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Asymmetric bending of lateral petals, a novel trait originated within Delphinium (Ranunculaceae), reinforces their mirrored helical rotation during flower opening

ABSTRACT: During the process of flower opening, most petals move downward in the direction of pedicel (i.e., epinastic movement). In most Delphinium flowers, however, their two lateral petals display a very peculiar movement, the mirrored helical rotation. Such a distinctive petal movement requires the twist of the stalk. However, in some lineages, their lateral petals also exhibit asymmetric bending that increases the degree of mirrored helical rotation, facilitating the formation of a 3D final shape. Notably, the petal asymmetric bending is a novel trait that has not been noticed yet so that its morphological nature, developmental process and molecular mechanisms remain largely unknown. Here, by using D. anthriscifolium as a model, we determined that the petal asymmetric bending was caused by localized expansion of cell width, accompanied with specialized arrangement of surface ornamentation, on the adaxial epidermis. Digital gene analyses, gene expression and functional studies revealed that a class I homeodomain-leucine zipper family transcription factor gene, DeanLATE MERISTEM IDENTITY1 (DeanLMI1), contributes to the petal asymmetric bending; knockdown of it led to the formation of explanate 2D petals. Specifically, DeanLMI1 promotes cell expansion in width and influences the arrangement of surface ornamentation, through regulating the auxin distribution, on the localized adaxial epidermis. These results not only provide a comprehensive portrait of petal asymmetric bending for the first time, but also shed some new insight into the mechanisms of flower opening and helical movement in plants.

ORGANISM(S): Delphinium anthriscifolium

PROVIDER: GSE249849 | GEO | 2023/12/11

REPOSITORIES: GEO

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Project description:TCP transcription factors from the CYC2-class are involved in the development of monosymmetric flowers in all core eudicot species analysed so far. In Antirrhinum majus, the CYC2/TCP transcription factor CYCLOIDEA (CYC) is the molecular key regulator driving the development of flower monosymmetry (Luo D, Carpenter R, Vincent C, Copsey L, Coen E: Origin of floral asymmetry in Antirrhinum. Nature 1996, 383:794-799). In the Brassicaceae Iberis amara, a stronger expression of the CYC2 gene IaTCP1 in the small adaxial petals likely leads to the reduced petal size in comparison to large abaxial petals, with hardly any IaTCP1 expression. This results in the formation of the monosymmetric Iberis flower (Busch A, Zachgo S: Control of corolla monosymmetry in the Brassicaceae Iberis amara. PNAS 2007, 104:16714-16719). In contrast, the orthologous TCP/CYC2 transcription factor TCP1 from Arabidopsis thaliana, which forms equally sized and shaped petal pairs, only shows an early and transient expression in the adaxial area of floral primordia. This implies that monosymmetry in the Brassicaceae evolved through a heterochronic expression shift of the TCP/CYC2 key regulator gene IaTCP1. Transgenic Arabidopsis plants overexpressing IaTCP1 and TCP1 develop smaller petals whereas transgenic plants overexpressing CYC from Antirrhinum majus produce larger flowers. In any case, petal size is affected. To compare the effects of the three CYC2 TCP transcription factors on downstream (regulatory) networks in Arabidopsis thaliana, a microarray analysis was conducted. The coding sequences of the TCP/CYC2 transcription factors IaTCP1, TCP1 and CYC were cloned into the pBAR vector (GenBank: AJ251014), resulting in the constructs #0522 (IaTCP1), #0569 (TCP1) and #0577 (CYC). In pBAR, all genes are under the control of the CaMV35S-promoter. Arabidopsis plants were transformed (via floral dip) with respective constructs and also with the empty vector (pBar). Transgenic plants (T1) with petal size deviation from the control (plants transformed with the empty vector and wild type) were selfed and resulting T2 lines with petal size deviations from control were selected. Inflorescence buds from secondary inflorescences were harvested from transgenic T2 plants that formed smaller (#0255 or #0569) or larger (#0577) petals in the main inflorescence. Total RNA was isolated and sent to the Integrated Functional Genomics Service at the University of MÃ¼nster, Germany, which carried out probe preparation, hybridization and statistical analysis of the data. Differential gene expression was always determined from a comparison of gene expression from #0522, #0569 and #0577, respectively, against the control (#pBar; inflorescence gene expression in plants transformed with an empty vector).

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Asymmetric bending of lateral petals, a novel trait originated within Delphinium (Ranunculaceae), reinforces their mirrored helical rotation during flower opening

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