Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation - PubMed (original) (raw)

Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation

Cristina Pina et al. Plant Physiol. 2005 Jun.

Abstract

Upon germination, pollen forms a tube that elongates dramatically through female tissues to reach and fertilize ovules. While essential for the life cycle of higher plants, the genetic basis underlying most of the process is not well understood. We previously used a combination of flow cytometry sorting of viable hydrated pollen grains and GeneChip array analysis of one-third of the Arabidopsis (Arabidopsis thaliana) genome to define a first overview of the pollen transcriptome. We now extend that study to approximately 80% of the genome of Arabidopsis by using Affymetrix Arabidopsis ATH1 arrays and perform comparative analysis of gene family and gene ontology representation in the transcriptome of pollen and vegetative tissues. Pollen grains have a smaller and overall unique transcriptome (6,587 genes expressed) with greater proportions of selectively expressed (11%) and enriched (26%) genes than any vegetative tissue. Relative gene ontology category representations in pollen and vegetative tissues reveal a functional skew of the pollen transcriptome toward signaling, vesicle transport, and the cytoskeleton, suggestive of a commitment to germination and tube growth. Cell cycle analysis reveals an accumulation of G2/M-associated factors that may play a role in the first mitotic division of the zygote. Despite the relative underrepresentation of transcription-associated transcripts, nonclassical MADS box genes emerge as a class with putative unique roles in pollen. The singularity of gene expression control in mature pollen grains is further highlighted by the apparent absence of small RNA pathway components.

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Figures

Figure 1.

Figure 1.

Snail view representation and principal component analysis of tissue-dependent gene expression patterns. A, 18,321 genes used for a snail view representation were ranked counterclockwise from top according to decreasing mean expression in seedlings. For each tissue, the mean pattern in seedlings (black line) is coplotted with the mean pattern of the specific tissue (gray dots). The radius encodes the logarithm of gene expression (values <1 were set to 1 for better visualization). B, Two thousand of the 3,734 genes expressed in the vegetative tissues and in pollen were analyzed by projecting the 5 tissue types (replicate datasets are shown) on the first 2 principal components. The first principal component separates pollen from the vegetative tissues, while the second principal component shows a further separation of the vegetative tissues within themselves.

Figure 2.

Figure 2.

Proportions of enriched and selectively expressed genes and classification of biological activities in Arabidopsis tissues. A, Genes called present in each of the Arabidopsis tissues were analyzed in terms of enriched and/or selective expression. Tissue-enriched genes have expression levels in any particular tissue that are at least 1.2-fold higher than in all the remaining tissues; selectively expressed genes are those called present only in the particular tissue analyzed. B, 8,463 genes represented on the ATH1 GeneChip that were classified into at least one GO category (as of September 2003) were regrouped into 14 biological activity classes. The transcription and RNA-processing classification includes transcription factors, basic transcriptional machinery, and RNA-processing factors; the cell fate category covers cell cycle, cell differentiation, and apoptosis-related molecules; transporters refers to membrane channels. The proportion of the genes expressed in each tissue assigned to the different activity classes is represented. The separated bars show this classification for the pollen-enriched genes.

Figure 3.

Figure 3.

Plot of intertissue distances for the different levels of the GO tree of biological process terms. Overall differences in term frequencies between any two Arabidopsis tissues at each level of the GO biological process tree were calculated using Cramer's V and interpreted as a measure of the distance or dissimilarity between the two tissues. Results vary between 0 and 1, lower values reflecting more similar relative frequencies of terms. A total of 16,024 genes represented on the ATH1 GeneChip and classified into GO categories (as of December 2003) were included in the analysis. The plot is representative of results obtained for molecular function and component GO trees.

Figure 4.

Figure 4.

Overview of potential cell cycle regulation in pollen. Pollen gene expression data for core genes of the cell cycle (see also Table II) are overlaid on a schematic overview of the G1/S (A) and G2/M (B) transitions. For proteins colored light gray, no transcripts were detected in pollen (absent call). Transcripts expressed in pollen (present call) are either expressed at a comparable level to the vegetative tissues or enriched (arrow up; fold change value) or depleted (arrow down; fold change value). Question marks indicate pathways that are still not fully demonstrated experimentally. (Modified from De Veylder et al., 2003).

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