Transcriptomic, morphological, and metabolomic differences in fir trees from a peri-urban forest under chronic ozone exposure

Urbanization modifies ecosystem conditions and evolutionary processes. This includes air pollution, mostly tropospheric ozone (O3), which leads to urban and peri-urban forest decline. Such is the case of fir (Abies religiosa) forests in the peripheral mountains west of Mexico City, which have been severely affected by O3 pollution since the 1970s. Interestingly, some young individuals with low O3—related damage have been observed within a zone of great O3 incidence, which might suggest rapid tolerance/adaptation to this pollutant. We compared asymptomatic and damaged individuals of the same age (≤15 years old; n = 10) using histological, metabolomic and transcriptomic methods. Plants were sampled during days of high (170 ppb) and moderate (87 ppb) O3 concentration periods. After verifying that all individuals clustered within the same 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 in needles from damaged than from asymptomatic individuals; such differences increased with needle age. Furthermore, damaged individuals had lower concentrations of various terpenoids (ß-Pinene, ß-Caryophylene Oxide, α-Caryophylene, ß-α-Cubebene and α-Muurolene) 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 between plants, likely modeled 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 for identifying tolerant germplasm for forest restoration.