Skip to main content
Log in

Microsporogenesis and pollen formation in cassava

  • Original Papers
  • Published:
Biologia Plantarum

Abstract

This article describes the complete microsporogenesis and pollen formation in cassava (Manihot esculenta Crantz) at the various developmental stages (pollen mother cell, meiosis, tetrads, early free spore, mid uninucleate, late uninucleate, binucleate and mature pollen grain). Light microscopy, transmission electron microscopy and confocal laser scanning microscopy were used for the study. Floral bud size and other inflorescence characteristics were correlated with specific stages of the microspore development. This association allows a rapid selection of floral buds with similar microspore developmental stages, useful when a large number of homogeneous cells are needed for analysis and for in vitro induction of androgenesis. This article also compares methods for digestion the exine wall in microspores.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

CLSM:

confocal laser scanning microscope

FISH:

fluorescent in situ hybridization

DAPI:

4′-6-diamidino-2-phenylindole

PMC:

pollen mother cell

EFS:

early free spore

T:

tapetum

M:

middle layer

EN:

endothecium

E:

anther epidermis

References

  • Alves, C.A.A.: Cassava botany and physiology. — In: Hillocks, R.J., Tresh J.M., Bellotti A.C. (ed.): Cassava: Biology, Production and Utilization. Pp. 67–89. CABI Publishing, London 2002.

    Chapter  Google Scholar 

  • Barinova, J., Zhexembekova, M., Barsova, E., Lukyanov, S., Heberle-Bors, E., Touraev, A.: Anthirinum majus mircospore maturation and transient transformation in vitro. — J. exp. Bot. 53: 1119–1129, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Berry, P.E., Cordeiro, I., Wiedenhoeft, A.C., Vitorino-Cruz, M.A., Ribes de Lima, L.: Brasiliocroton, a new crotonoid genus of Euhphorbiacea from Eastern Brazil. — Syst. Bot. 30: 357–365, 2005.

    Article  Google Scholar 

  • Blackmore, S., Wortley, A.H., Skvarla, J.J., Rowley, J.R.: Pollen wall development in flowering plants. — New Phytol. 174:483–498, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Boavida, L.C., Becker J.D., Feijó J.A.: The making of gametes in higher plants. — Int. J. dev. Biol. 49: 595–614, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Ceballos, H., Fregene, M., Pérez, J.C., Morante, N, Calle, F.: Cassava genetic improvement. — In: Kang, M.S., Priyadarshan P.M. (ed.) Breeding Major Food Staples. Pp. 365–391, Blackwell Publishing, Ames 2007.

    Chapter  Google Scholar 

  • Ceballos, H., Iglesias, C.A., Pérez J.C., Dixon A.G.O.: Cassava breeding: opportunities. — Plant mol. Biol. 56: 503–515, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Chen, C.B., Xu, Y.Y., Ma, H., Chong, K.: Cell biological characterization of male meiosis and pollen development in rice. — J. Integr. Plant Biol. 47: 734–744, 2005.

    Article  Google Scholar 

  • Custódio, L., Carneiro, M.F., Romano, A.: Microsporogenesis and anther culture in carob tree (Ceratonia siliqua L.). — Sci. Hort.104: 65–77, 2005.

    Article  Google Scholar 

  • Da Silva, R.M., Bandel, G., Faraldo, M.I.F., Martins, P.S.: Biología reprodutiva de etnovariedades de mandioca. — Sci. Agr. 58: 101–107, 2001. [In Span.]

    Article  Google Scholar 

  • De Carvalho, R.D., Guerra, M.: Cytogenetics of Manihot esculenta Crantz (cassava) and eight related species. — Hereditas 136: 159–168, 2002.

    Article  PubMed  Google Scholar 

  • De Souza, M.M., Pereira, T.N.S.: Development of pollen grain in yellow passion-fruit (Passiflora edulis f. flavicarpa; Passifloraceae). — Genet. mol. Biol. 23: 469–473, 2000.

    Article  Google Scholar 

  • Esau, K.: Anatomy of Seed Plants. — Wiley, New York 1977.

    Google Scholar 

  • Fan, Z., Armstrong, K.C., Keller, W.A.: Development of microspores in vivo and in vitro in Brassica napus L. — Protoplasma 147: 191–199, 1988.

    Article  Google Scholar 

  • Goldberg, R.B., Beals, T.P., Sanders, P.M.: Anther development: basic principles and practical applications. — Plant Cell 5:1217–1229, 1993.

    Article  PubMed  CAS  Google Scholar 

  • Halsey, M.E., Olsen, K.M., Taylor, N.J., Chavarriaga-Aguirre, P.: Reproductive biology of cassava (Manihot escultenta Crantz) and isolation of experimental field trials. — Crop Sci. 48: 49–58, 2008.

    Article  Google Scholar 

  • Heslop-Harrison, J.: Cytoplasm connections between angiosperm meiocytes. — Ann. Bot. 30: 221–230, 1966.

    Google Scholar 

  • Hrabina, M., Jain, K., Gouyon, B.: Cross-reactivity between pollen allergens from common Pooideae grasses and cultivated cereals. — Clin. exp. Allergy Rev. 8: 18–20, 2008.

    Article  CAS  Google Scholar 

  • Huang, B., Bird, S., Kemble, R., Simmonds, D., Keller, W., Miki, B.: Effects of culture density, conditioned medium and feeder cultures on microspore embryogenesis in Brassica napus L. cv. Topas. — Plant Cell Rep. 8: 594–597, 1990.

    Article  Google Scholar 

  • Jennings, D.L.: Variation in pollen and ovule fertility in varieties of cassava, and the effect of interspecific crossing on fertility. — Euphytica 12: 69–76, 1963.

    Article  Google Scholar 

  • Kasperbauer, M.J., Wilson, H.M:. Haploid plant production and use. — USDA Technol. Bull. 1586: 33–39, 1979.

    CAS  Google Scholar 

  • Kernan, Z., Ferrie, A.M.R.: Microspore embryogenesis and the development of a double haploidy protocol for cow cockle (Saponaria vaccaria). — Plant Cell Rep. 25: 274–280, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Khan, F.A., Ahmad, S., Siddiqui, S.A.: Microsporogenesis and development of male gametophyte in some Solanum species. — Beitr. Biol. Pflanz. 66: 1–7, 1991.

    Google Scholar 

  • Kindiger, B., Beckett, J.B.: A hematoxilin staining procedure for maize pollen grain chromosomes. — Stain Technol. 60: 265–269, 1985.

    PubMed  CAS  Google Scholar 

  • Koltunow, A.M., Truettner, J., Cox, K.H., Wallroth, M., Goldberg, R.B.: Different temporal and spatial gene expression. — Plant Cell 2: 1201–1224, 1990.

    Article  PubMed  CAS  Google Scholar 

  • Koti, S., Reddy, K.R., Kakani, V.G., Zhao, D., Reddy, V.R.: Soybean (Glycine max) pollen germination characteristics, flower and pollen morphology in response to enhanced ultraviolet-B radiation. — Ann. Bot. 94: 855–864, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Lauxen, M.S., Kaltchuk-Santos, E., Hu, C., Callegari-Jacquesi, S.M., Bodanese-Zanettini, M.H.: Association between floral bud size and developmental stage in soybean microspores. — Braz. Arch. Biol. Technol. 46: 515–520, 2003.

    Article  Google Scholar 

  • Lee, Y., Kim, E.S., Choi, Y. Hwang, I., Staiger, J., Chung, Y.Y., Lee, Y.: The Arabidopsis phosphatildylinositol-3-kinase is important for pollen development. — Plant Physiol. 147:1886–1897, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Li, D.X., Lin, M.Z., Wang, Y.Y., Tian, H.Q.: Synergid: a key link in fertilization of angiosperms. — Biol. Plant. 53: 401–407, 2009.

    Article  Google Scholar 

  • Liu, W., Zheng, M.Y., Polle, E.A., Konzak, C.F.: Highly efficient doubled-haploid production in wheat (Triticum aestivum L.) via induced microspore embryogenesis. — Crop Sci. 42: 686–692, 2002.

    Article  Google Scholar 

  • Mariani, C., Beuckeleer, M.D., Truettner, J., Leemans, J., Goldberg, R.B.: Induction of male sterility in plants by a chimaric ribonuclease gene. — Nature 347: 737–741, 1990.

    Article  CAS  Google Scholar 

  • Mascarenhas J.P.: The biochemistry of angiosperm pollen development. — Bot. Rev. 41: 259–314, 1975.

    Article  CAS  Google Scholar 

  • McCormick, S.: Control of male gametophyte development. — Plant Cell 16(Suppl.): S142–S153, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Nowack, M.K., Grini, P.E., Jakoby, M.J., Lafos, M., Koncz, C., Schnittger, A.: A positive signal from the fertilization of the egg cell sets off endosperm proliferation in angiosperm embryogenesis. — Nat. Genet. 38: 63–67, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Ospina, B., Ceballos, H.: La yuca en el tercer milenio.[Cassava in the Third Milenium.] — CIAT Publication, Cali 2002. [In Span.]

    Google Scholar 

  • Owen, H.A., Makaroff, C.A.: Ultrastructure of microsporogenesis and microgametogenesis in Arabidopsis thaliana (L.) Heynh. ecotype Wassilewskija (Brassicaceae). — Protoplasma 185: 7–21, 1995.

    Article  Google Scholar 

  • Ressayre, A., Raquin, C., Mignot, A., Godelle, B, Gouyon, P.H.: Correlated variation in microtubule distribution, callose deposition during male post-meiotic cytokinesis, and pollen aperture number across Nicotiana species (Solanaceae). — Amer. J.Bot. 89: 393–400, 2002.

    Article  Google Scholar 

  • Reynolds, E.S.: The use of lead citrate at high pH as an electron-opaque stain for electron microscopy. — J. cell. Biol. 17: 208–213, 1963.

    Article  PubMed  CAS  Google Scholar 

  • Rowley, J.R., Claugher, D., Skvarla, J.J.: Structure of the exine in Artemisia vulgaris (Asteraceae): a review. — Taiwania 44:1–21, 1999.

    Google Scholar 

  • Scott, R.J., Spielman, M., Dickinson, H.G.: Stamen structure and function. — Plant Cell 16(Suppl.): S46–S60, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Scott, R., Hodge, R., Paul, W., Draper, J.: The molecular biology of anther differentiation. — Plant Sci. 80: 167–191, 1991.

    Article  CAS  Google Scholar 

  • Summers, W.L., Jaramillo, J., Bailey, T.: Microspore developmental stage and anther length influence the induction of tomato anther callus. — HortScience 27: 838–840, 1992.

    Google Scholar 

  • Taskin, K.M., Turgut, K. Scott, R.J.: Apomeiotic pollen mother cell development in the apomictic Boechera species. — Biol. Plant. 53: 468–474, 2009.

    Article  Google Scholar 

  • Tomasi, P., Dierig, D.A., Backhaus, R.A., Pigg, K.B.: Floral bud and mean petal length as morphological predictors of microspore cytological stage in Lesquerella. — HortScience 34: 1269–1270, 1999.

    Google Scholar 

  • Widholm, J.M.: The use of fluorescein diacetate and phenolsaphranine for determining viability of the cultured plant cells. — Stain Technol. 47: 189–194, 1972.

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The excellent technical support on microscopy provided by José Arroyave is hereby recognized. Valuable comments by Dr. Stephen Blackmore on an earlier version of this manuscript have been incorporated. This work was supported through the grant project No. 2003 FS 121 and No. 2006 FS 062 by The Rockefeller Foundation, NY, USA, and Research Fellow Partnership Programme (RFPP), Switzerland.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to H. Ceballos.

Additional information

Previously at International Center for Tropical Agriculture

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, C., Lentini, Z., Tabares, E. et al. Microsporogenesis and pollen formation in cassava. Biol Plant 55, 469–478 (2011). https://doi.org/10.1007/s10535-011-0112-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10535-011-0112-9

Additional key words

Navigation