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Temporal-Spatial Transcriptome Analyses Provide Insights into the Development of Petaloid Androecium in Canna indica.

ABSTRACT: Canna indica (Zingiberales) is one of the most important ornamental species characterized with beautiful petaloid staminodes, which are considered to evolve from stamens. However, the genetic basis for the development of petaloid staminodes remains unclear largely because the genomic sequences are not available. By using RNA-Seq, we sequenced the transcripts in the flower of C. indica, and quantified the temporal gene expressions in flower primordium and differentiated flower, as well as the spatial gene expressions in petal and petaloid staminode. In total, 118,869 unigenes were assembled, among which 67,299 unigenes were annotated. Quantification analysis identified the differentially expressed genes in the temporal and spatial two comparisons, based on which, Gene Ontology enrichment analysis highlighted the representative terms in each sample, such as specification of organ number in flower primordium, growth in differentiated flower, secondary cell wall biogenesis in petal and cell division in petaloid staminode. Among the 51 analyzed MADS-box unigenes, 37 were up-regulated in differentiated flower compared with those in flower primordium. A-class unigenes were expressed higher in petal than in petaloid staminode, and C-class unigenes were expressed oppositely, whereas B-class unigenes demonstrated close expression levels in these two organs, indicating that petaloid staminode retains stamen identity to some degree. In situ hybridization provided more detailed expression patterns of these unigenes, and revealed the extended expression of B-class to the carpel at later stages when the style turned flat. These results constitute a preliminary basis for the study of flower development in C. indica and can be applied in further study of the evolution of Zingiberales.

SUBMITTER: Tian X

PROVIDER: S-EPMC4987385 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Temporal-Spatial Transcriptome Analyses Provide Insights into the Development of Petaloid Androecium in Canna indica.

Tian Xueyi X Yu Qianxia Q Liu Huanfang H Liao Jingping J

Frontiers in plant science 20160817

Canna indica (Zingiberales) is one of the most important ornamental species characterized with beautiful petaloid staminodes, which are considered to evolve from stamens. However, the genetic basis for the development of petaloid staminodes remains unclear largely because the genomic sequences are not available. By using RNA-Seq, we sequenced the transcripts in the flower of C. indica, and quantified the temporal gene expressions in flower primordium and differentiated flower, as well as the spa ...[more]

PMID: 27582744

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Project description:Flowers of the order Zingiberales demonstrate a remarkable trend of reduction in the number of fertile stamens; from five or six fertile, filamentous stamens bearing two thecae each in Musaceae and Strelitziaceae to just a single petaloid stamen bearing a single theca in Cannaceae and Marantaceae. As one progresses from ancestral to derived floral forms, 5-6 fertile stamens are replaced by 4-5 petaloid staminodes. In Cannaceae and Costaceae, all members of the androecial whorls exhibit petaloidy, including the fertile stamen. In Costaceae, a single fertile stamen develops two thecae embedded on a broad petaloid appendage, while in Cannaceae the single fertile stamen is further reduced to a single theca with a prominent, expanded petaloid appendage. Whether petaloidy of the fertile stamen is a synapomorphy of the entire ginger clade (including Cannaceae, Costaceae, Zingiberaceae and Marantaceae), or the result of independent convergent evolution in Cannaceae, Costaceae, and some Zingiberaceae, is unclear. We combine a developmental series of the formation of the petaloid fertile stamen in Canna indica with data on the expression of B- and C-class floral organ identity genes to elucidate the organogenetic identity of the petaloid stamen and staminodes. Our data indicate that the single fertile theca in C. indica and its petaloid appendage are derived from one-half of the primordium of a single stamen, with no contribution from the remaining part of the stamen (i.e. the second theca primordium) which aborts early in development. The petaloid appendage expands later, and develops from the position of the filament/connective of the developing theca. Floral identity gene expression shows that petal identity genes (i.e. B-class genes) are expressed in all floral organs studied while C-class gene AG-1 is expressed in an increasing gradient from sepals to gynoecium, and AG-2 is expressed in all floral organs except the petals. The canonical model for molecular specification of floral organ identity is not sufficient to explain petaloidy in the androecial whorl in Canna sp. Further studies understanding the regulation of gene networks are required.

Dataset Information

Temporal-Spatial Transcriptome Analyses Provide Insights into the Development of Petaloid Androecium in Canna indica.

Publications

Temporal-Spatial Transcriptome Analyses Provide Insights into the Development of Petaloid Androecium in Canna indica.

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