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.