Abstract
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.
Highlights
Petals are floral organs that play a major role in pollinator attraction
B-function relies on two proteins APETALA3/DEFICIENS (AP3) and PISTILLATA/GLOBOSA (PI) in Arabidopsis/Antirrhinum, respectively, which function as an obligate heterodimer within tetrameric complexes (Goto and Meyerowitz, 1994)
In two Ranunculaceae species where functional studies can be conducted using Virus-Induced Gene Silencing (VIGS), namely, Aquilegia coerulea and Nigella damascena, it has been shown that expression of AP3-3 genes is required for petal identity (Sharma et al, 2011; Gonçalves et al, 2013; Wang et al, 2016)
Summary
Petals are floral organs that play a major role in pollinator attraction. In flowers with a differentiated perianth, petals are defined as the second whorl of sterile organs surrounding the androecium; the first whorl of sterile organs is composed of sepals, which protect the fertile organs during development. In two Ranunculaceae species where functional studies can be conducted using Virus-Induced Gene Silencing (VIGS), namely, Aquilegia coerulea and Nigella damascena, it has been shown that expression of AP3-3 genes is required for petal identity (Sharma et al, 2011; Gonçalves et al, 2013; Wang et al, 2016) These lines of evidence indicate that AP3-3 orthologs play a crucial role in determining petal identity in Ranunculaceae. Because of the large size of the N. damascena genome (~10 Gb), no genomic data are available for this species yet To circumvent this limiting factor, we assembled and annotated a floral reference transcriptome and characterized differential gene expression between wild-type and mutant genotypes at the NdAP3-3 locus differing by the presence vs absence of petals. Genes were annotated and compared to known or suspected targets of B-function genes in other eudicot species (Bey et al, 2004; Wuest et al, 2012; Jiang et al, 2020), and the conservation of the petal gene network is discussed
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