Skip to main content
SpringerLink
Log in

A coevolutionary conundrum: the arms race between Diuraphis noxia (Kurdjumov) a specialist pest and its host Triticum aestivum (L.)

  • Review Paper
  • Published:
Arthropod-Plant Interactions Aims and scope Submit manuscript

Abstract

Aphids seemingly hold the competitive edge above plants in their arms race because of their long evolutionary time and standing association with endosymbionts. However, the advent of modern crop biotechnology has added a further component to the plant’s adaptive arsenal. In specialist associations, as in the case of Diuraphis noxia with its limited host range, both partners in the association exert innovative strategies during the macroevolutionary process that leads to the development of novel adaptive traits. In the current review, the concept of an uneven enigmatic arms race between the insect pest and its host is being argued. Many intricacies at play in the association are highlighted and adaptive strategies discussed, which may provide opportunities for either partner in the association to overcome the others’ barriers during their interaction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Notes

  1. Calculated using the formulae of Doležel and Bartoš (2005) where 1 pg = 0.978 Mb.

References

  • Aaronsohn A (1910) Agricultural and botanical explorations in Palestine. Bureau Plant Industry Bull USDA 180:1–63

    Google Scholar 

  • Argrawal AA, Fishbein M (2006) Plant defense syndromes. Ecology 87(7):S132–S149

    Article  Google Scholar 

  • Arumuganathan K, Earle ED (1991) Nuclear DNA content of some important plant species. Plant Mol Biol Rep 9:208–218

    Article  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • Baumann P, Lai C-Y, Baumann L, Rouhbakhsh D, Moran NA, Clark MA (1995) Mutualistic associations of aphids and prokaryotes: biology of the genus Buchnera. Appl Environ Microb 61(1):1–7

    CAS  Google Scholar 

  • Baumann P, Moran NA, Baumann L (1997) The evolution and genetics of aphid endosymbionts. Bioscience 47:12–20

    Article  Google Scholar 

  • Berger S, Sinha AK, Roitsch T (2007a) Plant physiology meets phytopathology: plant primary metabolism and plant-pathogen interactions. J Exp Bot 58:4019–4026

    Article  PubMed  CAS  Google Scholar 

  • Berger S, Benediktyova Z, Matous K, Bonfig K, Mueller MJ, Nedbal L, Roitsch T (2007b) Visualization of dynamics of plant-pathogen interaction by novel combination of chlorophyll fluorescence imaging and statistical analysis: differential effects of virulent and avirulent strains of P. syringae and of oxylipins on A. thaliana. J Exp Bot 58:797–806

    Article  PubMed  CAS  Google Scholar 

  • Bilgin DD, Aldea M, O’Neill BF, Benitez M, Li M, Clough SJ, DeLucia EH (2008) Elevated ozone alters soybean-virus interaction. Mol Plant Microbe Interact 21:1297–1308

    Article  PubMed  CAS  Google Scholar 

  • Bilgin DD, Zavala JA, Zhu J, Clough SJ, Ort DR, DeLucia EH (2010) Biotic stress globally downregulates photosynthesis genes. Plant Cell Environ 33:1597–1613

    Article  PubMed  CAS  Google Scholar 

  • Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Ann Rev Plant Biol 60:379–406

    Article  CAS  Google Scholar 

  • Bos JLB, Prince D, Pitino M, Maffei ME, Win J, Hogenhout SA (2010) A functional genomics approach identifies candidate effectors from the aphid species Myzus persicae (green peach aphid). PLoS Genetics 6 (11): e1001216, 1–13

    Google Scholar 

  • Botha A-M, Lacock L, van Niekerk C, Matsioloko MT, du Preez FB, Loots S, Venter E, Kunert KJ, Cullis CA (2005) Is Photosynthetic transcriptional regulation in Triticum aestivum L. cv. ‘TugelaDN’ a contributing factor for tolerance to Diuraphis noxia (Homoptera: Aphididae)? Plant Cell Rep 25:41–54

    Article  PubMed  CAS  Google Scholar 

  • Botha A-M, Li Y-C, Lapitan NLV (2006) Cereal host interactions with Russian wheat aphid: a review. J Plant Interact 1:211–222

    Article  CAS  Google Scholar 

  • Botha A-M, Swanevelder ZH, Schultz T, Van Eck L, Lapitan NLV (2008). Deciphering defense strategies that are elucidated in wheat containing different Dn resistance genes. In: Proceedings of the 11th wheat genetics symposium, Brisbane, Australia, August 24–29, 2008. p. O29 Edited by Appels R, Eastwood R, Lagudah E, Langridge P, Lynne MM (eds). Sydney University Press. ISBN: 9781920899141, http://hdl.handle.net/2123/3514

  • Botha A-M, Swanevelder ZH, Lapitan NLV (2010) Transcript profiling of wheat genes expressed during feeding by two different biotypes of Diuraphis noxia. J Environ Entomol 39(4):1206–1231

    Article  CAS  Google Scholar 

  • Botha A-M, Van Eck L, Jackson CS, Burger NFV, Schultz T (2011) Biotic stress and photosynthetic gene expression. In: Najafpour M (ed) Applied photosynthesis/book 2. INTECH Inc Open Access Publishers. ISBN 979-953-307-664-4

  • Botha A-M, Burger NFV, Castro A-M, El-Bouhsinni M, Jankielsohn A, Lapitan NLV, Pearce F, Puterka G, Smith CM, Surovcova M (2012) Next generation sequencing of the genomes of 10 international RWA biotypes. Joint meeting: 20th Biennial International Plant Resistance to Insects Workshop and Annual session of Western Extension/Education Research Activity-066 (WERA-066): integrated management of Russian wheat aphid and other cereal arthropod pests, April 1–4, 2012, Minneapolis, Minnesota, USA. Programme, poster # 3, p. 29. http://www.hpr2012.umn.edu/

  • Boyko EV, Smith CM, Vankatappa T, Bruno J, Deng Y, Starkey S, Klaahsen D (2006) The molecular basis of plant gene expression during aphid invasion: wheat Pto- and Pti-like sequences modulate aphid-wheat interaction. J Econ Entomol 99:1430–1445

    Article  PubMed  CAS  Google Scholar 

  • Brenchley R, Spanning M, Pheifer M, Barker GLA, D’Amore R, Allen AM, McKenzie N, Kramer M, Kerhornou A, Bolsen D, Kay S, Waite D, Trick M, Bancroft I, Gu Y, Huo M-C, Sehgal S, Gill B, Kainian S, Anderson O, Kersey P, Dvorak J, McCombie WR, Hall A, Mayer KFX, Edwards KJ, Bevan MW, Hall N (2012) Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature 705(491):705–710

    Article  CAS  Google Scholar 

  • Brues CT (1920) The selection of food plants by insects with special reference to lepidopterous larvae. Am Nat 54:313–332

    Article  Google Scholar 

  • Bruton DB, Mitchell F, Fletcher J, Pair SD, Wayadande A, Melcher U, Brady J, Bextine B, Popham TW (1998) Serratia marcescens, a phloem-colonizing, squash bug-transmitted bacterium: casual agent of cucurbit yellow vine disease. Plant Dis 87:512–520

    Article  Google Scholar 

  • Bruton DB, Brady J, Mitchell F, Bextine B, Wayadande A, Pair S, Fletcher J, Melcher U (2001) Yellow vine of cucurbits: pathogenicity of Serratia marcescens and transmission by Anasa tristis (abstract). Phytopathology 91(suppl.):S11

    Google Scholar 

  • Burd JD, Burton RL (1992) Characterization of plant damage caused by Russian wheat aphid (Homoptera: Aphididae). J Econ Entomol 85:2015–2022

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Chatterjee S, Almeida RPP, Lindow S (2008) Living in two worlds: the plant and insect lifestyles of Xylella fastidiosa. Annu Rev Phytopathol 46:243–271

    Article  PubMed  CAS  Google Scholar 

  • Chen Y, Evans J, Feldlaufer M (2006) Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera. J Invertbr Pathol 92:152–159

    Article  Google Scholar 

  • Chrisholm DT, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814

    Article  CAS  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

    Google Scholar 

  • Cooper WR, Dillwith JW, Puterka GJ (2011) Comparisons of salivary proteins from five aphid (Hemiptera: Aphididae) species. J Environ Entomol 40:151–156

    Article  CAS  Google Scholar 

  • Cui F, Smith CM, Reese J, Edwards O, Reeck G (2012) Polymorphisms in salivary-gland transcripts of Russian wheat aphid biotypes 1 and 2. Insect Sci 19:429–440

    Article  CAS  Google Scholar 

  • Darwin C (1859) On the Origin of Species, 1st edn. John Murray, London

    Google Scholar 

  • Davis GK (2012) Cyclical parthenogenesis and viviparity in aphids as evolutionary novelties. J Exp Zool 318B:448–459

    Article  Google Scholar 

  • Dethier VG (1954) Evolution of feeding preferences in phytophagous insects. Evolution 8:32–54

    Article  Google Scholar 

  • Dinant S, Bonnemain JL, Girousse C, Kehr J (2010) Phloem sap intricacy and interplay with aphid feeding. CR Biology 333:504–515

    Article  Google Scholar 

  • Dixon AFG (1998) Aphid ecology, 2nd edn. Chapman & Hall, London

    Google Scholar 

  • Doležel J, Bartoš J (2005) Plant DNA flow cytometry and the estimation of genome size. Am Bot 95:99–110

    Article  CAS  Google Scholar 

  • Drummond DA, Bloom JD, Adam C, Wilke CO, Arnold FH (2005) Why highly expressed proteins evolve slowly. Proc Natl Acad Sci USA 102:14338–14343

    Article  PubMed  CAS  Google Scholar 

  • Du Preez FB, Myburg AA, Venter E, Botha AM (2008) Resistance genes in the Triticeae and the dynamics of divergence before duplication. S Afr J Bot 74:51–64

    Article  CAS  Google Scholar 

  • Du YJ, Poppy GM, Powell W, Pickett JA, Wadhama IJ, Woodcock CM (1998) Identification of semichemicals released during aphid feeding that attract parasitoid Aphidius ervi. J Chem Ecol 24:1355–1368

    Article  CAS  Google Scholar 

  • Duron O, Hurst GDD (2013) Arthropods and inherited bacteria: from counting the symbionts to understanding how symbionts count. BMC Biol 11:45. http://www.biomedcentral.com/1741-7007/11/45

  • Eden-Green SJ, Billing E (1974) Fireblight. Rev Plant Pathol 53:353–365

    Google Scholar 

  • Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608

    Article  Google Scholar 

  • Esker PD, Nutter FW (2002) Assessing the risk of Stewart’s disease of corn through improved knowledge of the role of the corn flea beetle vector. Phytopathology 96:668–670

    Article  Google Scholar 

  • Ferreira SA, Boley RA (1992) Erwinia tracheiphila bacterial wilt of cucurbits. Department of Plant Pathology, CTAHR, University of Hawaii atMonoa (Online Database). Available at http://www.extento.hawaii.edu/Kbase/crop/Type/e_trach.htm

  • Fine PVA, Mesones I, Coley PD (2004) Herbivores promote habitat specialization by trees in Amazonian forests. Science 305:663–665

    Article  PubMed  CAS  Google Scholar 

  • Flor HH (1971) Current status of the gene-for-gene concept. Ann Rev Phytopath 9:275–296

    Article  Google Scholar 

  • Fogaça AC, Zaini PA, Wulff NA, da Silva PI, F’azio MA, Miranda A, Daffre S, da Silva AM (2010) Effects of the antimicrobial peptide gomesin on the global gene expression profile, virulence and biofilm formation of Xylella fastidiosa. FEMS Microbiol Lett 306:152–159

    Article  PubMed  CAS  Google Scholar 

  • Fouché A, Verhoeven RL, Hewitt PH, Walters MC, Kriel CF, De Jager J (1984) Russian wheat aphid (Diuraphis noxia) feeding damage on wheat, related cereals and a Bromus grass species. In: MC Walters (ed) Bloemfontein. Technical communication Department of Agriculture Republic of South Africa, vol 191, pp 22–33

  • Foyer C, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11(4):861–905

    Article  PubMed  CAS  Google Scholar 

  • Fraenkel G (1959) The raison d’être of secondary plant substances. Science 129:1466–1470

    Article  PubMed  CAS  Google Scholar 

  • Frost CJ, Mescher MC, Carlson JE, De Moraes CM (2008) Plant defense priming against herbivores getting ready for a different battle. Plant Physiol 146:818–824

    Article  PubMed  CAS  Google Scholar 

  • Futuyma DJ (2008) Sympatric speciation: norm or exception? In: Tilmon K (ed) Specialization, speciation, and radiation. Univ California Press, Berkeley, pp 136–148

    Google Scholar 

  • Futuyma DJ, Agrawal AA (2009) Macroevolution and the biological diversity of plants and herbivores. Proc Natl Acad Sci USA 106:18054–18061

    Article  PubMed  CAS  Google Scholar 

  • Gill BS, Appels R, Botha-Oberholster A-M, Buell CR, Bennetzen JL, Chalhoub B, Chumley F, Dvorak J, Iwanaga M, Keller B, Li W, McCombie WR, Ogihara Y, Quetier F, Sasaki T (2004) Workshop report: a workshop report on wheat genome sequencing: international genome research on wheat consortium. Genetics 168:1087–1096

    Article  PubMed  Google Scholar 

  • Giordanengo P, Brunissen L, Rusterucci C, Vincent C, van Bel A, Dinant S, Girousse C, Faucher M, Bonnemain JL (2010) Compatible plant-aphid interactions: how aphids manipulate plant responses. CR Biol 333:516–523

    Article  Google Scholar 

  • Gonzalez AJ, Tello JC, de Cara M (2005) First report of Erwinia persicina from Phaseolus vulgaris in Spain. Plant Dis 89:109

    Article  Google Scholar 

  • Haile FJ, Higley LC, Ni X, Quisenberry SS (1999) Physiological and growth tolerance in wheat to Russian wheat aphid (Homoptera: Aphididae) injury. Environ Entomol 28:787–794

    Google Scholar 

  • Heidel AJ, Baldwin IT (2004) Microarray analysis of salicylic acid-and jasmonic acid-signalling in responses of Nicotiana attenuate to attack by insects from multiple feeding guilds. Plant Cell Environ 27:1362–1373

    Article  CAS  Google Scholar 

  • Heng-Moss TM, Ni X, Macedo T, Markwell JP, Baxendale FP, Quisenberry SS, Tolmay V (2003) Comparison of chlorophyll and carotenoid concentrations among Russian wheat aphid (Homoptera: Aphididae)-infested wheat isolines. J Econ Entomol 96:475–481

    Article  PubMed  CAS  Google Scholar 

  • Hougen-Eitzman D, Rausher MD (1994) Interactions between herbivorous insects and plant–insect coevolution. Am Nat 143:677–697

    Article  Google Scholar 

  • Jankielsohn A (2011) Distribution and Diversity of Russian Wheat Aphid (Hemiptera: Aphididae) Biotypes in South Africa and Lesotho. J Econ Entomol 104(5):1736–1741

    Article  PubMed  Google Scholar 

  • Johal GS, Gray J, Gruis D, Briggs SP (1995) Convergent insights into mechanisms determining disease and resistance responses in plant–fungal interactions. Can J Bot 73(Suppl. 1):468–474

    Article  Google Scholar 

  • Jones DA, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  PubMed  CAS  Google Scholar 

  • Jones DA, Takemoto D (2004) Plant innate immunity—direct and indirect recognition of general and specific pathogen-associated molecules. Curr Opin Immunol 16:48–62

    Article  PubMed  CAS  Google Scholar 

  • Jones JW, Byers JR, Butts RA, Harris JL (1989) A new pest in Canada: Russian wheat aphid, Diuraphis noxia (Mordvilko) (Homoptera: Aphididae). Can Entomol 121:623–624. doi:10.4039/Ent121623-7

    Article  Google Scholar 

  • Jorde LB, Bamshad M, Rogers AR (1998) Using mitochondrial and nuclear DNA markers to reconstruct human evolution. Bioessays 20(2):126–136

    Article  PubMed  CAS  Google Scholar 

  • Keen NT (1990) Gene-for-gene complementarity in plant-pathogen interactions. Ann Rev Genet 24:425–429

    Article  Google Scholar 

  • Kellogg EA (2001) Evolutionary history of the grasses. Plant Physiol 125:1198–1205

    Article  PubMed  CAS  Google Scholar 

  • Kikuchi Y (2009) Endosymbiotic bacteria in insects: their diversity and culturability. Microbes Environ 24:195–204

    Article  PubMed  Google Scholar 

  • Labbate M, Zhu H, Thung L, Bandara R, Larsen MR, Willcox MDP, Givskov M, Rice SA, Kjelleberg S (2007) Quorum sensing regulation of adhesion in Serratia marcescens MG1 is surface dependent. J Bacteriol 189:2702–2711

    Article  PubMed  CAS  Google Scholar 

  • Laine A-L (2006) Evolution of host resistance: looking for coevolutionary hotspots at small spatial scales. Proc R Soc B 273:267–273

    Article  PubMed  Google Scholar 

  • Lapitan NLV, Li Y-C, Walters RSG, Peng Y, Peairs FB, Botha A-M (2007a) Limited nuclear and mitochondrial DNA variation among Russian wheat aphid (Diuraphis noxia) biotypes from the United States and Africa, American Entomological Society, San Diego, December 9–12. American Entomological Society, San Diego

    Google Scholar 

  • Lapitan NLV, Li Y-C, Peng Y, Botha A-M (2007b) Fractionated extracts of Russian wheat aphid eliciting defense responses in wheat. J Econ Entomol 100:990–999

    Article  PubMed  Google Scholar 

  • Latorre A, Gil R, Silva FJ, Moya A (2005) Chromosomal stasis versus plasmid plasticity in aphid endosymbiont Buchnera aphidicola. Heredity 95:339–347

    Article  PubMed  CAS  Google Scholar 

  • Leister D, Kurth J, Laurie DA, Yano M, Sasaki T et al (1998) Rapid reorganization of resistance gene homologues in cereal genomes. Proc Natl Acad Sci USA 95:370–375

    Article  PubMed  CAS  Google Scholar 

  • Liu X, Meng J, Starkey S, Smith CM (2011) Wheat gene expression is differentially affected by a virulent Russian wheat aphid biotype. J Chem Ecol 37:472–482

    Article  PubMed  CAS  Google Scholar 

  • Miles PW (1999) Aphid saliva. Biol Rev 74:41–85

    Article  Google Scholar 

  • Miller HL, Neese PA, Ketring DL, Dillwith JW (1994) Involvement of ethylene in aphid infestation of barley. J Plant Growth Regul 13:167–171

    Article  CAS  Google Scholar 

  • Mithöfer A, Boland W (2008) Recognition of herbivory-associated molecular patterns. Plant Physiol 146:825–831

    Article  PubMed  CAS  Google Scholar 

  • Monti V, Mandrioli M, Rivi M, Manicardi GV (2012) The vanishing clone: karyotypic evidence for extensive intraclonal genetics variation in the peach potato aphid, Myzus persicae (Hemiptera: Aphididae). Biol J Linn Soc 105:350–358

    Article  Google Scholar 

  • Moran NA (1996) Accelerated evolution and Muller’s rachet in endosymbiotic bacteria. Proc Natl Acad Sci USA 93:2873–2878

    Article  PubMed  CAS  Google Scholar 

  • Moran NA, Plague GR, Sandstrom JP et al (2003) A genomic perspective on nutrient provisioning by bacterial symbionts of insects. Proc Natl Acad Sci USA 100:14543–14548

    Article  PubMed  CAS  Google Scholar 

  • Moran NA, Dunbar HE, Wilcox JL (2005) Regulation of transcription in a reduced bacterial genome: nutrient-provisioning genes of the obligate symbiont Buchnera aphidicola. J Bacteriol 187:4229–4237

    Article  PubMed  CAS  Google Scholar 

  • Morrison WP, Pears FB (1998) Response model concept and economic impact. In: Quisenberry SS, Peairs FB (eds) A response model for an introduced pest—the Russian wheat aphid. Thomas Say Publications in Entomology. Entomological Society of America, Lanham, MD, pp 1–11

    Google Scholar 

  • Murugan M, Smith CM (2012) Barley tolerance of Russian wheat aphid biotype 2 herbivory involves expression of defense response and developmental genes. Plant Signal Behav 7:382–391

    Article  CAS  Google Scholar 

  • Mutti NS, Louis J, Pappan LK, Pappan K, Begum K, Chen MS, Park Y, Dittmer N, Marshall J, Reese JC, Reeck GR (2008) A protein from the salivary glands of the pea aphid, Acyrthosiphon pisum, is essential in feeding on a host plant. Proc Natl Acad Sci USA 105:9965–9969

    Article  PubMed  CAS  Google Scholar 

  • Nabity PD, Zavala JA, DeLucia EH (2009) Indirect suppression of photosynthesis on individual leaves by arthropod herbivory. Ann Bot 13:655–663

    Google Scholar 

  • Nadarasah G, Stavrinide J (2011) Insects as alternative hosts for phytopathogenic bacteria. FEMS Microbiol Rev 35:555–575

    Article  PubMed  CAS  Google Scholar 

  • Nicholson SJ, Hartson SD, Puterka GJ (2012) Proteomic analysis of secreted saliva from Russian Wheat Aphid (Diuraphis noxia Kurd.) biotypes that differ in virulence to wheat. J Proteomics 75(7):2252–2268

    Article  PubMed  CAS  Google Scholar 

  • Novotná J, Havelka J, Stary P, Kouteckŷ P, Vitková M (2011) Karyotype analysis of the Russian wheat aphid, Diuraphis noxia (Kurjumov) (Hemiptera: Aphididae) reveals a large X chromosome with rRNA and histone gene families. Genetica 139:281–289

    Article  PubMed  Google Scholar 

  • Núnĕz-Farfán J, Fornoni J, Valverde PL (2007) The evolution of resistance and tolerance to herbivores. Annu Rev Ecol Evol Syst 38:541–566

    Article  Google Scholar 

  • Painter RH (1951) Insect resistance in crop plants. The Macmillan Co., New York 520 pp

    Google Scholar 

  • Painter RH (1958) Resistance of plants to insects. Ann Rev Entomol 3:267–290

    Article  Google Scholar 

  • Plague GR, Dale C, Moran NA (2003) Low and homogeneous copy number of plasmid-borne symbiont genes affecting host nutrition in Buchnera aphidicola of the aphid Uroleucon ambrosiae. Mol Ecol 12:1095–1100

    Article  PubMed  CAS  Google Scholar 

  • Pollard DG (1973) Plant penetration by feeding aphids (Hemiptera Aphidoidae): a review. Bull Entamol Res 62:631–714

    Article  Google Scholar 

  • Puterka GJ, Burd JD, Burton RL (1992) Biotypic variation in a worldwide collection of Russian wheat aphid (Homoptera: Aphididae). J Econ Entomol 85:1497–1506

    Google Scholar 

  • Puterka GD, Black WC IV, Steiner WM, Burton RK (1993) Genetic variation and phylogenetic relationships among worldwide collections of the Russian wheat aphid, Diuraphis noxia (Mordvilko), inferred from allozyme and RAPD-PCR markers. Heredity 70:604–618

    Article  PubMed  CAS  Google Scholar 

  • Qubbaj T, Reineke A, Zebitz CPW (2005) Molecular interactions between rosy apple aphids, Dysaphis plantaginea, and resistant and susceptible cultivars of its primary host Malus domestica. Entomol Exp Appl 115:145–152

    Article  CAS  Google Scholar 

  • Remaudière G, Remaudière M (1997) Catalogue of the world’s Aphididae: Homoptera Aphididae. INRA Editions (ISSN 1150-3912). p 473

  • Rocha EPC, Feil EJ (2010) Mutational patterns connot explain genome composition: are there any neutral sites in the genomes of bacteria? PLoS Genetics 6:e1001104. doi:10.1371/journal.pgen.1001104

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Saona A, Navarro I, Bari R, Jones JDG (2007) Volatile emission triggered by multiple herbivore damage: beet armyworm and whitefly feeding on cotton plants. J Chem Ecol 29:2539–2550

    Article  Google Scholar 

  • Sandstrom J, Moran NA (1999) How nutritionally imbalanced is phloem sap for aphids? Entomol Exp Appl 91:203–210

    Article  Google Scholar 

  • Sandstrom J, Telang A, Moran NA (2000) Nutritional enhancement of host plants by aphids—a comparison of three aphid species on grasses. J Insect Physiol 46:33–40

    Article  PubMed  CAS  Google Scholar 

  • Santos M, Dianez F, Minano J, Marin F, Martinez S, de Cara M, Tello JC (2009) First report of Erwinia aphidicola from Phaseolus vulgaris and Pisum sativum in Spain. Plant Pathol 58:1171

    Article  Google Scholar 

  • Shanks RMQ, Stella NA, Kalivoda EJ, Doe MR, O’Dee DM, Lathrop KL, Guo FL, Nau GJ (2007) A Serratia marcescens OxyR homolog mediates surface attachment and biofilm formation. J Bacteriol 189:7262–7272

    Article  PubMed  CAS  Google Scholar 

  • Shufran KA, Kirkman LR, Puterka GJ (2007) Absence of mitochondrial DNA sequence variation in Russian wheat aphid (Hemiptera: Aphididae) populations consistent with a single introduction into United States. J Kansas Entomol Soc 80:319–326

    Article  Google Scholar 

  • Smith CM (2009) Global phylogenetics of an invasive species: evidence for multiple invasions into North America. Joint meeting of the Southwestern Branch of the Entomological Society of America and WERA066 (Western Extension/Education Research Activity), February 2009, Stillwater, Oklahoma

  • Smith CM, Boyko EV (2007) Mini review: the molecular bases of plant resistance and defense responses to aphid feeding: current status. Entomol Exp Appl 122:1–16

    Article  CAS  Google Scholar 

  • Smith CM, Clement SL (2012) Molecular bases of plant resistance to arthropods. Annu Rev Entomol 57:309–328

    Article  PubMed  CAS  Google Scholar 

  • Smith CM, Schotzko DJ, Zemetra RS, Souza EJ (1992) Categories of resistance in plant introductions of wheat resistant to the Russian wheat aphid (Homoptera: Aphididae). J Econ Entomol 85:1480–1484

    Google Scholar 

  • Smith CM, Boyko EV, Starkey S (2005) Differential expression of genes in wheat, Tritiucum aestivum L. controlling resistance to the Russian wheat aphid, Diuraphis noxia (Mordvilko). IOBC wprs Bull 28:11–20

    Google Scholar 

  • Smith CM, Liu XM, Wang LJ, Liu X, Chen MS, Starkey S, Bai J (2010) Aphid feeding activates expression of a transcriptome of oxylipin-based defense signals in wheat involved in resistance to herbivory. J Chem Ecol 36:260–276

    Article  PubMed  CAS  Google Scholar 

  • Spinelli F, Ciampolini F, Cresti M, Geider K, Costa G (2005) Influence of stigmatic morphology on flower colonization by Erwinia amylovora and Pantoea agglomerans. Eur J Plant Pathol 113:395–405

    Article  Google Scholar 

  • Srivastava PN (1987) Aphids. Their biology, natural enemies and control. Nutritional Physiology eds. Minks AK, Harrewijn pp. 99 – 121

  • Stavrinides J, No A, Ochman H (2010) A single genetic locus in the phytopathogen Pantoea stewartii enables gut colonization and pathogenicity in an insect host. Environ Microbiol 12:147–155

    Article  PubMed  CAS  Google Scholar 

  • Swanevelder ZH, Surridgte AKJ, Venter E, Botha A-M (2010) Limited endosymbiont variation in Diuraphis noxia (Hemiptera: Aphididae) biotypes from the USA and South Africa. J Econ Entomol 103:887–897

    Article  PubMed  CAS  Google Scholar 

  • Takken FLW, Tameling WIL (2009) To nibble at plant resistance proteins. Science 324:744–745

    Article  PubMed  CAS  Google Scholar 

  • Telang A, Sandstrom J, Dyreson E et al (1999) Feeding damage by Diuraphis noxia results in a nutritionally enhanced phloem diet. Entomol Exp Appl 91:412–493

    Article  Google Scholar 

  • Thao ML, Baumann L, Baumann P, Moran NA (1998) Endosymbionts (Buchnera) from the aphids Schizaphis graminum and Diuraphis noxia have different copy numbers of the plasmid containing the leucine biosynthetic genes. Curr Microbiol 36:238–240

    Article  PubMed  CAS  Google Scholar 

  • The Honeybee Genome Sequencing Consortium (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443:931–949

    Article  CAS  Google Scholar 

  • The International Aphid Genomics Consortium (2010) Genome sequence of the pea aphid Acryrthosiphon pisum. PLOS Biology 8:e1000313

    Article  CAS  Google Scholar 

  • Thompson JN (1999) Specific hypothesis on the geographic mosaic of coevolution. Am Nat 153:S1–S14. doi:10.1086/303208

    Article  Google Scholar 

  • Tian D, Traw MB, Chen JQ, Kreitman M, Bergelson J (2003) Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423:74–77

    Article  PubMed  CAS  Google Scholar 

  • Tjallingii WF (2006) Secretory secretions by aphids interacting with proteins of phloem wound responses. J Exp Bot 57:739–745

    Article  PubMed  CAS  Google Scholar 

  • Toft C, Fares MA (2012) Selection for translational robustness in Buchnera aphidicola, endosymbiotic bacteria of aphids. Mol Biol Evol 26:743–751

    Article  CAS  Google Scholar 

  • Tolmay VL, Lindeque RC, Prinsloo GJ (2007) Preliminary evidence of a resistance-breaking biotype of the Russian wheat aphid, Diuraphis noxia (Kurdjumov) (Homoptera: Aphididae), in South Africa. Afr Entomol 15:228–230

    Article  Google Scholar 

  • Turlings TCJ, Ton J (2006) Exploiting scents of distress: the prospect of manipulating herbivore-induced plant odours to enhance the control of agricultural pests. Curr Opin Plant Biol 9:421–427

    Article  PubMed  Google Scholar 

  • Turlings TCJ, Bernasconi M, Bertossa R, Bigler E, Caloz G, Dorn S (1998) The induction of volatile emissions in maize by three herbivore species with different feeding habits possible consequences for their natural enemies. Biol Control 12:122–129

    Article  Google Scholar 

  • van der Meijden E, Wijn M, Verkaar HJ (1988) Defense and regrowth, alternative plant strategies in the struggle against herbivores. Oikos 51:355–363

    Article  Google Scholar 

  • Van der Westhuizen AJ, Qian X-M, Botha A-M (1998) Differential induction of apoplastic peroxidase and chitinase activities in susceptible and resistant wheat cultivars by Russian wheat aphid infestation. Plant Cell Rep 18:132–137

    Article  Google Scholar 

  • Van der Westhuizen AJ, Qian X-M, Wilding M, Botha A-M (2002) Purification and immunocytochemical localization of a wheat β-1,3-glucanase induced by Russian wheat aphid infestation. SA J Sci 98:197–202

    Google Scholar 

  • Van Eck L (2011) Functional genomics approaches to cereal-aphid interactions. PhD. Dissertation, Colorado State University, Ft. Collins, USA, pp 95–133

  • Van Eck L, Schultz T, Leach JE, Scofield SR, Peairs FB, Botha A-M, Lapitan NLVT (2010) Virus-induced gene silencing of WRKY53 and an inducible phenylalanine ammonia-lyase in wheat reduces aphid resistance. Plant Biotechnol J. doi:10.1111/j.1467-7652.2010.00539.x

    PubMed  Google Scholar 

  • Van Zyl RA, Mathabe P, Hlongwane C, Botha A-M (2005) Proteins expressed in wheat (Triticum aestivum) in response to Russian wheat aphid (Diuraphis noxia) infestation. Comp Biochem Physiol A Mol Integr Physiol 141(3):S234–S234

    Google Scholar 

  • Voelckel C, Baldwin IT (2004) Herbivore-induced plant vaccination. Part II. Array-studies reveal the transience of herbivore specific transcriptional imprints and a distinct imprint from stress combinations. Plant J 38:650–663

    Article  PubMed  CAS  Google Scholar 

  • Voelckel C, Weisser WW, Baldwin IT (2004) An analysis of plant-aphid interactions by different microarray hybridization strategies. Mol Ecol 13:3187–3195

    Article  PubMed  CAS  Google Scholar 

  • Wall JD, Lohmueller KE, Plagnol V (2009) Detecting ancient admixture and estimating demographic parameters in multiple human populations. Mol Biol Evol 26(8):1823

    Article  PubMed  CAS  Google Scholar 

  • Walling LI (2008) Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiol 146:859–866

    Article  PubMed  CAS  Google Scholar 

  • Walters MC, Penn F, Du Toit F, Botha TC, Aalbersberg K, Hewitt PH, Broodryk SW (1980) The Russian wheat aphid. Farming S Afr Leaflet Ser Wheat G3:1–6

    Google Scholar 

  • Wayadande AC, Bruton B, Fletcher J, Pair S, Mitchell F (2005) Retention of cucurbit yellow vine disease bacterium Serratia marcescens through transstadial molt of vector Anasa tristis (Hemiptera: Coreida). Ann Entomol Soc Am 98:770–774

    Article  Google Scholar 

  • Whitney HM, Glover BJ (2013) Coevolution: plant-insect. eLS. John Wiley & Sons, Ltd. doi:10.1002/9780470015902.a0001762.pub2

  • Will T, van Bel AJ (2006) Physical and chemical interactions between aphids and plants. J Exp Bot 57:729–737

    Article  PubMed  CAS  Google Scholar 

  • Will T, Tjallingii WF, Thönnessen A, van Bel AJ (2007) Molecular sabotage of plant defense by aphid saliva. Proc Natl Acad Sci USA 104:10536–10541

    Article  PubMed  CAS  Google Scholar 

  • Will T, Kronemann SR, Furch AC, Tjallingii WF, van Bel AJ (2009) Aphid watery saliva counteracts sieve-tube occlusion: a universal phenomenon? J Exp Bot 212:3305–3312

    CAS  Google Scholar 

  • Wolpoff MH, Spuhler JN, Smith FH, Radovcic J, Pope G, Frayer DW, Eckhardt R, Clark G (1988) Modern human origins. Science 241:772–774

    Article  PubMed  CAS  Google Scholar 

  • Yao CB, Zehnder G, Bauske E, Klopper J (1996) Relationship between cucumber beetle (Coleoptera: Chrysomelidae) density and incidence of bacterial wilt of cucurbits. J Econ Entomol 89:510–514

    Google Scholar 

  • Yip KA, Patel P, Kim PM, Engelman DM, McDermott D, Gerstein M (2008) An integrated system for studying residue coevolution in proteins. Bioinformatics 24(2):290–292

    Article  PubMed  CAS  Google Scholar 

  • Yuan HY, Chen XP, Zhu LL, He GC (2005) Identification of genes responsive to brown planthopper Nilaparvata lugens Stal (Homoptera, Delphacidae) feeding in rice. Planta 221:105–112

    Article  PubMed  CAS  Google Scholar 

  • Zaayman D, Lapitan NLV, Botha A-M (2009) Dissimilar molecular defense responses are elicited in Triticum aestivum L. after infestation by different Diuraphis noxia (Kurdjumov) biotypes. Physiol Plant 135:1399–3054

    Google Scholar 

  • Zangerl AR, Berenbaum MR (2003) Phenotype matching in wild parsnip and parsnip webworms: causes and consequences. Evolution 57:806–815

    PubMed  CAS  Google Scholar 

  • Zangerl AR, Hamilton JG, Miller TJ, Crofts AR, Oxborough K, Berenbaum MR, DeLucia EH (2002) Impact of folivory on photosynthesis is greater than the sum of its holes. Proc Natl Acad Sci USA 99:1088–1091

    Article  PubMed  CAS  Google Scholar 

  • Zavala JA, Baldwin IT (2004) Fitness benefits of trypsin proteinase inhibitor expression in Nicotiana attenuata are greater than their costs when plants are attacked. BMC Ecology 4:11

    Article  PubMed  CAS  Google Scholar 

  • Zhu-Salzman K, Salzman TA, Ahn J-E, Koiwa H (2004) Transcriptional regulation of sorghum defense determinants against a phloem-feeding aphid. Plant Physiol 134:420–431

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Genetics, University of Stellenbosch, Matieland, ZA7602, South Africa

    A.-M. Botha

  2. Department of Genetics, University of Stellenbosch, P. O. Box X1, Matieland, ZA7601, South Africa

    A.-M. Botha

Authors
  1. A.-M. Botha
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A.-M. Botha.

Additional information

Handling Editor: Robert Glinwood.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 195 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Botha, AM. A coevolutionary conundrum: the arms race between Diuraphis noxia (Kurdjumov) a specialist pest and its host Triticum aestivum (L.). Arthropod-Plant Interactions 7, 359–372 (2013). https://doi.org/10.1007/s11829-013-9262-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11829-013-9262-3

Keywords

Search

Navigation