An Atlas of Type I MADS Box Gene Expression during Female Gametophyte and Seed Development in Arabidopsis

Abstract

Members of the plant type I MADS domain subfamily have been reported to be involved in reproductive development in Arabidopsis (Arabidopsis thaliana). However, from the 61 type I genes in the Arabidopsis genome, only PHERES1, AGAMOUS-LIKE80 (AGL80), DIANA, AGL62, and AGL23 have been functionally characterized, which revealed important roles for these genes during female gametophyte and early seed development. The functions of the other genes are still unknown, despite the fact that the available single T-DNA insertion mutants have been largely investigated. The lack of mutant phenotypes is likely due to a considerable number of recent intrachromosomal duplications in the type I subfamily, resulting in nonfunctional genes in addition to a high level of redundancy. To enable a breakthrough in type I MADS box gene characterization, a framework needs to be established that allows the prediction of the functionality and redundancy of the type I genes. Here, we present a complete atlas of their expression patterns during female gametophyte and seed development in Arabidopsis, deduced from reporter lines containing translational fusions of the genes to green fluorescent protein and b-glucuronidase. All the expressed genes were revealed to be active in the female gametophyte or developing seed, indicating that the entire type I subfamily is involved in reproductive development in Arabidopsis. Interestingly, expression was predominantly observed in the central cell, antipodal cells, and chalazal endosperm. The combination of our expression results with phylogenetic and protein interaction data allows a better identification of putative redundantly acting genes and provides a useful tool for the functional characterization of the type I MADS box genes in Arabidopsis.

The Emerging Importance of Type I MADS Box Transcription Factors for Plant Reproduction

“…Moreover, seven type I MADS box genes are highly expressed in Arabidopsis embryo sac cells, including AGL23, AGL61, and AGL80, consistent with previously published data (Portereiko et al, 2006;Bemer et al, 2008;M. Colombo et al, 2008;Steffen et al, 2008).Complementing transcriptomic investigations, the expression pattern of 60 type I MADS box genes in Arabidopsis by translational reporter fusions was recently reported (Bemer et al, 2010). A total of 42 genes were detected in the female gametophytes or developing seeds, confirming their predominant involvement in plant reproduction.…”

“…However, how AGL23 regulates chloroplast biogenesis is not clear since several pathways (e.g., carothenoid or lipid biosynthesis) could be under the control of AGL23. Expression studies showed that AGL23 expression correlates with the observed phenotypes since the putative AGL23 promoter drives GUS expression in the developing embryos at late globular stage when chloroplast biogenesis takes place and during embryo sac development as soon as the functional megaspore can be detected (M. .AGL23 shares high sequence similarity with AGL28, which is also expressed in developing embryos (Bemer et al, 2010 (Lee et al, 2000) upregulation, giving rise to the hypothesis that AGL28 plays a role in the autonomous flowering pathway (Yoo et al, 2006). However, homozygous agl28 mutant plants are viable, and no obvious aberrant phenotypes were observed (Yoo et al, 2006), making the suggested role for AGL28 in the regulation of flowering time premature.…”

Phylogenomic Synteny Network Analysis of MADS-Box Transcription Factor Genes Reveals Lineage-Specific Transpositions, Ancient Tandem Duplications, and Deep Positional Conservation

“…Also, the function of the different Type I genes is generally poorly characterized. However, several Type I genes have been reported to play a role in female gametogenesis, embryogenesis, and seed development (Portereiko et al, 2006;Bemer et al, 2010;Masiero et al, 2011).…”

The Differential Transcription Network between Embryo and Endosperm in the Early Developing Maize Seed

“…S17), implicating a differential transcriptional regulation between embryo and endosperm. It was previously reported that TFs of MADS function in seed and endosperm development (Kang et al, 2008;Sreenivasulu et al, 2008;Bemer et al, 2010;Le et al, 2010;Agarwal et al, 2011;Hehenberger et al, 2012). AGL62, a MADS protein of Arabidopsis, is the direct target of FIS Polycomb group repressive complex2 (PRC2), establishing the molecular basis for FIS PRC2-mediated endosperm cellularization (Hehenberger et al, 2012).…”

“…Several TF family members are likely to play a role in cell fate determination, including C2C2-YABBY (GRMZM2G167824 and GRMZM2G529859) and GeBP (GRMZM2G036966) homologs, as well as in cell growth regulation and germination, including WRKY (Zhang et al, 2011a;GRMZM5G816457) and bHLH (GRMZM2G042920) homologs. On the other hand, the majority of TFs enriched in endosperm were families such as MADS, SBP, NAC, bZIP, Myb, and C2C2-GATA, most of which have been implicated in seed development (Sreenivasulu et al, 2008;Bemer et al, 2010;Le et al, 2010;Agarwal et al, 2011). A total of 33 TF genes were selected for confirmation of the differential expression between embryo and endosperm with real-time RT-PCR analysis.…”