Glandular trichomes as a barrier against atmospheric oxidative stress: Relationships with ozone uptake, leaf damage, and emission of LOX products across a diverse set of species

Abstract

There is a spectacular variability in trichome types and densities and trichome metabolites across species, but the functional implications of this variability in protecting from atmospheric oxidative stresses remain poorly understood. The aim of this study was to evaluate the possible protective role of glandular and non-glandular trichomes against ozone stress. We investigated the interspecific variation in types and density of trichomes and how these traits were associated with elevated ozone impacts on visible leaf damage, net assimilation rate, stomatal conductance, chlorophyll fluorescence, and emissions of lipoxygenase pathway products in 24 species with widely varying trichome characteristics and taxonomy. Both peltate and capitate glandular trichomes played a critical role in reducing leaf ozone uptake, but no impact of non-glandular trichomes was observed. Across species, the visible ozone damage varied 10.1-fold, reduction in net assimilation rate 3.3-fold, and release of lipoxygenase compounds 14.4-fold, and species with lower glandular trichome density were more sensitive to ozone stress and more vulnerable to ozone damage compared to species with high glandular trichome density. These results demonstrate that leaf surface glandular trichomes constitute a major factor in reducing ozone toxicity and function as a chemical barrier that neutralizes the ozone before it enters the leaf.

Trichomes form an important first line of defence against adverse environment—New evidence for ozone stress mitigation

“…Detailed chemical analyses showed that the contents of the major triterpenoid and flavonoid aglycones correlated positively with glandular trichome density, indicating that glandular trichomes strongly affect leaf surface chemistry, and thus, hydrophobic properties and resistance traits to herbivores and pathogens. In this issue, Li et al () have examined the protective role of glandular and nonglandular trichomes against ozone stress covering a diverse set of plant species with different trichome types. Responsiveness of glandular trichomes to ozone has been previously reported, for example, by Pääkkönen, Günthardt‐Goerg, and Holopainen () and Prozherina et al () in silver birch leaves.…”

“…Li et al () used a step‐wise increase in ozone exposure to cause an acute oxidative stress treatment. Ozone fumigation is technically easy to manipulate within leaf chamber systems, allowing strict control of the experimental procedures.…”

“…The results were then correlated with visible leaf damage, gas exchange traits, chlorophyll fluorescence, and emissions of stress‐induced volatile organic compounds. Using this approach Li et al () convincingly showed that glandular trichomes (both peltate and capitate ones) have a critical role in reducing leaf ozone uptake, while nonglandular trichomes are not important in this defence action. The density of glandular trichomes correlated with the ozone sensitivity of the plant, indicated by visible leaf injuries and lipoxygenase (LOX) product emissions.…”

“…Considering the high temporal, spatial, and chemical flexibility of trichomes, the results by Li et al () encourage us to use glandular trichomes as a promising target for resistance breeding for improved oxidative stress tolerance. Progress could be made by integrating the data, knowledge, and know‐how from the genetic, hormonal, and metabolic regulation of trichome formation and adaptation with phenotyping and field testing.…”

“…Lihavainen et al (2017) also reported differences between the leaf sides in the response of trichomes to high humidity, reflecting differences in leaf surface chemistry, wettability, and water retention traits. Despite this complexity, the approach used by Li et al (2018), including both leaf surfaces in their study, provides strong evidence for the protective role of trichomes across a highly diverse set of species.…”