Histological, metabolomic, and transcriptomic differences in fir trees
from a peri-urban forest under chronic ozone exposure
Abstract
Urbanization modifies ecosystem conditions and evolutionary processes.
This includes air pollution, mostly as tropospheric ozone (O3), which
contributes to the decline of urban and peri-urban forests. A notable
case are fir(Abies religiosa) forests in the peripheral mountains
southwest of Mexico City, which have been severely affected by O3
pollution since the 1970s. Interestingly, some young individuals
exhibiting minimal O3—related damage have been observed within a zone
of significant O3 exposure. Using this setting as a natural experiment,
we compared asymptomatic and symptomatic individuals of similar age (≤15
years old; n = 10) using histological, metabolomic and transcriptomic
approaches. Plants were sampled during days of high (170 ppb) and
moderate (87 ppb) O3 concentration. Given that there have been
reforestation efforts in the region, with plants from different source
populations, we first confirmed that all analysed individuals clustered
within the local genetic group when compared to a species-wide panel
(Admixture analysis with ~1.5K SNPs). We observed
thicker epidermis and more collapsed cells in the palisade parenchyma of
needles from symptomatic individuals than from their asymptomatic
counterparts, with differences increasing with needle age. Furthermore,
symptomatic individuals exhibited lower concentrations of various
terpenes (ß-pinene, ß-caryophylene oxide, α-caryophylene and
ß-α-cubebene) than asymptomatic trees, as evidenced through GC-MS.
Finally, transcriptomic analyses revealed differential expression for
thirteen genes related to carbohydrate metabolism, plant defense, and
gene regulation. Our results indicate a rapid and contrasting phenotypic
response among trees, likely influenced by standing genetic variation
and/or plastic mechanisms. They open the door to future evolutionary
studies for understanding how O3 tolerance develops in urban
environments, and how this knowledge could contribute to forest
restoration.