The polyvalent sequestration ability of an economically important beetle.

Many specialized herbivorous insects sequester single classes of toxic secondary metabolites from their host plants as protection against natural enemies. If and how herbivores can use multiple classes of plant toxins across the large chemical diversity of plants for self-protection is unknown. We show that the polyphagous adults of the beetle Diabrotica virgifera are capable of selectively accumulating benzoxazinoids, cucurbitacins, and glucosinolates but not cyanogenic glycosides. Female beetles transfer the sequestered defense metabolites into their eggs, protecting them against generalist predators. Eggs containing a mixture of toxins are better protected than eggs with individual toxins. This work shows how herbivores can exploit plant chemical diversity to their own benefit as a novel adaptive mechanism that contributes to the structuring of multitrophic interaction networks.

Plant-to-plant defence induction in cotton is mediated by delayed release of volatiles upon herbivory.

Caterpillar feeding immediately triggers the release of volatile compounds stored in the leaves of cotton plants. Additionally, after 1 d of herbivory, the leaves release other newly synthesised volatiles. We investigated whether these volatiles affect chemical defences in neighbouring plants and whether such temporal shifts in emissions matter for signalling between plants. Undamaged receiver plants were exposed to volatiles from plants infested with Spodoptera caterpillars. For receiver plants, we measured changes in defence-related traits such as volatile emissions, secondary metabolites, phytohormones, gene expression, and caterpillar feeding preference. Then, we compared the effects of volatiles emitted before and after 24 h of damage on neighbouring plant defences. Genes that were upregulated in receiver plants following exposure to volatiles from damaged plants were the same as those activated directly by herbivory on a plant. Only volatiles emitted after 24 h of damage, including newly produced volatiles, were found to increase phytohormone levels, upregulate defence genes, and enhance resistance to caterpillars. These results indicate that the defence induction by volatiles is a specific response to de novo synthesised volatiles, suggesting that these compounds are honest signals of herbivore attack. These findings point to an adaptive origin of airborne signalling between plants.

Field evidence for the role of plant volatiles induced by caterpillar oral secretion in prey localization by predatory social wasps.

One assumed function of herbivore-induced plant volatiles (HIPVs) is to attract natural enemies of the inducing herbivores. Field evidence for this is scarce. In addition, the assumption that elicitors in oral secretions that trigger the volatile emissions are essential for the attraction of natural enemies has not yet been demonstrated under field conditions. After observing predatory social wasps removing caterpillars from maize plants, we hypothesized that these wasps use HIPVs to locate their prey. To test this, we conducted an experiment that simultaneously explored the importance of caterpillar oral secretions in the interaction. Spodoptera caterpillars pinned onto mechanically damaged plants treated with oral secretion were more likely to be attacked by wasps compared with caterpillars on plants that were only mechanically wounded. Both of the latter treatments were considerably more attractive than plants only treated with oral secretion or left untreated. Subsequent analyses of headspace volatiles confirmed differences in emitted volatiles that likely account for the differential predation across treatments. These findings highlight the importance of HIPVs in prey localization by social wasps, hitherto underappreciated potential biocontrol agents and provide evidence for the role that elicitors play in inducing attractive odour blends.

The Threat of the Fall Armyworm to Asian Rice Production Is Amplified by the Brown Planthopper.

The recent invasion of the fall armyworm (FAW) into Asia not only has had a major impact on maize yield but is feared to also pose a risk to rice production. We hypothesized that the brown planthopper (BPH) may aggravate this risk based on a recently discovered mutualism between the planthopper and the rice striped stem borer. Here we show that BPH may indeed facilitate a shift of FAW to rice. FAW females were found to strongly prefer to oviposit on BPH-infested rice plants, which emitted significantly elevated levels of five volatile compounds. A synthetic mixture of these compounds had a potent stimulatory effect on ovipositing females. Although FAW caterpillars exhibited relatively poor growth on both uninfested and BPH-infested rice, a considerable portion completed their development on young plants. Moreover, FAW were found to readily pupate and survive in exceedingly moist soils typical for rice cultivation, further highlighting FAW's potential to switch to rice. We conclude that BPH, by changing the bouquet of volatiles emitted by rice plants, may greatly facilitate this switch. These findings, together with a current increase of nonflooded upland rice in Asia, warrant careful monitoring and specific control measures against FAW to safeguard Asian rice production.

Single-cell transcriptome landscape elucidates the cellular and developmental responses to tomato chlorosis virus infection in tomato leaf.

Plant viral diseases compromise the growth and yield of the crop globally, and they tend to be more serious under extreme temperatures and drought climate changes. Currently, regulatory dynamics during plant development and in response to virus infection at the plant cell level remain largely unknown. In this study, single-cell RNA sequencing on 23 226 individual cells from healthy and tomato chlorosis virus-infected leaves was established. The specific expression and epigenetic landscape of each cell type during the viral infection stage were depicted. Notably, the mesophyll cells showed a rapid function transition in virus-infected leaves, which is consistent with the pathological changes such as thinner leaves and decreased chloroplast lamella in virus-infected samples. Interestingly, the F-box protein SKIP2 was identified to play a pivotal role in chlorophyll maintenance during virus infection in tomato plants. Knockout of the SlSKIP2 showed a greener leaf state before and after virus infection. Moreover, we further demonstrated that SlSKIP2 was located in the cytomembrane and nucleus and directly regulated by ERF4. In conclusion, with detailed insights into the plant responses to viral infections at the cellular level, our study provides a genetic framework and gene reference in plant-virus interaction and breeding in the future research.

Entomopathogenic nematodes as an effective and sustainable alternative to control the fall armyworm in Africa.

The recent invasion of the fall armyworm (FAW), a voracious pest, into Africa and Asia has resulted in unprecedented increases in insecticide applications, especially in maize cultivation. The health and environmental hazards posed by these chemicals have prompted a call for alternative control practices. Entomopathogenic nematodes are highly lethal to the FAWs, but their application aboveground has been challenging. In this study, we report on season-long field trials with an innocuous biodegradable gel made from carboxymethyl cellulose containing local nematodes that we specifically developed to target the FAW. In several Rwandan maize fields with distinct climatic conditions and natural infestation rates, we compared armyworm presence and damage in control plots and plots that were treated with either our nematode gel formulation, a commercial liquid nematode formulation, or the commonly used contact insecticide cypermethrin. The treatments were applied to the whorl of each plant, which was repeated three to four times, at 2-week intervals, starting when the plants were still seedlings. Although all three treatments reduced leaf damage, only the gel formulation decreased caterpillar infestation by about 50% and yielded an additional ton of maize per hectare compared with untreated plots. Importantly, we believe that the use of nematodes can be cost-effective, since we used nematode doses across the whole season that were at least 3-fold lower than their normal application against belowground pests. The overall results imply that precisely formulated and easy-to-apply nematodes can be a highly effective, affordable, and sustainable alternative to insecticides for FAW control.

Two horizontally acquired bacterial genes steer the exceptionally efficient and flexible nitrogenous waste cycling in whiteflies.

Nitrogen is an essential element for all life on earth. Nitrogen metabolism, including excretion, is essential for growth, development, and survival of plants and animals alike. Several nitrogen metabolic processes have been described, but the underlying molecular mechanisms are unclear. Here, we reveal a unique process of nitrogen metabolism in the whitefly Bemisia tabaci, a global pest. We show that it has acquired two bacterial uricolytic enzyme genes, B. tabaci urea carboxylase (BtUCA) and B. tabaci allophanate hydrolase (BtAtzF), through horizontal gene transfer. These genes operate in conjunction to not only coordinate an efficient way of metabolizing nitrogenous waste but also control B. tabaci's exceptionally flexible nitrogen recycling capacity. Its efficient nitrogen processing explains how this important pest can feed on a vast spectrum of plants. This finding provides insight into how the hijacking of microbial genes has allowed whiteflies to develop a highly economic and stable nitrogen metabolism network and offers clues for pest management strategies.

Rickettsia transmission from whitefly to plants benefits herbivore insects but is detrimental to fungal and viral pathogens.

Bacterial endosymbionts play important roles in the life histories of herbivorous insects by impacting their development, survival, reproduction, and stress tolerance. How endosymbionts may affect the interactions between plants and insect herbivores is still largely unclear. Here, we show that endosymbiotic Rickettsia belli can provide mutual benefits also outside of their hosts when the sap-sucking whitefly Bemisia tabaci transmits them to plants. This transmission facilitates the spread of Rickettsia but is shown to also enhance the performance of the whitefly and co-infesting caterpillars. In contrast, Rickettsia infection enhanced plant resistance to several pathogens. Inside the plants, Rickettsia triggers the expression of salicylic acid-related genes and the two pathogen-resistance genes TGA 2.1 and VRP, whereas they repressed genes of the jasmonic acid pathway. Performance experiments using wild type and mutant tomato plants confirmed that Rickettsia enhances the plants' suitability for insect herbivores but makes them more resistant to fungal and viral pathogens. Our results imply that endosymbiotic Rickettsia of phloem-feeding insects affects plant defenses in a manner that facilitates their spread and transmission. This novel insight into how insects can exploit endosymbionts to manipulate plant defenses also opens possibilities to interfere with their ability to do so as a crop protection strategy. IMPORTANCE: Most insects are associated with symbiotic bacteria in nature. These symbionts play important roles in the life histories of herbivorous insects by impacting their development, survival, reproduction as well as stress tolerance. Rickettsia is one important symbiont to the agricultural pest whitefly Bemisia tabaci. Here, for the first time, we revealed that the persistence of Rickettsia symbionts in tomato leaves significantly changed the defense pattern of tomato plants. These changes benefit both sap-feeding and leaf-chewing herbivore insects, such as increasing the fecundity of whitefly adults, enhancing the growth and development of the noctuid Spodoptera litura, but reducing the pathogenicity of Verticillium fungi and TYLCV virus to tomato plants distinctively. Our study unraveled a new horizon for the multiple interaction theories among plant-insect-bacterial symbionts.

A Horizontally Transferred Plant Fatty Acid Desaturase Gene Steers Whitefly Reproduction.

Polyunsaturated fatty acids (PUFAs) are essential nutrients for all living organisms. PUFA synthesis is mediated by Δ12 desaturases in plants and microorganisms, whereas animals usually obtain PUFAs through their diet. The whitefly Bemisia tabaci is an extremely polyphagous agricultural pest that feeds on phloem sap of many plants that do not always provide them with sufficient PUFAs. Here, a plant-derived Δ12 desaturase gene family BtFAD2 is characterized in B. tabaci and it shows that the BtFAD2-9 gene enables the pest to synthesize PUFAs, thereby significantly enhancing its fecundity. The role of BtFAD2-9 in reproduction is further confirmed by transferring the gene to Drosophila melanogaster, which also increases the fruit fly's reproduction. These findings reveal an extraordinary evolutionary scenario whereby a phytophagous insect acquired a family of plant genes that enables it to synthesize essential nutrients, thereby lessening its nutritional dependency and allowing it to feed and reproduce on many host plants.

Cowpea volatiles induced by beet armyworm or fall armyworm differentially prime maize plants.

Exposure to herbivore-induced plant volatiles (HIPVs) is known to enhance the defense responses in plants. This so-called priming effect has only been marginally studied in intercropping systems. We tested whether HIPVs from cowpea, which often serves as an intercrop alongside maize, can prime herbivore-induced volatile emissions in maize. Conventional volatile collection assays and real-time mass spectrometry revealed that maize plants that were exposed to HIPVs from cowpea infested with Spodoptera exigua caterpillars emitted more than control plants when they themselves were subsequently damaged by the same pest. The enhanced emission was only evident on the first day after infestation. Maize plants that were exposed to HIPVs from cowpea infested by S. frugiperda larvae showed no priming effect and released considerably less upon S. frugiperda infestation than upon S. exigua infestation. The latter may be explained by the fact that S. frugiperda is particularly well adapted to feed on maize and is known to suppress maize HIPV emissions. Our results imply that HIPVs from cowpea, depending on the inducing insect herbivore, may strongly prime maize plants. This deserves further investigation, also in other intercropping systems, as it can have important consequences for tritrophic interactions and crop protection.

Adaptive changes in pheromone production and release under rearing conditions in stink bugs.

BACKGROUND: Healthy cultures of arthropods are important for pest management programs (e.g. biocontrol). Little is known about how rearing conditions may affect pheromonal interactions. We investigated how rearing histories and densities affect pheromone emission/production in two stink bug species (Hemiptera: Heteroptera), the predatory bug Arma custos, a biocontrol agent, and the bean bug Riptortus pedestris, a pest on legume crops. RESULTS: Nymphs from newly established laboratory colonies of both species produced higher amounts of the defense (dispersal) compound, 4-oxo-(E)-hexenal (OHE), in the presence of conspecific nymphs. Also, when two or more A. custos males were placed together, the dorsal abdominal glands (DAGs) ceased to release aggregation pheromone, whereas the metathoracic glands (MTGs) increased the emission of defensive odors. These changes resulted from exposure to conspecific pheromone odors, as confirmed by exposing bugs to pheromone standards. Hence, pheromone emissions in these stink bugs are readily changed in response to the odors of conspecifics, which may become a problem after long-term rearing. Indeed, an old laboratory colony of A. custos (~30 generations) exhibited less-developed DAGs and reduced pheromone production. Instead, males released significantly more defensive odors from the enlarged MTGs. Furthermore, long-term rearing conditions appeared to favor nymphs that were able to share space with conspecifics by releasing less OHE, which has not yet occurred in the new laboratory colonies. CONCLUSION: Rearing density affects pheromone release in newly established laboratory colonies of stink bug species, whereas long-term rearing results in new pheromonal compositions coinciding with adaptive changes in gland development. © 2023 Society of Chemical Industry.

Aphid and caterpillar feeding drive similar patterns of induced defences and resistance to subsequent herbivory in wild cotton.

MAIN CONCLUSION: Our results indicate caterpillars and aphids cause similar levels of induced defences and resistance against caterpillars in wild cotton plants. These symmetrical effects are not consistent with patterns predicted by plant defensive signaling crosstalk and call for further work addressing the biochemical mechanisms underpinning these results. Plant-induced responses to attack often mediate interactions between different species of insect herbivores. These effects are predicted to be contingent on the herbivore's feeding guild, whereby prior feeding by insects should negatively impact subsequent feeding by insects of the same guild (induced resistance) but may positively influence insects of a different guild (induced susceptibility) due to interfering crosstalk between plant biochemical pathways specific to each feeding guild. We compared the effects of prior feeding by leaf-chewing caterpillars (Spodoptera frugiperda) vs. sap-sucking aphids (Aphis gossypii) on induced defences in wild cotton (Gossypium hirsutum) and the consequences of these attacks on subsequently feeding caterpillars (S. frugiperda). To this end, we conducted a greenhouse experiment where cotton plants were either left undamaged or first exposed to caterpillar or aphid feeding, and we subsequently placed caterpillars on the plants to assess their performance. We also collected leaves to assess the induction of chemical defences in response to herbivory. We found that prior feeding by both aphids and caterpillars resulted in reductions in consumed leaf area, caterpillar mass gain, and caterpillar survival compared with control plants. Concomitantly, prior aphid and caterpillar herbivory caused similar increases in phenolic compounds (flavonoids and hydroxycinnamic acids) and defensive terpenoids (hemigossypolone) compared with control plants. Overall, these findings indicate that these insects confer a similar mode and level of induced resistance in wild cotton plants, calling for further work addressing the biochemical mechanisms underpinning these effects.

Mealybug salivary microbes inhibit induced plant defenses.

BACKGROUND: Phenacoccus solenopsis is a polyphagous invasive mealybug that caused serious damage to crops worldwide. Phloem-sucking hemipterans are known to carry symbiotic microbes in their saliva. However, the role of salivary bacteria of P. solenopsis in modulating plant defenses remains limited. Exploring the impact of salivary bacteria on plant defense responses will contribute to the development of new targets for efficient control of invasive mealybugs. RESULTS: Salivary bacteria of the invasive mealybug P. solenopsis can suppress herbivore-induced plant defenses and thus enhance mealybug fitness. Mealybugs treated with an antibiotic showed decreased weight gain, fecundity and survival. Untreated mealybugs suppressed jasmonic acid (JA)-regulated defenses but activated salicylic acid (SA)-regulated defenses in cotton plants. In contrast, antibiotic-treated mealybugs triggered JA-responsive gene expression and JA accumulation, and showed shortened phloem ingestion. Reinoculating antibiotic-treated mealybugs with Enterobacteriaceae or Stenotrophomonas cultivated from mealybug saliva promoted phloem ingestion and fecundity, and restored the ability of mealybugs to suppress plant defenses. Fluorescence in situ hybridization visualization revealed that Enterobacteriaceae and Stenotrophomonas colonize salivary glands and are secreted into the mesophyll cells and phloem vessels. Exogenous application of the bacterial isolates to plant leaves inhibited JA-responsive gene expression and activated SA-responsive gene expression. CONCLUSION: Our findings imply that symbiotic bacteria in the saliva of the mealybug play an important role in manipulating herbivore-induced plant defenses, enabling this important pest to evade induced plant defenses and promoting its performance and destructive effects on crops. © 2023 Society of Chemical Industry.

Soil salinization disrupts plant-plant signaling effects on extra-floral nectar induction in wild cotton.

Plant-plant interactions via volatile organic compounds (VOCs) have received much attention, but how abiotic stresses affect these interactions is poorly understood. We tested the effect of VOCs exposure from damaged conspecifics on the production of extra-floral nectar (EFN) in wild cotton plants (Gossypium hirsutum), a coastal species in northern Yucatan (Mexico), and whether soil salinization affected these responses. We placed plants in mesh cages, and within each cage assigned plants as emitters or receivers. We exposed emitters to either ambient or augmented soil salinity to simulate a salinity shock, and within each group subjected half of the emitters to no damage or artificial leaf damage with caterpillar regurgitant. Damage increased the emission of sesquiterpenes and aromatic compounds under ambient but not under augmented salinity. Correspondingly, exposure to VOCs from damaged emitters had effect on receiver EFN induction, but this effect was contingent on salinization. Receivers produced more EFN in response to damage after being exposed to VOCs from damaged emitters when the latter were grown under ambient salinity, but not when they were subjected to salinization. These results suggest complex effects of abiotic factors on VOC-mediated plant interactions.

Sequestration of cucurbitacins from cucumber plants by Diabrotica balteata larvae provides little protection against biological control agents.

Cucurbitaceae plants produce cucurbitacins, bitter triterpenoids, to protect themselves against various insects and pathogens. Adult banded cucumber beetles (Diabrotica balteata), a common pest of maize and cucurbits, sequester cucurbitacins, presumably as a defensive mechanism against their natural enemies, which might reduce the efficacy of biological control agents. Whether the larvae also sequester and are protected by cucurbitacins is unclear. We profiled cucurbitacin levels in four varieties of cucumber, Cucumis sativus, and in larvae fed on these varieties. Then, we evaluated larval growth and resistance against common biocontrol organisms including insect predators, entomopathogenic nematodes, fungi and bacteria. We found considerable qualitative and quantitative differences in the cucurbitacin levels of the four cucumber varieties. While two varieties were fully impaired in their production, the other two accumulated high levels of cucurbitacins. We also observed that D. balteata larvae sequester and metabolize cucurbitacins, and although the larvae fed extensively on both belowground and aboveground tissues, the sequestered cucurbitacins were mainly derived from belowground tissues. Cucurbitacins had no detrimental effects on larval performance and, surprisingly, did not provide protection against any of the natural enemies evaluated. Our results show that D. balteata larvae can indeed sequester and transform cucurbitacins, but sequestered cucurbitacins do not impact the biocontrol potential of common natural enemies used in biocontrol. Hence, this plant trait should be conserved in plant breeding programs, as it has been demonstrated in previous studies that it can provide protection against plant pathogens and generalist insects. Supplementary Information: The online version contains supplementary material available at 10.1007/s10340-022-01568-3.

Experimental Growth Conditions affect Direct and Indirect Defences in two Cotton Species.

Cotton has been used as a model plant to study direct and indirect plant defence against herbivorous insects. However, the plant growing conditions could have an important effect on the outcome of such plant defence studies. We examined how common experimental growth conditions influence constitutive and inducible defences in two species of cotton, Gossypium hirsutum and G. herbaceum. We induced plants by applying caterpillar regurgitant to mechanical wounds to compare the induction levels between plants of both species grown in greenhouse or phytotron conditions. For this we measured defence metabolites (gossypol and heliocides) and performance of Spodoptera frugiperda caterpillars on different leaves, the emission of plant volatiles, and their attractiveness to parasitic wasps. Induction increased the levels of defence metabolites, which in turn decreased the performance of S. frugiperda larvae. Constitutive and induced defence levels were the highest in plants grown in the phytotron (compared to greenhouse plants), G. hirsutum and young leaves. Defence induction was more pronounced in plants grown in the phytotron and in young leaves. Also, the differences between growing conditions were more evident for metabolites in the youngest leaves, indicating an interaction with plant ontogeny. The composition of emitted volatiles was different between plants from the two growth conditions, with greenhouse-grown plants showing more variation than phytotron-grown plants. Also, G. hirsutum released higher amounts of volatiles and attracted more parasitic wasps than G. herbaceum. Overall, these results highlight the importance of experimental abiotic factors in plant defence induction and ontogeny of defences. We therefore suggest careful consideration in selecting the appropriate experimental growing conditions for studies on plant defences.

Xenorhabdus bovienii subsp. africana subsp. nov., isolated from Steinernema africanum entomopathogenic nematodes.

Four Gram-negative bacterial strains isolated from Steinernema africanum entomopathogenic nematodes were biochemically and molecularly characterized to determine their taxonomic position. Results of 16S rRNA gene sequencing indicated that they belong to the class Gammaproteobacteria, family Morganellaceae, genus Xenorhabdus, and that they are conspecific. The average 16S rRNA gene sequence similarity between the newly isolated strains and the type strain of its more closely related species, Xenorhabdus bovienii T228T, is 99.4 %. We therefore selected only one of them, XENO-1T, for further molecular characterization using whole genome-based phylogenetic reconstructions and sequence comparisons. Phylogenetic reconstructions show that XENO-1T is closely related to the type strain of X. bovienii, T228T, and to several other strains that are thought to belong to this species. To clarify their taxonomic identities, we calculated average nucleotide identity (ANI) and digital DNA-DNA hybridization (dDDH) values. We observed that the ANI and dDDH values between XENO-1T and X. bovienii T228T are 96.3 and 71.2 %, respectively, suggesting that XENO-1T represents a novel subspecies within the X. bovienii species. Noteworthy, the dDDH values between XENO-1T and several other X. bovienii strains are between 68.7 and 70.9 % and ANI values are between 95.8 and 96.4 %, which could be interpreted, in some instances, as that XENO-1T represents a new species. Considering that for taxonomic description the genomic sequences of the type strains are compared, and to avoid future taxonomic conflicts, we therefore propose to assign XENO-1T to a new subspecies within X. bovienii. ANI and dDDH values between XENO-1T and any other of the species with validly published names of the genus are lower than 96 and 70 %, respectively, supporting its novel status. Biochemical tests and in silico genomic comparisons show that XENO-1T exhibit a unique physiological profile that differs from all the Xenorhabdus species with validly published names and from their more closely related taxa. Based on this, we propose that strain XENO-1T represents a new subspecies within the X. bovienii species, for which we propose the name X. bovienii subsp. africana subsp. nov, with XENO-1T (=CCM 9244T=CCOS 2015T) as the type strain.

Can herbivores sharing the same host plant be mutualists?

Resource partitioning is considered to be a prerequisite for coexisting species to evolve from competition to mutualism. This is uniquely different for two major pest insects of rice. These herbivores preferentially opt to coinfest the same host plants, and through plant-mediated mechanisms, cooperatively utilize these plants in a mutualistic manner.

The N-terminal subunit of vitellogenin in planthopper eggs and saliva acts as a reliable elicitor that induces defenses in rice.

Vitellogenins (Vgs) are critical for the development and fecundity of insects. As such, these essential proteins can be used by plants to reliably sense the presence of insects. We addressed this with a combination of molecular and chemical analyses, genetic transformation, bioactivity tests, and insect performance assays. The small N-terminal subunit of Vgs of the planthopper Nilaparvata lugens (NlVgN) was found to trigger strong defense responses in rice when it enters the plants during feeding or oviposition by the insect. The defenses induced by NlVgN not only decreased the hatching rate of N. lugens eggs, but also induced volatile emissions in plants, which rendered them attractive to a common egg parasitoid. VgN of other planthoppers triggered the same defenses in rice. We further show that VgN deposited during planthopper feeding compared with during oviposition induces a somewhat different response, probably to target the appropriate developmental stage of the insect. We also confirm that NlVgN is essential for planthopper growth, development, and fecundity. This study demonstrates that VgN in planthopper eggs and saliva acts as a reliable and unavoidable elicitor of plant defenses. Its importance for insect performance precludes evolutionary adaptions to prevent detection by rice plants.