Differential transcriptome analysis reveals insight into monosymmetric corolla development of the crucifer Iberis amara

Abstract

BackgroundIn the co-evolution between insects and plants, the establishment of floral monosymmetry was an important step in angiosperm development as it facilitated the interaction with insect pollinators and, by that, likely enhanced angiosperm diversification. In Antirrhinum majus, the TCP transcription factor CYCLOIDEA is the molecular key regulator driving the formation of floral monosymmetry. Although most Brassicaceae form a polysymmetric corolla, six genera develop monosymmetric flowers with two petal pairs of unequal size. In the monosymmetric crucifer Iberis amara, formation of the different petal pairs coincides with a stronger expression of the CYC-homolog IaTCP1 in the small, adaxial petals.ResultsIn this study, RNA-Seq was employed to reconstruct the petal transcriptome of the non-model species Iberis amara. About 9 Gb of sequence data was generated, processed and re-assembled into 18,139 likely Iberis unigenes, from which 15,983 showed high sequence homology to Arabidopsis proteins. The transcriptome gives detailed insight into the molecular mechanisms governing late petal development. In addition, it was used as a scaffold to detect genes differentially expressed between the small, adaxial and the large, abaxial petals in order to understand the molecular mechanisms driving unequal petal growth. Far more genes are expressed in adaxial compared to abaxial petals implying that IaTCP1 activates more genes than it represses. Amongst all genes upregulated in adaxial petals, a significantly enhanced proportion is associated with cell wall modification and cell-cell signalling processes. Furthermore, microarrays were used to detect and compare quantitative differences in TCP target genes in transgenic Arabidopsis plants ectopically expressing different TCP transcription factors.ConclusionsThe increased occurrences of genes implicated in cell wall modification and signalling implies that unequal petal growth is achieved through an earlier stop of the cell proliferation phase in the small, adaxial petals, followed by the onset of cell expansion. This process, which forms the monosymmetric corolla of Iberis amara, is likely driven by the enhanced activity of IaTCP1 in adaxial petals.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-014-0285-4) contains supplementary material, which is available to authorized users.

An Independent Evolutionary Origin for Insect Deterrent Cucurbitacins inIberis amara

“…Iberis amara in Brassicaceae has previously been used as a model species to understand the evolution of monosymmetric petals ( Busch et al 2014 ), in this paper, we report how I. amara evolved to produce cucurbitacins, a new chemical defense in the Brassicaceae for insect herbivores like Pieris rapae and Phyllotreta nemorum , which otherwise feed on many brassicaceous species ( Nielsen et al 1977 ; Sachdev-Gupta et al 1993 ). We elucidated the first three committed steps of the cucurbitacin biosynthesis in I. amara , and showed that the cucurbitacin pathway in this species has evolved independently to the corresponding pathway in cucurbitaceous species.…”

How to build a fruit: Transcriptomics of a novel fruit type in the Brassiceae

“…Overall, GO terms within fruits and between species are similar (Fig 3 and S1 Fig), as expected, because all sections and replicates are from developing fruit with shared components (e.g., ovary wall, septum). Additionally, GO analyses of top terms do not usually vary between closely related species [64,65]. However, despite similarities in gene ontology, the origin of heteroarthrocarpy may still be explained by deviation in expression patterns of one or more of the valve margin pathway genes [18,22–26].…”

How to Build a Fruit: Transcriptomics of a Novel Fruit Type in the Brassiceae

“…Because dehiscence is susceptible to misexpression and loss of function mutations in the valve margin pathway (21,24–28), broad changes in gene ontology are unnecessary to explain heteroarthrocarpy. Additionally, GO analyses of top terms do not usually vary between closely related species (65,66). However, similarities in gene ontology do not imply similarity between all expressed transcripts, so variation of just a few transcripts may still be the driving factor behind heteroarthrocarpy.…”