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Signaling after the first bite: the role of insect elicitor and jasmonic acid metabolism in shaping plant-insect interactions

Aart Pieter van Doorn

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Abstract

Plants and insects share a long evolutionary history, and in this time insects have specialized themselves on plant species, whereas plants have evolved many different ways of defense against these herbivores. An important part of plant defense is the recognition of insect herbivores, and plants have evolved mechanisms to perceive the oral secretions (OS) of feeding insects, allowing them to activate a tailored defense response. After the perception of these oral secretions, the plant hormone jasmonic acid (JA) is quickly biosynthesized. This JA accumulation will activate defense gene expression, leading to an accumulation of plant defense compounds and proteins throughout the plant. In this thesis, I have explored the metabolism of an insect elictor on the wounded plant surface, and investigated the metabolism of jasmonic acid after wounding alone, and simulated herbivory by wounding and applying oral secretions. These studies showed that in the interaction between Nicotiana attenuata and its herbivore Manduca sexta, the fatty-acid amino-acid conjugate 18:3-Glu is rapidly converted to at least three different compounds, one of which is also an active elicitor of JA and plant-produced volatiles. The role of JA metabolism was studies in the wild species Solanum nigrum, as tools for this study we created transgenic plants silenced for genes in JA biosynthesis , metabolism of JA to JA-Ile and the perception of jasmonates. Jasmonate profiling showed that COI1 and JAR4 played both important, but only partly overlapping roles in the metabolism of JA to JA-Ile and other jasmonates. Moreover, it was shown that in contrast to JA biosynthesis and JA perception, the conversion of JA to JA-Ile was not responsible for the activation of plant defenses in the systemic leaf. These results together suggest that both insect elicitor and jasmonic acid modification have been important in shaping the relationship between plants and their insect herbivores.

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What this paper is about

Plants and insects share a long evolutionary history, and in this time insects have specialized themselves on plant species, whereas plants have evolved many different ways of defense against these herbivores. An important part of plant defense is the recognition of insect herbivores, and plants have evolved mechanisms to perceive the oral secretions (OS) of feeding insects, allowing them to activate a tailored defense response. After the perception of these oral secretions, the plant hormone jasmonic acid (JA) is quickly biosynthesized. This JA accumulation will activate defense gene expression, leading to an accumulation of plant defense compounds and proteins throughout the plant. In this thesis, I have explored the metabolism of an insect elictor on the wounded plant surface, and investigated the metabolism of jasmonic acid after wounding alone, and simulated herbivory by wounding and applying oral secretions. These studies showed that in the interaction between Nicotiana attenuata and its herbivore Manduca sexta, the fatty-acid amino-acid conjugate 18:3-Glu is rapidly converted to at least three different compounds, one of which is also an active elicitor of JA and plant-produced volatiles. The role of JA metabolism was studies in the wild species Solanum nigrum, as tools for this study we created transgenic plants silenced for genes in JA biosynthesis , metabolism of JA to JA-Ile and the perception of jasmonates. Jasmonate profiling showed that COI1 and JAR4 played both important, but only partly overlapping roles in the metabolism of JA to JA-Ile and other jasmonates. Moreover, it was shown that in contrast to JA biosynthesis and JA perception, the conversion of JA to JA-Ile was not responsible for the activation of plant defenses in the systemic leaf. These results together suggest that both insect elicitor and jasmonic acid modification have been important in shaping the relationship between plants and their insect herbivores.

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Available abstract

Plants and insects share a long evolutionary history, and in this time insects have specialized themselves on plant species, whereas plants have evolved many different ways of defense against these herbivores. An important part of plant defense is the recognition of insect herbivores, and plants have evolved mechanisms to perceive the oral secretions (OS) of feeding insects, allowing them to activate a tailored defense response. After the perception of these oral secretions, the plant hormone jasmonic acid (JA) is quickly biosynthesized. This JA accumulation will activate defense gene expression, leading to an accumulation of plant defense compounds and proteins throughout the plant. In this thesis, I have explored the metabolism of an insect elictor on the wounded plant surface, and investigated the metabolism of jasmonic acid after wounding alone, and simulated herbivory by wounding and applying oral secretions. These studies showed that in the interaction between Nicotiana attenuata and its herbivore Manduca sexta, the fatty-acid amino-acid conjugate 18:3-Glu is rapidly converted to at least three different compounds, one of which is also an active elicitor of JA and plant-produced volatiles. The role of JA metabolism was studies in the wild species Solanum nigrum, as tools for this study we created transgenic plants silenced for genes in JA biosynthesis , metabolism of JA to JA-Ile and the perception of jasmonates. Jasmonate profiling showed that COI1 and JAR4 played both important, but only partly overlapping roles in the metabolism of JA to JA-Ile and other jasmonates. Moreover, it was shown that in contrast to JA biosynthesis and JA perception, the conversion of JA to JA-Ile was not responsible for the activation of plant defenses in the systemic leaf. These results together suggest that both insect elicitor and jasmonic acid modification have been important in shaping the relationship between plants and their insect herbivores.

Key concepts: Jasmonic acid, Elicitor, Manduca sexta, Biology, Plant defense against herbivory, Insect, Jasmonate, Methyl jasmonate

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