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

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.

Molecular basis for three-dimensional elaboration of theAquilegiapetal spur

“…Previous work [9] defined a model of spur development in which a wave of cell division cessation progresses simultaneously from the entire margin of the organ and moves towards the nascent nectary, promoting a localized bulge that constitutes the first stage of spur development ( figure 1a). The transition from cell division to expansion that marks Phase I begins when the petal is approximately 1 mm in length, as measured from the petal attachment point to the nascent spur tip, which corresponds to what we have defined as early stage 10 (staging given in electronic supplementary material, table S2; figure 1c).…”

“…The Aquilegia homologue of HISTONE4 (HIS4) has been previously characterized [9]. For KNOX genes, nine annotated loci were identified.…”

Breaking the mold: understanding the evolution and development of lateral organs in diverse plant models

“…In contrast, work in Aquilegia has demonstrated that homologs of the KNOX genes are not expressed during spur development [59 ]. Instead, cell-level studies of Aquilegia petal spur development reveal that modification of both cell division and expansion patterns are critical to spur development and diversification [60]. Unlike what has been observed in flat leaves or petals, the cell division arrest front is highly modified such that divisions persist only in the area surrounding the nascent nectary, creating a prepatterned spur cup (Figure 2d).…”

How Have Advances in Comparative Floral Development Influenced Our Understanding of Floral Evolution?

“…For example, spur reductions in orchids of subtribe Orchidinae have been interpreted as cases of pedomorphosis caused by an earlier offset of growth (Box et al 2008). Interestingly, the dramatic variation in spur length across species of Aquilegia is almost exclusively the result of heterochronic changes in the duration of anisotropic cell elongation (Puzey et al 2011).…”