Introduction
Leaf traits represent the functional strategies of plants, encompassing growth, carbon economies, and resource exploitation and conservation, which vary across species and environmental conditions (Deans et al. 2020, Xing et al. 2021). Understanding leaf trait variation is critical for the prediction of plant responses to global climate changes (Stotz et al. 2021). Leaf trichomes are derived from epidermal cells on the surfaces of leaves, which not only provide structural defenses against herbivores (Dalin et al. 2008), but also play multiple additional physiological and ecological roles (Ehleringer et al. 1976, Bickford 2016, Sack and Buckley 2020). Leaf trichomes can reduce the absorbance of solar radiation and UV damage, as well as decrease the leaf transpiration rate and temperature by increasing boundary layer resistance (Ripley et al. 1999, Sack and Buckley 2020). This, in turn, affects the photosynthesis rate and water use efficiency of plants (Ripley et al. 1999, Konrad et al. 2015), as well as determines plant fitness against adverse environmental conditions (Ehleringer 1988, Jon and Douglas 1994). Previous studies have examined the functions of leaf trichomes and their control factors, which have been extensively investigated under variable manipulation conditions and regional scales (Pérez-Estrada et al. 2000, Paulino et al. 2020). However, little is known about how leaf trichomes vary along a large geographic gradient in individual plant species, which can advance our understanding of spatial variations in leaf traits and plant adaptive strategies under climate change.
Leaf trichome densities can vary between plant species under localized environmental conditions and are affected by changes in light intensity, temperature, rainfall, CO2 concentrations, UV-radiation, and soil nutrients (Pérez-Estrada et al. 2000, Abdala‐Roberts et al. 2016, Thitz et al., 2017, Moles et al. 2020). Leaf trichome densities typically increase under sunny and dry environments and decrease under shady and wet conditions (Kessler et al. 2007). In fact, leaf trichomes serve as an effective barrier against solar radiation (Skelton et al. 2012), which can increase light reflectivity to reduce photoinhibition and cool leaves to maintain optimal photosynthetic temperatures (Pérez-Estrada et al. 2000). In addition, high trichome densities also may enhance resistance against drought by increasing the thicknesses of leaf boundary layers, reducing conductivity for water vapor diffusion, and limiting water loss through transpiration (Bickford 2016). Kenzo et al. (2008) found that the leaf trichomes of Mallotus macrostachyus contributed to high leaf water use efficiencies under drought conditions. However, other studies found drought stress did not induce trichome production (Piritta et al. 2010). Furthermore, the formation and development of trichomes can be significantly influenced by temperature (Skelton et al. 2012, Amada et al. 2020). However, it remains unclear exactly which environmental factors primarily drive spatial variations in leaf trichome densities.
Previous studies have primarily focused on the isolated roles of given traits (Poorter et al. 2009; Li et al. 2020). However, environmental stresses are often combined; thus, a given functional trait can provide resistance against multiple stressors, whereas multiple functional traits may also coordinate in response to a given stress (Read et al. 2014, Sack and Buckley 2020, Xing et al. 2021). Leaf size is essential for leaf thermoregulation, where the leaf mass per area (LMA) reflects the investment of structural tissues per area and leaf veins determine water transport efficiencies, all of which are variable under environmental changes (Fauset et al. 2018, Du et al. 2021). Stomata regulate water and gas exchange between plants and the ambient atmosphere (Hetherington and Woodward 2003), whereas stomatal guard and trichome cells share the same development origins and are distributed at specific distances across the epidermal surfaces of leaves (Holroyd et al. 2002). Negative correlations between the trichome and stomatal densities (SD) have also been observed in other studies (Galdon-Armero et al. 2018). The coordinated development of trichomes and stomata may influence plant water use efficiencies and environmental adaptations (Galdon-Armero et al. 2018; Bertolino et al. 2019), which may reflect a trade‐off between the proportions of cells that possess trichomes and guard cell fates (Simon et al. 2020). Yet, it remains unclear whether the relationships between leaf trichomes and other functional traits may co-vary with stomata in response to environmental changes.
For this work, we investigated the leaf trichome density of 44 in situQ. variabilis populations across Eastern Asia and evaluated their associations with environmental factors and other functional leaf traits (e.g., leaf area (LA), LMA, vein density (VD), stomatal size (SS), and SD) using a piecewise structural equation model (SEM). Furthermore, a common garden was established with 15 of the 44 populations at the middle latitude to further examine adaptive variation of leaf trichomes. We hypothesized that leaf trichomes possess highly environmental variation and can coordinate with stomata in response to environmental changes. To test the hypotheses, we investigated how leaf trichome density varied along an extensive climate gradient (which spanned subtropical to temperate biomes) and its driving factors. Further, the relationships between trichome density and functional leaf traits in response to environmental changes were examined, particularly for stomata.