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BACKGROUND: Due to the increasing presence of insecticide resistance across cereal aphid populations, new aphid management strategies, including the engineering of host resistance to aphids into commercial wheat varieties, are required. Previous studies have identified ancestor wheat, Triticum monococcum accessions MDR045 and MDR049, with resistance against the grain aphid, Sitobion avenae. To test the hypothesis that resistance can be accounted for by antixenosis (reduced attractiveness of host plants) via the release of repellent volatile organic compounds (VOCs), we explored the response of S. avenae to MDR045 and MDR049 following S. avenae herbivory, using behaviour and electrophysiology experiments. RESULTS: In four-arm olfactometry assays, alate S. avenae showed aphid density-dependent reduced preference to VOC extracts from T. monococcum MDR045 and MDR049. By contrast, alate S. avenae showed aphid density-dependent increased preference to extracts from aphid-susceptible hexaploid wheat, Triticum aestivum var. Solstice and T. monococcum MDR037. Coupled gas chromatography-electroantennography (GC-EAG), using the antennae of alate S. avenae, located 24 electrophysiologically active compounds across all tested accessions. Synthetic blends created from 21 identified EAG-active compounds confirmed bioactivity of corresponding VOC extracts in four-arm olfactometry assays against alate S. avenae. CONCLUSION: Our data suggest that resistance of T. monococcum MDR045 and MDR049 to S. avenae can be at least partially accounted for by antixenosis through antennal perception of specific repellent VOC blends induced by S. avenae feeding behaviour. © 2024 The Author(s). Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

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BACKGROUND: Aphis gossypii Glover is a prevalent phytophagous insect that inflicts significant damage on cucumber plants. Recent studies have provided insights into plant communication and signal transduction within conspecifics. However, understanding of the effect of these communication mechanisms on adjacent cucumbers and their resident aphids, especially in the context of an aphid infestation, is still in its early stages. RESULTS: Utilizing a partitioned root configuration, a tendency for aphids to gather on nearby cucumber leaves of non-infested plants was observed. Furthermore, neighboring plants near aphid-infested cucumber plants showed a reduction in aphid reproduction rates. Concurrently, these plants exhibited a significant increase in reactive oxygen species (ROS) levels, along with enhanced defensive and antioxidant enzymatic responses. Analysis of the microbial community in the rhizosphere showed significant differences in species composition among the samples. Among these, the bacterial families Microbacteriaceae and Rhizobiaceae, along with the fungal species Leucocoprinus ianthinus and Mortierella globalpina, exhibited increases in their relative abundance in cucumber seedlings located near aphid-infested plants. Significantly, this study unveiled robust correlations between dominant microbial phyla and physiological indicators, primarily associated with aphid resistance mechanisms in plants. CONCLUSION: The results show that aphid-infested cucumber plants trigger oxidative stress responses in adjacent seedlings through complex interplant communication mechanisms. In addition, these plants cause changes in the composition of the rhizospheric microbial community and the physiological activity of neighboring plants, consequently boosting their natural resistance to aphids. This study provides essential theoretical foundations to guide the development of sustainable strategies for managing cucumber aphids. © 2024 Society of Chemical Industry.

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(E)-ß-Farnesene (EBF) serves as the primary component of the alarm pheromone used by most aphid pest species. Pyrethrum (Tanacetum cinerariifolium) exhibits tissue-specific regulation of EBF accumulation and release, effectively mimicking the aphid alarm signal, deterring aphid attacks while attracting aphid predators. However, cultivated chrysanthemum (Chrysanthemum morifolium), a popular and economically significant flower, is highly vulnerable to aphid infestations. In this study, we investigated the high expression of the pyrethrum EBF synthase (TcEbFS) gene promoter in the flower head and stem, particularly in the parenchyma cells. Subsequently, we introduced the TcEbFS gene, under the control of its native promoter, into cultivated chrysanthemum. This genetic modification led to increased EBF accumulation in the flower stem and young flower bud, which are the most susceptible tissues to aphid attacks. Analysis revealed that aphids feeding on transgenic chrysanthemum exhibited prolonged probing times and extended salivation durations during the phloem phase, indicating that EBF in the cortex cells hindered their host-location behavior. Interestingly, the heightened emission of EBF was only observed in transgenic chrysanthemum flowers after mechanical damage. Furthermore, we explored the potential of this transgenic chrysanthemum for aphid resistance by comparing the spatial distribution and storage of terpene volatiles in different organs and tissues of pyrethrum and chrysanthemum. This study provides valuable insights into future trials aiming for a more accurate replication of alarm pheromone release in plants. It highlights the complexities of utilizing EBF for aphid resistance in cultivated chrysanthemum and calls for further investigations to enhance our understanding of this defense mechanism.

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The multicellular trichomes of cucumber (Cucumis sativus L.) serve as the primary defense barrier against external factors, whose impact extends beyond plant growth and development to include commercial characteristics of fruits. The aphid (Aphis gossypii Glover) is one of prominent pests in cucumber cultivation. However, the relationship between physical properties of trichomes and the aphid resistance at molecular level remains largely unexplored. Here, a spontaneous mutant trichome morphology (tm) was characterized by increased susceptibility towards aphid. Further observations showed the tm exhibited a higher and narrower trichome base, which was significantly distinguishable from that in wild-type (WT). We conducted map-based cloning and identified the candidate, CsTM, encoding a C-lectin receptor-like kinase. The knockout mutant demonstrated the role of CsTM in trichome morphogenesis. The presence of SNP does not regulate the relative expression of CsTM, but diminishes the CsTM abundance of membrane proteins in tm. Interestingly, CsTM was found to interact with CsTIP1;1, which encodes an aquaporin with extensive reports in plant resistance and growth development. The subsequent aphid resistance experiments revealed that both CsTM and CsTIP1;1 regulated the development of trichomes and conferred resistance against aphid by affecting cytoplasmic H2O2 contents. Transcriptome analysis revealed a significant enrichment of genes associated with pathogenesis, calcium binding and cellulose synthase. Overall, our study elucidates an unidentified mechanism that CsTM-CsTIP1;1 alters multicellular trichome morphology and enhances resistance against aphid, thus providing a wholly new perspective for trichome morphogenesis in cucumber.

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Reports on development of resilient wheat mutants to aphid infestation-causing heavy losses to wheat production in many parts of the world, are scanty. The present study aimed to identify genetic diversity of wheat mutants in terms of varying degree of resistance to aphid infestation which can help protect wheat crop, improve yields and enhance food security. Resistance response to aphid infestation was studied on newly developed 33 wheat mutants, developed through irradiating seed of an elite wheat cultivar "Punjab-11" with gamma radiations, during three normal growing seasons at two sites. Data on various traits including aphid count per plant, biochemical traits, physiological traits and grain yield was recorded. Meteorological data was also collected to unravel the impact of environmental conditions on aphid infestation on wheat plants. Minimum average aphid infestation was found on Pb-M-2725, Pb-M-2550, and Pb-M-2719 as compared to the wild type. High yielding mutants Pb-M-1323, Pb-M-59, and Pb-M-1272 supported the moderate aphid infestation. The prevailing temperature up to 25 °C showed positive correlation (0.25) with aphid count. Among biochemical traits, POD (0.34), TSP (0.33), TFA (0.324) exhibited a high positive correlation with aphid count. In addition, CAT (0.31), TSS (0.294), and proline content (0.293) also showed a positive correlation with aphid count. However, all physiological traits depicted negative correlation with aphid count, while, a very weak correlation (0.12) was found between mean aphid count and grain yield. In PCA biplots, the biochemical variables clustered together with aphid count, while physiological variables grouped with grain yield. Biochemical parameters contributed most, towards first dimension of the PCA (48.6%) as compared to the physiological variables (13%). The FAMD revealed that mutant lines were major contributor towards total variation; Pb-M-1027, Pb-M-1323, Pb-M-59 were found to be the most diverse lines. The PCA revealed that biochemical parameters played a significant role in explaining variations in aphid resistance, emphasizing their importance in aphid defense mechanisms. The identified mutants can be utilized by the international wheat community for getting insight into the molecular circuits of resistant mechanism against aphids as well as for designing new KASP markers. This study also highlights the importance of considering both genetic and environmental factors in the development of resilient wheat varieties and pave the way for further investigations into the molecular mechanisms underpinning aphid resistance in wheat.

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Lilies (Lilium spp.) are famous bulb flowers worldwide, with high ornamental value. Aphid damage has seriously constrained the development of the lily industry. In this study, the aphid resistance of 16 lily cultivars and 2 wild lily species was characterized in the field and greenhouse. Leaf color parameters, stomatal density and size, thickness of leaf layers, leaf waxy content, and leaf water content were determined to explore the constitutive resistance of lilies. The results show that there was a significant positive correlation between the number of aphids in the field and in the greenhouse (p ≤ 0.05, r = 0.47). This indicated that the level of aphid infestation in both the field and the greenhouse is generally consistent across different types of lily plants. Among these 18 lilies, 'Palazzo', 'Nymph', 'Cameleon' and L. lancifolium were resistant to A. gossypii, while 'Black Beauty' and 'Magnefique' had poor resistance. The correlation analysis results showed that the number of aphids was negatively correlated with leaf abaxial surface a*, stomatal size, water content, and thickness of leaf palisade tissue and positively correlated with leaf distal axial surface b*, C*, and waxy content. Among them, the correlation between the number of aphids and the thickness of leaf palisade tissue reached a significant level (p ≤ 0.05, r = -0.521). This indicated that the thickness of the palisade tissue of lily leaves might be an important factor influencing the proliferation of aphids. This study not only screened out aphid-resistant lilies but also established a crucial research foundation for the targeted breeding and molecular breeding of lilies with aphid resistance.

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Cotton-melon aphid, Aphis gossypii Glover (Hemiptera: Aphididae), is emerging as a potential threat to cotton cultivation worldwide. The resistance categories in Gossypium arboreum to A. gossypii still need to be explored. We screened 87 G. arboreum and 20 Gossypium hirsutum genotypes against aphids under natural field conditions. Twenty-six selected genotypes from these 2 species were tested under glasshouse conditions for resistance categories (antixenosis, antibiosis, and tolerance). Resistance categories were assessed by no-choice antibiosis assay, free-choice aphid settling assay, cumulative aphid days using population buildup tests, chlorophyl loss index, and damage ratings. No-choice antibiosis experiment revealed that the G. arboreum genotypes GAM156, PA785, CNA1008, DSV1202, FDX235, AKA2009-6, DAS1032, DHH05-1, GAM532, and GAM216 had a significant adverse effect on aphid development time, longevity, and fecundity. Gossypium arboreum genotypes CISA111 and AKA2008-7 expressed a low level of antixenosis but possessed antibiosis and tolerance. Aphid resistance persisted uniformly at different plant developmental stages studied. The chlorophyl loss percentage and damage rating scores were lower in G. arboreum than in G. hirsutum genotypes, indicating the existence of tolerance in G. arboreum to aphids. Logical relations analysis of resistance contributing factors depicted the presence of antixenosis, antibiosis, and tolerance in the G. arboreum genotypes PA785, CNA1008, DSV1202, and FDX235, indicating their utility for evaluating the mechanisms of resistance and aphid resistance introgression breeding into G. hirsutum to develop commercially cultivated cotton lines.

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The corn leaf aphid (Rhopalosiphum maidis) is a major maize pest that frequently causes substantial yield losses. Exploring the genetic basis of resistance to aphids is important for improving maize yield and quality. Here, we used a maize recombinant inbred line population derived from two parents with different susceptibility to aphids, B73 (susceptible) and Abe2 (resistant), and performed quantitative trait locus (QTL) mapping using aphid resistance scores as an indicator. We mapped a stable QTL, qRTA6, to chromosome 6 using data from 2 years of field trials, which explained 40.12-55.17% of the phenotypic variation. To further investigate the mechanism of aphid resistance in Abe2, we constructed transcriptome and metabolome libraries from Abe2 and B73 leaves with or without aphid infestation at different time points. Integrating QTL mapping and transcriptome data revealed three aphid resistance candidate genes (Zm00001d035736, Zm00001d035751, and Zm00001d035767) associated with the hypersensitive response, the jasmonic acid pathway, and protein ubiquitination. Integrated transcriptomic and metabolomic analysis revealed that the differentially expressed genes and metabolites were enriched in flavonoid biosynthesis. These findings extend our understanding of the molecular mechanisms controlling aphid resistance in maize, and the QTL and candidate genes are valuable resources for increasing this resistance.

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Aphid (Aphis gossypii Glover) attack frequently results in a significant loss of output and deterioration of fruit quality in cucumber (Cucumis sativus L.). Phloem protein 2 (PP2) is conserved as a phloem lectin in plants, and few studies have been conducted on the regulatory mechanism of PP2. Based on our previous study of CsPP2-A1 in cucumber, to further investigate the biological function of CsPP2-A1, we compared the changes of selectivity, non-selectivity, colonization, reproductions of aphids, and the phenotype in wild type (WT), CsPP2-A1 overexpressing (CsPP2-A1-OE), and CsPP2-A1 interfering (CsPP2-A1-RNAi) cucumber plants after inoculation with aphids. We found that CsPP2-A1-OE cucumber plants generated resistance to aphids. The aphid colonization rate and number of reproductions of CsPP2-A1-OE cucumber plants were significantly lower than that of WT and CsPP2-A1-RNAi cucumber plants. Through Pearson's correlation and principal component analysis (PCA), it was found that CsPP2-A1 played a crucial role in the balance of reactive oxygen species (ROS) in plants. Overexpression of the CsPP2-A1 resulted in increased levels of antioxidant enzyme, eliminating ROS and preventing the damage by ROS in cucumber. Furthermore, nutritional imbalance for aphids and content of secondary metabolites were increased in overexpressed CsPP2-A1 cucumber plants, and thus preventing aphid attack. These together may improve cucumber resistance against aphids and the mechanism of CsPP2-A1 defense against aphids was preliminarily explored.

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Cowpea aphids (Aphis craccivora Koch) double as a direct damaging pest and a virus vector to cowpea, threatening the economic yield of the crop. Given the multiple ecotypes, different alleles have been implicated in aphid resistance, necessitating the identification of key genes involved. The present study implemented a genome-wide scan using 365 cowpea mini-core accessions to decipher loci involved in resistance to aphid ecotype from Kano, Nigeria. Accessions were artificially inoculated with A. craccivora in insect-proof cages and damage severity assessed at 21 days after infestation. Significant phenotypic differences based on aphid damage severity were registered among the accessions. Skewed phenotypic distributions were depicted in the population, suggesting the involvement of major genes in the control of resistance. A genome-wide scan identified three major regions on chromosomes Vu10, Vu08 and Vu02, and two minor ones on chromosomes Vu01 and Vu06, that were significantly associated with aphid resistance. These regions harbored several genes, out of which, five viz Vigun01g233100.1, Vigun02g088900.1, Vigun06g224900.1, Vigun08g030200.1 and Vigun10g031100.1 were the most proximal to the peak single nucleotide polymorphisms (SNPs) positions. These genes are expressed under stress signaling, mechanical wounding and insect feeding. The uncovered loci contribute towards establishing a marker-assisted breeding platform and building durable resistance against aphids in cowpea.

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Brassica carinata (BBCC, 2n = 34) is commonly known as Ethiopian mustard, Abyssinian mustard, or carinata. Its excellent agronomic traits, including resistance to biotic and abiotic stresses, make it a potential genetic donor for interspecific hybridization. Myzus persicae (green peach aphid, GPA) is one of the most harmful pests of Brassica crops, significantly effecting the yield and quality. However, few aphid-resistant Brassica crop germplasms have been utilized in breeding practices, while the underlying biochemical basis of aphid resistance still remains poorly understood. In this study, we examined the genetic diversity of 75 B. carinata accessions and some plant characteristics that potentially contribute to GPA resistance. Initially, the morphological characterization showed abundant diversity in the phenotypic traits, with the dendrogram indicating that the genetic variation of the 75 accessions ranged from 0.66 to 0.98. A population structure analysis revealed that these accessions could be grouped into two main subpopulations and one admixed group, with the majority of accessions (86.67%) clustering in one subpopulation. Subsequently, there were three GPA-resistant B. carinata accessions, BC13, BC47, and BC51. The electrical penetration graph (EPG) assay detected resistance factors in the leaf mesophyll tissue and xylem. The result demonstrated that the Ethiopian mustard accessions were susceptible when the phloem probing time, the first probe time, and the G-wave time were 20.51-32.51 min, 26.36-55.54 s, and 36.18-47.84 min, respectively. In contrast, resistance of the Ethiopian mustard accessions was observed with the phloem probing time, the first probe time, and G-wave time of 41.18-70.78 min, 181.07-365.85 s, and 18.03-26.37 min, respectively. In addition, the epidermal characters, leaf anatomical structure, glucosinolate composition, defense-related enzyme activities, and callose deposition were compared between the resistant and susceptible accessions. GPA-resistant accessions had denser longitudinal leaf structure, higher wax content on the leaf surface, higher indole glucosinolate level, increased polyphenol oxidase (PPO) activity, and faster callose deposition than the susceptible accessions. This study validates that inherent physical and chemical barriers are evidently crucial factors in the resistance against GPA infestation. This study not only provide new insights into the biochemical basis of GPA resistance but also highlights the GPA-resistant B. carinata germplasm resources for the future accurate genetic improvement of Brassica crops.

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Callose synthase plays an essential role in plant growth and development and in response to all sorts of stresses through regulating callose formation. However, few research about the function and mechanism of the insect resistance of callose synthase genes have been reported in cotton. In this study, a cotton callose synthase gene GhCalS5 was cloned, and its function and mechanism of resistance to cotton aphids were analyzed. The expression of GhCalS5 was significantly upregulated in both, leaves and stems of cotton plants at 48 h after cotton aphid infestation and in the leaves of cotton plants at 24 h after salicylic acid treatment. The overexpression of GhCalS5 enhanced cotton resistance to cotton aphids. Expectedly silencing of GhCalS5 reduced cotton resistance to cotton aphids. Overexpression of GhCalS5 enhanced callose formation in cotton leaves. Our results suggest that GhCalS5 is involved in cotton resistance against cotton aphids by influencing callose formation.

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The sugarcane woolly aphid is one of the main pests of sugarcane worldwide. The Pinellia pedatisecta agglutinin (PPA) gene has been demonstrated to function towards aphid resistance in other crops. In our study, in order to investigate the PPA function towards aphid control in sugarcane and its underlying mechanism, the PPA gene was overexpressed in a sugarcane Zhongzhe 1 (ZZ1) cultivar in independent transgenic sugarcane lines. It was confirmed in this study that PPA transgenic sugarcane can resist aphids via detecting the aphids' development and tracing the survival number on PPA-transgenic sugarcane lines as well as PPA negative control lines. The mechanism of PPA lectin-associated defense against aphids was preliminarily explored. Stomatal patterning differences of sugarcane leaves between PPA-transgenic sugarcane lines and negative control lines were found. PPA overexpression led to an increase in stomata number and a decrease in stomata size that might have changed the transpiration status, which is critical for aphids' passive feeding. Moreover, the antioxidant enzyme, sugar, tannin and chlorophyll content in sugarcane leaves before and after aphid infestation was determined. The results indicated that PPA overexpression in sugarcane resulted in an increase in antioxidant enzyme activity and tannin content, as well as a reduction in the decline of certain sugars. These together may improve sugarcane resistance against the sugarcane woolly aphid.

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The grain aphid Sitobion avenae (Fabricius) is one of the most destructive pests of wheat (Triticum aestivum). Deployment of resistant wheat germplasm appears as an excellent solution for this problem. Elite bread wheat cultivars only have limited resistance to this pest. The present study was carried out to investigate the potential of the tetraploid wheat (Triticum turgidum) variety Lanmai, which showed high resistance to S. avenae at both seedling and adult plant stages, as a source of resistance genes. Based on apterous adult aphids' fecundity tests and choice bioassays, Lanmai has been shown to display antixenosis and antibiosis. Suppression subtractive hybridization (SSH) was employed to identify and isolate the putative candidate defense genes in Lanmai against S. avenae infestation. A total of 134 expressed sequence tags (ESTs) were identified and categorized based on their putative functions. RT-qPCR analysis of 30 selected genes confirmed their differential expression over time between the resistant wheat variety Lanmai and susceptible wheat variety Polan305 during S. avenae infestation. There were 11 genes related to the photosynthesis process, and only 3 genes showed higher expression in Lanmai than in Polan305 after S. avenae infestation. Gene expression analysis also revealed that Lanmai played a critical role in salicylic acid and jasmonic acid pathways after S. avenae infestation. This study provided further insights into the role of defense signaling networks in wheat resistance to S. avenae and indicates that the resistant tetraploid wheat variety Lanmai may provide a valuable resource for aphid tolerance improvement in wheat.

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Resistant variety screening is widely recommended for the management of Sitobion avenae. The purpose of this study was to assess responses of six wheat varieties (lines) to S. avenae. The aphid quantity ratio (AQR) was used to assess S. avenae resistance. Pearson's correlation coefficient was used to perform a correlation analysis between AQR, biological parameters, and the accumulation of total phenolic and flavonoid content. When compared to the other cultivars, the results showed that two cultivars, Yongliang No.15 and Ganchun No.18, had high resistance against S. avenae. The correlation analysis revealed a positive relationship between total phenol and flavonoid content accumulation and developmental duration (DD), and a negative relationship between accumulation and weight gain (WG) and mean relative growth rate (MRGR). The correlation between flavonoid and biological parameters was statistically stronger than the correlation between total phenol and biological parameters. This research provides critical cues for screening and improving aphid-resistant wheat varieties in the field and will aid in our understanding of the resistance mechanism of wheat varieties against S. avenae.

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Melatonin is a well-known signaling molecule that mediates a range of physiological activities and various stress reactions in plants. We comprehensively tested the effect of melatonin on the development of root hairs and glandular trichomes and found that melatonin pretreatment of tobacco seeds significantly increased the length of root hairs. Furthermore, melatonin-treated tobacco exhibited significantly higher density of trichomes and larger glandular heads on long-stalk glandular trichomes than untreated plants, which resulted in enhanced secretion in glandular trichomes. Exogenous melatonin enhanced the aphid resistance of plants by facilitating the accumulation of cembranoids in the glandular trichomes and alleviated cadmium toxicity by increasing the Cd-exudation capacity of long glandular trichomes. Metabolic analysis indicated that the contents of 108 metabolites significantly changed upon melatonin treatment, with the contents of those that are directly/indirectly involved in melatonin metabolism changing the most. Further, KEGG pathway analysis suggested that the metabolic pathways of amino acids, reducing sugar, secondary metabolites, indole alkaloid biosynthesis, purine, pyrimidine, and ABC transporters were greatly influenced by exogenous melatonin application. Moreover, metabolisms of melatonin-related antioxidants and pyrimidine nucleoside antibiotics were enhanced after melatonin treatment. Melatonin improved tobacco resistance to high salinity, drought, and extreme temperature stresses, as indicated by improved photosynthetic and antioxidant capacities in treated vs. untreated plants. This study lays a foundation for the comprehensive application of melatonin to increase the stress tolerance of plants.

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KEY MESSAGE: Methyl jasmonate treatment and aphid resistance assays reveal different roles in herbivore defensive responses between tobacco glandular and non-glandular trichomes. These roles correlate with trichome gene expression patterns. In plants, trichomes greatly contribute to biotic stress resistance. To better understand the different defensive functions between glandular and non-glandular trichomes, we used Nicotiana tabacum as a model. This species bears three types of trichomes: long and short stalk glandular trichomes (LGT and SGT, respectively), and non-glandular trichomes (NGT). Tobacco accession T.I.1068 (lacking NGT) and T.I.1112 (lacking LGT) were used for the experiment. After methyl jasmonate (MeJA) treatment, LGT formation was promoted not only in T.I.1068, but also in T.I.1112, whereas NGT remained absent in T.I.1068, and was slightly reduced in T.I.1112. Diterpenoids, which play important roles in herbivore resistance, accumulated abundantly in T.I.1068 and were elevated by MeJA; however, they were not found in T.I.1112 but became detectable after MeJA treatment. The aphid resistance of T.I.1068 was higher than that of T.I.1112, and both were enhanced by MeJA, which was closely correlated with LGT density. Trichomes detached from T.I.1068 and T.I.1112 were used for RNA-Seq analysis, the results showed that pentose phosphate, photosynthesis, and diterpenoid biosynthesis genes were much more expressed in T.I.1068 than in T.I.1112, which was consistent with the vigorous diterpenoid biosynthesis in T.I.1068. In T.I.1112, citrate cycle, propanoate, and glyoxylate metabolism processes were enriched, and some defensive protein genes were expressed at higher levels than those in T.I.1068.These results suggested that LGT plays a predominant role in aphid resistance, whereas NGT could strengthen herbivore resistance by accumulating defensive proteins, and the roles of LGT and NGT are associated with their gene expression patterns.

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KEY MESSAGE: NtCycB2 negatively regulates the initiation of tobacco long stalk glandular trichomes and influences the expression of diterpenoid biosynthesis- and environmental stress resistance-related genes. Many asterid plants possess multicellular trichomes on their surface, both glandular and non-glandular. The CycB2 gene plays a key role in multicellular trichome initiation, but has distinct effects on different types of trichomes; its mechanisms remain unknown. In tomato (Solanum lycopersicum), SlCycB2 negatively regulates non-glandular trichome formation, but its effects on glandular trichomes are ambiguous. In this study, we cloned the SlCycB2 homolog of Nicotiana tabacum, NtCycB2, and analyzed its effect on three types of trichomes, long stalk glandular trichomes (LGT), short stalk glandular trichomes (SGT), and non-glandular trichomes (NGT). Knocking out NtCycB2 (NtCycB2-KO) promoted LGT formation, while overexpression of NtCycB2 (NtCycB2-OE) decreased LGT density. SGT and NGT were not significantly influenced in either NtCycB2-KO or NtCycB2-OE plants, indicating that NtCycB2 regulated only LGT formation in tobacco. In addition, compared with NtCycB2-OE and control plants, NtCycB2-KO plants produced more trichome exudates, including diterpenoids and sugar esters, and exhibited stronger aphid resistance. To further elucidate the function of NtCycB2, RNA-Seq analysis of the NtCycB2-KO, NtCycB2-OE, and control plants was conducted. 2,552 and 1,933 differentially expressed genes (DEGs) were found in NtCycB2-KO and NtCycB2-OE plants, respectively. Gene Ontology analysis of the common DEGs revealed that ion transport, carbohydrate and amino acid metabolism, photosynthesis, and transcription regulation processes were significantly enriched. Among these DEGs, diterpenoid biosynthesis genes were upregulated in NtCycB2-KO plants and downregulated in NtCycB2-OE plants. Two MYB transcription factors and several stress resistance-related genes were also identified, suggesting they may participate in regulating LGT formation and aphid resistance.

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BACKGROUND: Pyramiding different resistance genes into one plant genotype confers enhanced resistance at the phenotypic level, but the molecular mechanisms underlying this effect are not well-understood. In soybean, aphid resistance is conferred by Rag genes. We compared the transcriptional response of four soybean genotypes to aphid feeding to assess how the combination of Rag genes enhanced the soybean resistance to aphid infestation. RESULTS: A strong synergistic interaction between Rag1 and Rag2, defined as genes differentially expressed only in the pyramid genotype, was identified. This synergistic effect in the Rag1/2 phenotype was very evident early (6 h after infestation) and involved unique biological processes. However, the response of susceptible and resistant genotypes had a large overlap 12 h after aphid infestation. Transcription factor (TF) analyses identified a network of interacting TF that potentially integrates signaling from Rag1 and Rag2 to produce the unique Rag1/2 response. Pyramiding resulted in rapid induction of phytochemicals production and deposition of lignin to strengthen the secondary cell wall, while repressing photosynthesis. We also identified Glyma.07G063700 as a novel, strong candidate for the Rag1 gene. CONCLUSIONS: The synergistic interaction between Rag1 and Rag2 in the Rag1/2 genotype can explain its enhanced resistance phenotype. Understanding molecular mechanisms that support enhanced resistance in pyramid genotypes could facilitate more directed approaches for crop improvement.

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Benzoxazinoids are important secondary metabolites in gramineae plants and have inhibitory and toxic effects against a wide range of herbivore pests. However, the relationship between benzoxazinoid level and plant resistance to aphids remains controversial. In this study, we investigated the relationship between benzoxazinoids composition and concentration in wheat leaves and the resistance to the grain aphid Sitobion avenae. Overall, six benzoxazinoids were detected and identified by mass spectrometry based metabolites profiling, including three lactams, two hydroxamic acids, and one methyl derivative. The constitutive levels of these benzoxazinoids were significantly different among the wheat varieties/lines. However, none of these benzoxazinoids exhibited considerable correlation with aphid resistance. S. avenae feeding elevated the level of 2-O-ß-D-glucopyranosyloxy-4,7-dimethoxy-(2H)-1,4-benzoxazin-3(4H)-one (HDMBOA-Glc) and reduced the level of 2-O-ß-D-glucopyranosyloxy-4-hydroxy-7-(2H)-methoxy-1,4-benzoxazin-3(4H)-one (DIMBOA-Glc) in some of the wheat varieties/lines. Moreover, aphid-induced level of DIMBOA-Glc was positively related with callose deposition, which was closely associated with aphid resistance. Wheat leaves infiltrated with DIMBOA-Glc caused a noticeable increase of callose deposition and the effect was in a dose dependent manner. This study suggests that the constitutive level of benzoxazinoids has limited impact on S. avenae. Aphid feeding can affect the balance of benzoxazinoids metabolism and the dynamic level of benzoxazinoids can act as a signal of callose deposition for S. avenae resistance. This study will extend our understanding of aphid-wheat interaction and provides new insights in aphid-resistance wheat breeding.