De novo comparative transcriptome analysis of a rare cicada, with identification of candidate genes related to adaptation to a novel host plant and drier habitats.

Although the importance of host plant chemistry in plant-insect interactions is widely recognized, our understanding about the genetic basis underlying the relationship between changes in midgut proteins and adaptation of plant-feeding insects to novel host plants and habitats is very limited. To address this knowledge gap, the transcriptional profiles of midguts among three populations of the cicada Subpsaltria yangi Chen were compared. Among which, the Hancheng (HC) and Fengxiang (FX) populations occurring in the Loess Plateau feed on Ziziphus jujuba Mill. var. spinosa (Bunge) Hu ex H. F. Chow, while the population occurring in a much drier habitat in the Helan (HL) Mountains is locally specialized on a chemically divergent plant, Ephedra lepidosperma C. Y. Cheng.Based on comparative analysis, 1826 (HL vs HC) differentially expressed genes (DEGs) and 723 DEGs (HL vs FX) were identified between the populations utilizing different host plants, including 20, 36, 2, 5 and 2 genes related to digestion, detoxification, oxidation-reduction, stress response and water-deprivation response, respectively, and 35 genes presumably associated with osmoregulation. However, only 183 DEGs were identified between the HC and FX populations, including two genes related to detoxification, two genes related to stress response, and one gene presumably associated with osmoregulation. These results suggest that the weakest expression differences were between the populations utilizing the same host plant and occurring in the closest habitats, which may help explain the metabolic mechanism of adaptation in S. yangi populations to novel host plants and new niches.The observed differences in gene expression among S. yangi populations are consistent with the hypothesis that the host plant shift and habitat adaptation in the HL population was facilitated by differential regulation of genes related to digestion, detoxification, oxidation-reduction, stress response, water-deprivation response and osmoregulation. The results may inform future studies on the molecular mechanisms underlying the relationship between changes in midgut proteins and adaptation of herbivorous insects to novel host plants and new niches.