Lignans dramatically enhance the resistance of Fraxinus velutina Torr. by adjusting the dominant bacterium group of Agrilus planipennis Fairmaire

Abstract

BACKGROUND Velvet ash (Fraxinus velutina Torr.) is an important wood and ornamental tree species. Emerald ash borer (EAB), Agrilus planipennis Fairmaire, is a major wood borer of velvet ash. The aim of this study was to identify the secondary metabolites of velvet ash involved in regulating the dominant bacterium group of EAB. RESULTS The amount of lignans in the phloem of infested trees had increased by 290.96% because of A. planipennis infection. The addition of lignans to the artificial diet significantly reduced the weight of the larvae and decreased the dominant bacterial group in the larval midgut, such as Pseudomonadaceae, Xanthomonadaceae, and Enterobacteriaceae. The FvPLR1, a key gene for lignan synthesis, was obtained based on the phloem transcriptome of velvet ash. The expression of FvPLR1 in the phloem of the infested tree was significantly higher than that in the noninfested tree. Meanwhile, FvPLR1 silenced by virus‐induced gene silencing showed that its expression level and the lignan content were decreased by 69.91% and 31.65%, respectively. Interestingly, silencing FvPLR1 induced alterations in the dominant bacteria group in the larvae, with the reverse trend in the lignan‐fed treatment. CONCLUSION The evidence showed that FvPLR1 was a positive regulator. The increasing synthesis of lignans leads to resistance improvement in velvet ash, which will provide comprehensive insights into the tree defense system to wood borer infestation. © 2021 Society of Chemical Industry

Gut Bacteria of Wood-Boring Streltzoviella insularis and Their Involvement in Pinoresinol Degradation of Ash Tree (Fraxinus sp.) Host

“…One of the simplest lignan compounds, pinoresinols, has been reported to have insecticidal, antifeedant, as well as growth and molting inhibitory activities against several insect species. , For example, pinoresinols have been shown to inhibit the growth of Rhodnius prolixus (Hemiptera) and Drosophila melanogaster (Diptera) and also prevent the ecdysis in the first mentioned species. , In addition, despite no consistent differences in constitutive levels of pinoresinol have been detected, pinoresinol A has been suggested to be involved in the resistance of a Chinese native Manchurian ash (Fraxinus mandschurica) against the emerald ash borer, and its concentration being elevated to reach nearly 2 times higher concentration in infested resistant trees compared to susceptible ones, , suggesting that pinoresinol played a role in ash defense against wood borers. However, to our knowledge, investigation of ash responses to wood borers or the role of pinoresinols is solely based on studies with the emerald ash borer, , warranting further confirmation of the function of pinoresinols on other wood-boring insects.…”

“…are native to parts of Asia, North America, and Europe and are also widely planted ornamental trees. − Besides their notorious pest, the emerald ash borer (Agrilus planipennis, Buprestidae) and ash trees also host other wood-boring insect species, such as Lepidopteran pests Podosesia syringae and Streltzoviella insularis . Ash trees are rich in coumarins, secoiridoids, and phenylethanoids, while simple phenolics, monolignols, lignans, and flavonoids are also common. − Recently, lignans (a group of polyphenolics) have been suggested to be involved in ash responses against wood-boring pest stress . One of the simplest lignan compounds, pinoresinols, has been reported to have insecticidal, antifeedant, as well as growth and molting inhibitory activities against several insect species. , For example, pinoresinols have been shown to inhibit the growth of Rhodnius prolixus (Hemiptera) and Drosophila melanogaster (Diptera) and also prevent the ecdysis in the first mentioned species. , In addition, despite no consistent differences in constitutive levels of pinoresinol have been detected, pinoresinol A has been suggested to be involved in the resistance of a Chinese native Manchurian ash (Fraxinus mandschurica) against the emerald ash borer, and its concentration being elevated to reach nearly 2 times higher concentration in infested resistant trees compared to susceptible ones, , suggesting that pinoresinol played a role in ash defense against wood borers.…”

“…14−17 Recently, lignans (a group of polyphenolics) have been suggested to be involved in ash responses against wood-boring pest stress. 18 One of the simplest lignan compounds, pinoresinols, has been reported to have insecticidal, antifeedant, as well as growth and molting inhibitory activities against several insect species. 19,20 For example, pinoresinols have been shown to inhibit the growth of Rhodnius prolixus (Hemiptera) and Drosophila melanogaster (Diptera) and also prevent the ecdysis in the first mentioned species.…”

“…21,22 In addition, despite no consistent differences in constitutive levels of pinoresinol have been detected, 16 pinoresinol A has been suggested to be involved in the resistance of a Chinese native Manchurian ash (Fraxinus mandschurica) against the emerald ash borer, and its concentration being elevated to reach nearly 2 times higher concentration in infested resistant trees compared to susceptible ones, 23,24 suggesting that pinoresinol played a role in ash defense against wood borers. However, to our knowledge, investigation of ash responses to wood borers or the role of pinoresinols is solely based on studies with the emerald ash borer, 18,24 warranting further confirmation of the function of pinoresinols on other wood-boring insects.…”

“…For example, gut microbiota of Gypsy moth (Lymantria dispar) are able to metabolize plant defensive secondary chemicals . Similarly, bacterial associates of Dendroctonus ponderosae bark beetles, such as the genus Pseudomonas , can metabolize host tree monoterpenes and/or diterpene acids. ,,− Various insect species, such as termites, are also shown to harbor beneficial gut microbiota with cellulolytic activity, and given that cellulose is especially abundant in woody tissues, such bacterial partners are especially important for wood-boring insects, whereas further understanding how insect symbiotic bacteria influence host plant defenses is increasingly important given that those insect symbiotic bacteria may have great potential for application in pest management. ,− …”