☆ 4.7 Article

Transcriptome Analysis Reveals Putative Target Genes of APETALA3-3 During Early Floral Development in Nigella damascena L.

FRONTIERS IN PLANT SCIENCE (2021)

Journal

FRONTIERS IN PLANT SCIENCE

Volume 12, Issue -, Pages -

Publisher

FRONTIERS MEDIA SA

DOI: 10.3389/fpls.2021.660803

Keywords

APETALA3; RNA-seq; AP3 target genes; petal; Nigella damascena; floral mutant; Ranunculaceae; Arabidopsis

Funding

Institut Diversite, Ecologie et Evolution du Vivant (IDEEV) [AAP2013, AAP2015]

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Abstract

By analyzing the transcriptome of a Ranunculaceae species, it was found that the gene network of the AP3-III lineage shows a certain level of conservation in species with petals of different evolutionary origins. The study identified a small set of conserved genes that determine petal identity and early development in core eudicots and Ranunculaceae, despite the independent evolutionary origin of petals in these taxa.

Even though petals are homoplastic structures, their identity consistently involves genes of the APETALA3 (AP3) lineage. However, the extent to which the networks downstream of AP3 are conserved in species with petals of different evolutionary origins is unknown. In Ranunculaceae, the specificity of the AP3-III lineage offers a great opportunity to identify the petal gene regulatory network in a comparative framework. Using a transcriptomic approach, we investigated putative target genes of the AP3-III ortholog NdAP3-3 in Nigella damascena at early developmental stages when petal identity is determined, and we compared our data with that from selected eudicot species. We generated a de novo reference transcriptome to carry out a differential gene expression analysis between the wild-type and mutant NdAP3-3 genotypes differing by the presence vs. absence of petals at early stages of floral development. Among the 1,620 genes that were significantly differentially expressed between the two genotypes, functional annotation suggested a large involvement of nuclear activities, including regulation of transcription, and enrichment in processes linked to cell proliferation. Comparing with Arabidopsis data, we found that highly conserved genes between the two species are enriched in homologs of direct targets of the AtAP3 protein. Integrating AP3-3 binding site data from another Ranunculaceae species, Aquilegia coerulea, allowed us to identify a set of 18 putative target genes that were conserved between the three species. Our results suggest that, despite the independent evolutionary origin of petals in core eudicots and Ranunculaceae, a small conserved set of genes determines petal identity and early development in these taxa.

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A MITE insertion abolishes the AP3-3 self-maintenance regulatory loop in apetalous flowers of Nigella damascena

Natalia Conde e Silva, Martine Leguilloux, Arnaud Bellec, Nathalie Rodde, Juliette Aubert, Domenica Manicacci, Catherine Damerval, Helene Berges, Yves Deveaux

Summary: A self-regulatory loop similar to that regulating euAP3 in core eudicots controls AP3-3 gene expression in an early diverging eudicot, but distinct mechanisms regulate tissue specificities in Arabidopsis and Nigella. MADS-box transcription factors play important roles in floral organ identity by binding to specific motifs in the promoter of their target genes. In Nigella, the lack of expression of NdAP3-3 gene in the apetalous morph is due to a Miniature Inverted-repeat Transposable Element (MITE) insertion that affects mRNA splicing. Specific CArG features in the promoter of NdAP3-3 gene determine its petal-specific expression in Nigella.

JOURNAL OF EXPERIMENTAL BOTANY (2023)