Scientists in China and Germany recently identified a novel compound in wild tobacco Nicotiana attenuata leaves that confers broad resistance to Empoasca leafhopper pests. The research employed a multi-omics approach and was conducted by Prof. LI Dapeng from the Center for Excellence in Molecular Plant Sciences of the Chinese Academy of Sciences in collaboration with a research group from the Max Planck Institute for Chemical Ecology (MPICE) led by Prof. Ian T. Baldwin and Dr. BAI Yuechen. The study was published a cover article in Science on Feb. 4.
Plants are at the bottom of the food chain and are continually threatened by pathogens and herbivorous insects. But the vast majority of attackers are unable to cause damage due to broad-based plant resistance, also known as non-host resistance. This resistance is permanent and effective. However, the mechanisms that lead to this resistance, particularly to herbivorous pests, are largely unknown.
In this study, scientists were able to identify a chemical substance responsible for the resistance of Nicotiana attenuata plants to sucking leafhoppers (Empoasca spp.) as well as the genes needed for its production. “Our research uncovered how native plants use chemical reprogramming to defend themselves against opportunistic leafhoppers in nature,” said first author Dr. BAI.
The plant hormone jasmonic acid is the basis for a defense-signaling cascade that can protect tobacco plants. However, scientists at MPICE discovered in 2004 that tobacco plants with such defenses impaired were attacked by leafhoppers—insects usually unable to harm tobacco plants with functional defenses. The researchers proved that, in nature, plants are continuously “tested” by herbivorous insects in order to find out whether they can serve as a food source. In most cases, the plants are able to defend themselves effectively.
Consistent with these findings, another study by the institute showed that leafhoppers colonized the very plants in natural tobacco populations whose jasmonic acid signaling pathway was weaker than in other tobacco plants. “However, at that time, it was still unknown which specific defense mechanisms triggered by jasmonic acid were responsible for resistance to the leafhoppers,” said Prof. LI.
To answer this question, scientists crossed 26 genetically different natural parental lines. This population, which was crossed according to a fixed scheme over nine years, was planted in its natural habitat in Arizona, USA, where it could be attacked by opportunistic leafhoppers. When leafhoppers attacked these plants, the severity of the damage helped identify the genetic reasons why a particular plant became a host plant for leafhoppers.
In addition, scientists investigated which chemical changes were elicited in plants after attack and which genes were activated. During this investigation they found a new unstable substance—caffeoylputrescine-green-leaf-volatile compound (CPH)—which is responsible for permanent resistance to leafhoppers. Through bioinformatic detective work and by using plants that were specifically modified in certain defense and signal transduction genes, they were able to determine which three metabolic pathways were involved in the production of this chemical. Finally, they reconstituted the biosynthetic pathway for the defense substance CPH in two related plants—the field bean Vicia faba and the tomato species Solanum chilense—and demonstrated its efficacy against leafhoppers.
"By combining sophisticated molecular biology and chemical analysis methods, we were able to identify and characterize not only a previously unknown defense substance, but also the genes responsible for its synthesis,” said Prof. Ian Baldwin. “Our approach can be described as natural history-guided forward genetics. Natural history and the observation of the feeding behavior of leafhoppers has driven our discovery process. Because when it comes to chemistry, nature remains the mother of invention.”
In further studies, scientists want to find out how the synthesis of this chemical defense is coordinated in the plant and which other factors and specific regulators are crucial for its production, especially under natural conditions. Leafhoppers of the genus Empoasca, especially the potato leafhopper Empoasca fabae, can cause major crop damage by sucking on the leaves of young plants and transmitting viral diseases. Higher temperatures have led to a threatening spread of these insects.
Natural history–guided omics reveals plant defensive chemistry against leafhopper pests
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