In general, the leaves of most plants in QTP are small to adapt to the high altitude and dry-cold habitat [1, 9], whereas R. tanguticum is an exception. The evolved changes in leaf shape and structure have provided an ideal solution to its adaptive advantage.
In the R. tanguticum adult leaves, five lateral veins are produced from the petiole, and the midrib is an extension of the petiole. Lateral veins are inclined above the blade resulting in certain angles between the lateral veins and the plane of the extended midrib. The five veins are not in the same plane, which is the basis for the stereostructure of the leaf blade (Fig. 1d). The most dramatic change of the leaf shape has been the change of a single leaf plane to a three-dimensional structure (Fig. 1c and Additional file 3: Figure S2). In the juvenile to adult transition, the leaf undergoes a transformation from a small oval plane to a giant palmatipartite stereostructure. Due to the 5-vein stereostructure, the whole leaf appears to be divided into more than ten different zones. Because the palmatipartite leaves resemble chicken feet, one of the Chinese common names of this species is “Chicken feet Rheum”. To our knowledge, although this is not the first observation for the three-dimensional structure of Rheum leaves, this has been the first systematic study to explore the underlying mechanism for the adaptive change of R. tanguticum leaves.
The leaf size and shape of the same individual varied noticeably along with the life cycle in some plant species is termed as heteroblasty [13, 14]. Heteroblasty usually means leaf morphology change in the same plant; in R. tanguticum, it includes both morphologicaland structural changes. Therefore, R. tanguticum is a typical example of heteroblasty, which can be called isomerized heteroblasty.
The stereostructure of R. tanguticumappears to be the main reason for the leaf temperature variation. Because of the high altitude and strong solar radiation in QTP [8, 9], the temperature of the large leaves rises quickly under the sun, but more slowly or even decreases in the shade (Fig. 2 and Additional file 5: Figure S4). The highest leaf temperature in our study was 38.00℃, which was 22.00℃ higher than ambient temperature of 16.00℃. Previous studies [15–17] showed that broad leaves reached up to 20.00℃ above ambient temperature. According to the thermal imaging in our study, the average highest temperature of R. tanguticum leaf was up to about 29.27℃, which was 13.27℃ above ambient temperature (16.00℃). The heterogeneity of sun exposure on the large leaves is the reason of leaf-to-air temperature differences, rather than the result . In the area of QTP with low temperature, the locally elevated leaf temperature could increase the enzymatic activity and therefore improve the photosynthetic efficiency. With the short growing season, the rapid accumulation of metabolites promotes R. tanguticum to grow taller with large leaves. Local leaf temperature could rise to higher than 30.00℃, therefore the photosynthesis efficiency in this part of the R. tanguticum leaf could reach the level of tropical plants.
Temperature plays one of the key roles in plant growth. Generally, ambient temperature is used to estimate the growth rate or biomass in most plants species when leaf temperature is close to ambient temperature. However, in our study, there were large leaf-to-air temperature differences betweenR. tanguticum leaves and the ambient (Fig. 2). So if ambient temperature were used to estimate the growth rate of R. tanguticum, there would be a large bias. According to the Van’t Hoff relationship for monomolecular reactions, variation of leaf temperature for more than 10℃ could change the photosynthesis efficiency for more than two folds. Hence it is more accurate to use leaf temperature rather than ambient air temperature to estimate photosynthesis efficiency of plants with large leaves . The leaf-to-air temperature differences could also explain another outstanding question as why C4 plants can thrive in QTP or other cold environments .
Under the strong light, orbiculate leaves get heated up rapidly if the size of the leaves is large enough. The temperature becomes especially high at the edges of the orbiculate leaves. Consequently, the orbiculate leaves are easily damaged by scorch at the edges of the leaves . However, for large leaves of R. tanguticum, the scorched area was usually in the internal part, but not at the leaf edges (Fig. 3). In addition, the scorches of R. tanguticum leaf were small patches rather than continuous large regions (Fig. 3). The scorching was inevitable, yet it would not cause fatal damage to the plants. For R. tanguticum, the stereostructure of leaf plays an important role in preventing serious leaf scorching. More work is needed in the future to determine if leaf structure (on an anatomical level) of R. tanguticum also contributes to the resistance of sun scorching.
In the ecosystem of QTP, even the small leaves of 1 to 2-year old R. tanguticum plants are larger than other plants (Fig. 1b and Table 1); hence they have the risk of sun scorch (Fig. 3). Therefore, in order to adapt to the strong solar radiation of plateau ecosystem, R. tanguticum has evolved to have changes in the leaf shape and structure during the long period of evolution.
In the stereostructure leaves, there are three possible mechanisms to regulate the leaf temperature. First, compared to the plane leaf with the same leaf area, there is less solar radiation on the stereo-plamatipartite leaf of R. tanguticumabout 50% decrease in plants more than 5-year old), and this would prevent the leaf temperature rising too fast or too high. There are angles between the blades and the midrib (Fig. 1c). The older the R. tanguticum plants, the larger the leaves, however, the intersection angles between the blades and the midrib also become smaller, hence more apparent of the stereostructure of the leaf blade. This represents a permanent partial leaf fold without energy expenditure, compared to the temporary leaf fold of some plants exposed to high light . Second, temperature variation facilitates the formation of local airflow in the stereostructure leaf. Some part of the leaf is in the sunlight, while other part is in the shadow of the leaf itself (self-shading, Fig. 2) or other leaf. Because the light exposure is opposite in the bilateral sides of the veins, it creates a greater temperature difference, which is in favor of the formation of air circulation around the leaf (Additional file 6: airflow indicated by smoke in the leaf). Third, deep lobing may also reduce leaf temperature. Vogel  showed that deep lobing not only improved heat transfer, but notably reduced its dependence on orientation. In addition, it was found that pinnately compound leaves dissipate heat more effectively than simple ones .
Transpiration can decrease the leaf temperature, but the process requires energy and water. Besides transpiration, plants use various ways to decrease leaf temperature, especially in dry environments . Leaf can also prevent or decrease scorch by physical structure such as pubescence or even by leaf movement [20, 23], but these processes require energy input. By contrast, R. tanguticum takes advantage of leaf physical structure change for thermoregulation. Thus, this mechanism employs the external force of the infrastructure in exchange of the consumption of energy and water. This may be another reason why R. tanguticum has large leaves but adapts well in QTP.