Sugarcoat it – how phloem sap-feeding insects prevent activation of chemical defenses from their host plants

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Our research group at the Max Planck Institute for Chemical Ecology largely focuses on figuring out how herbivores and plant pathogens use chemistry to deal with the complex cocktails of chemical defenses produced by plants. We started with insects such as the voracious armyworm caterpillars, and recently we’ve been working with the smaller and more challenging phloem feeders, such as aphids and whiteflies. Some of the herbivores we study benefit greatly from creative biochemistry aimed at circumventing plant toxicity, and some adapt so well to particular chemical defenses that they specialize on plants containing those compounds, occupying a niche that most other insects might find unappetizing.

Caterpillars are messy eaters. They bite big pieces off leaves, salivate all over the place, and this gives plants the opportunity to accordingly activate lots of defensive chemistry. Many of the compounds we study are even thought to require this “messiness” to function – they are only pro-toxins, and must be activated by plant enzymes when the plant tissues are shredded and chewed.

Piercing-sucking phloem feeders, on the other hand, feed much more elegantly. They have straw-like mouthparts that allow them to feed stealthily on the plant sap, much like a mosquito sucking our blood. Many researchers thus assume that such pro-toxins end up not being activated – and why would these insects then even care to spend energy in detoxifying them!?

As it turns out, stealthy as they might be, these insects do activate the plant pro-toxins when feeding, and would therefore benefit from strategies to detoxify such plant defenses. A number of years ago, our director Jonathan Gershenzon and I embarked on a collaboration with Shai Morin and his group at the Hebrew University of Jerusalem, who observed that crucifer chemical defenses (glucosinolates) help defend those plants against the whitefly Bemisia tabaci in many ways. Using our analytical experience with glucosinolates, we could detect some known derivatives in the sticky honeydew excreted by whiteflies when feeding on crucifer plants: desulfoglucosinolates, detoxification compounds also produced by the diamondback moth Plutella xylostella (a terrible worldwide pest of crucifers) and the desert locust Schistocerca gregaria (which feeds on a multitude of plants and has been wreaking agricultural havoc through Africa, the Middle-East and Southwest Asia this year).

However, when we looked through the insect honeydew with a less targeted LC-MS approach, it became evident that this whitefly has more tricks in its toolset. We now report that this insect, as well as all other phloem feeders we tested so far, is quite efficient in attaching sugars onto some of the pro-toxins it ingests, forming derivatives that had never been observed before. Using 13C labeling, our tireless student Michael Easson could show with Stephan Winter and colleagues in Braunschweig that this reaction depends on sucrose as a sugar donor (and not UDP-glucose as many other glucosylation reactions). Very importantly, Michael saw that it also prevents activation of the plant pro-toxin, so it has the potential to benefit the insect. This clever approach costs the whitefly nearly no energy, as sucrose is such a concentrated surplus nutrient in a phloem-feeder’s diet! In fact, this has many parallels with how whiteflies and aphids lower the osmotic pressure of sugars in their food during digestion and, as it turns out, the enzymes needed for these transformations seem to be closely related.

The whitefly Bemisia tabaci has multiple biochemical strategies to cope with activated chemical defenses of a host plant, here depicted as the major glucosinolate of broccoli and Arabidopsis thaliana Col-0, glucoraphanin: a novel glucosylation (top) and a desulfation reaction (bottom), both of which are pre-emptive detoxification strategies. If both of these fail, the general mercapturic acid pathway (middle) acts on the toxic isothiocyanate derivatives.
Whitefly design by Kimberly Falk.

Many questions remain, of course. For now, we’re really interested in figuring out how pervasive this strategy is: what other insects use it, and what other classes of compounds do they deactivate? We also want to know how much this newly discovered reaction really benefits these insects, and can we somehow use this information to help us control these pests? In a way, that’s the long-term goal of our research – can we get to better know our enemy, and thus design better tools to keep it off our food crops? We’re very excited to see how this will develop over the next years!

Daniel G. Vassão

Project Group Leader, Max Planck Institute for Chemical Ecology

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