Uncorrelated evolution of leaf and petal venation patterns across the angiosperm phylogeny

Abstract

Early angiosperm evolution, beginning approximately 140 million years ago, saw many innovations that enabled flowering plants to alter ecosystems globally. These included the development of novel, flower-based pollinator attraction mechanisms and the development of increased water transport capacity in stems and leaves. Vein length per area (VLA) of leaves increased nearly threefold in the first 30-40 million years of angiosperm evolution, increasing the capacity for transpiration and photosynthesis. In contrast to leaves, high water transport capacities in flowers may not be an advantage because flowers do not typically contribute to plant carbon gain. Although flowers of extant basal angiosperms are hydrated by the xylem, flowers of more recently derived lineages may be hydrated predominantly by the phloem. In the present study, we measured leaf and flower VLA for a phylogenetically diverse sample of 132 species from 52 angiosperm families to ask (i) whether flowers have lower VLA than leaves, (ii) whether flowers of basal angiosperm lineages have higher VLA than more recently derived lineages because of differences between xylem and phloem hydration, and (iii) whether flower and leaf VLA evolved independently. It was found that floral structures had lower VLA than leaves, but basal angiosperm flowers did not have higher VLA than more derived lineages. Furthermore, the independent evolution of leaf and petal VLA suggested that these organs may be developmentally modular. Unlike leaves, which have experienced strong selection for increased water transport capacity, flowers may have been shielded from such selective pressures by different developmental processes controlling VLA throughout the plant bauplan.

Hydraulic conductance and the maintenance of water balance in flowers

“…Other traits similarly varied approximately two orders of magnitude (Figs & ). VLA exhibited a similar range to that seen by Roddy et al (), ranging from 0.21 mm mm −2 for Agapanthus africanus to 12.02 for Calycanthus occidentalis . Within clades, VLA ranged for the basal angiosperms (magnoliids and Illicium ) from 2.96 mm mm −2 for Liriodendron tulipifera to 12.02 mm mm −2 for Calycanthus occidentalis , for the monocots from 0.21 mm mm −2 for Agapanthus africanus to 1.65 mm mm −2 for Iris douglasiana , and for the eudicots from 1.12 mm mm −2 for Rhododendron sp.…”

Floral Mass per Area and Water Maintenance Traits Are Correlated with Floral Longevity in Paphiopedilum (Orchidaceae)

“…For Arabidopsis thaliana , quantitative trait loci mapping of leaf- and flower-size traits has not revealed any correlations between those trait categories (Juenger et al, 2005). Furthermore, Roddy et al (2013) found no proof of correlated evolution for leaf and petal venation patterns across the angiosperm phylogeny. Those earlier results, as well as our data, suggest that the physiological traits of leaves and flowers may arise from non-correlated selection pressures and functions.…”

“…In fact, the “leaf economic spectrum” occurs across all major terrestrial plant groups, where a higher (LMA) is invested in longer-lived leaves (Wright et al, 2004; Sack et al, 2013; John et al, 2017). The role of water transport traits in flower evolution is complex, with phylogeny an important determinant of flower hydraulic characteristics (e.g., vein density) that has evolved independently of leaves (Roddy et al, 2013). In addition, the benefits associated with longevity are also very different in flowers when compared to leaves.…”

Water relations of Calycanthus flowers: Hydraulic conductance, capacitance, and embolism resistance

“…In previous studies of K flower and other hydraulic traits (Roddy et al, ; Roddy, Brodersen, & Dawson, ), flowers of the genus Calycanthus (Calycanthaceae; Zhou, Renner, & Wen, ) consistently had traits associated with high rates of water supply via the xylem (i.e., high vein length per area), high water loss (minimum epidermal conductance; g min ), and high hydraulic conductance ( K flower ). These extreme trait values, particularly for Calycanthus occidentalis , suggest that these flowers can transport substantial amounts of water, possibly even outpacing leaf transpiration.…”