Leaf trichomes are highly coordinated with stomata in response
to climate changes
Stomata control gas exchange between plants and the environment and
serve as the main conduit for the loss of transpiration water and the
influx of CO2 (Hetherington and Woodward 2003). Our
results revealed that leaf trichomes were positively correlated with
stomatal density and negatively so with stomatal size (Fig. 4), which
suggested that the development of leaf trichomes may impact stomatal
behavior. In a previous study, Du et al. (2021) reported that stomatal
density was related to the LA and LMA, whereas the stomatal size was
associated with LA and VD in field populations, while there was no
relationship between stomatal and leaf traits in the common garden.
These results implied that the coordination between stomatal and leaf
traits may be due to long-term local adaptations. However, in the
present study the trichome density not only showed a significant
correlation with mature trees in the field, but also showed the same
results as seedlings in the common garden (Figs. 4 and 6). These results
suggested that there was an evolving intimate relationship between the
leaf trichomes and stomata. This signified that leaf trichomes may
closely coordinate with stomata guard cells and collectively influence
plant transpiration, photosynthesis, and water use efficiencies, as
demonstrated by Galdon-Armero et al. (2018) and Paulino et al. (2020).
In effect, stomatal guard cells and trichome cells have shared
developmental origins (Holroyd et al. 2002), where trichome formation
can lead to changes in stomatal density. Simon et al. (2020) reported
that glabrous leaves had a greater stomatal density compared with hairy
leaves in Arabidopsis halleri . Other studies found there was a
negative relationship between trichome and stomata densities inPhaseolus vulgaris (Silva et al. 1999) and Solanum
lycopersicum (Galdon-Armero et al. 2018). These studies indicated that
there might be a trade-off between trichome formation and stomatal
development. However, the results of our experiments were distinct from
these previous studies, as they indicated that there was a positive
relationship between trichome and stomata densities regardless of
whether the plants were grown in the field or in the common garden. One
possible explanation was that there was a synergic relationship that
existed between the stomata and trichome in response to environment
changes, rather than trade-off relationships reported in earlier studies
(Cach-Pérez et al. 2016, Simon et al. 2020). This was likely due to the
requirement of high stomata densities for corresponding trichomes that
covered the surfaces of the stomatal pores to assist plants with the
joint control of water-gas exchange. For example, we observed that when
the stomata density increased under drought conditions, the trichome
density also needed to be increased accordingly (Fig. 3) (Du et al.
2021). These results implied that the level of trichome development
appeared to be coupled with that of stomatal development, where both
were likely impacted by environmental signals.
How distinct given traits such as LMA, stomata, and trichome density
vary with environment changes has been widely examined (Buckley 2019,
Bhusal et al. 2021), yet it remains unclear whether diverse functional
traits can coordinate in response to specific environmental conditions
(Sack and Buckley 2020). In the present study, the modelling results
revealed that precipitation may be the major driving factor for the
spatial variation in leaf trichomes (Figs. 2 and 3). In combination with
previous work (Du et al. 2021), these results showed that the trichome
density, stomata density, and LMA increased with lower precipitation,
which was consistent with the study of Salgado-Negret et al. (2015), who
found that Aextuxion punctatun growing under drier conditions had
higher LMA, trichome, and stomata densities compared to that under wet
environments. Interestingly, there was a correlation between the
trichome densities, as well as LMA and stomata densities. One possible
interpretation was that the leaves with higher LMA generally had lower
mesophyll conductance (Wu et al. 2020); thus, they needed to be coupled
with higher stomata densities (Du et al. 2021) to increase the stomatal
conductance, which determines leaf temperatures and photosynthesis.
Correspondingly, higher trichome densities are required to cover the
surface of the stomata to increase the resistance of the boundary layer,
thereby reducing transpiration related water loss and increasing leaf
wettability (Konrad et al. 2015). Our results suggested that plants with
higher LMA and trichome and stomata density may be an important
adaptation strategy against drought. Importantly, our results revealed
that multiple functional traits may co-vary and coordinate in response
to a given environmental pressure.