Comparative transcriptome analysis of Tamarixia radiata (Hymenoptera: Eulophidae) reveals differentially expressed genes upon heat shock

Alexa, 2010 Alves, 2014, Biology of the Huanglongbing vector Diaphorina citri (Hemiptera: Liviidae) on different host plants, J. Econ. Entomol., 107, 691, 10.1603/EC13339 Ashraf, 2021 Aubert, 1984, 9 Bale, 2002, Herbivory in global climate change research: direct effects of rising temperature on insect herbivores, Glob. Chang. Biol., 8, 1, 10.1046/j.1365-2486.2002.00451.x Basha, 2012, Small heat shock proteins and α-crystallins: dynamic proteins with flexible functions, Trends Biochem. Sci., 37, 106, 10.1016/j.tibs.2011.11.005 Bové, 2006, Huanglongbing: a destructive, newly-emerging, century-old disease of citrus, J. Plant Pathol., 7 Cheng, 2016, Cloning of heat shock protein genes (hsp70, hsc70 and hsp90) and their expression in response to larval diapause and thermal stress in the wheat blossom midge,Sitodiplosis mosellana, 95, 66 Chien, 1995, Influences of host densities on the population increase of the eulophid wasp, Tamarixia radiata, and its host-killing ability, Plant Prot. Bull., 37, 81 Chien, 1991, Parasitic strategy, morphology and life history of Tamarixia radiata (Hymenoptera; Eulophidae), Chin. J. Entomol., 11, 264 Damos, 2012, Temperature-driven models for insect development and vital thermal requirements, Psyche: J. Entomol., 2012 Day, 2002, Increasing temperature accelerates protein unfolding without changing the pathway of unfolding, J. Mol. Biol., 322, 189, 10.1016/S0022-2836(02)00672-1 Du, 2019, Mitochondrial genome of Tamarixia radiata (Hymenoptera: Chalcidoidea: Eulophidae) and phylogenetic analysis, Mitochondrial DNA B Resour., 4, 2839, 10.1080/23802359.2019.1660259 Esaki, 2017, Deviation of the typical AAA substrate-threading pore prevents fatal protein degradation in yeast Cdc48, Sci. Rep., 7, 5475, 10.1038/s41598-017-05806-y Étienne, 2001, Biological control of Diaphorina citri (Hemiptera: Psyllidae) in Guadeloupe by imported Tamarixia radiata (Hymenoptera: Eu Feder, 1999, Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology, Annu. Rev. Physiol., 61, 243, 10.1146/annurev.physiol.61.1.243 Garczynski, 2011, Characterization of three transcripts encoding small heat shock proteins expressed in the codling moth, Cydia pomonella (Lepidoptera: Tortricidae), Insect Sci., 18, 473, 10.1111/j.1744-7917.2010.01401.x Garrad, 2016, The effect of rearing temperature on development, body size, energetics and fecundity of the diamondback moth, Bull. Entomol. Res., 106, 175, 10.1017/S000748531500098X Garrido, 2012, The small heat shock proteins family: the long forgotten chaperones, Int. J. Biochem. Cell Biol., 44, 1588, 10.1016/j.biocel.2012.02.022 Gómez-Torres, 2014, Thermal hygrometric requirements for the rearing and release of Tamarixia radiata (Waterston) (Hymenoptera, Eulophidae), Rev. Bras. Entomol., 58, 291, 10.1590/S0085-56262014000300011 Gómez-Torres, 2012, Life table of Tamarixia radiata (Hymenoptera: Eulophidae) on Diaphorina citri (Hemiptera: Psyllidae) at different temperatures, J. Econ. Entomol., 105, 338, 10.1603/EC11280 Grabherr, 2011, Full-length transcriptome assembly from RNA-seq data without a reference genome, Nat. Biotechnol., 29, 644, 10.1038/nbt.1883 Grafton-Cardwell, 2013, Biology and management of Asian citrus psyllid, vector of the huanglongbing pathogens, Annu. Rev. Entomol., 58, 413, 10.1146/annurev-ento-120811-153542 Guo, 2020, Comprehensive assessment of candidate reference genes for gene expression studies using RT-qPCR in Tamarixia radiata, a predominant parasitoid of Diaphorina citri, Genes (Basel), 11, 1178, 10.3390/genes11101178 Guo, 2018, Comparisons of expression levels of heat shock proteins (hsp70 and hsp90) from Anaphothrips obscurus (Thysanoptera: Thripidae) in polymorphic adults exposed to different heat shock treatments, J. Insect Sci., 18, 10.1093/jisesa/iey059 Hall, 2013, Asian citrus psyllid, Diaphorina citri, vector of citrus huanglongbing disease, Entomol. Exp. Appl., 146, 207, 10.1111/eea.12025 Hoddle, 2014, Host range testing of Tamarixia radiata (Hymenoptera: Eulophidae) sourced from the Punjab of Pakistan for classical biological control of Diaphorina citri (Hemiptera: liviidae: euphyllurinae: Diaphorinini) in California, J. Econ. Entomol., 107, 125, 10.1603/EC13318 Howard, 2011, Promotion of plasma membrane repair by vitamin E, 2, 1 Kanehisa, 2000, 28, 27 Kang, 2017, Cognitive function of Artemisia argyi H. fermented by Monascus purpureus under TMT-induced learning and memory deficits in ICR mice, Evid. Based. Complement. Alternat. Med., 10.1155/2017/5809370 Kawasaki, 2002, SakA MAP kinase is involved in stress signal transduction, sexual development and spore viability in Aspergillus nidulans, Mol. Microbiol., 45, 1153, 10.1046/j.1365-2958.2002.03087.x King, 2015, Insect heat shock proteins during stress and diapause, Annu. Rev. Entomol., 60, 59, 10.1146/annurev-ento-011613-162107 Langmead, 2009, Ultrafast and memory-efficient alignment of short DNA sequences to the human genome, Genome Biol., 10, R25, 10.1186/gb-2009-10-3-r25 Li, 2011, RSEM: accurate transcript quantification from RNA-seq data with or without a reference genome, 12, 323 Li, 2019, Comparative transcriptome analysis of the heat stress response in Monochamus alternatus Hope (Coleoptera: Cerambycidae), Front. Physiol., 10, 1568, 10.3389/fphys.2019.01568 Li, 2018, Temperature and host age effects on the life history of Tamarixia radiata, a dominant parasitoid of citrus psyllid Diaphorina citri, Crop Prot., 114, 32, 10.1016/j.cropro.2018.08.004 Liu, 2017, Transcriptomic profiling reveals differentially expressed genes associated with pine wood nematode resistance in masson pine (Pinus massoniana lamb.), Sci. Rep., 7, 4693, 10.1038/s41598-017-04944-7 Liu, 2017, BMC Genomics, 18, 974, 10.1186/s12864-017-4355-5 Livak, 2001, Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method, Methods, 25, 402, 10.1006/meth.2001.1262 Lu, 2016, Identification of a heat shock protein 90 gene involved in resistance to temperature stress in two wing-morphs of Nilaparvata lugens (Stål), Comp. Biochem. Physiol. A. Mol. Integr. Physiol., 197, 1, 10.1016/j.cbpa.2016.02.019 Ludwig, 2005, Ethylene-mediated cross-talk between calcium-dependent protein kinase and MAPK signaling controls stress responses in plants, Proc. Natl. Acad. Sci. U. S. A., 102, 10736, 10.1073/pnas.0502954102 McCalla, 2019, The influence of temperature variation on life history parameters and thermal performance curves of Tamarixia radiata (Hymenoptera: Eulophidae), a parasitoid of the Asian citrus psyllid (Hemiptera: Liviidae), J. Econ. Entomol., 112, 1560, 10.1093/jee/toz067 Mehlen, 1996, Small stress proteins as novel regulators of apoptosis. Heat shock protein 27 blocks Fas/APO-1- and staurosporine-induced cell death, J. Biol. Chem., 271, 16510, 10.1074/jbc.271.28.16510 Minami, 1996, Regulation of the heat-shock protein 70 reaction cycle by the mammalian DnaJ homolog, Hsp40, J. Biol. Chem., 271, 19617, 10.1074/jbc.271.32.19617 Monaghan, 2009, Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation, Ecol. Lett., 12, 75, 10.1111/j.1461-0248.2008.01258.x Newmyer, 2001, Dominant-interfering Hsc70 mutants disrupt multiple stages of the clathrin-coated vesicle cycle in vivo, J. Cell Biol., 152, 607, 10.1083/jcb.152.3.607 Niu, 2011, A substrate-specific cytochrome P450 monooxygenase, CYP6AB11, from the polyphagous navel orangeworm (Amyelois transitella), Insect Biochem. Mol. Biol., 41, 244, 10.1016/j.ibmb.2010.12.009 Pan, 2010, The hippo signaling pathway in development and cancer, Dev. Cell, 19, 491, 10.1016/j.devcel.2010.09.011 Plafker, 2010, Oxidative stress and the ubiquitin proteolytic system in age-related macular degeneration, Adv. Exp. Med. Biol., 664, 447, 10.1007/978-1-4419-1399-9_51 Qin, 2013, Characterization and functional analysis of four glutathione S-transferases from the migratory locust,Locusta migratoria, 8 Qin, 2003, Cloning and characterization of a member of the Hsp70 gene family from Locusta migratoria, a highly thermotolerant insect, Cell Stress Chaperones, 8, 144, 10.1379/1466-1268(2003)008<0144:CACOAM>2.0.CO;2 Ragland, 2017, From bacterial killing to immune modulation: recent insights into the functions of lysozyme, PLoS Pathog., 13, 10.1371/journal.ppat.1006512 Ramos Aguila, 2021, Temperature-dependent biological control effectiveness of Tamarixia radiata (Hymenoptera: Eulophidea) under laboratory conditions, J. Econ. Entomol., 10.1093/jee/toab130 Ravagnan, 2001, Heat-shock protein 70 antagonizes apoptosis-inducing factor, Nat. Cell Biol., 3, 839, 10.1038/ncb0901-839 Ritossa, 2005, A new puffing pattern induced by temperature shock and DNP in drosophila, Experientia, 18, 571, 10.1007/BF02172188 Shi, 2012, Glutathione S-transferase (GST) genes in the red flour beetle, Tribolium castaneum, and comparative analysis with five additional insects, Genomics, 100, 327, 10.1016/j.ygeno.2012.07.010 Spreen, 2014, An economic assessment of the impact of Huanglongbing on citrus tree plantings in Florida, HortScience, 49, 1052, 10.21273/HORTSCI.49.8.1052 Sun, 2005, Small heat shock proteins: molecular structure and chaperone function, Cell. Mol. Life Sci., 62, 2460, 10.1007/s00018-005-5190-4 Takayama, 2003, Heat-shock proteins as regulators of apoptosis, Oncogene, 22, 9041, 10.1038/sj.onc.1207114 Tang, 2014, Transcriptome immune analysis of the invasive beetle Octodonta nipae (Maulik) (Coleoptera: Chrysomelidae) parasitized by Tetrastichus brontispae Ferrière (Hymenoptera: Eulophidae), PLoS One, 9 Tang, 1990, On the parasite complex of Diaphorina citri Kuwayama (Homoptera: Psyllidae) in Asian-Pacific and other areas, 240 Tang, 1989, A preliminary survey on the parasite complex of Diaphorina citri Kuwayama (Homoptera: Psyllidae) in Fujian, 10 Trapnell, 2010, Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation, Nat. Biotechnol., 28, 511, 10.1038/nbt.1621 Udono, 1993, Heat shock protein 70-associated peptides elicit specific cancer immunity, J. Exp. Med., 178, 1391, 10.1084/jem.178.4.1391 Wang, 2019, Genome-wide identification and characterization of HSP gene superfamily in whitefly (Bemisia tabaci) and expression profiling analysis under temperature stress, Insect Sci., 26, 44, 10.1111/1744-7917.12505 Xie, 2011, KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases, Nucleic Acids Res., 39, W316, 10.1093/nar/gkr483 Xiong, 2001, Abiotic stress signal transduction in plants: molecular and genetic perspectives, Physiol. Plant., 112, 152, 10.1034/j.1399-3054.2001.1120202.x Xiong, 2019, Comp. Biochem. Physiol. Genomics Proteomics, 30, 256, 10.1016/j.cbd.2019.03.009 Yi, 2021, Transcriptome responses to heat and cold stress in prepupae of Trichogramma chilonis, Ecol. Evol., 11, 4816, 10.1002/ece3.7383 Yonehara, 1996, Heat-induced chaperone activity of HSP90, J. Biol. Chem., 271, 2641, 10.1074/jbc.271.5.2641 Zhang, 2015, Transcriptome responses to heat- and cold-stress in ladybirds (Cryptolaemus montrouzieri Mulasnt) analyzed by deep-sequencing, Biol. Res., 48, 66, 10.1186/s40659-015-0054-3 Zhou, 2018, Comparative analysis of the Monochamus alternatus immune system, Insect Sci., 25, 581, 10.1111/1744-7917.12453