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Plant multitrophic interactions are extremely complex, and the underlying mechanisms are not easy to unravel. Using tomato plants as a model system, we demonstrated that a soil fungus, Trichoderma afroharzianum, widely used as a biocontrol agent of plant pathogens, negatively affects the development and survival of the lepidopteran pest Spodoptera littoralis by altering the gut microbiota and its symbiotic contribution to larval nutrition. Our results indicate that insect-plant interactions can be correctly interpreted only at the metaorganism level, focusing on the broad network of interacting holobionts which spans across the soil and the above-ground biosphere. Here, we provide a new functional framework for studying these intricate trophic networks and their ecological relevance.
Abstract
Plants generate energy flows through natural food webs, driven by competition for resources among organisms, which are part of a complex network of multitrophic interactions. Here, we demonstrate that the interaction between tomato plants and a phytophagous insect is driven by a hidden interplay between their respective microbiotas. Tomato plants colonized by the soil fungus Trichoderma afroharzianum, a beneficial microorganism widely used in agriculture as a biocontrol agent, negatively affects the development and survival of the lepidopteran pest Spodoptera littoralis by altering the larval gut microbiota and its nutritional support to the host. Indeed, experiments aimed to restore the functional microbial community in the gut allow a complete rescue. Our results shed light on a novel role played by a soil microorganism in the modulation of plant–insect interaction, setting the stage for a more comprehensive analysis of the impact that biocontrol agents may have on ecological sustainability of agricultural systems.
With ash trees decimated by the emerald ash borer, where do other insects that depend on ash go? A new study shows landscape managers that choosing the right replacements for ash is critical for such ash-reliant native insects, such as Ceratomia undulosa, shown here. (Photo by Joseph Berger, Bugwood.org)
By Andrew Porterfield
Andrew Porterfield
Across the northeastern United States, the ash tree has been heading toward extinction since 2002. That year, the emerald ash borer (Agrilus planipennis), native to northeastern Asia, was first identified in Michigan. Since then, landscape managers, horticulturalists, and entomologists have been looking at alternative plants to support species of Lepidoptera (moths and butterflies) that have evolved to depend on the ash.
But finding the right plant can be challenging, as evidenced in a study published in January in Environmental Entomology, which found that, at least for three species of ash-dependent moths, alternative non-native plants vary significantly in their effects on the moths’ larval development. The study was led by Grace Horne, as part of her undergraduate thesis at Colby College in Maine, in collaboration with researchers at The Caterpillar Lab in New Hampshire and the Oak Spring Garden Foundation in Virginia. Horne is now a Ph.D. student in entomology at the University of California, Davis.
Grace Horne
Most insect herbivores have evolved to feed on just a small number of plant types. “Compared to many regionally native plants capable of hosting large communities of locally adapted insect herbivores, introduced and invasive plants generally support less biodiverse food webs and host fewer insect populations … than native congeners,” the authors write.
To see how that adaptation could work among ash-dependent insects, Horne and her team tested three types of hawkmoths on native ash. These insects represent just three of nearly 300 arthropods (and 100 lepidopterans) that associate with ash. They also tested their developmental reactions to three alternative plants: lilac (Syringa vulgaris), weeping forsythia (Forsythia suspensa), and European privet (Ligustrum vulgare).
The researchers reared three ash-specialist moth species—Ceratomia undulosa, Sphinx kalmiae, and Sphinx chersis (known as the great ash sphinx)—from hatching to pupa stage. During the summer of 2020 in southern New Hampshire, they raised 154 C. undulosa, 123 S. kalmiae, and 166 S. chersis caterpillars on the host plants in a laboratory. To confirm their laboratory results, the researchers also placed six C. undulosa caterpillars on field trees. They also conducted field surveys along suburban roads of alternative host plants, identifying caterpillar species on those trees.
Larval growth for all three species varied greatly by host plant. “Perhaps the biggest surprise for us was just how variable the responses were,” Horne says. “For example, Sphinx kalmiae did quite well on lilac, but Sphinx chersis perished entirely on the same plant. We expected that these congeners might have similar tolerances of the non-native plants, but this was not the case.”
Specifically, caterpillars raised on non-native plants took longer to reach pupation than those raised on ash. Ceratomia undulosa and Sphinx chersis showed higher mortality rates on non-native plants than on native ash. In addition, despite normal caterpillar growth, most pupae of all three species reared on privet exhibited malformed wing buds and were probably not viable. “This malformation … was another major surprise,” Horne says. “We attributed this to some sort of nutrient deficiency, but further work will have to be done to elucidate the specific mechanism causing this deformity.”
Sphinx kalmiae is one of the three ash-specialist moth species included in the study, shown here on privet (Ligustrum vulgare) under ultraviolet light during a field survey. Grace Horne, lead author on the study, says “Many caterpillars glow under UV light, so they are easy to spot amongst the foliage at night.” (Photo by Grace Horne)
The findings counter anecdotal accounts of success in raising C. undulosa and S. kalmiae on privet, an invasive plant in eastern North America (and especially invasive in the southeastern U.S.). Privet, the authors write, “may constitute an ecological trap for some ash-feeding insects in North America,” but they warn that further verification is needed.
The study underscored the need to continue preserving ash trees but also to remove privet, all in order to support ash-dependent lepidopterans. “The choices made by zoning commissions, city planners, landscape architects, and homeowners determine integral components of food webs, and the size of the native insect community that can be supported is becoming increasingly relevant when making landscaping decisions,” the researchers write.
Andrew Porterfield is a writer, editor, and communications consultant for academic institutions, companies, and nonprofits in the life sciences. He is based in Camarillo, California. Follow him on Twitter at @AMPorterfield or visit his Facebook page.
Soybean virus may give plant-munching bugs a boost in survival
PennState
UNIVERSITY PARK, Pa. — Most viral infections negatively affect an organism’s health, but one plant virus in particular — soybean vein necrosis orthotospovirus, often referred to as SVNV — may actually benefit a type of insect that commonly feeds on soybean plants and can transmit the virus to the plant, causing disease, according to Penn State research.
In a laboratory study, the Penn State College of Agricultural Sciences researchers found that when soybean thrips — small insects ranging from 0.03 to 0.20 inches long — were infected with SVNV, they tended to survive longer and reproduce better than thrips that were not infected.
Asifa Hameed, who led the study while completing her doctoral degree in entomology at Penn State and is now a senior scientist of entomology at Ayub Agricultural Research Institute in Multan, Pakistan, said the findings give key insight into how the virus spreads in plants and affects its insect hosts.
“In addition to prolonging the life of the insects, SVNV infection also shortened the doubling time of soybean thrip populations,” Hameed said.
An ant holds an oak gall containing wasp larvae. Researchers discovered an elaborate relationship among ants, wasps and oak trees. Credit: Andrew Deans, Penn State
When eight-year-old Hugo Deans discovered a handful of BB-sized objects lying near an ant nest beneath a log in his backyard, he thought they were a type of seed. His father, Andrew Deans, professor of entomology at Penn State, however, knew immediately what they were—oak galls, or plant growths triggered by insects. What he didn’t realize right away was that the galls were part of an elaborate relationship among ants, wasps and oak trees, the discovery of which would turn a century of knowledge about plant-insect interactions on its head.
Looking back, Hugo, now 10, says that he “thought they were seeds, and I felt excited because I didn’t know ants collected seeds. I always thought ants would eat food scraps and stuff around the house. Then I got more excited when [my dad] told me they were galls, because [my dad] was so excited. I was surprised that ants would collect galls because why would they do that?”
According to Andrew Deans, who is also the director of Penn State’s Frost Entomological Museum, many plant-insect interactions are well documented. For example, most “cynipid” wasp species have long been known to induce oak trees to produce protective galls—or growths—around their larvae to ensure the safety of their developing offspring. Additionally, certain plants—including bloodroot (Sanguinaria canadensis), a wildflower native to North America—produce edible appendages, called elaiosomes, on their seeds to attract ants, which then disperse the seeds by carrying them back to their nests. This latter example is referred to as “myrmecochory”—or seed dispersal by ants.
“In myrmecochory, ants get a little bit of nutrition when they eat the elaiosomes, and the plants get their seeds dispersed to an enemy-free space,” Deans explains. “The phenomenon was first documented over 100 years ago and is commonly taught to biology students as an example of a plant-insect interaction.”
The team’s new research—initiated by Hugo’s discovery of galls lying near an ant nest—revealed a much more complex type of myrmecochory, one that combined the wasp-oak gall interaction with the edible appendage-ant interaction.
“First, we observed that, while these galls normally contain a fleshy pale-pink ‘cap,’ the galls near the ant nest did not have these caps, suggesting that maybe they were eaten by the ants,” says Deans. “Ultimately, this led us to discover that gall wasps are manipulating oaks to produce galls, and then taking another step and manipulating ants to retrieve the galls to their nests, where the wasp larvae may be protected from gall predators or receive other benefits. This multi-layered interaction is mind blowing; it’s almost hard to wrap your mind around it.”
The team’s findings published in the journal American Naturalist.
https://www.youtube.com/embed/5z4lz8lX-uA?color=whiteResearchers discovered that not only do gall wasps manipulate oaks to produce galls, but they also manipulate ants to retrieve the galls to their nests, where the wasp larvae may be protected from gall predators or receive other benefits. Credit: Michael Tribone
Investigating the interaction
To better understand the interaction, the researchers conducted a series of field and laboratory experiments. First, to determine if, like eliaosomes, the oak gall caps—which the researchers named kapéllos (Greek for “cap”)—were indeed edible and attractive to ants, the team directly observed oak galls in ant colonies in the wild in Western New York and central Pennsylvania. Additionally, they set up video cameras to capture additional animal/gall interactions. In both locations, they saw ants transporting galls to their nests. Within the nests, all the edible caps were removed, while the galls themselves remained intact.
In a second set of experiments to determine if kapéllos functioned similarly to elaiosomes, the researchers investigated ant preference for oak galls vs. bloodroot seeds. They set up seed/gall bait stations and observed that ants removed the same number of seeds and galls, suggesting no difference in ant preference.
Next, the scientists conducted a laboratory experiment to document whether ants collected galls because of their nutritious kapéllos. They set up three petri-dish treatments—containing entire galls, gall bodies with kapéllos removed or kapéllos with gall bodies removed—along with a control dish containing a different type of gall that did not have an edible appendage. They introduced ants to the petri dishes. They found that ant interest did not differ between the control galls and the kapéllo-free treatment galls, both of which lacked edible components. By contrast, ant interest was greater for galls with intact kapéllos and for kapéllos alone than for control galls.
“We showed that galls with caps were far more attractive to ants than galls without caps and that the caps by themselves were also attractive to the ants,” says John Tooker, professor of entomology. “This suggested that the caps must have evolved as a way to entice ants.”
Finally, the team asked, “What’s in kapéllos that make them so attractive to ants?” According to Tooker, the chemistry of elaiosomes is well studied and known to contain nutritious fatty acids. Therefore, the team compared the chemical compositions of kapéllos to elaiosomes and found that kapéllos, too, contained healthful fatty acids.
“The fatty acids that are abundant in gall caps and eliosomes seem to be mimicking dead insects,” says Tooker. “Ants are scavengers that are out trying to find and grab anything that’s suitable to bring back to their colony, so it’s not an accident that the gall caps and the elaiosomes both have fatty acids typical of dead insects.”
The last, and according to the researchers, most intriguing, question the team pursued was, “Which came first in evolutionary time? The elaiosome interaction or the gall interaction?”
“Given that myrmecochory was described more than a century ago and has been well-researched and taught in schools, one might assume that the elaiosome interaction came first, but that assumption may be wrong for several reasons,” says Robert J. Warren II, professor of biology, SUNY Buffalo State.
One reason, he explained, is that myrmecochorous plants, like bloodroots, comprise only a very small percentage of all plant species and, therefore, may not contribute enough food resources to drive natural selection in ants. Oak galls, however, are widely abundant. In fact, says Warren, they were once so abundant that they were regularly used to fatten livestock.
“If these galls were so abundant and evolved this tactic of growing this cap thousands of years ago, that could have been a strong driver of natural selection in ants,” says Warren. “It could be that ants were long used to picking up galls with caps, and then when spring wildflowers began to produce seeds that happened to have an edible appendage, ants were already predisposed to picking up things with a fatty acid appendage.”
Deans noted that the team recently received a grant to conduct phylogenetic work to further investigate which of these interactions came first in evolutionary time.
“Understanding how these interactions evolved and how they work helps to untangle just a little bit more of the complexity of life on Earth,” he says.
On what it felt like to contribute to such an important discovery, Hugo says “I bet other kids have made similar discoveries but never knew how important they might be. I feel really happy and proud to know I was part of an important scientific discovery. It’s weird to think just some ants collecting what I thought were seeds was actually an important scientific breakthrough.”
When asked if he wants to be an entomologist like his dad when he grows up, given that he’s already made his first scientific discovery, Hugo says “not really. I want to be different … unique … when I grow up.”
More information: Robert J. Warren et al, Oak Galls Exhibit Ant Dispersal Convergent with Myrmecochorous Seeds, The American Naturalist (2022). DOI: 10.1086/720283
by Daniel Fleiter, Max Planck Institute for Biology Tübingen
Leaf Beetle. Credit: Max Planck Institute for Biology Tübingen
Insects are known to rely on microbial protection during immobile developmental stages, such as eggs. But despite the susceptibility of pupae to antagonistic challenges, the role of microbes in ensuring defense during an insect’s metamorphosis remained an open question. Scientists from Germany and Panama have now discovered a novel defensive partnership between a fungus and a leaf beetle. The microbe provides a protective layer around the beetle’s pupae and thus prevents predation. In exchange, the beetle disperses the fungus to its host plant, expanding its range. Now published in Current Biology, the researchers present the results of their study.
Antagonistic interactions are widespread in nature, spurring the evolution of protective traits. In insects, as with other animals, symbioses with beneficial microbes can serve as a source of defensive adaptations.
In their study, biologists from the Max Planck Institute for Biology in Tübingen, the University of Tübingen, both Germany, and the Smithsonian Tropical Research Institute, Panama, discovered a mutualistic partnership between the ascomycete Fusarium oxysporum and Chelymorpha alternans, a leaf beetle: The fungus protects the pupae of the leaf beetle against predators. And in exchange, the beetle disperses the fungus to its host plants and thus contributes to its transmission.
“The fungus retained a metabolic profile that reflects its dual lifestyle,” explains Hassan Salem, Research Group Leader at the Max Planck Institute for Biology and senior author of the study. “Our findings show a mutualism ensuring pupal protection for an herbivorous beetle on the one hand, in exchange for symbiont dissemination and propagation on the other hand,” Salem adds.
A microbial dimension to pupal defense
Previous research across numerous study systems described such partnerships with microbes and insects by examining eggs and other juvenile phases. But for the critical pupal stage, the role of microbial protection remained unexplored. And despite birds and some rodents posing threats to pupae, it is rather the smallest predators and parasitoids such as ground beetles, ants and wasps that pursue them in the wild.
“Structural and chemical adaptations are known to protect pupae against predators and other threats. But microbes appear to also play an important role when we consider how a beetle defends itself during metamorphosis,” comments Aileen Berasategui, an Early Career Researcher at the Cluster of Excellence “Controlling Microbes to Fight Infections” (CMFI), University of Tübingen and the first author of the study.
A protective microbial coat
The research team was driven by the observation that a dense microbial growth appears to form at the onset of pupation. Sequence- and culture-based approaches revealed this growth to be Fusarium oxysporum. To understand and demonstrate their hypothesis of a mutual partnership, the researchers performed field studies in Panama while they explored the survival rates of pupae with and without the protective fungus.
Based on follow up investigation using sweet potato plants, the research team further determined that the leaf beetle carries and distributes the fungus to uninfected plants. As the beetles carry the fungus on legs during the adult stage, this resulted in widespread infection of the plants.
The leaf beetle Chelymorpha alternans belongs to the speciose Cassidinae subfamily of leaf beetles. Many members of this group appear to carry the morphological features of the symbiosis with Fusarium oxysporum, the most conspicuous being the microbial coat that covers pupae. When the symbiosis evolved and how it is maintained are central questions that members of this international team hope to uncover.
More information: Aileen Berasategui et al, The leaf beetle Chelymorpha alternans propagates a plant pathogen in exchange for pupal protection, Current Biology (2022). DOI: 10.1016/j.cub.2022.07.065
Device Sniffs Out the “Smell-fingerprints” of Pestered Plants
USDA ARS
For media inquiries contact: Jan Suszkiw, (202) 734-1176 January 11, 2022
A team of Agricultural Research Service (ARS) and university scientists has developed an electronic nose to sniff out whitefly infestations of tomato plants.
The “E-Nose” works by detecting a specific cocktail of chemicals, called volatile organic compounds (VOCs), that tomato plants release into the air when attacked by whiteflies. In nature, these chemicals put other plants on high alert. Scientists are hoping the E-nose will also warn growers so they can fine-tune their use of whitefly-killing insecticides, biocontrol agents like parasitic wasps or other measures.
According to Heping Zhu, an agricultural engineer with the ARS Application Technology Research Unit in Wooster, Ohio, who co-developed the E-nose with collaborators at The Ohio State and University of Tennessee-Knoxville, whiteflies are top insect pests of U.S. fresh-market tomatoes, which were valued at $721 million in 2020.
Left unchecked, adult whiteflies and their immature nymphs probe the undersides of tomato plant leaves for sap, causing them to turn yellow, curl or drop off. Whitefly feeding can also cause uneven ripening of fruit and transmit viral diseases that weaken the plants further.
Whitefly monitoring typically involves checking for a threshold number of the pests per leaf on a sampling of plants or captured in sticky traps—both a time-consuming process.
Towards that end, the researchers designed a prototype E-nose device about the size of a shoebox that can operate in the greenhouse. According to Zhu, the device mimics the mammalian sense of smell and brain’s ability to recognize certain odors. But instead of a nasal passage, receptor cells and an olfactory bulb, the E-nose uses gas sensors, data acquisition modules and other components.
A key feature of the E-nose is a nerve-like circuitry board that helps convert VOC samples from the air into digital signals. These signals in turn are transmitted to the system’s “brain,” namely, a mathematical algorithm programmed to recognize specific types and concentrations—or “smell-fingerprints”—of VOCs that tomato plants give off when attacked.
In greenhouse tests, the E-nose displayed the VOC fingerprints of such plants as different lines with different colors that rose sharply and steadily to the right of an LED screen. Moreover, the system distinguished the smell-fingerprints of whitefly-infested tomato plants from un-infested ones, as well as plants whose leaves were punctured with pins for comparison.
With additional testing and development, the E-nose could give greenhouse growers another monitoring tool to use in deciding where, when, and how best to tamp down whitefly infestations before they reach economically damaging levels. Besides whiteflies, the E-nose also successfully sniffed out tomato-infesting aphids and insect pests of other greenhouse crops.
“The future E-nose system can be designed as a hand-held device for growers to take samples from individual plants,” Zhu said. “It can also be designed as a computer-controlled cloud networking system which consists of multiple smart sensors placed at different locations in the greenhouse, so the computer can automatically collect samples and monitor infestations 24 hours a day.”
Details of the team’s findings were published in the October 2021 issue of Chemosensors and in the August 2019 issue of Sensors.
The Agricultural Research Service is the U.S. Department of Agriculture’s chief scientific in-house research agency. Daily, ARS focuses on solutions to agricultural problems affecting America. Each dollar invested in agricultural research results in $17 of economic impact.
A cluster of monarch butterflies overwintering in California. Credit: Mark Chappell, UC Riverside
Monarch butterflies and their close relatives thrive on poisonous milkweed, thanks to genetic mutations that block the effects of the plant’s toxins while allowing the poisons to accumulate in the caterpillar or adult insects as deterrents to hungry predators.
Turns out some of those insect-eating predators evolved similar mutations in order to feast on monarchs.
In a study appearing this week in the journal Current Biology, researchers at the University of California, Berkeley, and UC Riverside report monarch-like genetic mutations in the genomes of four organisms that are known to eat monarchs: the black-headed grosbeak, a migratory bird that snacks on the butterflies at their overwintering home in Mexico; the eastern deer mouse, a close relative of the Mexican black-eared deer mouse that feeds on butterflies that fall to the ground; a tiny wasp that parasitizes monarch eggs; and a nematode that parasitizes insect larvae that feed on milkweed.
All four organisms have evolved mutations in one or more copies of a gene for the sodium-potassium pump—the same mutations, in fact, as milkweed butterflies, and ones that the researchers and their collaborators showed two years ago were critical to the monarch’s ability to eat milkweed without succumbing to its toxins.
The toxins are cardiac glycosides that interfere with this pump, which helps enable heartbeats and nerve firing. It’s so important in humans that we use a third of all the energy we generate from food to power the pump. It’s not surprising, then, that when the toxins throw a wrench in the pump, the heart and other organs stop, too. Even horses and humans can die of cardiac arrest if they consume enough of the milkweed toxins, which are still used as an arrow poison by hunter-gatherer groups in Africa. Until recently, small amounts of related chemicals from foxglove were widely used to treat congestive heart failure.
“The toxins move up the food chain from plants—what biologists call the first trophic level—to insect herbivores, the second, and then to predators and parasitoids—a third trophic level,” said evolutionary biologist Noah Whiteman, UC Berkeley professor of integrative biology and of molecular and cell biology. “In response, the predators and parasitoids have evolved resistance to the toxins at the same sites that we discovered were changing in the monarch, and sometimes to the same amino acids. This might be the first time that the same resistance mutations have been found in the third and second trophic levels that evolved in response to the latter feeding on toxic plants. “
“It’s remarkable that convergent evolution occurred at the molecular level in all these animals,” said co-author Simon “Niels” Groen, assistant professor of evolutionary systems biology in UC Riverside’s nematology department and a former UC Berkeley postdoctoral fellow. “Plant toxins caused evolutionary changes across at least three levels of the food chain.”
In places like Mexico where monarch butterflies overwinter by the thousands to millions, the black-headed grosbeak is one of few birds that can eat them without vomiting. Researchers discovered that the bird has evolved similar genetic mutations as those found in the monarch that allow both to handle milkweed toxins, which accumulate in the butterfly and are deterrents to most predators. Credit: Mark Chappell, UC Riverside
Birds do it, wasps do it. Even nematodes do it.
Since the 1980s, biologists have known that monarchs and a few other butterflies, and even some beetles, aphids and other insects, have adapted to feeding on milkweed plants and storing the toxins in their bodies—even through metamorphosis—to deter predators. In the last decade, geneticists tracked down the actual genetic mutations that allowed this, all of which were in the sodium pump and allowed the pump to work, despite the toxins. Whiteman speculated that those animals that eat the butterflies must have evolved resistance mutations as well. But were they the same?
When the genome of the black-headed grosbeak was published last year, Whiteman and Groen immediately looked for and found sodium pump mutations nearly identical to those that evolved in the monarch. The researchers subsequently expanded the study, scanning previously sequenced genomes from other monarch-eating animals, and found similar mutations.
The black-headed grosbeak (Pheucticus melanocephalus), a summer resident of California, migrates to Mexico and is known for gobbling up monarchs at the places where they overwinter in the mountains of Michoacán state. One study found that the black-headed grosbeak and another bird, the black-backed oriole (Icterus abeillei), consumed hundreds of thousands to 1 million monarchs over a single winter.
It was evident from their behavior, however, that the two birds were not equally resistant to the milkweed toxins stored in the butterfly’s body. While the grosbeak would tear off the wings and consume the abdomen whole, the oriole would gut the abdomen after de-winging the butterfly and eat only the insides. The outside, or cuticle, has a higher concentration of cardiac glycoside toxins, as do the wings. Orioles also discarded monarchs with higher levels of cardiac glycosides.
The new study reveals how the grosbeak can tolerate the toxins in the monarch: It has evolved single-nucleotide mutations in its sodium pump genes in two of the same three locations where monarchs evolved mutations that help make them the most resistant organism to the milkweed’s cardiac glycosides. None of the other 150 or so sparrow-related “passerine” birds whose genomes are known has these mutations in both of the most widely expressed copies of the sodium pump gene. The oriole’s genome has yet to be sequenced.
This graphic shows how milkweed toxins move from the plant through monarch caterpillars and butterflies into the black-headed grosbeak that feasts on them. To become resistant to the toxins, the grosbeak evolved mutations in its sodium pump (lower left) that are identical to two of the three mutations the monarch itself developed to make it resistant. Credit: UC Berkeley image by Julie Johnson
“It solves this mystery from 40 years ago where the biology was pretty well worked out, but we just couldn’t go down to the lowest level of organization possible, the genome, to see how grosbeaks are doing this,” Whiteman said. “It looks like, amazingly, they are evolving resistance using the same kind of machinery in the same places in the genetic code as the monarch and the aphids, the bugs and the beetles, that feed on milkweeds, as well.”
The biologists found that the wasp (Trichogramma pretiosum) also has two mutations in the same place as the monarch in the sodium pump gene. The nematode (Steinernema carpocapsae) has changes at all three locations in the sodium pump gene that also evolved in the monarch butterfly, including the one location that confers the most resistance. These nematodes have been found in the soil around milkweed plants in New York and may parasitize the grubs of beetles that feed on milkweed roots and presumably the larvae of other insects, including butterflies.
The fact that the eastern deer mouse (Peromyscus maniculatus)—a close relative of the black-eared deer mouse (P. melanotis), a monarch-feeding specialist—has all three mutations in its most widely expressed copies of the sodium pump gene was already known and not surprising, Whiteman said. The rat and other rodents have mutations in their sodium pump genes that allow them to resist cardiac glycosides and other substances that would be toxic to other mammals.
It’s unclear whether there are additional adaptations that help the black-headed grosbeak and other monarch predators like the black-eared deer mouse deal with the toxins, Groen said. He is planning to explore this question in future studies. Whiteman suspects that other organisms in the food chain that starts with milkweed will be found to have mutations similar to those found in the monarch.
“My guess is, there are other parasitoids out there, and predators that have also evolved resistance mutations that are interacting with monarchs, and it’s just a matter of time before they’re discovered,” he said. “We know that this isn’t the only way to evolve resistance to cardiac glycosides, but it seems to be the predominant way—targeting this particular pump.”
A study on insect pests of pea plants finds that which pest attacks first changes how the plant mounts defenses, how effective those defenses are, and the eventual nutritional quality of the plants. The experiment examined scenarios in which pea plants were first attacked by pea aphid (Acrythosiphon pisum, left) and pea leaf weevil (Sitona lineatus, right). Pea aphid also affects plants by transmitting pea enation mosaic virus. (Aphid photo by Joseph Berger, Bugwood.org; weevil photo by Pest and Diseases Image Library , Bugwood.org)
By Saumik Basu, Ph.D.
The order of arrival and feeding of different insect pests impact a plant’s ability to fight back by altering its defense response and nutritional quality. My colleagues and I have unfolded the complexity of these interactions in our research to understand potential implications in pest control strategies.
The Palouse region of eastern Washington and northern Idaho is home for cultivation of cool-season legumes such as peas, lentils, chickpeas, and fava beans. A piercing-sucking vector herbivore, pea aphid (Acyrthosiphon pisum) and an aphid-borne pathogen, pea enation mosaic virus (PEMV), have long worried farmers in the Palouse with crop yield loss ranging from 30–40 percent and major outbreaks of pea aphids reported every 6–9 years. In addition to the pea aphid-PEMV mediated pathosystem, a more innocuous-seeming, chewing, non-vector herbivore, the pea leaf weevil (Sitona lineatus), takes tiny feeding bites from pea leaves and has also been found to significantly affect plant susceptibility. These organisms co-occur in the Palouse region, and interactions between them can affect plant signaling pathways and nutritional status.
Saumik Basu, Ph.D., is a postdoctoral research associate in the Department of Entomology at Washington State University in Pullman, Washington. (Photo courtesy of Saumik Basu, Ph.D.)
Pea leaf weevil adults overwinter outside of pea fields and migrate into fields in the late spring to lay eggs. After hatching of eggs, larvae burrow into the soil to feed and pupate before adults re-emerge in the summer and continue feeding on peas. First-generation pea leaf weevil adults typically attack plants before arrival of pea aphids and PEMV, but second-generation pea leaf weevils typically attack plants after pea aphid and PEMV have arrived. However, the responses of pea plants based on the number of stressors and their order of attack and the underlying molecular mechanisms that mediate these interactions are largely unknown.
Many studies have already investigated the effects of single pest on plants. But managing multiple pests concurrently is highly challenging. Our recent study published in August in Molecular Ecology is among the few published works that investigate complex plant-mediated interactions of multiple biotic stressors. To better understand plant responses to multiple stressors and to assess how these responses are affected by order of arrival of stressors and food web complexity, we investigated the response of pea plants to various attack sequences from these two pests and PEMV.
In a series of greenhouse experiments performed in collaboration with colleagues at Washington State University and Cornell University, we investigated what happens to pea plants when they face different sequences of pest attacks and virus exposure. We created experiments in which weevils and then pea aphids feasted on pea plants, and we contrasted the results with the reverse attack order. We also included scenarios where some pea plants were infected with PEMV while others remained uninfected. After removing the pests, we let the plants grow, and then we measured the plant’s defense phytohormone levels, expressions of associated defense genes, and nutritional status.
We found that, when pea leaf weevils feast on peas first, it enhances some of the anti-pathogen defense responses of the pea plants, helping them to become more resilient to PEMV infection. But, when the weevilsdine after the aphids, it lowers the anti-pathogen defenses, allowing the virus to spread more easily. In turn, PEMV-infected plants had stronger anti-herbivore defense responses, since they induce production of compounds that interfere with the pest feeding. Further complicating the issue, we also found in this study that, when weevils induced anti-pathogen defense responses, the nutritional quality of pea plants was lowered by decreasing the plant’s available amino acids.
We strongly believe that these complex interactions convey important implications to design sustainable pest- and pathogen-management strategies. If we know beforehand when these interactions are happening, that information will give farmers a best possible remedy to prevent their fields from these attacks by choosing proper timing, using appropriate pest control agents, and controlling the pests during the most susceptible stage of their life cycles. While using broad spectrum insecticides (e.g., pyrethroids) may enhance pest management efficiency against multiple pests in different attack orders, this approach comes with problems associated with non-target insects. Better understanding of the dynamics of pest-attack orders, however, can allow for more effective use of targeted approaches, such as biological control agents (e.g., lady beetles); pesticides that are less harmful to natural enemies, non-target insects, and pollinators; and biofertilizers (e.g., soil mutualistic rhizobia).
This study is a part of our ongoing series of investigations to assess complex interactions among many organisms that a plant may encounter in a food web ecosystem. Our earlier study published in May in Functional Ecology investigated the antagonistic relationship between PEMV and a root-colonizing and nitrogen-fixing bacteria called rhizobia. Our next study in this series looks at the interactions between the pea leaf weevil and soil rhizobia.
These complex relationships of multiple biotic stressors are crucial to understanding how plants respond to these attackers and are critical for developing sustainable management strategies against devastating pests and pathogens to boost crop yield and agroeconomy.
WUR research finds: Plants can prepare for insect attack sequence
Plants are under attack by a variety of insect species. They have defence mechanisms to deal with this, including chemicals or sturdier leaves. It has now been found that, when wild black mustard plants defend themselves against an initial enemy, they already anticipate the need to later fend off other, different enemies. In fact, they even prepare for the most likely sequence of attackers. This research has now been published in the scientific journal Nature Plants.
The article is based on doctoral research carried out by Daan Mertens and Maite Fernandéz de Bobadilla, working in the team headed by Erik Poelman, associate professor in the Laboratory of Entomology at Wageningen University & Research.
“We’re increasingly moving towards sustainable forms of agriculture and horticulture, which includes drastically reducing the use of pesticides,” says Poelman. “For arable farmers, that means having to deal with a greater variety of insects attacking their crops. Plant breeders used to focus on resistance to the most problematic insects, while broad-spectrum pesticides were used to deal with other herbivores. Now we have to change our approach, and in doing so we can learn from wild plant species and how they deal with a diversity of insects.”
This is a substantial change of direction, explains Mertens. “Previously, there would be a focus on breeding plants that deal with a specific insect problem. Now, plant breeding has to create crops that are flexible in their defences and can deal with all kinds of enemies. It’s about moving toward a systems approach.”
Specific reaction for each enemy Plants can never be sure if or when they will be subjected to an attack. Most species resolve this uncertainty by only fully investing in defences (such as the production of defensive chemicals) when they are actually being attacked. This means that, when herbivorous insects are absent, the plants can fully invest their resources (products of photosynthesis such as sugars and starch) into their own growth and reproduction.
“Plants have a fairly specific sense of which insects are attacking them,” says Mertens. “They notice insect attack from the way the cells are damaged, the compounds that are then released, and the characteristics of the insects’ saliva. They can interpret those signals to mount a targeted defence.”
However, the defences targeted at one insect species may not be effective against attack by other insect species.
An added complication is that a plant’s specific reaction to aphids, for example, can reduce its resistance to caterpillars, as plants have a variety of mechanisms to develop different kinds of defences. These mechanisms are triggered by plant hormones that may interact when regulating a defence response.
How do plants defend themselves against multiple attacks from herbivores? (WUR)
Risk management So how can a wild plant, with insects literally swarming around it, still manage to look after itself so well? “They’re prepared for the damaging insects to arrive in a specific sequence,” says Mertens. “Early in the season it might be a particular species of aphid, and later a particular species of caterpillar. They organize their defences and ensure that they can deal with these different insects over time. It seems like a conscious form of risk management, but it has emerged through natural selection. They can handle the most common sequence of events.”
By means of an unusually large experiment, the researchers showed that this is indeed how the plant’s strategy works. They observed the defence mechanism used by black mustard on 90 combinations of insect attacks and linked these results to three years of research into the frequency of the interactions on plants in the wild. Similar tests in the past were limited to perhaps five combinations.
This ambitious approach has resulted in valuable new insights. “We’ve linked our understanding of plant physiology to ecology,” explains Poelman. “The old idea that insects feeding on plant sap trigger a reaction which then diminishes a plant’s potential defence against caterpillars has turned out to be too simple. Our work confirms research on the physiological reactions of the plant against aphids and caterpillars, but also reveals that in many instances the plant does not become more susceptible to insects with a different feeding pattern. The presence of a particular combination or sequence of insects in the wild appears to be a better predictor of resistance than the characteristics of the individual insect species.”
For more information: Wageningen University & Research www.wur.nl
On the island of Madagascar there lives a large moth with a tongue long enough to make Gene Simmons green with envy. Its name? Xanthopan praedicta. Its business? Sucking the pollen out of a very long and skinny orchid.
This moth’s whole history is absurd. Charles Darwin predicted its existence when he first saw the shape of the Angraecum sesquipedale orchid (which apparently prompted him to exclaim, “Good heavens, what insect can suck it?”). About 2 decades later, in 1903, the moth was actually discovered, and ever since, the Malagasy variant has been considered a subspecies of its mainland counterpart, X. morganii. But no longer.
Using a slew of morphological and genetic tests, scientists argue the island moth is substantially different enough from its mainland counterpart to merit its elevation to the species level, the Natural History Museum announced yesterday.
Working with a combination of wild moths and museum specimens, the team reports that DNA barcoding, a technique that can be used to identify organisms by looking at DNA sequence differences in the same gene or genes, shows the moth’s genetics differ by as much as 7.8% in key gene sequences, which actually makes the morganii moths more closely related to a few other mainland subspecies than praedicta.
But what about the tongues? The Malagasy moths take the prize here, with proboscises that measure 6.6 centimeters longer on average, as seen in the picture above. Adding to their legend, the team also reported finding one individual praedicta specimen with a proboscis that measured a whopping 28.5 centimeters when fully stretched, which would constitute “an absolute record” for any moth tongue ever measured. Congratulations!
Cowpea is one of Africa’s most important cash crop, and has been found to detect larvae and reduce feeding damage (Image by Toby Hudson)
A new study has unlocked the hidden ways in which important cash crops such as cowpea (Vigna unguiculata) tackle localised pest invasion and damage using natural defence mechanisms. Insights such as these are key for the future protection of our global agricultural production in the light of increasing pest outbreaks and crop damage.
Scientists have published research in which they have found an immune receptor in cowpea cells that can detect the saliva of caterpillars feeding on their leaves, causing a series of natural defence responses such as the release of chemicals that limit the rapid growth capabilities of the larvae. An example of such a defence mechanism is found when the bean pod borer (Maruca vitrata) larvae feed on cowpea, causing the release of a pheromone which attracts parasites to then feed on the larvae.
“Despite chemical controls, crop yield losses to pests and diseases generally range from 20 to 30 percent worldwide. Yet many varieties are naturally resistant or immune to specific pests,” explains biologist Adam Steinbrenner from the University of Washington. “Our findings are the first to identify an immune recognition mechanism that sounds the alarm against chewing insects.”
As of yet, very little is known about how plants are able to identify and combat pest threats, however this new study which is built on previous research by the same team has found that certain peptides known as inceptins are found in the saliva of the larval pests such as the beet armyworm (Spodoptera exigua) larvae – which is one of greatest threats to cowpea crops across Asia and North America. The beet armyworm is native to Southeast Asia and has colonised parts of America since the late 1800s. This pest is extremely damaging to crop foliage, with larvae being found to consume more than other major crop pests such as the diamondback moth (Plutella xylostella).
Beet armyworm larvae (Image by Russ Ottens, University of Georgia)
The inceptins are the spark that causes the cowpea defence mechanisms against feeding pests, ultimately resulting in larval damage or death. The research found inceptin receptors (INRs) on cowpea plant calls specifically. Unfortunately, there are limited ways to study cowpea crops, resulting in the team having to use tobacco plants to test how the INRs work in practice.
By inserting the gene for INR production into tobacco crops, the team were able to test what would happen in the presence of armyworm larvae. It was found that the INRs were triggered in response to the presence of certain protein fragments in the saliva of feeding caterpillars, as well as in response to direct feeding damage on leaves. The fragments of saliva protein that caused the defence response was found to be pieces of cowpea proteins that were broken down by the caterpillar during feeding. In the tobacco test crops, the presence of these proteins triggered the release of a plant hormone that is known to occur when under threat, resulting in the suppression of insect growth.
“Like many plant immune receptors, this receptor is encoded only by certain plant species but can be transferred across families to confer new signalling and defence functions,” the author wrote.
With the genomic techniques used in this study, the team were able to discover hidden information about plants natural defence mechanisms against pest damage. With the increasing global demand for food as well as more prevalent agricultural pest outbreaks, such studies must be conducted on numerous important food crops and a variety of environmental climates so we can better prepare for and mitigate future threats.
If you would like to read more on this subject, please see the links below:
For more information:
Global Plant Protection News 