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.