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Genomic Variations in the Tea Leafhopper Reveal the Basis of Its Adaptive Evolution.

ABSTRACT: Tea green leafhopper (TGL), Empoasca onukii, is of biological and economic interest. Despite numerous studies, the mechanisms underlying its adaptation and evolution remain enigmatic. Here, we use previously untapped genome and population genetics approaches to examine how the pest adapted to different environmental variables and thus has expanded geographically. We complete a chromosome-level assembly and annotation of the E. onukii genome, showing notable expansions of gene families associated with adaptation to chemoreception and detoxification. Genomic signals indicating balancing selection highlight metabolic pathways involved in adaptation to a wide range of tea varieties grown across ecologically diverse regions. Patterns of genetic variations among 54 E. onukii samples unveil the population structure and evolutionary history across different tea-growing regions in China. Our results demonstrate that the genomic changes in key pathways, including those linked to metabolism, circadian rhythms, and immune system functions, may underlie the successful spread and adaptation of E. onukii. This work highlights the genetic and molecular basis underlying the evolutionary success of a species with broad economic impacts, and provides insights into insect adaptation to host plants, which will ultimately facilitate more sustainable pest management.

SUBMITTER: Zhao Q

PROVIDER: S-EPMC10225489 | biostudies-literature | 2022 Dec

REPOSITORIES: biostudies-literature

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Genomic Variations in the Tea Leafhopper Reveal the Basis of Its Adaptive Evolution.

Zhao Qian Q Shi Longqing L He Weiyi W Li Jinyu J You Shijun S Chen Shuai S Lin Jing J Wang Yibin Y Zhang Liwen L Yang Guang G Vasseur Liette L You Minsheng M

Genomics, proteomics & bioinformatics 20220828 6

Tea green leafhopper (TGL), Empoasca onukii, is of biological and economic interest. Despite numerous studies, the mechanisms underlying its adaptation and evolution remain enigmatic. Here, we use previously untapped genome and population genetics approaches to examine how the pest adapted to different environmental variables and thus has expanded geographically. We complete a chromosome-level assembly and annotation of the E. onukii genome, showing notable expansions of gene families associated ...[more]

PMID: 36041663

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Project description:Tea green leafhopper [Empoasca (Matsumurasca) onukii Matsuda] is one of the most devastating pests of tea plants (Camellia sinensis), greatly impacting tea yield and quality. A thorough understanding of the interactions between the tea green leafhopper and the tea plant would facilitate a better pest management. To gain more insights into the molecular and biochemical mechanisms behind their interactions, a combined analysis of the global transcriptome and metabolome reconfiguration of the tea plant challenged with tea green leafhoppers was performed for the first time, complemented with phytohormone analysis. Non-targeted metabolomics analysis by ultra-performance liquid chromatography quadrupole time-of-flight mass spectrometry (UPLC-QTOF MS), together with quantifications by ultra-performance liquid chromatography triple quadrupole mass spectrometry (UPLC-QqQ MS), revealed a marked accumulation of various flavonoid compounds and glycosidically bound volatiles but a great reduction in the level of amino acids and glutathione upon leaf herbivory. RNA-Seq data analysis showed a clear modulation of processes related to plant defense. Genes pertaining to the biosynthesis of phenylpropanoids and flavonoids, plant-pathogen interactions, and the biosynthesis of cuticle wax were significantly up-regulated. In particular, the transcript level for a CER1 homolog involved in cuticular wax alkane formation was most drastically elevated and an increase in C29 alkane levels in tea leaf waxes was observed. The tea green leafhopper attack triggered a significant increase in salicylic acid (SA) and a minor increase in jasmonic acid (JA) in infested tea leaves. Moreover, transcription factors (TFs) constitute a large portion of differentially expressed genes, with several TFs families likely involved in SA and JA signaling being significantly induced by tea green leafhopper feeding. This study presents a valuable resource for uncovering insect-induced genes and metabolites, which can potentially be used to enhance insect resistance in tea plants.

Project description:Unravelling the strength, frequency, and distribution of selective variants along the genome as well as the underlying factors shaping this distribution are fundamental goals of evolutionary biology. Antagonistic host-pathogen coevolution is thought to be a major driver of genome evolution between interacting species. While rapid evolution of pathogens has been documented in several model organisms, the genetic mechanisms of their adaptation are still poorly understood and debated, particularly the role of sexual reproduction. Here, we apply a population genomic approach to infer genome-wide patterns of selection among 13 isolates of Zymoseptoria tritici, a fungal pathogen characterized by extremely high genetic diversity, gene density, and recombination rates. We report that the genome of Z. tritici undergoes a high rate of adaptive substitutions, with 44% of nonsynonymous substitutions being adaptive on average. This fraction reaches 68% in so-called effector genes encoding determinants of pathogenicity, and the distribution of fitness effects differs in this class of genes as they undergo adaptive mutations with stronger positive fitness effects, but also more slightly deleterious mutations. Besides the globally high rate of adaptive substitutions, we report a negative relationship between pN/pS and the fine-scale recombination rate and a strong positive correlation between the rate of adaptive nonsynonymous substitutions (ωa) and recombination rate. This result suggests a pervasive role of both background selection and Hill-Robertson interference even in a species with an exceptionally high recombination rate (60 cM/Mb on average). While transposable elements (TEs) have been suggested to contribute to adaptation by creating compartments of fast-evolving genomic regions, we do not find a significant effect of TEs on the rate of adaptive mutations. Overall our study suggests that sexual recombination is a significant driver of genome evolution, even in rapidly evolving organisms subject to recurrent mutations with large positive effects.

Dataset Information

Genomic Variations in the Tea Leafhopper Reveal the Basis of Its Adaptive Evolution.

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Genomic Variations in the Tea Leafhopper Reveal the Basis of Its Adaptive Evolution.

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