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Comparative gut transcriptome analysis reveals differences between virulent and avirulent Russian wheat aphids, Diuraphis noxia

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Abstract

The Russian wheat aphid, Diuraphis noxia, is a destructive pest of cereal crops that exhibits virulence to D. noxia resistance genes in wheat. Therefore, it is important to identify D. noxia virulence factors. The insect gut, the primary site of defense to ingested toxins, is also a likely site of differential gene expression in virulent insects. Comparative analyses of gut transcriptomes from virulent and avirulent D. noxia can improve an understanding of aphid gut physiology and may reveal factors critical to compatible D. noxia–wheat interactions. A total of 4,600 clones were sequenced from gut cDNA libraries prepared from avirulent (biotype 1) and virulent (biotype 2) D. noxia feeding on biotype 1-resistant wheat. A majority of the sequences (66 % in biotype 1, 64 % in biotype 2) matched those from the NR database. BLASTx analysis of sequences with the highest E-values revealed that 59 % of the biotype 1 sequences matched those of the pea aphid, Acyrthosiphon pisum. However, only 17 % of the biotype 2 sequences were similar to those of A. pisum. RT-qPCR expression analyses confirmed that the biotype 2 gut transcriptome differs significantly from that of biotype 1. A transcript coding the tRNA-Leu gene was significantly up-regulated in the biotype 2 transcriptome, strongly suggesting that leucine metabolism is a critical factor in biotype 2 survival. Many more transcripts encoding protease inhibitors occurred in the avirulent biotype 1 gut than in the gut of virulent biotype 2. However, more protease transcripts occurred in the biotype 2 gut than in the biotype 1 gut, suggesting that the avirulent biotype produces protease inhibitors in response to plant proteases. The virulent biotype 2 produces trypsin-like and chymotrypsin-like serine protease counter-defenses to overcome biotype 1-resistant plants.

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References

  • Bajgar A, Jindra M, Doleze D (2012) Autonomous regulation of the insect gut by circadian genes acting downstream of juvenile hormone signaling. Proc Natl Acad Sci USA. doi:10.1073/pnas.1217060110

  • Basky Z (2003) Biotypic and pest status differences between Hungarian and South African populations of Russian wheat aphid, Diuraphis noxia (Kurdjumov) (Homoptera: Aphididae). Pest Manag Sci 59:1152–1158

    Article  CAS  PubMed  Google Scholar 

  • Berzonsky WA, Ding H, Haley SD, Lamb RJ, McKenzie RIH, Ohm HW, Patterson FL, Peairs FB, Porter DR, Ratcliffe RH, Shanower TG (2003) Breeding wheat for resistance to insects. Plant Breed Rev 22:221–296

    Google Scholar 

  • Boigegrain R-A, Pugnière M, Paroutaud P, Castrod B, Brehélin M (2000) Low molecular weight serine protease inhibitors from insects are proteins with highly conserved sequences. Insect Biochem Mol Biol 30:145–152

    Article  CAS  PubMed  Google Scholar 

  • Boissière A, Tchioffo MT, Bachar D, Abate L, Marie A, Nsango SE, Shahbazkia HR, Awono-Ambene PH, Levashina EA, Christen R et al (2012) Midgut microbiota of the malaria mosquito vector Anopheles gambiae and interactions with Plasmodium falciparum infection. PLoS Pathog 8:e1002742

    Article  PubMed Central  PubMed  Google Scholar 

  • Bown DP, Gatehouse JA (2004) Characterization of digestive carboxypeptidase from the insect pest corn earworm (Helicoverpa armigera) with novel specificity towards C-terminal glutamate residues. Eur J Biochem 10:2000–2011

    Article  Google Scholar 

  • Buchner P (1965) Endosymbiosis of animals with plant microorganisms. Interscience Publishers, New York

    Google Scholar 

  • Burd JD, Porter DR, Puterka GJ, Haley SD, Peairs FB (2006) Biotypic variation among North American Russian wheat aphid populations. J Econ Entomol 99:1862–1866

    Article  PubMed  Google Scholar 

  • Chi YH, Salzman RA, Balfe S, Ahn JE, Sun W, Moon J, Yun DJ, Lee SY, Higgins TJV, Pittendrigh B, Murdock LL, Zhu-Salzman K (2009) Cowpea bruchid midgut transcriptome response to a soybean cystatin–costs and benefits of counter-defence. Insect Mol Biol 18:97–110

    Article  CAS  PubMed  Google Scholar 

  • Clua AA, Castro AM, Ramos S, Chidichimo H, Dixon AFG (2004) The biological characteristics and distribution of Schizaphis graminum and Diuraphis noxia in Argentina and Chile. Eur J Entomol 101:193–198

    Article  Google Scholar 

  • Dolatti L, Ghareyazie B, Moharramipour S, Noori-Daloii MR (2005) Evidence for regional diversity and host adaptation in Iranian populations of the Russian wheat aphid. Entomol Exp Appl 114:171–180

    Article  CAS  Google Scholar 

  • Douglas AE (2003) Nutritional physiology of aphids. Adv Insect Physiol 31:73–140

    Article  CAS  Google Scholar 

  • ffrench-Constant RH, Anthony N, Aronstein K, Rocheleau T, Stilwell G (2000) Cyclodiene insecticide resistance: from molecular to population genetics. Annu Rev Entomol 45:449–466

    Article  CAS  PubMed  Google Scholar 

  • Gerardo NM, Altincicek B, Anselme C, Atamian H, Barribeau SM, de Vos M, Duncan EJ, Evans JD, Gabaldón T, Ghanim M et al (2010) Immunity and other defenses in pea aphids, Acyrthosiphon pisum. Genome Biol 11:R21

    Article  PubMed Central  PubMed  Google Scholar 

  • Goates BS, Sumerford DV, Hellmich RL, Lewis LC (2008) Mining an Ostrinia nubilalis midgut expressed sequence tag (EST) library for candidate genes and single nucleotide polymorphisms (SNPs). Insect Mol Biol 17:607–620

    Article  Google Scholar 

  • Goggin FL (2007) Plant–aphid interactions: molecular and ecological perspectives. Curr Opin Plant Biol 10:399–408

    Article  CAS  PubMed  Google Scholar 

  • Grossheim NA (1914) The barley aphid, Brachycolus noxius Mordvilko. In: Memoirs of the National History Museum of the Zemstvo of the Government of Taurida, Sinferopol, vol 3, pp 35–78

  • Haley SD, Peairs FB, Walker CB, Rudolph JB, Randolph TL (2004) Occurrence of new Russian wheat aphid biotype in Colorado. Crop Sci 44:1589–1592

    Article  Google Scholar 

  • Hunter WB, Dang PM, Bausher MG, Chaparro JX, McKendree W, Shatters RG Jr, McKenzie CL, Sinisterra XH (2003) Aphid biology: expressed genes from alate Toxoptera citricida, the brown citrus aphid. J Insect Sci 3:23

    CAS  PubMed Central  PubMed  Google Scholar 

  • Khajuria C, Zhu Y-C, Chen MS, Buschman LL, Higgins RA, Yao J, Muthukrishnan S, Zhu KY (2009) Expressed sequence tags from the European corn borer (Ostrinia nubilalis) larval gut: identification of the genes potentially involved in Bacillus thuringiensis toxicity and resistance. BMC Genom 10:286

    Article  Google Scholar 

  • Khan SA, Murugan M, Starkey S, Smith CM (2009) Inheritance and categories of resistance in wheat to Russian wheat aphid (Hemiptera: Ahididae) biotype 1 and biotype 2. J Econ Entomol 102:1654–1662

    Article  CAS  PubMed  Google Scholar 

  • Kikuchi Y, Hayatsu M, Hosokawa T, Nagayama A, Tago K, Fukatsu T (2012) Symbiont-mediated insecticide resistance. Proc Natl Acad Sci USA 109:8618–8622

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lazzari S, Starkey S, Reese J, Ray-Chandler A, McCubrey R, Smith CM (2009) Feeding behavior of Russian wheat aphid (Hemiptera: Aphididae) biotype 2 in response to wheat exhibiting antibiosis and tolerance resistance. J Econ Entomol 102:1291–1300

    Article  CAS  PubMed  Google Scholar 

  • Malinga JN, Kinuya MG, Kamau AW, Wanjama JK, Awalla JO, Pathak RS (2007) Biotypic and genetic variation within tropical populations of Russian wheat aphid, Diuraphis noxia (Kurdjumov) (Homoptera: Aphididae) in Kenya. J Entomol 4:350–361

    Article  CAS  Google Scholar 

  • Mao J, Zeng F (2012) Feeding-based RNA interference of a gap gene is lethal to the pea aphid, Acyrthosiphon pisum. Plos ONE 7:e48718. doi:10.1371/journal.pone.0048718

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Marasas C (1999) Wheat management practices and adoption of the Russian wheat aphid integrated control programme in the study area. Socio-economic impact of the Russian wheat aphid integrated control programme. PhD thesis, University of Pretoria, Pretoria, South Africa

  • Moran NA, Baumann P (2000) Bacterial endosymbionts in animals. Curr Opin Microbiol 3:270–275

    Article  CAS  PubMed  Google Scholar 

  • Mornhinweg DW, Brewer MJ, Porter DR (2006) Effect of Russian wheat aphid on yield and yield components of field grown susceptible and resistant spring barley. Crop Sci 49:36–42

    Article  Google Scholar 

  • Morris K, Lorenzen MD, Hiromasa Y, Tomich JM, Oppert C, Elpidina EN, Vinokurov K, Jurat-Fuentes JL, Fabrick J, Oppert B (2009) Tribolium castaneum larval gut transcriptome and proteome: a resource for the study of the coleopteran gut. J Proteome Res 8:3889–3898

    Article  CAS  PubMed  Google Scholar 

  • Nishikori K, Kubo T, Morioka M (2009) Morph-dependent expression and subcellular localization of host serine carboxypeptidase in bacteriocytes of the pea aphid associated with degradation of the endosymbiotic bacterium Buchnera. Zool Sci 6:415–420

    Article  Google Scholar 

  • Pedra JHF, Brandt A, Westerman R, Lobo N, Li HM, Romero-Severson J, Murdock LL, Pittendrigh BR (2003) Transcriptome analysis of the cowpea weevil bruchid: identification of putative proteinases and a-amylases associated with food breakdown. Insect Mol Biol 12:405–412

    Article  CAS  PubMed  Google Scholar 

  • Ramsey JS, Wilson AC, de Vos M, Sun Q, Tamborindeguy C, Winfield A, Malloch G, Smith DM, Fenton B, Gray SM, Jander G (2007) Genomic resources for Myzus persicae: EST sequencing. SNP identification, and microarray design. BMC Genom 8:423

    Article  Google Scholar 

  • Ramsey JS, Rider DS, Walsh T, de Vos M, Gordon K, Ponnala L, Roe BA, Jander G (2010) Comparative analysis of detoxification enzymes in Acrythrosiphon pisum and Myzus persicae. Insect Mol Biol 19:155–164

    Article  CAS  PubMed  Google Scholar 

  • Ribeiro JM, Alarcon-Chaidez F, Francischetti IM, Mans BJ, Mather TN, Valenzuela JG, Wikel SK (2006) An annotated catalog of salivary gland transcripts from Ixodes scapularis ticks. Insect Biochem Mol Biol 36:111–129

    Article  CAS  PubMed  Google Scholar 

  • Saadati F, Bandani AR (2011) Effects of serine protease inhibitors on growth and development and digestive serine proteinases of the Sunn pest, Eurygaster integriceps. J Insect Sci 11:72

    Article  PubMed Central  PubMed  Google Scholar 

  • Sabater-Munoz B, Legeai F, Rispe C, Bonhomme J, Dearden P, Dossat C, Duclert A, Gauthier J-P, Ducray DG, Hunter W et al (2006) Large-scale gene discovery in the pea aphid Acyrthosiphon pisum (Hemiptera). Genome Biol 7:21

    Article  Google Scholar 

  • Simpson RM, Newcomb RD, Gatehouse HS, Crowhurst RN, Chagne D, Gatehouse LN, Markwick NP, Beuning LL, Murray C, Marshall SD, Yauk Y-K, Nain B, Wang Y-Y, Gleave AP, Christeller JT (2007) Expressed sequence tags from the midgut of Epiphyas postvittana (Walker) (Lepidoptera: Tortricidae). Insect Mol Biol 16:675–690

    Article  CAS  PubMed  Google Scholar 

  • Sinha DK, Lakshmi M, Anuradha G, Rahman SJ, Siddiq EA, Bentur JS, Nair S (2011) Serine proteases-like genes in the Asian rice gall midge show differential expression in compatible and incompatible interactions with rice. Int J Mol Sci 12:2842–2852

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Smith CM, Belay T, Stauffer C, Stary P, Kubeckova I, Starkey S (2004) Identification of Russian wheat aphid (Homoptera: Aphididae) biotypes virulent to the Dn4 resistance gene. J Econ Entomol 97:1112–1117

    Article  CAS  PubMed  Google Scholar 

  • Souza EJ (1998) Host plant resistance to Russian wheat aphid (Homoptera: Aphididae) in wheat and barley. In: Quisenberry SS, Peairs FB (eds) A Response Model for an Introduced Pest-The Russian Wheat Aphid. Thomas Say Publication in Entomology, Entomological Society of America, MD, pp 122–147

    Google Scholar 

  • Starý P (1996) The expansive Russian Wheat Aphid, Diuraphis noxia (Mordw.) detected in the Czech Republic. Anzeiger Schädlingskunde/J Pest Sci 69:19–20

    Google Scholar 

  • Swanevelder ZH, Surridge AK, Venter E, Botha AM (2010) Limited endosymbiont variation in Diuraphis noxia (Hemiptera: Aphididae) biotypes from the United States and South Africa. J Econ Entomol 103:887–897

    Article  CAS  PubMed  Google Scholar 

  • Tagu D, Prunier-Leterme N, Legeai F, Gauthier JP, Duclerc A, Sabater-Muñoz B, Bonhomme J, Simon JC (2004) Annotated expressed sequence tags for studies of the regulation of reproductive modes in aphids. Insect Biochem Mol Biol 8:809–822

    Article  Google Scholar 

  • Tagu D, Sabater-Muñoz B, Simon J-C (2005) Deciphering reproductive polyphenism in aphids. Invertebr Reprod Dev 48:71–80

    Article  Google Scholar 

  • Terra WR, Ferreira C (2005) Biochemistry of digestion. In: Gilbert LI, Iatrou K, Gill SS (eds) Comprehensive molecular insect science. Elsevier, Pergamon, Oxford, UK, pp 171–224

    Chapter  Google Scholar 

  • Tolmay V, du Toit F, Smith CM (2006) Registration of Russian wheat aphid resistant near isogenic lines developed in South Africa. Crop Sci 46:478–480

    Article  Google Scholar 

  • Vandewoestijne S, Schtickzelle N, Baguette M (2008) Positive correlation between genetic diversity and fitness in a large, well-connected metapopulation. BMC Biol 6:46

    Article  PubMed Central  PubMed  Google Scholar 

  • Walters MC, Penn F, Du Toit F, Botha TC, Aalbersberg K, Hewitt PH, Broodryk SW (1980) The Russian wheat aphid. Farm South Africa Leafl Serv Wheat G3:1–6

    Google Scholar 

  • Wang Y, Gilbreath TM III, Kukutla P, Yan G, Xu J (2011) Dynamic gut microbiome across life history of the malaria mosquito Anopheles gambiae in Kenya. PLoS ONE 6:e24767

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Webster JA, Kenkel P (1999) Benefits of managing small-grain pests with plant resistance. In: Wiseman BR, Webster JA (eds) Economic, environmental and social benefits of resistance in field crops. Thomas Say Publication in Entomology, Entomological Society of America, MD, pp 87–114

    Google Scholar 

  • Weiland AA, Peairs FB, Randolph JB, Rudolph JB, Haley SD, Puterka GJ (2008) Biotypic diversity in Colorado Russian wheat aphid (Hemiptera: Aphididae) populations. J Econ Entomol 101:569–574

    Article  PubMed  Google Scholar 

  • Wilkinson TL, Ishikawa H (2000) Injection of essential amino acids substitutes for bacterial supply in aposymbiotic pea aphids (Acyrthosiphon pisum). Entomol Exp Appl 94:85–91

    Article  CAS  Google Scholar 

  • Zhang R, Liang H, Ren L, Zhang G (2001) Induced life cycle transition from holocycly to anholocycly of the Russian wheat aphid (Homoptera: Aphididae). Sci China Ser C Life Sci 44:1–4

    Article  Google Scholar 

  • Zhang S, Shukle R, Mittapalli O, Zhu Y-C, Reese JC, Wang H, Hua B-Z, Chen MS (2010) The gut transcriptome of a gall midge, Mayetiola destructor. J Insect Physiol 56:1198–1206

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Dr. Marcelo Ortigao for critical reviews of drafts of the manuscript. This research was supported by grants to CMS from the Kansas Wheat Commission, the Kansas Crop Improvement Association, and the Kansas Agricultural Experiment Station. This is contribution No. 13-356-J of the Kansas Agricultural Experiment Station. This research was performed in the Gene Expression Facility at Kansas State University, which was supported through the National Science Foundation Grant, DBI 0421427.

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Correspondence to C. Michael Smith.

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Communicated by Handling Editor: Joseph Dickens.

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Anathakrishnan, R., Sinha, D.K., Murugan, M. et al. Comparative gut transcriptome analysis reveals differences between virulent and avirulent Russian wheat aphids, Diuraphis noxia . Arthropod-Plant Interactions 8, 79–88 (2014). https://doi.org/10.1007/s11829-014-9293-4

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