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Transcriptome analysis of haploid male gametophyte development in Arabidopsis

David Honys12 and David Twell3

Author Affiliations

1 Institute of Experimental Botany AS CR, Rozvojová 135, CZ-165 02, Praha 6, Czech Republic

2 Department of Plant Physiology, Faculty of Sciences, Charles University, Viničná 5, CZ-128 44, Praha 2, Czech Republic

3 Department of Biology, University of Leicester, University Road, Leicester LE1 7RH, UK

Genome Biology 2004, 5:R85  doi:10.1186/gb-2004-5-11-r85

Published: 27 October 2004

Abstract

Background

The haploid male gametophyte generation of flowering plants consists of two- or three-celled pollen grains. This functional specialization is thought to be a key factor in the evolutionary success of flowering plants. Moreover, pollen ontogeny is also an attractive model in which to dissect cellular networks that control cell growth, asymmetric cell division and cellular differentiation. Our objective, and an essential step towards the detailed understanding of these processes, was to comprehensively define the male haploid transcriptome throughout development.

Results

We have developed staged spore isolation procedures for Arabidopsis and used Affymetrix ATH1 genome arrays to identify a total of 13,977 male gametophyte-expressed mRNAs, 9.7% of which were male-gametophyte-specific. The transition from bicellular to tricellular pollen was accompanied by a decline in the number of diverse mRNA species and an increase in the proportion of male gametophyte-specific transcripts. Expression profiles of regulatory proteins and distinct clusters of coexpressed genes were identified that could correspond to components of gametophytic regulatory networks. Moreover, integration of transcriptome and experimental data revealed the early synthesis of translation factors and their requirement to support pollen tube growth.

Conclusions

The progression from proliferating microspores to terminally differentiated pollen is characterized by large-scale repression of early program genes and the activation of a unique late gene-expression program in maturing pollen. These data provide a quantum increase in knowledge concerning gametophytic transcription and lay the foundations for new genomic-led studies of the regulatory networks and cellular functions that operate to specify male gametophyte development.