The Potential Roles of Unique Leaf Structure for the Adaptation of Rheum tanguticum Maxim. ex Balf. in Qinghai-Tibetan Plateau

Abstract

Leaves are essential plant organs with numerous variations in shape and size. The leaf size is generally smaller in plants that thrive in areas of higher elevation and lower annual mean temperature. The Qinghai-Tibetan Plateau is situated at an altitude of >4000 m with relatively low annual average temperatures. Most plant species found on the Qinghai-Tibetan Plateau have small leaves, with Rheum tanguticum Maxim. ex Balf. being an exception. Here, we show that the large leaves of R. tanguticum with a unique three-dimensional (3D) shape are potentially an ideal solution for thermoregulation with little energy consumption. With the increase in age, the shape of R. tanguticum leaves changed from a small oval plane to a large palmatipartite 3D shape. Therefore, R. tanguticum is a highly heteroblastic species. The leaf shape change during the transition from the juvenile to the adult phase of the development in R. tanguticum is a striking example of the manifestation of plant phenotypic plasticity. The temperature variation in different parts of the leaf was a distinct character of leaves of over-5-year-old plants. The temperature of single-plane leaves under strong solar radiation could accumulate heat rapidly and resulted in temperatures much higher than the ambient temperature. However, leaves of over-5-year-old plants could lower leaf temperature by avoiding direct exposure to solar radiation and promoting local airflow to prevent serious tissue damage by sunburn. Furthermore, the net photosynthesis rate was correlated with the heterogeneity of the leaf surface temperature. Our results demonstrate that the robust 3D shape of the leaf is a strategy that R. tanguticum has developed evolutionarily to adapt to the strong solar radiation and low temperature on the Qinghai-Tibetan Plateau.

Keywords: 3D leaf shape; Qinghai–Tibetan Plateau; Rheum tanguticum; heteroblasty; leaf thermoregulation; leaf-surface temperature; phenotypic plasticity.

Figure 1

Leaf morphology of R. tanguticum: (a) Leaves of R. tanguticum transitioning from juvenile to adult phase; (b) R. tanguticum on the Qinghai–Tibetan Plateau; (c) Determination of the intersection angle between the blades around the middle of five first-order veins (α) and the intersection angle between blades around the second-order vein (β); (d) Five first-order veins in the leaf of an over-5-year-old R. tanguticum plant.

Figure 2

Different temperatures were detected in the leaf blade on the opposite sides of the first-order veins: (A) tip of the middle of five first-order veins; (B) middle of the third of five first-order veins; (C) base of the middle of five first-order veins; (D) middle of the fourth of five first-order veins.

Figure 3

Thermal imaging showing temperature variation within the leaf of over-5-year-old plant of R. tanguticum: (a) thermal imaging; (b) visible imaging.

Figure 4

Time-course analysis of temperature change of R. tanguticum leaves: Tair, air temperature; S, temperature of small leaves from 1–2-year-old plants; Leaf temperatures from two sides of the first-order vein: leaf tip (A left and A right) and base (C left and C right) of the middle of five first-order veins, and middle of the fourth of five first-order veins (D left and D right) position in over-5-year-old leaf.

Figure 5

Sun-scorched damages of R. tanguticum leaves: (a) 1–2-year-old plants; (b) over-5-year-old plants.

Figure 6

Leaf physiological parameters in different positions of large leaves from over-5-year-old plants (n = 5): (a) net photosynthesis rate (Pn); (b) transpiration rate (E); (c) stomatal conductance rate (C); (d) photosynthetically active radiation (PAR); (e) vapor pressure deficit (VPD). Tleaf, leaf temperature. Leaf positions on two sides of the middle of five first-order veins are labeled for the tip (A left and A right) and base (C left and C right). Leaf middle positions on the opposite sides of the fourth of five first-order veins are labeled (D left and D right).