Male reproductive development: gene expression profiling of maize anther and pollen ontogeny

Jiong Ma,John Fernandes,David S Skibbe,Virginia Walbot

doi:10.1186/gb-2008-9-12-r181

Abstract

BackgroundDuring flowering, central anther cells switch from mitosis to meiosis, ultimately forming pollen containing haploid sperm. Four rings of surrounding somatic cells differentiate to support first meiosis and later pollen dispersal. Synchronous development of many anthers per tassel and within each anther facilitates dissection of carefully staged maize anthers for transcriptome profiling.ResultsGlobal gene expression profiles of 7 stages representing 29 days of anther development are analyzed using a 44 K oligonucleotide array querying approximately 80% of maize protein-coding genes. Mature haploid pollen containing just two cell types expresses 10,000 transcripts. Anthers contain 5 major cell types and express >24,000 transcript types: each anther stage expresses approximately 10,000 constitutive and approximately 10,000 or more transcripts restricted to one or a few stages. The lowest complexity is present during meiosis. Large suites of stage-specific and co-expressed genes are identified through Gene Ontology and clustering analyses as functional classes for pre-meiotic, meiotic, and post-meiotic anther development. MADS box and zinc finger transcription factors with constitutive and stage-limited expression are identified.ConclusionsWe propose that the extensive gene expression of anther cells and pollen represents the key test of maize genome fitness, permitting strong selection against deleterious alleles in diploid anthers and haploid pollen. Because flowering plants show a substantial bias for male-sterile compared to female-sterile mutations, we propose that this fitness test is general. Because both somatic and germinal cells are transcriptionally quiescent during meiosis, we hypothesize that successful completion of meiosis is required to trigger maturation of anther somatic cells.

Highlights

During flowering, central anther cells switch from mitosis to meiosis, forming pollen containing haploid sperm
Much is known about the specification of floral organs in plants, including the grasses [2], and about meiosis [3], the genes regulating the switch from mitosis to meiosis in specific cells remain largely undefined, as do the genes regulating differentiation of anther somatic cells [4]
We wished to address the following questions: is the decrease in transcript diversity at the entry into meiosis maintained for the six day duration of this process? Are discrete transcription factors expressed during preand post-meiotic anther development? Given that the cell walls of several cell types are extensively remodeled during anther development, can we identify cell wall-associated processes expressed in patterns reflecting these anatomical changes?

Summary

Introduction

Central anther cells switch from mitosis to meiosis, forming pollen containing haploid sperm. Genome Biology 2008, Volume 9, Issue 12, Article R181 Ma et al R181.2 growth, and a subset of these meristems switch later in development to produce flowers, a process that depletes the local stem cell population completely. For example, just a single cell differentiates to perform meiosis, resulting in a single embryo sac containing one haploid egg. In contrast, groups of cells in anthers differentiate for meiosis to produce large numbers of haploid pollen grains containing the sperm [1]. Much is known about the specification of floral organs in plants, including the grasses [2], and about meiosis [3], the genes regulating the switch from mitosis to meiosis in specific cells remain largely undefined, as do the genes regulating differentiation of anther somatic cells [4]

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