Ozone Impact on Emission of Biogenic Volatile Organic Compounds in Three Tropical Tree Species From the Atlantic Forest Remnants in Southeast Brazil

Abstract

Plants emit a broad number of Biogenic Volatile Organic Compounds (BVOCs) that can impact urban ozone (O₃) production. Conversely, the O₃ is a phytotoxic pollutant that causes unknown alterations in BVOC emissions from native plants. In this sense, here, we characterized the constitutive and O₃-induced BVOCs for two (2dO₃) and four (4dO₃) days of exposure (O₃ dose 80 ppb) and evaluated the O₃ response by histochemical techniques to detect programmed cell death (PCD) and hydrogen peroxide (H₂O₂) in three Brazilian native species. Croton floribundus Spreng, Astronium graveolens Jacq, and Piptadenia gonoacantha (Mart.) JF Macbr, from different groups of ecological succession (acquisitive and conservative), different carbon-saving defense strategies, and specific BVOC emissions. The three species emitted a very diverse BVOC composition: monoterpenes (MON), sesquiterpenes (SEQ), green leaf volatiles (GLV), and other compounds (OTC). C. floribundus is more acquisitive than A. graveolens. Their most representative BVOCs were methyl salicylate-MeSA (OTC), (Z) 3-hexenal, and (E)-2-hexenal (GLV), γ-elemene and (-)-β-bourbonene (SEQ) β-phellandrene and D-limonene (MON), while in A. graveolens were nonanal and decanal (OTC), and α-pinene (MON). Piptadenia gonoachanta is more conservative, and the BVOC blend was limited to MeSA (OTC), (E)-2-hexenal (GLV), and β-Phellandrene (MON). The O₃ affected BVOCs and histochemical traits of the three species in different ways. Croton floribundus was the most O₃ tolerant species and considered as an SEQ emitter. It efficiently reacted to O₃ stress after 2dO_3, verified by a high alteration of BVOC emission, the emergence of the compounds such as α-Ionone and trans-ß-Ionone, and the absence of H₂O₂ detection. On the contrary, A. graveolens, a MON-emitter, was affected by 2dO₃ and 4dO₃, showing increasing emissions of α-pinene and β-myrcene, (MON), γ-muurolene and β-cadinene (SEQ) and H₂O₂ accumulation. Piptadenia gonoachanta was the most sensitive and did not respond to BVOCs emission, but PCD and H₂O₂ were highly evidenced. Our results indicate that the BVOC blend emission, combined with histochemical observations, is a powerful tool to confirm the species' tolerance to O₃. Furthermore, our findings suggest that BVOC emission is a trade-off associated with different resource strategies of species indicated by the changes in the quality and quantity of BVOC emission for each species.

Keywords: VOC; ecological chemical trait; isoprenoid compounds; tropical plants; tropospheric ozone.

Figure 1

Localization of programmed cell death (PCD) visualized by Evans blue staining. (A,B) Astronium graveolens, with PCD not observed in CT (A) or 4dO₃ samples (B); (C,D) Croton floribundus, with PCD, observed in palisade parenchyma cells of 4dO₃ samples (D) but not in CT samples (C); (E,G) Piptadenica gonoacantha with PCD observed in palisade parenchyma cells of 4dO₃ samples (F) but not in CT samples (E) and the leaf pulvinus (G). H₂O₂ deposits brown-stained by DAB. (H,I) Astronium graveolens, with H₂O₂ observed in palisade parenchyma cells of 4dO₃ samples (I) but not in CT samples (H); (J,K) C. floribundus, with H₂O₂ not observed in CT (J) or 4dO₃ samples (K); (L–N) Piptadenica gonoacantha with H₂O₂ observed in palisade parenchyma cells of 4dO₃ samples (M) but not in CT samples (L) and the leaf pulvinus (N). A–F and H–M, scale bars = 150 μm. G,N, scale bars = 250 μm.

Figure 2

Constitutive emission rates and percentage of different classes of biogenic volatile organic compounds (BVOCs): monoterpenes (MON), sesquiterpenes (SEQ), green leaf volatiles (GLV), and other compounds (OTC) in seedling of (A) Astronium graveolens, (B) Croton floribundus, and (C) Piptadenica gonoacantha exposed to control conditions (CT). Data are mean ± standard error.

Figure 3

Non-metric multidimensional scaling (nMDS) representation of the SIMPER procedure, used to describe the BVOCs of each species and the effect of O₃ treatment on each species.

Figure 4

Constitutive emission rates and percentage of different classes of BVOCs: MON, SEQ, GLV, and OTC in seedlings of (A) Astronium graveolens and (B) Croton floribundus exposed to CT and filtered air enriched with 80 ppb of ozone for 2 (2dO₃) and 4 days (4dO₃). Data are mean ± standard error.