Transcriptome profiling revealed potentially important roles of defensive gene expression in the divergence of insect biotypes: a case study with the cereal aphid Sitobion avenae.

BACKGROUND: Many insects can develop differential biotypes on variable host plants, but the underlying molecular factors and mechanisms are not well understood. To address this issue, transcriptome profiling analyses were conducted for two biotypes of the cereal aphid, Sitobion avenae (Fabricius), on both original and alternative plants. RESULTS: Comparisons between both biotypes generated 4174 differentially expressed unigenes (DEGs). In their response to host plant shift, 39 DEGs were shared by both biotypes, whereas 126 and 861 DEGs occurred only in biotypes 1 and 3, respectively. MMC (modulated modularity clustering) analyses showed that specific DEGs of biotypes 1 and 3 clustered into five and nine transcriptional modules, respectively. Among these DEGs, defense-related genes underwent intensive expression restructuring in both biotypes. However, biotype 3 was found to have relatively lower gene transcriptional plasticity than biotype 1. Gene enrichment analyses of the abovementioned modules showed functional divergence in defensive DEGs for the two biotypes in response to host transfer. The expression plasticity for some defense related genes was showed to be directly related to fecundity of S. avenae biotypes on both original and alternative plants, suggesting that expression plasticity of key defensive genes could have significant impacts on the adaptive potential and differentiation of S. avenae biotypes on different plants. CONCLUSIONS: The divergence patterns of transcriptional plasticity in defense related genes may play important roles in the phenotypic evolution and differentiation of S. avenae biotypes. Our results can provide insights into the role of gene expression plasticity in the divergence of insect biotypes and adaptive evolution of insect populations.

Genetic Divergence of Two Sitobion avenae Biotypes on Barley and Wheat in China.

Host plant affinity and geographic distance can play critical roles in the genetic divergence of insect herbivores and evolution of insect biotypes, but their relative importance in the divergence of insect populations is still poorly understood. We used microsatellite markers to test the effects of host plant species and geographic distance on divergence of two biotypes of the English grain aphid, Sitobion avenae (Fabricius). We found that clones of S. avenae from western provinces (i.e., Xinjiang, Gansu, Qinghai and Shaanxi) had significantly higher genetic diversity than those from eastern provinces (i.e., Anhui, Henan, Hubei, Zhejiang and Jiangsu), suggesting their differentiation between both areas. Based on genetic diversity and distance estimates, biotype 1 clones of eastern provinces showed high genetic divergence from those of western provinces in many cases. Western clones of S. avenae also showed higher genetic divergence among themselves than eastern clones. The Mantel test identified a significant isolation-by-distance (IBD) effect among different geographic populations of S. avenae, providing additional evidence for a critical role of geography in the genetic structure of both S. avenae biotypes. Genetic differentiation (i.e., FST) between the two biotypes was low in all provinces except Shaanxi. Surprisingly, in our analyses of molecular variance, non-significant genetic differentiation between both biotypes or between barley and wheat clones of S. avenae was identified, showing little contribution of host-plant associated differentiation to the divergence of both biotypes in this aphid. Thus, it is highly likely that the divergence of the two S. avenae biotypes involved more geographic isolation and selection of some form than host plant affinity. Our study can provide insights into understanding of genetic structure of insect populations and the divergence of insect biotypes.

Transcriptome Profiling Revealed Potentially Critical Roles for Digestion and Defense-Related Genes in Insects' Use of Resistant Host Plants: A Case Study with Sitobion Avenae.

Using host plant resistance (HPR) in management of insect pests is often environmentally friendly and suitable for sustainable development of agricultural industries. However, this strategy can be limited by rapid evolution of insect populations that overcome HPR, for which the underlying molecular factors and mechanisms are not well understood. To address this issue, we analyzed transcriptomes of two distinct biotypes of the grain aphid, Sitobion avenae (Fabricius), on wheat and barley. This analysis revealed a large number of differentially expressed genes (DEGs) between biotypes 1 and 3 on wheat and barley. The majority of them were common DEGs occurring on both wheat and barley. GO and KEGG enrichment analyses for these common DEGs demonstrated significant expression divergence between both biotypes in genes associated with digestion and defense. Top defense-related common DEGs with the most significant expression changes included three peroxidases, two UGTs (UDP-glycosyltransferase), two cuticle proteins, one glutathione S-transferases (GST), one superoxide dismutase, and one esterase, suggesting their potentially critical roles in the divergence of S. avenae biotypes. A relatively high number of specific DEGs on wheat were identified for peroxidases (9) and P450s (8), indicating that phenolic compounds and hydroxamic acids may play key roles in resistance of wheat against S. avenae. Enrichment of specific DEGs on barley for P450s and ABC transporters suggested their key roles in this aphid's detoxification against secondary metabolites (e.g., alkaloids) in barley. Our results can provide insights into the molecular factors and functions that explain biotype adaptation in insects and their use of resistant plants. This study also has significant implications for developing new resistant cultivars, developing strategies that limit rapid development of insect biotypes, and extending resistant crop cultivars' durability and sustainability in integrated management programs.

Life-history responses of insects to water-deficit stress: a case study with the aphid Sitobion avenae.

BACKGROUND: Drought may become one of the greatest challenges for cereal production under future warming scenarios, and its impact on insect pest outbreaks is still controversial. To address this issue, life-history responses of the English grain aphid, Sitobion avenae (Fabricius), from three areas of different drought levels were compared under three water treatments. RESULTS: Significant differences were identified in developmental time, fecundity and adult weight among S. avenae clones from moist, semiarid and arid areas under all the three water treatments. Semiarid and arid area clones tended to have higher heritability for test life-history traits than moist area clones. We identified significant selection of water-deficit on the developmental time of 1st instar nymphs and adult weight for both semiarid and arid area clones. The impact of intermediate and severe water-stress on S. avenae's fitness was neutral and negative (e.g., decreased fecundity and weight), respectively. Compared with arid-area clones, moist- and semiarid-area clones showed higher extents of adaptation to the water-deficit level of their respective source environment. Adult weight was identified as a good indicator for S. avenae's adaptation potential under different water-stress conditions. After their exposure to intermediate water-deficit stress for only five generations, adult weight and fecundity tended to decrease for moist- and semiarid-area clones, but increase for arid-area clones. CONCLUSIONS: It is evident from our study that S. avenae clones from moist, semiarid and arid areas have diverged under different water-deficit stress, and such divergence could have a genetic basis. The impact of drought on S. avenae's fitness showed a water-level dependent pattern. Clones of S. avenae were more likely to become adapted to intermediate water-deficit stress than severe water-deficit stress. After continuous water-deficit stress of only five generations, the adaptation potential of S. avenae tended to decrease for moist and semiarid area clones, but increase for arid area clones. The rapid shift of aphids' life-history traits and adaptation potential under drought could have significant implications for their evolutionary dynamics and outbreak risks in future climate change scenarios.

Morphology and Ultrastructure of Antennal Sensilla in Male and Female Agrilus mali (Coleoptera: Buprestidae).

The apple buprestid beetle, Agrilus mali Matsumura, is an invasive pest causing significant damages to rare wild apple forests of Xinjiang. The morphology, abundance and distribution of antennal sensilla in both sexes of this pest were examined. We found that the antennae of A. mali females were longer than those of males. Five types of antennal sensilla were characterized, including trichodea (subtypes Tr.1, Tr.2, and Tr.3), chaetica (subtypes Sc.1, Sc.2, Sc.3, and Sc.4), basiconica (subtypes Ba. 1, Ba. 2, Ba. 3 and Ba.4), Böhm bristles (subtypes BB. 1, and BB. 2), and multiporous grooved sensilla. The most abundant sensilla of Ba.2 tended to occur mainly on flagellomeres 5-8 in both sexes. The last three flagellomeres tended to have the most abundant Tr.1 in both sexes. Overall, the abundance and distribution of these sensilla appeared to be highly conserved in both sexes, and their olfactory organs seemed to cluster on flagellomeres 6-8. However, some sex dimorphisms were also observed. Tr.3 and BB.2 were found only in females. Sensilla of Sc.2 were found on the pedicel and first two flagellomeres only in males. When compared with males, females showed a higher number of Sc.3, but a lower number of Sc.4 on the pedicel. These results indicate that contact cues could be important in intersexual communication in A. mali. The functional roles of these sensilla and their implications in A. mali behaviors are discussed, and further studies of identified chemosensitive sensilla can provide a foundation for developing semiochemical-based management strategies.

Comparison of fitness traits and their plasticity on multiple plants for Sitobion avenae infected and cured of a secondary endosymbiont.

Regiella insecticola has been found to enhance the performance of host aphids on certain plants, but its functional role in adaptation of host aphids to plants is still controversial. Here we evaluate the impacts of R. insecticola infections on vital life-history traits of Sitobion avenae (Fabricius), and their underlying genetic variation and phenotypic plasticity on three plants. It was shown that effects of R. insecticola on S. avenae's fitness (i.e., developmental time and fecundity) were neutral on oat or wheat, but negative on rye. Infections of R. insecticola modified genetic variation that underlies S. avenae's life-history traits. This was demonstrated by comparing life-history trait heritabilities between aphid lines with and without R. insecticola. Moreover, there were enhanced negative genetic correlations between developmental time and fecundity for R. insecticola infected lines, and structural differences in G-matrices of life-history traits for the two types of aphid lines. In R. insecticola-infected aphid lines, there were increases in plasticities for developmental times of first and second instar nymphs and for fecundity, showing novel functional roles of bacterial symbionts in plant-insect interactions. The identified effects of R. insecticola infections could have significant implications for the ecology and evolution of its host populations in natural conditions.