Trans-driven variation in expression is common among detoxification genes in the extreme generalist herbivore Tetranychus urticae

The extreme adaptation potential of the generalist herbivore Tetranychus urticae (the two-spotted spider mite) to pesticides as well as diverse host plants has been associated with clade-specific gene expansions in known detoxifying enzyme families, and with extensive and rapid transcriptional responses. However, how this broad transcriptional potential is regulated remains largely unknown. Using a parental/F1 design in which four inbred strains were crossed to a common inbred strain, we assessed the genetic basis and inheritance of gene expression variation in T. urticae. Mirroring known phenotypic variation in the progenitor strains of the inbreds, we confirmed that the inbred strains we created were genetically distinct, varied markedly in pesticide resistance, and also captured variation in host plant fitness as is commonly observed in this species. By examining differences in gene expression between parents and allele-specific expression in F1s, we found that variation in RNA abundance was more often explained in trans as compared to cis, with the former associated with dominance in inheritance. Strikingly, in a gene ontology analysis, detoxification genes of the cytochrome P450 monooxygenase (CYP) family, as well as dioxygenases (DOGs) acquired from horizontal gene transfer from fungi, were specifically enriched at the extremes of trans-driven up- and downregulation. In particular, multiple CYPs and DOGs with broad substrate-specificities for pesticides or plant specialized compounds were exceptionally highly upregulated as a result of trans-regulatory variation, or in some cases synergism of cis and trans, in the most multi-pesticide resistant strains. Collectively, our findings highlight the potential importance of trans-driven expression variation in genes associated with xenobiotic metabolism and host plant use for rapid adaptation in T. urticae, and also suggests modular control of these genes, a regulatory architecture that might ameliorate negative pleiotropic effects.

[1]  B. Vanholme,et al.  Intradiol ring cleavage dioxygenases from herbivorous spider mites as a new detoxification enzyme family in animals , 2022, BMC biology.

[2]  Richard M. Clark,et al.  Concerted cis and trans effects underpin heightened defense gene expression in multi-herbivore resistant maize lines. , 2022, The Plant journal : for cell and molecular biology.

[3]  T. Van Leeuwen,et al.  Interactions With Plant Defences Isolate Sympatric Populations of an Herbivorous Mite , 2022, Frontiers in Ecology and Evolution.

[4]  M. Mansoor,et al.  Methoxyfenozide tolerance in Chrysoperla carnea: Inheritance, dominance and preliminary detoxification mechanisms , 2022, PloS one.

[5]  W. Jonckheere,et al.  QTL mapping suggests that both cytochrome P450-mediated detoxification and target-site resistance are involved in fenbutatin oxide resistance in Tetranychus urticae. , 2022, Insect biochemistry and molecular biology.

[6]  M. Riga,et al.  Over-expression in cis of the midgut P450 CYP392A16 contributes to abamectin resistance in Tetranychus urticae. , 2022, Insect biochemistry and molecular biology.

[7]  W. Jonckheere,et al.  Pyrethroid target-site resistance mutations in populations of the honey bee parasite Varroa destructor (Acari: Varroidae) from Flanders, Belgium , 2021, Experimental and Applied Acarology.

[8]  Richard M. Clark,et al.  Adaptive divergence and post-zygotic barriers to gene flow between sympatric populations of a herbivorous mite , 2021, Communications biology.

[9]  É. Sucena,et al.  Wolbachia and host intrinsic reproductive barriers contribute additively to postmating isolation in spider mites , 2021, Evolution; international journal of organic evolution.

[10]  R. Nauen,et al.  Transcriptional regulation of xenobiotic detoxification genes in insects - An overview. , 2021, Pesticide biochemistry and physiology.

[11]  Richard M. Clark,et al.  High-resolution genetic mapping reveals cis-regulatory and copy number variation in loci associated with cytochrome P450-mediated detoxification in a generalist arthropod pest , 2021, bioRxiv.

[12]  P. Wittkopp,et al.  Molecular and evolutionary processes generating variation in gene expression , 2020, Nature Reviews Genetics.

[13]  R. Feyereisen,et al.  Diversity and evolution of the P450 family in arthropods. , 2020, Insect biochemistry and molecular biology.

[14]  Daojun Yuan,et al.  Unraveling cis and trans regulatory evolution during cotton domestication , 2019, Nature Communications.

[15]  Richard M. Clark,et al.  High-resolution QTL mapping in Tetranychus urticae reveals acaricide-specific responses and common target-site resistance after selection by different METI-I acaricides. , 2019, Insect biochemistry and molecular biology.

[16]  A. Wijonarko,et al.  Inheritance and Realized Heritability of Resistance to Imidacloprid in the Brown Planthopper, Nilaparvata lugens (Hemiptera: Delphacidae), From Indonesia , 2019, Journal of Economic Entomology.

[17]  Richard M. Clark,et al.  Long-Term Population Studies Uncover the Genome Structure and Genetic Basis of Xenobiotic and Host Plant Adaptation in the Herbivore Tetranychus urticae , 2018, Genetics.

[18]  T. Van Leeuwen,et al.  Transcriptomic Plasticity in the Arthropod Generalist Tetranychus urticae Upon Long-Term Acclimation to Different Host Plants , 2018, G3: Genes, Genomes, Genetics.

[19]  F. Jones,et al.  Predominance of cis-regulatory changes in parallel expression divergence of sticklebacks , 2018, bioRxiv.

[20]  N. Hawkins,et al.  The evolutionary origins of pesticide resistance , 2018, Biological reviews of the Cambridge Philosophical Society.

[21]  T. Van Leeuwen,et al.  A massive incorporation of microbial genes into the genome of Tetranychus urticae, a polyphagous arthropod herbivore , 2018, Insect molecular biology.

[22]  J. Vontas,et al.  The role of glutathione S-transferases (GSTs) in insecticide resistance in crop pests and disease vectors. , 2018, Current opinion in insect science.

[23]  D. Lowry,et al.  Gene regulatory divergence between locally adapted ecotypes in their native habitats , 2018, Molecular ecology.

[24]  M. Grbic,et al.  Plant-Herbivore Interactions: A Case of an Extreme Generalist, the Two-Spotted Spider Mite Tetranychus urticae. , 2017, Molecular plant-microbe interactions : MPMI.

[25]  M. Riga,et al.  The relative contribution of target-site mutations in complex acaricide resistant phenotypes as assessed by marker assisted backcrossing in Tetranychus urticae , 2017, Scientific Reports.

[26]  David Levine,et al.  SeqArray—a storage‐efficient high‐performance data format for WGS variant calls , 2017, Bioinform..

[27]  Richard M. Clark,et al.  Disruption of a horizontally transferred phytoene desaturase abolishes carotenoid accumulation and diapause in Tetranychus urticae , 2017, Proceedings of the National Academy of Sciences.

[28]  A. Gassmann,et al.  Assessment of Inheritance and Fitness Costs Associated with Field-Evolved Resistance to Cry3Bb1 Maize by Western Corn Rootworm , 2017, Toxins.

[29]  L. Tirry,et al.  A mutation in the PSST homologue of complex I (NADH:ubiquinone oxidoreductase) from Tetranychus urticae is associated with resistance to METI acaricides. , 2017, Insect biochemistry and molecular biology.

[30]  D. Heckel,et al.  Horizontal Gene Transfer Contributes to the Evolution of Arthropod Herbivory , 2016, Genome biology and evolution.

[31]  M. Williamson,et al.  Novel Mutations in the Voltage-Gated Sodium Channel of Pyrethroid-Resistant Varroa destructor Populations from the Southeastern USA , 2016, PloS one.

[32]  T. Van Leeuwen,et al.  The Molecular Evolution of Xenobiotic Metabolism and Resistance in Chelicerate Mites. , 2016, Annual review of entomology.

[33]  Matthew Stephens,et al.  False discovery rates: a new deal , 2016, bioRxiv.

[34]  L. Tirry,et al.  Molecular analysis of cyenopyrafen resistance in the two-spotted spider mite Tetranychus urticae. , 2016, Pest management science.

[35]  Thomas D. Wu,et al.  GMAP and GSNAP for Genomic Sequence Alignment: Enhancements to Speed, Accuracy, and Functionality , 2016, Statistical Genomics.

[36]  M. Riga,et al.  Functional characterization of the Tetranychus urticae CYP392A11, a cytochrome P450 that hydroxylates the METI acaricides cyenopyrafen and fenpyroximate. , 2015, Insect biochemistry and molecular biology.

[37]  F. Hendrickx,et al.  Adaptation of a polyphagous herbivore to a novel host plant extensively shapes the transcriptome of herbivore and host , 2015, Molecular ecology.

[38]  R. Feyereisen,et al.  Genotype to phenotype, the molecular and physiological dimensions of resistance in arthropods. , 2015, Pesticide biochemistry and physiology.

[39]  Heiko Vogel,et al.  Molecular mechanisms of insect adaptation to plant secondary compounds. , 2015, Current opinion in insect science.

[40]  L. Kruglyak,et al.  The role of regulatory variation in complex traits and disease , 2015, Nature Reviews Genetics.

[41]  W. Huber,et al.  Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 , 2014, Genome Biology.

[42]  Paul Theodor Pyl,et al.  HTSeq—a Python framework to work with high-throughput sequencing data , 2014, bioRxiv.

[43]  D. Heckel,et al.  Bacterial origin of a diverse family of UDP-glycosyltransferase genes in the Tetranychus urticae genome. , 2014, Insect biochemistry and molecular biology.

[44]  M. Reichelt,et al.  Evolution in an ancient detoxification pathway is coupled with a transition to herbivory in the drosophilidae. , 2014, Molecular biology and evolution.

[45]  J. Kopecký,et al.  Point mutations in the sodium channel gene conferring tau-fluvalinate resistance in Varroa destructor. , 2014, Pest management science.

[46]  M. Orsucci,et al.  Combining experimental evolution and field population assays to study the evolution of host range breadth , 2014, Journal of evolutionary biology.

[47]  M. Riga,et al.  Abamectin is metabolized by CYP392A16, a cytochrome P450 associated with high levels of acaricide resistance in Tetranychus urticae. , 2014, Insect biochemistry and molecular biology.

[48]  Matthew Fraser,et al.  InterProScan 5: genome-scale protein function classification , 2014, Bioinform..

[49]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[50]  Wen-Hsiung Li,et al.  Inheritance of gene expression level and selective constraints on trans- and cis-regulatory changes in yeast. , 2013, Molecular biology and evolution.

[51]  Richard M. Clark,et al.  A burst of ABC genes in the genome of the polyphagous spider mite Tetranychus urticae , 2013, BMC Genomics.

[52]  Heng Li.  Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM , 2013, 1303.3997.

[53]  Richard M. Clark,et al.  A link between host plant adaptation and pesticide resistance in the polyphagous spider mite Tetranychus urticae , 2012, Proceedings of the National Academy of Sciences.

[54]  David Levine,et al.  A high-performance computing toolset for relatedness and principal component analysis of SNP data , 2012, Bioinform..

[55]  Yves Van de Peer,et al.  ORCAE: online resource for community annotation of eukaryotes , 2012, Nature Methods.

[56]  A. Lynd,et al.  A cis-regulatory sequence driving metabolic insecticide resistance in mosquitoes: functional characterisation and signatures of selection. , 2012, Insect biochemistry and molecular biology.

[57]  M. Riga,et al.  The cys-loop ligand-gated ion channel gene family of Tetranychus urticae: implications for acaricide toxicology and a novel mutation associated with abamectin resistance. , 2012, Insect biochemistry and molecular biology.

[58]  Guangchuang Yu,et al.  clusterProfiler: an R package for comparing biological themes among gene clusters. , 2012, Omics : a journal of integrative biology.

[59]  Pablo Cingolani,et al.  © 2012 Landes Bioscience. Do not distribute. , 2022 .

[60]  Stefan R. Henz,et al.  The genome of Tetranychus urticae reveals herbivorous pest adaptations , 2011, Nature.

[61]  Bradley P. Coe,et al.  Genome structural variation discovery and genotyping , 2011, Nature Reviews Genetics.

[62]  M. DePristo,et al.  A framework for variation discovery and genotyping using next-generation DNA sequencing data , 2011, Nature Genetics.

[63]  M. DePristo,et al.  The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. , 2010, Genome research.

[64]  L. Tirry,et al.  Acaricide resistance mechanisms in the two-spotted spider mite Tetranychus urticae and other important Acari: a review. , 2010, Insect biochemistry and molecular biology.

[65]  C Joel McManus,et al.  Regulatory divergence in Drosophila revealed by mRNA-seq. , 2010, Genome research.

[66]  Serban Nacu,et al.  Fast and SNP-tolerant detection of complex variants and splicing in short reads , 2010, Bioinform..

[67]  Joaquín Dopazo,et al.  ETE: a python Environment for Tree Exploration , 2010, BMC Bioinformatics.

[68]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[69]  Yu Cheng Zhu,et al.  Inheritance mode and realized heritability of resistance to imidacloprid in the brown planthopper, Nilaparvata lugens (Stål) (Homoptera: Delphacidae). , 2009, Pest management science.

[70]  Bartek Wilczynski,et al.  Biopython: freely available Python tools for computational molecular biology and bioinformatics , 2009, Bioinform..

[71]  B. Charlesworth.  Effective population size and patterns of molecular evolution and variation , 2009, Nature Reviews Genetics.

[72]  David L Stern,et al.  Is Genetic Evolution Predictable? , 2009, Science.

[73]  R. Nauen,et al.  Resistance mechanisms to mitochondrial electron transport inhibitors in a field-collected strain of Tetranychus urticae Koch (Acari: Tetranychidae). , 2009, Bulletin of entomological research.

[74]  M. Gerstein,et al.  RNA-Seq: a revolutionary tool for transcriptomics , 2009, Nature Reviews Genetics.

[75]  Montgomery Slatkin,et al.  Linkage disequilibrium — understanding the evolutionary past and mapping the medical future , 2008, Nature Reviews Genetics.

[76]  J. Pascussi,et al.  The tangle of nuclear receptors that controls xenobiotic metabolism and transport: crosstalk and consequences. , 2008, Annual review of pharmacology and toxicology.

[77]  Nathan M. Springer,et al.  Allele-Specific Expression Patterns Reveal Biases and Embryo-Specific Parent-of-Origin Effects in Hybrid Maize[W] , 2007, The Plant Cell Online.

[78]  John D. Hunter,et al.  Matplotlib: A 2D Graphics Environment , 2007, Computing in Science & Engineering.

[79]  C. Thummel,et al.  The DHR96 nuclear receptor regulates xenobiotic responses in Drosophila. , 2006, Cell metabolism.

[80]  Richard M. Clark,et al.  A distant upstream enhancer at the maize domestication gene tb1 has pleiotropic effects on plant and inflorescent architecture , 2006, Nature Genetics.

[81]  L. Feuk,et al.  Structural variation in the human genome , 2006, Nature Reviews Genetics.

[82]  Andrew G. Clark,et al.  Evolutionary changes in cis and trans gene regulation , 2004, Nature.

[83]  D. Schluter,et al.  Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks , 2004, Nature.

[84]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[85]  M. Navajas,et al.  Genetic Differentiation in Tetranychus Urticae (Acari: Tetranychidae): polymorphism, host races or sibling species? , 2004, Experimental & Applied Acarology.

[86]  R. Lenski,et al.  Parallel changes in gene expression after 20,000 generations of evolution in Escherichia coli , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[87]  R. ffrench-Constant,et al.  A Single P450 Allele Associated with Insecticide Resistance in Drosophila , 2002, Science.

[88]  D. Wright,et al.  Cross-resistance and inheritance of resistance to Bacillus thuringiensis toxin Cry1Ac in diamondback moth (Plutella xylostella L) from lowland Malaysia. , 2001, Pest management science.

[89]  T. C. Nesbitt,et al.  fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. , 2000, Science.

[90]  H. Preisler,et al.  Pesticide Bioassays With Arthropods , 1991 .

[91]  A. Limin,et al.  Sources and inheritance of resistance to Russian wheat aphid in Triticum species amphiploids and Triticum tauschii. , 1991 .

[92]  J. A. Mckenzie,et al.  Ecological genetics of insecticide and acaricide resistance. , 1987, Annual review of entomology.

[93]  C. F. Wilkinson,et al.  Detoxication Enzymes in the Guts of Caterpillars: An Evolutionary Answer to Plant Defenses? , 1971, Science.

[94]  B. F. Stone.  A formula for determining degree of dominance in cases of monofactorial inheritance of resistance to chemicals. , 1968, Bulletin of the World Health Organization.

[95]  W. Helle,et al.  GENETIC AFFINITIES BETWEEN ADJACENT POPULATIONS OF SPIDER MITES (TETRANYCHUS URTICAE KOCH) , 1965 .