87–96

    Article  Google Scholar 

  • Dinis AM, Mesquita JF (2002) Peroxisome evolution during the pollen development in Magnolia × soulangeana Soul.-Bod. (Magnoliaceae). Bol Soc Brot, ser 2 71:105–117

    Google Scholar 

  • Dinis AM, Santos Dias JD, Mesquita JF (2000) Ultrastructure of the mature pollen of Michelia figo (Lour.) Spreng. (Magnoliaceae). J Submicrosc Cytol Pathol 32:591–601

    PubMed  CAS  Google Scholar 

  • Eady C, Lindsey K, Twell D (1995) The significance of microspore division and division symmetry for vegetative cell-specific transcription and generative cell differentiation. Plant Cell 7:65–74

    Article  PubMed  CAS  Google Scholar 

  • Eliseu SA, Dinis AM (2008) Ultrastructure and cytochemistry of Eucalyptus globulus (Myrtaceae) pollen grain. Grana 47:39–51. doi:10.1080/00173130801923364

    Article  Google Scholar 

  • Evans DE, Taylor PE, Singh MB, Knox RB (1992) The interrelationship between the accumulation of lipids, protein and the level of acyl carrier protein during the development of Brassica napus L. pollen. Planta 186:343–354

    Article  CAS  Google Scholar 

  • Fischer U, Men S, Grebe M (2004) Lipid function in plant cell polarity. Curr Opin Plant Biol 7:670–676. doi:10.1016/j.pbi.2004.09.007

    Article  PubMed  CAS  Google Scholar 

  • Footitt S, Dietrich D, Fait A, Fernie AR, Holdsworth MJ, Baker A, Theodoulou FL (2007) The COMATOSE ATP-binding cassette transporter is required for full fertility in Arabidopsis. Plant Physiol 144:1467–1480

    Article  PubMed  CAS  Google Scholar 

  • Graham IA (2008) Seed storage oil mobilization. Annu Rev Plant Biol 59:115–142. doi:10.1146/annurev.arplant.59.032607.092938

    Article  PubMed  CAS  Google Scholar 

  • Hayashi Y, Hayashi M, Hayashi H, Hara-Nishimura I, Nishimura M (2001) Direct interaction between glyoxysomes and lipid bodies in cotyledons of the Arabidopsis thaliana ped1 mutant. Protoplasma 218:83–94

    Article  PubMed  CAS  Google Scholar 

  • Heslop-Harrison J, Dickinson HG (1967) A cycle of sphaerosome aggregation and disaggregation correlated with the meiotic divisions in Lilium. Phytomorphology 17:195–199

    Google Scholar 

  • Hess MW (1995) High-pressure freeze fixation reveals novel features during ontogenesis of the vegetative cell in Ledebouria pollen: an ultrastructural and cytochemical study. Biochem Cell Biol 73:1–10

    Article  PubMed  CAS  Google Scholar 

  • Hsieh K, Huang A (2004) Endoplasmic reticulum, oleosins, and oils in seeds and tapetum cells. Plant Physiol 136:3427–3434

    Article  PubMed  CAS  Google Scholar 

  • Jiang P-L, Wang C-S, Hsu C-M, Jauh G-Y, Tzen TC (2007) Stable oil bodies sheltered by a unique oleosin in Lily pollen. Plant Cell Physiol 48:812–821. doi:10.1093/pcp/pcm051

    Article  PubMed  CAS  Google Scholar 

  • Kim HU, Hsieh K, Ratnayake C, Huang A (2002) A novel group of oleosins is present inside the pollen of Arabidopsis. J Biol Chem 277:22677–22684. doi:10.1074/jbc.M109298200

    Article  PubMed  CAS  Google Scholar 

  • Kuang A, Musgrave ME (1996) Dynamics of vegetative cytoplasm during generative cell formation and pollen maturation in Arabidopsis thaliana. Protoplasma 194:81–90

    Article  PubMed  CAS  Google Scholar 

  • Lancelle SA, Callaham DA, Hepler PK (1986) A method for rapid freeze fixation of plant cells. Protoplasma 131:153–165

    Article  Google Scholar 

  • Murphy DJ (2001) The biogenesis and functions of lipid bodies in animals, plants and microorganisms. Prog Lipid Res 40:325–438

    Article  PubMed  CAS  Google Scholar 

  • Noher de Halac I, Fama G, Cismondi IA (1992) Changes in lipids and polysaccharides during pollen ontogeny in Oenothera anthers. Sex Plant Reprod 5:110–116

    Google Scholar 

  • Noguchi T (1990) Consumption of lipid granules and formation of vacuoles in the pollen tube of Tradescantia reflexa. Protoplasma 156:19–28

    Article  Google Scholar 

  • Pacini E, Guarnieri M, Nepi M (2006) Pollen carbohydrates and water content during development, presentation, and dispersal: a short review. Protoplasma 228:73–77. doi:10.1007/s00709-006-0169-z

    Article  PubMed  CAS  Google Scholar 

  • Pais MS, Feijó JA (1987) Microbody proliferation during the microsporogenesis of Ophrys lutea Cav. (Orchidaceae). Protoplasma 138:149–155

    Article  Google Scholar 

  • Park SK, Twell D (2001) Novel patterns of ectopic cell plate growth and lipid body distribution in the Arabidopsis gemini pollen1 mutant. Plant Physiol 126:899–909

    Article  PubMed  CAS  Google Scholar 

  • Piffanelli P, Ross JHE, Murphy DJ (1997) Intra- and extracellular lipid composition and associated gene expression patterns during pollen development in Brassica napus. Plant J 11:549–562

    Article  PubMed  CAS  Google Scholar 

  • Piffanelli P, Ross JHE, Murphy DJ (1998) Biogenesis and function of the lipidic structures of pollen grains. Sex Plant Reprod 11:65–80

    Article  CAS  Google Scholar 

  • Poxleitner M, Rogers SW, Samuels AL, Browse J, Rogers JC (2006) A role for caleosin in degradation of oil-body storage lipid during seed germination. Plant J 47:917–933

    Article  PubMed  CAS  Google Scholar 

  • Rodríguez-García MI, M’rami-Alaoui M, Fernández MC (2003) Behavior of storage lipids during development and germination of olive (Olea europaea L.) pollen. Protoplasma 231:237–244. doi:10.1007/s00709-002-0076-x

    Google Scholar 

  • Roland J-C (1978) General preparation and staining of thin sections. In: Hall JL (ed) Electron microscopy and cytochemistry of plant cells. Elsevier/North-Holland Biomedical, Amsterdam Oxford New York, pp 1–62

    Google Scholar 

  • Ross JHE, Milanesi C, Murphy DJ, Cresti M (2000) Rapid-freeze fixation and substitution improves tissue preservation of microspores and tapetum in Brassica napus. Sex Plant Reprod 12:237–240

    Article  Google Scholar 

  • Sunderland N, Huang B (1987) Ultrastructural aspects of pollen dimorphism. Int Rev Cytol 107:175–220

    Article  Google Scholar 

  • Thiéry JP (1967) Mise en évidence des polysaccharides sur coupes fines en microscopie électronique. J Microsc 6:987–1018

    Google Scholar 

  • Twell D, Park SK, Lalanne E (1998) Asymmetric division and cell-fate determination in developing pollen. Trends Plant Sci 3:305–310

    Article  Google Scholar 

  • Voelker DR (2006) Bridging gaps in phospholipids transport. Trends Biochem Sci 30:396–404

    Article  CAS  Google Scholar 

  • Wang X (2004) Lipid signaling. Curr Opin Plant Biol 7:329–336. doi:10.1016/j.pbi.2004.03.012

    Article  PubMed  CAS  Google Scholar 

  • Weibel ER (1979) Stereological methods. Practical methods for biological morphometry. Academic, London

    Google Scholar 

  • Wetzel CLR, Jensen WA (1992) Studies of pollen maturation in cotton: the storage reserve accumulation phase. Sex Plant Reprod 5:117–127

    Article  Google Scholar 

  • Williams MA (1977) Quantitative methods in biology. In: Glauert AM (ed) Pratical methods in electron microscopy, vol 6. North-Holland Publishing, Amsterdam New York Oxford, pp 5–84

    Google Scholar 

  • Yamamoto Y, Nishimura M, Hara-Nishimura I, Noguchi T (2003) Behavior of vacuoles during microspore and pollen development in Arabidopsis thaliana. Plant Cell Physiol 44:1192–1201

    Article  PubMed  CAS  Google Scholar 

  • Zhang JZ, Laudencia-Chingcuanco DL, Comai L, Li M, Harada JJ (1994) Isocitrate lyase and malate synthase genes from Brassica napus L. are active in pollen. Plant Physiol 104:857–864

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank JD Santos Dias for technical assistance and Dr R Teixeira for improving the English. This work was supported by grants from Fundação para a Ciência e Tecnologia (FCT), Portugal.

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The authors declare that they have no conflict of interest.

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Correspondence to Augusto M. Dinis.

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Dinis, A.M., Coutinho, A.P. Interaction of lipid bodies with other cell organelles in the maturing pollen of Magnolia × soulangeana (Magnoliaceae). Protoplasma 238, 35–46 (2009). https://doi.org/10.1007/s00709-009-0071-6

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  • DOI: https://doi.org/10.1007/s00709-009-0071-6

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