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.2012 Apr 22;279(1733):1640-5.
doi: 10.1098/rspb.2011.1873. Epub 2011 Nov 16.

Evolution of spur-length diversity in Aquilegia petals is achieved solely through cell-shape anisotropy

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Evolution of spur-length diversity in Aquilegia petals is achieved solely through cell-shape anisotropy

Joshua R Puzey et al. Proc Biol Sci..

Abstract

The role of petal spurs and specialized pollinator interactions has been studied since Darwin. Aquilegia petal spurs exhibit striking size and shape diversity, correlated with specialized pollinators ranging from bees to hawkmoths in a textbook example of adaptive radiation. Despite the evolutionary significance of spur length, remarkably little is known about Aquilegia spur morphogenesis and its evolution. Using experimental measurements, both at tissue and cellular levels, combined with numerical modelling, we have investigated the relative roles of cell divisions and cell shape in determining the morphology of the Aquilegia petal spur. Contrary to decades-old hypotheses implicating a discrete meristematic zone as the driver of spur growth, we find that Aquilegia petal spurs develop via anisotropic cell expansion. Furthermore, changes in cell anisotropy account for 99 per cent of the spur-length variation in the genus, suggesting that the true evolutionary innovation underlying the rapid radiation of Aquilegia was the mechanism of tuning cell shape.

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Figures

Figure 1.
Figure 1.
Aquilegia flowers exhibit considerable spur-length diversity. (a)A. vulgaris, (b)A. canadensis, (c)A. coerulea and (d)A. longissima. Scale bars, 1 cm.
Figure 2.
Figure 2.
Cell divisions cease very early in spur development. (a–d)In situ localization ofAqHIS4 in developingA. vulgaris flowers was used to determine the pattern and extent of cell divisions in early petal development.AqHIS4 expression, visualized by purple staining, marks cell divisions. Arrowheads, petals; arrow, initiating spur. (a) Two youngA. vulgaris flower buds (in brackets) showing ubiquitousAqHIS4 expression indicating diffuse cell divisions. (b) Older flower showing ubiquitous cell divisions in the petal while cell divisions have ceased in the stamens (St). (c)A. vulgaris petal with initiating spur. Cell divisions are most concentrated at the initiating spur and have ceased in the tip of the developing petal, as indicated by a dotted line. (d)A. vulgaris spur of lengthL ≈ 5 mm with noAqHIS4 expression evident, indicating that all cell divisions have ceased. (e) The number of cells in a single cell file extending the entire length of developingA. canadensis (green inverted triangles),A. coerulea (pink circles) andA. longissima (yellow diamonds) spurs, counted from the attachment point to the nectary. The number of cells plateaus to a constant value early in development when the spur is approximately 5–9 mm long. Error bars indicate counting errors. Scale bars, (a,b) 0.5 mm and (c,d) 1 mm.
Figure 3.
Figure 3.
Cell anisotropy drivesA. coerulea petal spur development. (a) Developmental series ofA. coerulea petals. Both cellular measurements and spur radiusr are recorded at the positions as measured from the nectary tip along the length of the spur. To compare between developmental stages, the position along the spur is also measured byz, which increases from 0 at the nectary to 1 at the attachment point. (b) Light microscope images are analysed to determine cell anisotropyε =l/w and cell areaA =lw at the positionz along the spur. (c) Waterfall plot ofε versusz at different developmental stages measured by the spur lengthL. (d) The maximum cell anisotropyεmax is highly correlated with spur lengthL. (e) Using measurements of cell anisotropy and cell area, in concert with an initial spur determined by averaging experimental spur profiles, numerically calculated spur shapes are generated without any free parameters at the same developmental stages shown in panel (a). Numerical spurs are shaded according to local cell anisotropy. (f) Numerically calculated spur profiles (circles) are overlaid on experimentally measured spur profiles (solid curves). Scale bars, 1 cm.
Figure 4.
Figure 4.
Cytoskeleton perturbations decouple isotropic cell expansion from cell anisotropy. (a) Oryzalin (Oz), a microtubule depolymerization agent, was applied to the entire surface of singleAquilegia spurs after they had achieved a short tubular shape of lengthL ≈ 1 cm (ii). Untreated petal from the same flower is shown as a control (i). Photos of petals were taken approximately 6 days after initial application of oryzalin. (b)(i) Anisotropically shaped cells from untreated spur. (ii) Image of oryzalin-treated spur showing isotropically shaped cells. (c) Comparison of cell areaA and anisotropyε between cells from oryzalin-treated spurs (n = 270) and from untreated samples (n = 127). Scale bar, 1 cm.
Figure 5.
Figure 5.
Cell anisotropy plays an essential role in spur-length diversity. (a) Petals from four differentAquilegia species. From left to right:A. vulgaris,A. canadensis,A. coerulea andA. longissima. Insets for each species show a cellular region of identical width of approximately 30 µm. (b) The ratio of final to initial spur lengthLf/Li versus the fractional increase in cell areaAf/Ai is plotted to show that changes in spur length are not correlated with changes in cell area (R2 = 0.233, Pearson'sr = −0.482). (c)Lf/Li is plotted versus the fractional increase in cell anisotropyεf/εi, measured atz ≈ 1/3, indicating that spur-length diversity is characterized by cell anisotropy (R2 = 0.990, Pearson'sr = 0.995). (d) Total petal lengthLp is plotted versus time, demonstrating that all species follow the same growth curve but differ in developmental duration. Vertical error bars indicate range in initial spur lengthLi and horizontal error bars in (b,c) are comparable with marker size. Scale bar, 1 cm.
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References

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