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.