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. 2019 Apr 19:10:9.
doi: 10.1186/s13227-019-0122-9. eCollection 2019.

Evidence of a largely staminal origin for the Jaltomata calliantha (Solanaceae) floral corona

Affiliations

Evidence of a largely staminal origin for the Jaltomata calliantha (Solanaceae) floral corona

Jamie L Kostyun et al. Evodevo. .

Abstract

Background: Understanding the evolution of novel features requires homology assessments at different levels of biological organization. In flowering plants, floral coronas that play various roles in plant-pollinator interactions have evolved multiple times independently, but are highly variable in their final position and overall morphology. Coronas of the Solanaceae species Jaltomata calliantha are found between the corolla and stamens, adjacent to the gynoecium, and form cups that house copious amounts of their characteristic blood red nectar. To test the hypothesis that J. calliantha coronas evolved as an outgrowth of stamens and therefore have staminal identity, we assessed their development, floral organ identity gene expression, and cellular morphology.

Results: Jaltomata calliantha coronas emerge after the initiation of all conventional floral organs on the abaxial side of the proximally modified stamens and then expand medially and laterally to form nectar cups. Overlapping expression of the B-class organ identity genes JcAPETALA3 and both JcPISTILLATA/GLOBOSA orthologs (JcGLO1 and JcGLO2), and the C-class-like gene JcAGAMOUS1-like, unites the stamens and corona. Epidermal cell shape also connects the adaxial surface of coronas and petals, and the stamen base, with remaining floral organs showing divergent cell types.

Conclusions: Our data, based on multiple lines of evidence, support a largely staminal origin for J. calliantha coronas. However, since slightly enlarged stamen bases are found in Jaltomata species that lack coronas, and J. calliantha stamen bases share cell types with petals, we hypothesize that stamen bases recruited part of the petal identity program prior to fully expanding into a corona.

Keywords: ABCDE genes; Corona; Jaltomata; Nectar; Novel floral organs.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Emergence of the J. calliantha corona in late flower development. ac Scanning electron micrographs of mid-stage flower buds, prior to a coronal outgrowth at the base of stamens. d Young stamen base with filament detached showing outgrowth of the corona. e Side view of d indicating outgrowth of the corona on the abaxial side of the stamen around the base of the gynoecium. f Scanning electron micrograph of a fully expanded and mature stamen base covered with trichomes. g Dehydrated mature flower with stamen filaments and most of the perianth removed to reveal the corona lobes and swollen stamen bases. h Close-up of the two-lobed corona between two stamen bases from g. i Close-up of the inner organs of open flowers showing five stamens emerging from green swollen bases that contact the gynoecium base on their adaxial side. Petals have been trimmed back to reveal five corona cups between the swollen stamen bases, on top of the petal bases, and adjacent to the gynoecium. Secretion of light-colored nectar into the corona cups begins shortly after flower anthesis. jl Nectar becomes darker red as the flower ages, and pools in the slightly heart-shaped corona cups. sep sepal, pet petal, st stamen, stb stamen base, fil stamen filament, cor corona, gyn gynoecium. Scale bars = 100 µm for (af) and 1 mm for (gl)
Fig. 2
Fig. 2
Cell morphologies of J. calliantha floral organs. a Jigsaw-shaped cells on the abaxial (lower) surface of the sepal. b Jigsaw-shaped cells on the adaxial (upper) sepal surface. c Slightly raised rounded cells of the adaxial petals. d Jigsaw-shaped cell of the abaxial petals. e Elongated cells of anthers. f Flattened and highly elongated cells of the stamen filaments. g Slightly raised rounded cells of the stamen base. h Slightly raised rounded cells of the corona. i Toothed elongated cells of the style. j Highly rounded cells of the ovary surface. k, l Sections through a mid-stage toluidine blue-stained flower bud showing mature conventional floral organs, prior to corona growth. m Initiation of corona development as a ring of tissue connecting the stamen bases. n, o Late-stage corona and petal development revealing similar inner layers of dark blue-stained rapidly dividing cells. p Section from the same flower as k, l toward the center of the flower showing the swollen stamen base stamen thecae. q Cartoon of a wax-embedded J. calliantha flower illustrating the angle of sectioning in np. Note that the fused corolla (light green) is artificially pushed upward to enclose the inner corona (red), stamens (purple), and gynoecium (yellow). pet petals, st stamens, gyn gynoecium, rec receptacle, cor corona, stb swollen stamen base. Scale bars = 100 µm for (aj) and 1 mm for (kp)
Fig. 3
Fig. 3
Bayesian majority-rule tree of angiosperm (A. thaliana, Solanaceae, and Aquilegia sp.) MIKC MADS-box genes from the ABCDE clades. J. calliantha genes are highlighted in bold. Posterior probability support values are shown above each branch if > 0.90
Fig. 4
Fig. 4
Quantitative RT-PCR of differentially expressed ABC genes across J. calliantha floral organs and development. a JcAPETALA3 (JcAP3) is expressed as predicted in petals and stamens, and in late emerging coronas. b JcPISTILLATA/JcGLOBOSA2 (JcPI/JcGLO2) is expressed as predicted in petals and stamens, and in late emerging coronas. c JcAGAMOUS (JcAG) is unexpectedly expressed in leaves, sepals, and petals, and in late emerging coronas. d JcAGAMOUS-LIKE 1 (JcAGL1) is expressed as predicted in stamens and carpels, and in late emerging coronas. e JcAPETALA1 (JcAP1) is expressed broadly in floral organs, but is not detected in stamens. f Overlapping expression domains in each floral organ. Black, strong relative expression; gray, weak relative expression. Bars in graphs denote averages of three biological replicates with standard errors. Colors mark expression in the same floral organs between the graphs and floral diagrams. Leaves, black; sepals, green; petals, blue; stamens, yellow; coronas, red; and carpels, orange

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