Hydraulic differences between flowers and leaves are driven primarily by pressure-volume traits and water loss

Abstract

Flowers are critical for successful reproduction and have been a major axis of diversification among angiosperms. As the frequency and severity of droughts are increasing globally, maintaining water balance of flowers is crucial for food security and other ecosystem services that rely on flowering. Yet remarkably little is known about the hydraulic strategies of flowers. We characterized hydraulic strategies of leaves and flowers of ten species by combining anatomical observations using light and scanning electron microscopy with measurements of hydraulic physiology (minimum diffusive conductance (gmin) and pressure-volume (PV) curves parameters). We predicted that flowers would exhibit higher gmin and higher hydraulic capacitance than leaves, which would be associated with differences in intervessel pit traits because of their different hydraulic strategies. We found that, compared to leaves, flowers exhibited: 1) higher gmin, which was associated with higher hydraulic capacitance (CT); 2) lower variation in intervessel pit traits and differences in pit membrane area and pit aperture shape; and 3) independent coordination between intervessel pit traits and other anatomical and physiological traits; 4) independent evolution of most traits in flowers and leaves, resulting in 5) large differences in the regions of multivariate trait space occupied by flowers and leaves. Furthermore, across organs intervessel pit trait variation was orthogonal to variation in other anatomical and physiological traits, suggesting that pit traits represent an independent axis of variation that have as yet been unquantified in flowers. These results suggest that flowers, employ a drought-avoidant strategy of maintaining high capacitance that compensates for their higher gmin to prevent excessive declines in water potentials. This drought-avoidant strategy may have relaxed selection on intervessel pit traits and allowed them to vary independently from other anatomical and physiological traits. Furthermore, the independent evolution of floral and foliar anatomical and physiological traits highlights their modular development despite being borne from the same apical meristem.

Evidence of combined flower thermal and drought vulnerabilities portends reproductive failure under hotter‐drought conditions

“…After rehydration, the water potential of flowers ( Ψ flower ) and leaves ( Ψ leaf ) and their respective mass were repeatedly measured as they dehydrated on the bench. Before each water potential measurement, samples were enclosed in humidified plastic bags for about 30 min to allow equilibration (An et al, 2023; Rodriguez‐Dominguez et al, 2018). After the measurements, flowers and leaves of each species were oven‐dried at 70°C for 48 h to obtain their dry mass.…”

“…As an advantage, the build of this hydrostatic skeleton would probably require a lower carbon investment [e.g., lower values of tissue mass area (TMA) and tissue dry matter content (TDMC)] in an organ that, when compared to leaves, usually has a much shorter lifespan (Roddy et al, 2021). However, although the comparative analysis of the differential carbon and water allocation between organs may provide important insights into key aspects of flower physiology, few studies to date have focused on such comparative analysis (An et al, 2023; Bourbia et al, 2020; Liu et al, 2017; Roddy et al, 2013; Roddy et al, 2019; Roddy, 2023).…”

Monocots and eudicots have more conservative flower water use strategies than basal angiosperms

“…Several studies have shown that extant basal angiosperm lineages require large amounts of water to maintain flower functioning (Feild et al 2009a,b;Roddy et al 2016Roddy et al , 2018. In contrast, in monocots and eudicots, flowers probably rely on stored water to maintain turgidity and delay desiccation (Feild et al 2009b;Roddy et al 2016Roddy et al , 2019Roddy et al , 2023An et al 2023). There is limited information on the diversity of floral hydraulic structure and function in basal angiosperms and their derived clades, specifically in relation to anatomy of the pedicel xylem.…”

Flowers are leakier than leaves but cheaper to build

“…However, under drought conditions, leaf stomata close to limit water loss, causing any remaining water vapor flux to be due to the minimum epidermal surface conductance (g min ), which is due to the conductance of the cuticle and any incompletely closed stomata (Kerstiens, 1996;Duursma et al, 2019;Márquez et al, 2022). After drought-induced stomatal closure in leaves, water loss from flowers can be as high as or even exceed water loss from leaves (Sinha et al, 2022;An et al, 2023), suggesting that corolla g min may hinder the ability of plants to maintain floral display during periods of water stress (Lambrecht, 2013;Buschhaus et al, 2015;Bourbia et al, 2020). Yet, despite the influence of g min on flower and whole-plant hydration and its role in regulating flower temperature, g min has been measured on flowers of only a few species (Patiño & Grace, 2002;Roddy et al, 2016;Roddy, 2019;Bourbia et al, 2020).…”

“…Here, we compared flowers and leaves in a set of physiological traits that influence water balance, particularly during drought (Brodribb et al, 2007;Boyce et al, 2009;Simonin et al, 2013;Roddy et al, 2016Roddy et al, , 2018Duursma et al, 2019;Bourbia et al, 2020;An et al, 2023). We measured g min , water content per unit projected surface area (W area ) and dry mass (W mass ), vein density (D v ), and dry mass per area (leaf mass per area, LMA, or petal mass per area, PMA) of flowers and leaves for over 100 species from 41 angiosperm families growing in a common garden to determine how these physiological traits differ among organs and influence the costs of floral construction and maintenance.…”