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

Yi-Dong An; Adam B Roddy; Tian-Hao Zhang; Guo-Feng Jiang

doi:10.3389/fpls.2023.1130724

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

Front Plant Sci. 2023 May 31:14:1130724. doi: 10.3389/fpls.2023.1130724. eCollection 2023.

Authors

Yi-Dong An¹, Adam B Roddy², Tian-Hao Zhang¹, Guo-Feng Jiang¹

Affiliations

¹ Guangxi Key Laboratory of Forest Ecology and Conservation, Guangxi Colleges and Universities Key Laboratory for Cultivation and Utilization of Subtropical Forest Plantation, and State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Forestry, Guangxi University, Nanning, Guangxi, China.
² Institute of Environment, Department of Biological Sciences, Florida International University, Miami, FL, United States.

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 (g _min) and pressure-volume (PV) curves parameters). We predicted that flowers would exhibit higher g _min 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 g _min, which was associated with higher hydraulic capacitance (C _T); 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 g _min 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.

Keywords: drought tolerance; flower; hydraulics; leaf; minimum cuticular conductance; photosynthesis; water relations; xylem.

Grants and funding

This work was supported by grants from the Natural Science Foundation of Guangxi Province (Key Program 2022GXNSFDA035059), the National Natural Science Foundation of China (grant number 31860195), and Bama county program for talents in science and technology, Guangxi, China (20210020, 20220011) to G-FJ. ABR was supported by grant CMMI-2029756 from the US National Science Foundation.