Herbivore-induced volatile emission from old-growth black poplar trees under field conditions

Abstract

Herbivory is well known to trigger increased emission of volatile organic compounds (VOCs) from plants, but we know little about the responses of mature trees. We measured the volatiles emitted by leaves of old-growth black poplar ( Populus nigra ) trees after experimental damage by gypsy moth ( Lymantria dispar ) caterpillars in a floodplain forest, and studied the effect of herbivory on the transcript abundance of two genes involved in the biosynthesis of VOCs, and the accumulation of defence phytohormones. Herbivory significantly increased volatile emission from the experimentally damaged foliage, but not from adjacent undamaged leaves in the damaged branches (i.e., no systemic response). Methylbutyraldoximes, 4,8-dimethyl-1,3,7-nonatriene (DMNT), ( Z )-3-hexenol and ( E )-β-ocimene, amongst other compounds, were found to be important in distinguishing the blend of herbivore-damaged vs. undamaged leaves. Herbivory also increased expression of PnTPS3 (described here for the first time) and PnCYP79D6-v4 genes at the damaged sites, these genes encode for an ( E )-β-ocimene synthase and a P450 enzyme involved in aldoxime formation, respectively, demonstrating de novo biosynthesis of the volatiles produced. Herbivore-damaged leaves had significantly higher levels of jasmonic acid and its conjugate (−)-jasmonic acid-isoleucine. This study shows that mature trees in the field have a robust response to herbivory, producing induced volatiles at the damaged sites even after previous natural herbivory and under changing environmental conditions, however, further studies are needed to establish whether the observed absence of systemic responses is typical of mature poplar trees or if specific conditions are required for their induction.

Insect Herbivory Strongly Modifies Mountain Birch Volatile Emissions

“…Among individual compounds, we observed induction of the emissions of the homoterpene DMNT and products of the lipoxygenase pathway (LOX products, or GLVs), particularly (E)-2-hexenal, which is commonly emitted after insect herbivore feeding and is suggested to be involved in plant-to-plant signaling (Kessler and Baldwin, 2002). DMNT is usually synthesized de novo in response to herbivore attack (Kessler and Baldwin, 2002) and plays a role in attracting enemies of the herbivores (McCormick et al, 2019). We also found other volatiles associated with the attraction of herbivore enemies, such as the monoterpenes, linalool and (E)-β-ocimene (Clavijo McCormick et al, 2012), whose emissions also increased with increasing insect herbivory.…”

“…For instance, simultaneous feeding on cotton plants (Gossypium hirsutum L.) by phloem-feeding whiteflies (Bemisia tabaci) and tissue-chewing caterpillars (Spodoptera exigua) reduced BVOC emissions as compared to feeding by only caterpillars (Rodriguez-Saona et al, 2003). Second, the observed differences in BVOC responses to herbivory between geographical locations of the experiment could also be due to the inherent differences in abiotic and biotic environments between the locations, such as different insect outbreak histories or genetic differences (López-Goldar et al, 2019;McCormick et al, 2019). For example, the two locations were at different phases of the geometrid moth outbreak cycle: In the Abisko area, the latest moth population peak was in 2012 (Olofsson et al, 2013), whereas in the Tromsø area, it was in 2014 (Vindstad et al, 2019, see also www.coat.no/en/Tundraforest-ecotone).…”

“…Third, it could be that control branches or other parts of the trees were experiencing damage by other herbivores and that could cause a systemic response in the control branches (Hilker and Schmülling, 2019). McCormick et al (2019), who assessed herbivore-induced BVOCs under field conditions, argued that laboratory studies conducted under well-controlled conditions show contrasting results to field studies. It suggests that confounding factors are experienced in the field and therefore, to better understand the ecological relevance of herbivore-induced BVOC emissions, more experiments should be conducted in as near-natural conditions as possible.…”

Potential of Climate Change and Herbivory to Affect the Release and Atmospheric Reactions of BVOCs from Boreal and Subarctic Forests

“…Several studies have shown that the constitutive emission rates of these compounds from the foliage [ 9 , 37 , 39 , 40 ], bark [ 41 , 42 ], and root systems [ 12 , 13 , 43 ] of trees are related to abiotic conditions. Many of these compounds are also emitted at an order of magnitude higher rates from herbivore or fungal pathogen-damaged plants [ 44 , 45 , 46 , 47 , 48 , 49 ]. Some of the compounds, such as GLVs and sesquiterpenes (SQT), are mostly detected in emissions after feeding damage [ 50 ].…”

Herbivory and Attenuated UV Radiation Affect Volatile Emissions of the Invasive Weed Calluna vulgaris

“…However, feeding damage by L. suturalis did not cause higher emission of this group of compounds in our study. Perhaps this is because plants in the field are subject to previous and continuous damage, unlike plants in controlled laboratory studies that are naïve to herbivore damage [55]. In fact, higher emissions of the green leaf volatiles (Z)-3-hexenyl acetate, (Z)-3-hexenyl 2-methylbutyrate, (Z)-3-hexenol and (Z)-3-hexenyl butyrate were instead found at the site where L. suturalis was not present.…”