Editorial: Inducing Plant Resistance Against Insects Using Exogenous Bioactive Chemicals: Key Advances and Future Perspectives.

Due to the constraints and hazards of using insecticides such as development of insect resistance, severe decline in availability of conventional pesticides and off-target effects on beneficial insects (Desneux et al., 2007), there is an urgent need to develop the underpinning science to protect crop harvests from insect pests in the face of rising demand for food (Savary et al., 2019). Given the recent advances in our understanding of plant-insect interactions, it is proposed that boosting the overall plant immunity could provide novel alternative control tactics. Constitutively increasing defense could have a negative trade-off with growth or yield (Huot et al., 2014) and therefore inducing resistance could be a more attractive prospect

Wild potato ancestors as potential sources of resistance to the aphid Myzus persicae.

BACKGROUND: Plant resistance to insects can be reduced by crop domestication which means their wild ancestors could provide novel sources of resistance. Thus, crossing wild ancestors with domesticated crops can potentially enhance their resistance against insects. However, a prerequisite for this is identification of sources of resistance. Here, we investigated the response of three wild potato (Solanum stoloniferum Schltdl.) accessions and cultivated potato (Solanum tuberosum) to aphid (Myzus persicae Sulzer) herbivory. RESULTS: Results revealed that there was a significant reduction in aphid survival and reproduction on wild potato accessions (CGN18333, CGN22718, CGN23072) compared to cultivated (Desiree) potato plants. A similar trend was observed in olfactometer bioassay; the wild accessions had a repellent effect on adult aphids. In contrast, among the tested wild potato accessions, the parasitoid Diaeretiella rapae (M'Intosh) was significantly attracted to volatiles from CGN18333. Volatile analysis showed that wild accessions emitted significantly more volatiles compared to cultivated potato. Principal component analysis (PCA) of volatile data revealed that the volatile profiles of wild and cultivated potato are dissimilar. β-Bisabolene, (E)-β-farnesene, trans-α-bergamotene, D-limonene, (E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene (TMTT), and p-Cymen-7-ol were the main volatiles contributing to the emitted blends, suggesting possible involvement in the behavioural response of both M. persicae and D. rapae. CONCLUSION: Our findings show that the tested wild accessions have the potential to be used to breed aphid-resistant potatoes. This opens new opportunities to reduce the aphid damage and to enhance the recruitment of natural enemies

An Indirect Defence Trait Mediated through Egg-Induced Maize Volatiles from Neighbouring Plants.

Attack of plants by herbivorous arthropods may result in considerable changes to the plant's chemical phenotype with respect to emission of herbivore-induced plant volatiles (HIPVs). These HIPVs have been shown to act as repellents to the attacking insects as well as attractants for the insects antagonistic to these herbivores. Plants can also respond to HIPV signals from other plants that warn them of impending attack. Recent investigations have shown that certain maize varieties are able to emit volatiles following stemborer egg deposition. These volatiles attract the herbivore's parasitoids and directly deter further oviposition. However, it was not known whether these oviposition-induced maize (Zea mays, L.) volatiles can mediate chemical phenotypic changes in neighbouring unattacked maize plants. Therefore, this study sought to investigate the effect of oviposition-induced maize volatiles on intact neighbouring maize plants in 'Nyamula', a landrace known to respond to oviposition, and a standard commercial hybrid, HB515, that did not. Headspace volatile samples were collected from maize plants exposed to Chilo partellus (Swinhoe) (Lepidoptera: Crambidae) egg deposition and unoviposited neighbouring plants as well as from control plants kept away from the volatile emitting ones. Behavioural bioassays were carried out in a four-arm olfactometer using egg (Trichogramma bournieri Pintureau & Babault (Hymenoptera: Trichogrammatidae)) and larval (Cotesia sesamiae Cameron (Hymenoptera: Braconidae)) parasitoids. Coupled Gas Chromatography-Mass Spectrometry (GC-MS) was used for volatile analysis. For the 'Nyamula' landrace, GC-MS analysis revealed HIPV production not only in the oviposited plants but also in neighbouring plants not exposed to insect eggs. Higher amounts of EAG-active biogenic volatiles such as (E)-4,8-dimethyl-1,3,7-nonatriene were emitted from these plants compared to control plants. Subsequent behavioural assays with female T. bournieri and C. sesamiae parasitic wasps indicated that these parasitoids preferred volatiles from oviposited and neighbouring landrace plants compared to those from the control plants. This effect was absent in the standard commercial hybrid we tested. There was no HIPV induction and no difference in parasitoid attraction in neighbouring and control hybrid maize plants. These results show plant-plant signalling: 'Nyamula' maize plants emitting oviposition-induced volatiles attractive to the herbivore's natural enemies can induce this indirect defence trait in conspecific neighbouring undamaged maize plants. Maize plants growing in a field may thus benefit from this indirect defence through airborne signalling which may enhance the fitness of the volatile-emitting plant by increasing predation pressure on herbivores

A maize landrace that emits defense volatiles in response to herbivore eggs possesses a strongly inducible terpene synthase gene.

Maize (Zea mays) emits volatile terpenes in response to insect feeding and egg deposition to defend itself against harmful pests. However, maize cultivars differ strongly in their ability to produce the defense signal. To further understand the agroecological role and underlying genetic mechanisms for variation in terpene emission among maize cultivars, we studied the production of an important signaling component (E)-caryophyllene in a South American maize landrace Braz1006 possessing stemborer Chilo partellus egg inducible defense trait, in comparison with the European maize line Delprim and North American inbred line B73. The (E)-caryophyllene production level and transcript abundance of TPS23, terpene synthase responsible for (E)-caryophyllene formation, were compared between Braz1006, Delprim, and B73 after mimicked herbivory. Braz1006-TPS23 was heterologously expressed in E. coli, and amino acid sequences were determined. Furthermore, electrophysiological and behavioral responses of a key parasitic wasp Cotesia sesamiae to C. partellus egg-induced Braz1006 volatiles were determined using coupled gas chromatography electroantennography and olfactometer bioassay studies. After elicitor treatment, Braz1006 released eightfold higher (E)-caryophyllene than Delprim, whereas no (E)-caryophyllene was detected in B73. The superior (E)-caryophyllene production by Braz1006 was positively correlated with high transcript levels of TPS23 in the landrace compared to Delprim. TPS23 alleles from Braz1006 showed dissimilarities at different sequence positions with Delprim and B73 and encodes an active enzyme. Cotesia sesamiae was attracted to egg-induced volatiles from Braz1006 and synthetic (E)-caryophyllene. The variation in (E)-caryophyllene emission between Braz1006 and Delprim is positively correlated with induced levels of TPS23 transcripts. The enhanced TPS23 activity and corresponding (E)-caryophyllene production by the maize landrace could be attributed to the differences in amino acid sequence with the other maize lines. This study suggested that the same analogous genes could have contrasting expression patterns in different maize genetic backgrounds. The current findings provide valuable insight not only into genetic mechanisms underlying variation in defense signal production but also the prospect of introgressing the novel defense traits into elite maize varieties for effective and ecologically sound protection of crops against damaging insect pests

Potential roles of selected forage grasses in management of fall armyworm (Spodoptera frugiperda) through companion cropping

Production of maize, Zea mays L. (Poaceae), in sub-Saharan Africa is threatened by a new invasive pest, fall armyworm (FAW), Spodoptera frugiperda (JE Smith) (Lepidoptera: Noctuidae). To mitigate this threat, push-pull companion cropping, a system originally developed for management of lepidopteran stemborers, may be used to control FAW. The original system involved trap crops that functioned as a 'pull' component to attract moths away from the main crop. How grass species can be used as trap crops in a push-pull system to control FAW is a question that remains to be answered, because maize is already a highly preferred host plant. Therefore, we tested oviposition preference of FAW female moths in no-choice and two-choice experiments and larval performance on six selected grasses (Poaceae) to assess their roles as trap crop 'pull' plants in the system. In no-choice tests, numbers of eggs deposited on Brachiaria brizantha (Hochst. ex A. Rich.) R. Webster cv. 'Piata', cv. 'Mulato II', and cv. 'Xaraes', and Napier grass (Pennisetum purpureum K. Schumach) cv. 'South Africa' were not statistically different from those deposited on maize. In two-choice tests between grasses and maize, there were no significant differences in number of eggs laid when the plants were of the same size. However, in two-choice tests with maize plants half of the size of the grasses, significantly more eggs were laid on B. brizantha cv. Xaraes and P. purpureum cv. South Africa than on maize, suggesting that crop phenology could make a difference. Numbers of larvae arrested on grass leaf cuts were considerably lower than those on maize leaf cuts after 48 h. In two-choice tests with maize, molasses grass (Melinis minutiflora P. Beauv.) was the only grass that was significantly preferred to maize for larval settlement after 24 h. After 48 h in the two-choice test, it was the only grass that retained larvae, although the larval count was significantly lower than on maize. Our data show that none of the grasses tested were strongly preferred to maize, but the results indicate plants attractive to FAW adults and larvae that could be utilized in a multiple trap crop approach to target various stages of the pest. Furthermore, results indicate the importance of planting these companion plants earlier than maize

TPS46, a Rice Terpene Synthase Conferring Natural Resistance to Bird Cherry-Oat Aphid, Rhopalosiphum padi (Linnaeus).

Plant terpene synthases (TPSs) are key enzymes responsible for terpene biosynthesis, and can play important roles in defense against herbivore attack. In rice, the protein sequence of TPS46 was most closely related to maize TPS10. However, unlike maize tps10, tps46 was also constitutively expressed in rice even in the absence of herbivore attack. Potential roles or constitutive emissions of specific volatiles may due to the constitutive expressions of tps46 in rice. Therefore, in the present study, RNA interference (Ri) and overexpression (Oe) rice lines were generated to investigate the potential function of TPS46 in Oryza sativa sp. japonica. Interestingly, the rice plants become more susceptible to Rhopalosiphum padi when expression of tps46 was silenced compared with Wt in greenhouse conditions. Artificial infestation bioassays further confirmed that Ri rice lines were susceptible to R. padi, whereas Oe rice lines were repellent to R. padi. Based on GC-MS and ToF-MS analysis, a total of eight volatile products catalyzed by TPS46 in rice were identified. Among them, only limonene and Eβf could be detected in all the Ri, Oe, and Wt lines, whereas other six volatiles were only found in the blend of volatiles from Oe lines. Moreover, the amount of constitutive limonene and Eβf in the Ri lines was significantly lower than in Wt lines, while the amounts of these two volatiles in the Oe line were obviously higher than in control rice. Our data suggested that the constitutive emissions of Eβf and limonene regulated by the constitutive expression of tps46 may play a crucial role in rice defense against R. padi. Consequently, tps46 could be a potential target gene to be employed for improving the resistance of plants to aphids

Optimising Vine Weevil, Otiorhynchus sulcatus F. (Coleoptera: Curculionidae), Monitoring Tool Design.

Vine weevil, Otiorhynchus sulcatus F. (Coleoptera: Curculionidae), is an economically important insect pest of horticultural crops. To identify an effective and reliable monitoring system for adult vine weevil, this study investigated the influence of colour, height and entrance position on the efficacy of a model monitoring tool using modified paper cups as refuges. Vine weevil preferences were determined by the number of individuals recorded within a refuge. When provided with a binary choice between black or white refuges, vine weevil adults showed a preference for black refuges. Vine weevils provided with a range of coloured refuges (blue, green, red and yellow) in addition to black and white refuges showed a preference for black and blue over the other colours and white refuges in group choice experiments. Refuge height and entrance position also influenced vine weevil behaviour with individuals exhibiting a preference for taller refuges and those with entrance openings around the refuge base. These results provide insights into refuge selection by adult vine weevils, which can be exploited to improve monitoring tool design. The importance of developing an effective monitoring tool for vine weevil adults as part of an integrated pest management programme is discussed

Evaluation of African Maize Cultivars for Resistance to Fall Armyworm Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) Larvae

The fall armyworm (FAW) has recently invaded and become an important pest of maize in Africa causing yield losses reaching up to a third of maize annual production. The present study evaluated different aspects of resistance of six maize cultivars, cropped by farmers in Kenya, to FAW larvae feeding under laboratory and field conditions. We assessed the arrestment and feeding of FAW neonate larvae in no-choice and choice experiments, development of larvae-pupae, food assimilation under laboratory conditions and plant damage in a field experiment. We did not find complete resistance to FAW feeding in the evaluated maize cultivars, but we detected differences in acceptance and preference when FAW larvae were given a choice between certain cultivars. Moreover, the smallest pupal weight and the lowest growth index were found on ’SC Duma 43′ leaves, which suggests an effect of antibiosis of this maize hybrid against FAW larvae. In contrast, the highest growth index was recorded on ‘Rachar’ and the greatest pupal weight was found on ‘Nyamula’ and ‘Rachar’. The density of trichomes on the leaves of these maize cultivars seems not to be directly related to the preference of neonates for feeding. Plant damage scores were not statistically different between cultivars in the field neither under natural nor artificial infestation. However, plant damage scores in ‘Nyamula’ and ‘Jowi’ tended to be lower in the two last samplings of the season compared to the two initial samplings under artificial infestation. Our study provides insight into FAW larval preferences and performance on some African maize cultivars, showing that there are differences between cultivars in these variables; but high levels of resistance to larvae feeding were not found

Maize Chlorotic Mottle Virus Induces Changes in Host Plant Volatiles that Attract Vector Thrips Species

Maize lethal necrosis is one of the most devastating diseases of maize causing yield losses reaching up to 90% in sub-Saharan Africa. The disease is caused by a combination of maize chlorotic mottle virus (MCMV) and any one of cereal viruses in the Potyviridae group such as sugarcane mosaic virus. MCMV has been reported to be transmitted mainly by maize thrips (Frankliniella williamsi) and onion thrips (Thrips tabaci). To better understand the role of thrips vectors in the epidemiology of the disease, we investigated behavioral responses of F. williamsi and T. tabaci, to volatiles collected from maize seedlings infected with MCMV in a four-arm olfactometer bioassay. Volatile profiles from MCMV-infected and healthy maize plants were compared by gas chromatography (GC) and GC coupled mass spectrometry analyses. In the bioassays, both sexes of F. williamsi and male T. tabaci were significantly attracted to volatiles from maize plants infected with MCMV compared to healthy plants and solvent controls. Moreover, volatile analysis revealed strong induction of (E)-4,8-dimethyl-1,3,7-nonatriene, methyl salicylate and (E,E)-4,8,12-trimethyltrideca-1,3,7,11-tetraene in MCMV-infected maize seedlings. Our findings demonstrate MCMV induces changes in volatile profiles of host plants to elicit attraction of thrips vectors. The increased vector contact rates with MCMV-infected host plants could enhance virus transmission if thrips feed on the infected plants and acquire the pathogen prior to dispersal. Uncovering the mechanisms mediating interactions between vectors, host plants and pathogens provides useful insights for understanding the vector ecology and disease epidemiology, which in turn may contribute in designing integrated vector management strategies

Zucchini Plants Alter Gene Expression and Emission of (E)-β-Caryophyllene Following Aphis gossypii Infestation

Zucchini (Cucurbita pepo L.) is widely cultivated in temperate regions. One of the major production challenges is the damage caused by Aphis gossypii (Homoptera: Aphididae), a polyphagous aphid, which can negatively affect its host plant, both directly by feeding and indirectly by vectoring viruses. To gain insights into the transcriptome events that occur during the zucchini-aphid interaction and to understand the early-to-late defense response through gene expression profiles, we performed RNA-sequencing (RNA-Seq) on zucchini leaves challenged by A. gossypii (24, 48, and 96 h post-infestation; hpi). Data analysis indicated a complex and dynamic pattern of gene expression and a transient transcriptional reconfiguration that involved more than 700 differentially expressed genes (DEGs), including a large number of defense-related genes. The down-regulation of key genes of plant immunity, such as leucine-rich repeat (LRR) protein kinases, transcription factors, and genes associated with direct (i.e., protease inhibitors, cysteine peptidases, etc.) and indirect (i.e., terpene synthase) defense responses, suggests the aphid ability to manipulate plant immune responses. We also investigated the emission of volatile organic compounds (VOCs) from infested plants and observed a reduced emission of (E)-β-caryophyllene at 48 hpi, likely the result of aphid effectors, which reflects the down-regulation of two genes involved in the biosynthesis of terpenoids. We showed that (E)-β-caryophyllene emission was modified by the duration of plant infestation and by aphid density and that this molecule highly attracts Aphidius colemani, a parasitic wasp of A. gossypii. With our results we contributed to the identification of genes involved in cucurbit plant interactions with phloem feeders. Our findings may also help pave the way toward developing tolerant zucchini varieties and to identify molecules for sustainable management of harmful insect populations