Plant–aphid interactions with a focus on legumes
Lars G. Kamphuis A B , Katherine Zulak A , Ling-Ling Gao A , Jonathan Anderson A B and Karam B. Singh A B C
+ Author Affiliations
- Author Affiliations
A CSIRO Plant Industry, Private Bag 5, Wembley, WA 6913, Australia.
B The UWA Institute of Agriculture, University of Western Australia, Crawley, WA 6009, Australia.
C Corresponding author. Email: karam.singh@csiro.au
This paper originates from a presentation at the ‘VI International Conference on Legume Genetics and Genomics (ICLGG)’ Hyderabad, India, 2–7 October 2012.
Submitted: 10 April 2013 Accepted: 29 May 2013 Published: 25 July 2013
Abstract
Sap-sucking insects such as aphids cause substantial yield losses in agriculture by draining plant nutrients as well as vectoring viruses. The main method of control in agriculture is through the application of insecticides. However, aphids rapidly evolve mechanisms to detoxify these, so there is a need to develop durable plant resistance to these damaging insect pests. The focus of this review is on aphid interactions with legumes, but work on aphid interactions with other plants, particularly Arabidopsis and tomato is also discussed. This review covers advances on the plant side of the interaction, including the identification of major resistance genes and quantitative trait loci conferring aphid resistance in legumes, basal and resistance gene mediated defence signalling following aphid infestation and the role of specialised metabolites. On the aphid side of the interaction, this review covers what is known about aphid effector proteins and aphid detoxification enzymes. Recent advances in these areas have provided insight into mechanisms underlying resistance to aphids and the strategies used by aphids for successful infestations and have significant impacts for the delivery of durable resistance to aphids in legume crops.
Additional keywords: antibiosis, antixenosis, defence signaling, defense signalling, legume, sap-sucking insect.
References
Ade J, Deyoung BJ, Golstein C, Innes RW (2007) Indirect activation of a plant nucleotide binding site-leucine-rich repeat protein by a bacterial protease. Proceedings of the National Academy of Sciences of the United States of America 104, 2531–2536.| Indirect activation of a plant nucleotide binding site-leucine-rich repeat protein by a bacterial protease.Crossref | GoogleScholarGoogle Scholar |
Adio AM, Casteel CL, De Vos M, Kim JH, Joshi V, Li B, Juéry C, Daron J, Kliebenstein DJ, Jander G (2011) Biosynthesis and defensive function of Nδ-acetylornithine, a jasmonate-induced Arabidopsis metabolite. The Plant Cell 23, 3303–3318.
| Biosynthesis and defensive function of Nδ-acetylornithine, a jasmonate-induced Arabidopsis metabolite.Crossref | GoogleScholarGoogle Scholar |
Annan IB, Tingey WM, Schaefers GA, Tjallingii WF, Backus EA, Saxena KN (2000) Stylet penetration activities by Aphis craccivora (Homoptera: Aphididae) on plants and excised plant parts of resistant and susceptible cultivars of cowpea (Leguminosae). Annals of the Entomological Society of America 93, 133–140.
| Stylet penetration activities by Aphis craccivora (Homoptera: Aphididae) on plants and excised plant parts of resistant and susceptible cultivars of cowpea (Leguminosae).Crossref | GoogleScholarGoogle Scholar |
Atamian HS, Eulgem T, Kaloshian I (2012) SlWRKY70 is required for Mi-1-mediated resistance to aphids and nematodes in tomato. Planta 235, 299–309.
| SlWRKY70 is required for Mi-1-mediated resistance to aphids and nematodes in tomato.Crossref | GoogleScholarGoogle Scholar |
Atamian HS, Chaudhary R, Dal Cin V, Bao E, Girke T, Kaloshian I (2013) In planta expression or delivery of potato aphid Macrosiphum euphorbiae effectors Me10 and Me23 enhances aphid fecundity. Molecular Plant-Microbe Interactions 26, 67–74.
| In planta expression or delivery of potato aphid Macrosiphum euphorbiae effectors Me10 and Me23 enhances aphid fecundity.Crossref | GoogleScholarGoogle Scholar |
Bata HD, Singh BB, Singh SR, Ladeinde Ta O (1987) Inheritance of resistance to aphid in cowpea. Crop Science 27, 892–894.
| Inheritance of resistance to aphid in cowpea.Crossref | GoogleScholarGoogle Scholar |
Bhattarai KK, Li Q, Liu Y, Dinesh-Kumar SP, Kaloshian I (2007a) The Mi-1-mediated pest resistance requires Hsp90 and Sgt1. Plant Physiology 144, 312–323.
| The Mi-1-mediated pest resistance requires Hsp90 and Sgt1.Crossref | GoogleScholarGoogle Scholar |
Bhattarai KK, Xie QG, Pourshalimi D, Younglove T, Kaloshian I (2007b) Coi1-dependent signaling pathway is not required for Mi-1-mediated potato aphid resistance. Molecular Plant-Microbe Interactions 20, 276–282.
| Coi1-dependent signaling pathway is not required for Mi-1-mediated potato aphid resistance.Crossref | GoogleScholarGoogle Scholar |
Bhattarai KK, Atamian HS, Kaloshian I, Eulgem T (2010) WRKY72-type transcription factors contribute to basal immunity in tomato and Arabidopsis as well as gene-for-gene resistance mediated by the tomato R gene Mi-1. The Plant Journal 63, 229–240.
| WRKY72-type transcription factors contribute to basal immunity in tomato and Arabidopsis as well as gene-for-gene resistance mediated by the tomato R gene Mi-1.Crossref | GoogleScholarGoogle Scholar |
Blackman RL, Eastop VF (1984) ‘Aphids on the world’s crops; an identification and information guide.’ (John Wiley & Sons: Chichester, UK)
Carolan JC, Fitzroy CIJ, Ashton PD, Douglas AE, Wilkinson TL (2009) The secreted salivary proteome of the pea aphid Acyrthosiphon pisum characterised by mass spectrometry. Proteomics 9, 2457–2467.
| The secreted salivary proteome of the pea aphid Acyrthosiphon pisum characterised by mass spectrometry.Crossref | GoogleScholarGoogle Scholar |
Casteel CL, Walling LL, Paine TD (2006) Behavior and biology of the tomato psyllid, Bactericerca cockerelli, in response to the Mi-1.2 gene. Entomologia Experimentalis et Applicata 121, 67–72.
| Behavior and biology of the tomato psyllid, Bactericerca cockerelli, in response to the Mi-1.2 gene.Crossref | GoogleScholarGoogle Scholar |
Cevik V, King GJ (2002a) High-resolution genetic analysis of the Sd-1 aphid resistance locus in Malus spp. Theoretical and Applied Genetics 105, 346–354.
| High-resolution genetic analysis of the Sd-1 aphid resistance locus in Malus spp.Crossref | GoogleScholarGoogle Scholar |
Cevik V, King GJ (2002b) Resolving the aphid resistance locus Sd-1 on a BAC contig within a sub-telomeric region of Malus linkage group 7. Genome 45, 939–945.
| Resolving the aphid resistance locus Sd-1 on a BAC contig within a sub-telomeric region of Malus linkage group 7.Crossref | GoogleScholarGoogle Scholar |
Chen M-S, Zhao H-X, Zhu YC, Scheffler B, Liu X, Liu X, Hulbert S, Stuart JJ (2008) Analysis of transcripts and proteins expressed in the salivary glands of Hessian fly (Mayetiola destructor) larvae. Journal of Insect Physiology 54, 1–16.
| Analysis of transcripts and proteins expressed in the salivary glands of Hessian fly (Mayetiola destructor) larvae.Crossref | GoogleScholarGoogle Scholar |
Chiozza MV, O’Neal ME, Macintosh GC (2010) Consitutive and induced differential accumulation of amino acid in leaves of susceptible and resistant soybean plants in response to the soybean aphid (Hemiptera: Aphididae). Environmental Entomology 39, 856–864.
| Consitutive and induced differential accumulation of amino acid in leaves of susceptible and resistant soybean plants in response to the soybean aphid (Hemiptera: Aphididae).Crossref | GoogleScholarGoogle Scholar |
Cooper WC, Jia L, Goggin FL (2004) Acquired and R-gene-mediated resistance against the potato aphid in tomato. Journal of Chemical Ecology 30, 2527–2542.
| Acquired and R-gene-mediated resistance against the potato aphid in tomato.Crossref | GoogleScholarGoogle Scholar |
Cooper JL, Till BJ, Laport RG, Darlow MC, Kleffner JM, Jamai A, El-Mellouki T, Liu S, Ritchie R, Nielsen N, Bilyeu KD, Meksem K, Comai L, Henikoff S (2008) TILLING to detect induced mutations in soybean. BMC Plant Biology 8, 9
| TILLING to detect induced mutations in soybean.Crossref | GoogleScholarGoogle Scholar |
De Geyter E, Smagghe G, Rhabe Y, Geelen R (2012) Triterpene saponins of Quillaja saponaria show strong aphicidal and deterrent activity against the pea aphid Acyrthosiphon pisum. Pest Management Science 68, 164–169.
| Triterpene saponins of Quillaja saponaria show strong aphicidal and deterrent activity against the pea aphid Acyrthosiphon pisum.Crossref | GoogleScholarGoogle Scholar |
de Ilarduya OM, Xie QG, Kaloshian I (2003) Aphid-induced defense responses in Mi-1-mediated compatible and incompatible tomato interactions. Molecular Plant-Microbe Interactions 16, 699–708.
| Aphid-induced defense responses in Mi-1-mediated compatible and incompatible tomato interactions.Crossref | GoogleScholarGoogle Scholar |
De La Fuente Van Bentem S, Vossen JH, De Vries KL, van Wees S, Tameling WIL, Dekker HL, de Koster CG, Haring MA, Takken FLW, Cornelissen BJC (2005) Heat shock protein 90 and its co-chaperone protein phosphatase 5 interact with distinct regions of the tomato I-2 disease resistance protein. The Plant Journal 43, 284–298.
| Heat shock protein 90 and its co-chaperone protein phosphatase 5 interact with distinct regions of the tomato I-2 disease resistance protein.Crossref | GoogleScholarGoogle Scholar |
De Vos M, Jander G (2009) Myzus persicae (green peach aphid) salivary components induce defence responses in Arabidopsis thaliana. Plant, Cell & Environment 32, 1548–1560.
| Myzus persicae (green peach aphid) salivary components induce defence responses in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
De Vos M, Van Oosten VR, Van Poecke RM, Van Pelt JA, Pozo MJ, Mueller MJ, Buchala AJ, Métraux J-P, Van Loon LC, Dicke M, Pieterse CMJ (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Molecular Plant-Microbe Interactions 18, 923–937.
| Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack.Crossref | GoogleScholarGoogle Scholar |
de Vos M, Cheng WY, Summers HE, Raguso RA, Jander G (2010) Alarm pheromone habituation in Myzus persicae has fitness consequences and causes extensive gene expression changes. Proceedings of the National Academy of Sciences of the United States of America 107, 14 673–14 678.
| Alarm pheromone habituation in Myzus persicae has fitness consequences and causes extensive gene expression changes.Crossref | GoogleScholarGoogle Scholar |
Diaz-Montano J, Reese JC, Louis J, Campbell LR, Schapaugh WT (2007) Feeding behavior by the soybean aphid (Hemiptera: Aphididae) on resistant and susceptible soybean genotypes. Journal of Economic Entomology 100, 984–989.
| Feeding behavior by the soybean aphid (Hemiptera: Aphididae) on resistant and susceptible soybean genotypes.Crossref | GoogleScholarGoogle Scholar |
Digilio MC, Corrado G, Sasso R, Coppola V, Iodice L, Pasquariello M, Bossi S, Maffei ME, Coppola M, Pennacchio F, Rao R, Guerrieri E (2010) Molecular and chemical mechanisms involved in aphid resistance in cultivated tomato. New Phytologist 187, 1089–1101.
| Molecular and chemical mechanisms involved in aphid resistance in cultivated tomato.Crossref | GoogleScholarGoogle Scholar |
Dogimont C, Bendahmane A, Pitrat M, Burget-Bigeard E, Hagen L (2007) Gene resistant to Aphis gossypii. United States of America Patent no. 0070016977.
Du Y, Poppy GM, Powell W, Pickett JA, Wadhams LJ, Woodcock CM (1998) Identification of semiochemicals released during aphid feeding that attract the parasitoid Aphidius ervi. Journal of Chemical Ecology 24, 1355–1368.
| Identification of semiochemicals released during aphid feeding that attract the parasitoid Aphidius ervi.Crossref | GoogleScholarGoogle Scholar |
Edwards OR, Singh KB (2006) Resistance to insect pests: what do legumes have to offer? Euphytica 147, 273–285.
| Resistance to insect pests: what do legumes have to offer?Crossref | GoogleScholarGoogle Scholar |
Ellis C, Karafyllidis I, Turner JG (2002) Constitutive activation of jasmonate signaling in an Arabidopsis mutant correlates with enhanced resistance to Erysiphe cichoracearum, Pseudomonas syringae, and Myzus persicae. Molecular Plant-Microbe Interactions 15, 1025–1030.
| Constitutive activation of jasmonate signaling in an Arabidopsis mutant correlates with enhanced resistance to Erysiphe cichoracearum, Pseudomonas syringae, and Myzus persicae.Crossref | GoogleScholarGoogle Scholar |
Ellwood SR, D’ Souza NK, Kamphuis LG, Burgess TI, Nair RM, Oliver RP (2006) SSR analysis of the Medicago truncatula SARDI core collection reveals substantial diversity and unusual genotype dispersal throughout the Mediterranean basin. Theoretical and Applied Genetics 112, 977–983.
| SSR analysis of the Medicago truncatula SARDI core collection reveals substantial diversity and unusual genotype dispersal throughout the Mediterranean basin.Crossref | GoogleScholarGoogle Scholar |
Figueroa CC, Prunier-Leterme N, Rispe C, Sepúlveda F, Fuentes-Contreras E, Sabater-Muñoz B, Simon J-C, Tagu D (2007) Annotated expressed sequence tags and xenobiotic detoxification in the aphid Myzus persicae (Sulzer). Insect Science 14, 29–45.
| Annotated expressed sequence tags and xenobiotic detoxification in the aphid Myzus persicae (Sulzer).Crossref | GoogleScholarGoogle Scholar |
Golawska S (2007) Deterrence and toxicity of plant saponins for the pea aphid Acyrthosiphon pisum Harris. Journal of Chemical Ecology 33, 1598–1606.
| Deterrence and toxicity of plant saponins for the pea aphid Acyrthosiphon pisum Harris.Crossref | GoogleScholarGoogle Scholar |
Gao L, Anderson JP, Klingler JP, Nair RM, Edwards OR, Singh KB (2007a) Involvement of the octadecanoid pathway in bluegreen aphid resistance in Medicago truncatula. Molecular Plant-Microbe Interactions 20, 82–93.
| Involvement of the octadecanoid pathway in bluegreen aphid resistance in Medicago truncatula.Crossref | GoogleScholarGoogle Scholar |
Gao LL, Horbury R, Nair RM, Edwards OR, Singh KB (2007b) Characterization of resistance to multiple aphid species (Hemiptera: Aphididae) in Medicago truncatula. Bulletin of Entomological Research 97, 41–48.
| Characterization of resistance to multiple aphid species (Hemiptera: Aphididae) in Medicago truncatula.Crossref | GoogleScholarGoogle Scholar |
Gao LL, Klingler JP, Anderson JP, Edwards OR, Singh KB (2008) Characterization of pea aphid resistance in Medicago truncatula. Plant Physiology 146, 996–1009.
| Characterization of pea aphid resistance in Medicago truncatula.Crossref | GoogleScholarGoogle Scholar |
Gao LL, Kamphuis LG, Kakar K, Edwards OR, Udvardi MK, Singh KB (2010) Identification of potential early regulators of aphid resistance in Medicago truncatula via transcription factor expression profiling. New Phytologist 186, 980–994.
| Identification of potential early regulators of aphid resistance in Medicago truncatula via transcription factor expression profiling.Crossref | GoogleScholarGoogle Scholar |
Goławska S, Lukasik I (2009) Acceptance of low-saponin lines of alfalfa with varied phenolic concentrations by pea aphid (Homoptera: Aphididae). Biologia 64, 377–382.
| Acceptance of low-saponin lines of alfalfa with varied phenolic concentrations by pea aphid (Homoptera: Aphididae).Crossref | GoogleScholarGoogle Scholar |
Guo S, Kamphuis LG, Gao L-L, Edwards OR, Singh KB (2009) Two independent resistance genes in the Medicago truncatula cultivar Jester confer resistance to two different aphid species of the genus Acyrthosiphon. Plant Signaling & Behavior 4, 328–331.
| Two independent resistance genes in the Medicago truncatula cultivar Jester confer resistance to two different aphid species of the genus Acyrthosiphon.Crossref | GoogleScholarGoogle Scholar |
Guo S, Kamphuis LG, Gao L-L, Klingler JP, Lichtenzveig J, Edwards O, Singh KB (2012) Identification of distinct quantitative trait loci associated with defense against the closely related aphids Acyrthosiphon pisum and A. kondoi in Medicago truncatula. Journal of Experimental Botany 63, 3913–3922.
| Identification of distinct quantitative trait loci associated with defense against the closely related aphids Acyrthosiphon pisum and A. kondoi in Medicago truncatula.Crossref | GoogleScholarGoogle Scholar |
Hammond-Kosack KE, Parker JE (2003) Deciphering plant-pathogen communication: fresh perspectives for molecular resistance breeding. Current Opinion in Biotechnology 14, 177–193.
| Deciphering plant-pathogen communication: fresh perspectives for molecular resistance breeding.Crossref | GoogleScholarGoogle Scholar |
Harmel N, Letocart E, Cherqui A, Giordanengo P, Mazzucchelli G, Guillonneau F, De Pauw E, Haubruge E, Francis F (2008) Identification of aphid salivary proteins: a proteomic investigation of Myzus persicae. Insect Molecular Biology 17, 165–174.
| Identification of aphid salivary proteins: a proteomic investigation of Myzus persicae.Crossref | GoogleScholarGoogle Scholar |
Heyns I, Groenewald E, Marais F, Du Toit F, Tolmay V (2006) Chromosomal location of the Russian wheat aphid resistance gene, Dn5. Crop Science 46, 630–636.
| Chromosomal location of the Russian wheat aphid resistance gene, Dn5.Crossref | GoogleScholarGoogle Scholar |
Hill CB, Li Y, Hartman GL (2004) Resistance of Glycine species and various cultivated legumes to the soybean aphid (Homoptera: Aphididae). Journal of Economic Entomology 97, 1071–1077.
| Resistance of Glycine species and various cultivated legumes to the soybean aphid (Homoptera: Aphididae).Crossref | GoogleScholarGoogle Scholar |
Hill CB, Li Y, Hartman GL (2006) A single dominant gene for resistance to the soybean aphid in the soybean cultivar Dowling. Crop Science 46, 1601–1605.
| A single dominant gene for resistance to the soybean aphid in the soybean cultivar Dowling.Crossref | GoogleScholarGoogle Scholar |
Hill CB, Kim K-S, Crull L, Diers BW, Hartman GL (2009) Inheritance of resistance to the soybean aphid in soybean PI 200538. Crop Science 49, 1193–1200.
| Inheritance of resistance to the soybean aphid in soybean PI 200538.Crossref | GoogleScholarGoogle Scholar |
Hogenhout SA, Bos JIB (2011) Effector proteins that modulate plant-insect interactions. Current Opinion in Plant Biology 14, 422–428.
| Effector proteins that modulate plant-insect interactions.Crossref | GoogleScholarGoogle Scholar |
Hunter WB, Dang PM, Bausher MG, Chaparro JX, McKendree W, Shatters Jr, RG, Hunter WB, Dang PM, Bausher MG, Chaparro JX, McKendree W, Shatters Jr, RG, (2003) Aphid biology: expressed genes from alate Toxoptera citricida, the brown citrus aphid. Journal of Insect Science 3, 23
Hwang C-F, Williamson VM (2003) Leucine-rich repeat-mediated intramolecular interactions in nematode recognition and cell death signaling by the tomato resistance protein Mi. The Plant Journal 34, 585–593.
| Leucine-rich repeat-mediated intramolecular interactions in nematode recognition and cell death signaling by the tomato resistance protein Mi.Crossref | GoogleScholarGoogle Scholar |
Hwang C-F, Bhakta AV, Truesdell GM, Pudlo WM, Williamson VM (2000) Evidence for a role of the N terminus and leucine-rich repeat region of the Mi gene product in regulation of localized cell death. The Plant Cell 12, 1319–1329.
International Aphid Genomics Consortium (2010) Genome sequence of the pea aphid Acyrthosiphon pisum. PLOS Biology 8, e1000313
| Genome sequence of the pea aphid Acyrthosiphon pisum.Crossref | GoogleScholarGoogle Scholar |
Jaubert-Possamai S, Le Trionnaire G, Bonhomme J, Christophides GK, Rispe C, Tagu D (2007) Gene knockdown by RNAi in the pea aphid Acyrthosiphon pisum. BMC Biotechnology 7, 63
| Gene knockdown by RNAi in the pea aphid Acyrthosiphon pisum.Crossref | GoogleScholarGoogle Scholar |
Jones JDG, Dangl JL (2006) The plant immune system. Nature 444, 323–329.
| The plant immune system.Crossref | GoogleScholarGoogle Scholar |
Joseph S, Peter KV (2003) Inheritance of aphid resistance in cowpea. Legume Research 26, 57–59.
Jun T-H, Rouf Mian MA, Michel AP (2012) Genetic mapping revealed two loci for soybean aphid resistance in PI 567301B. Theoretical and Applied Genetics 124, 13–22.
| Genetic mapping revealed two loci for soybean aphid resistance in PI 567301B.Crossref | GoogleScholarGoogle Scholar |
Kamphuis LG, Gao L-L, Singh KB (2012) Identification and characterization of resistance to cowpea aphid (Aphis craccivora Koch.) in Medicago truncatula. BMC Plant Biology 12, 101
| Identification and characterization of resistance to cowpea aphid (Aphis craccivora Koch.) in Medicago truncatula.Crossref | GoogleScholarGoogle Scholar |
Kempema LA, Cui X, Holzer FM, Walling LL (2007) Arabidopsis transcriptome changes in response to phloem-feeding silverleaf whitefly nymphs. Similarities and distinctions in responses to aphids. Plant Physiology 143, 849–865.
| Arabidopsis transcriptome changes in response to phloem-feeding silverleaf whitefly nymphs. Similarities and distinctions in responses to aphids.Crossref | GoogleScholarGoogle Scholar |
Klingler J, Creasy R, Gao L, Nair RM, Calix AS, Jacob HS, Edwards OR, Singh KB (2005) Aphid resistance in Medicago truncatula involves antixenosis and phloem-specific, inducible antibiosis, and maps to a single locus flanked by NBS-LRR resistance gene analogs. Plant Physiology 137, 1445–1455.
| Aphid resistance in Medicago truncatula involves antixenosis and phloem-specific, inducible antibiosis, and maps to a single locus flanked by NBS-LRR resistance gene analogs.Crossref | GoogleScholarGoogle Scholar |
Klingler JP, Edwards OR, Singh KB (2007) Independent action and contrasting phenotypes of resistance genes against spotted alfalfa aphid and bluegreen aphid in Medicago truncatula. New Phytologist 173, 630–640.
| Independent action and contrasting phenotypes of resistance genes against spotted alfalfa aphid and bluegreen aphid in Medicago truncatula.Crossref | GoogleScholarGoogle Scholar |
Klingler JP, Nair RM, Edwards OR, Singh KB (2009) A single gene, AIN, in Medicago truncatula mediates a hypersensitive response to both bluegreen aphid and pea aphid, but confers resistance only to bluegreen aphid. Journal of Experimental Botany 60, 4115–4127.
| A single gene, AIN, in Medicago truncatula mediates a hypersensitive response to both bluegreen aphid and pea aphid, but confers resistance only to bluegreen aphid.Crossref | GoogleScholarGoogle Scholar |
Knoth C, Ringler J, Dangl JL, Eulgem T (2007) Arabidopsis WRKY70 is required for full RPP4-mediated disease resistance and basal defense against Hyaloperonospora parasitica. Molecular Plant-Microbe Interactions 20, 120–128.
| Arabidopsis WRKY70 is required for full RPP4-mediated disease resistance and basal defense against Hyaloperonospora parasitica.Crossref | GoogleScholarGoogle Scholar |
Kos M, Houshyani B, Overeem A-J, Bouwmeester HJ, Weldegergis BT, van Loon JJA, Dicke M, Vet LEM (2013) Genetic engineering of plant volatile terpenoids: effects on a herbivore, a predator and a parasitoid. Pest Management Science 69, 302–311.
| Genetic engineering of plant volatile terpenoids: effects on a herbivore, a predator and a parasitoid.Crossref | GoogleScholarGoogle Scholar |
Le Signor C, Savois V, Aubert G, Verdier J, Nicolas M, Pagny G, Moussy F, Sanchez M, Baker D, Clarke J, Thompson R (2009) Optimizing TILLING populations for reverse genetics in Medicago truncatula. Plant Biotechnology Journal 7, 430–441.
| Optimizing TILLING populations for reverse genetics in Medicago truncatula.Crossref | GoogleScholarGoogle Scholar |
Li J, Brader G, Palva ET (2004) The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. The Plant Cell 16, 319–331.
| The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense.Crossref | GoogleScholarGoogle Scholar |
Li J, Brader G, Kariola T, Palva ET (2006) WRKY70 modulates the selection of signaling pathways in plant defense. The Plant Journal 46, 477–491.
| WRKY70 modulates the selection of signaling pathways in plant defense.Crossref | GoogleScholarGoogle Scholar |
Li Y, Hill CB, Carlson SR, Diers BW, Hartman GL (2007) Soybean aphid resistance genes in the soybean cultivars Dowling and Jackson map to linkage group M. Molecular Breeding 19, 25–34.
| Soybean aphid resistance genes in the soybean cultivars Dowling and Jackson map to linkage group M.Crossref | GoogleScholarGoogle Scholar |
Li Y, Zou J, Li M, Bilgin DD, Vodkin LO, Hartman GL, Clough SJ (2008) Soybean defence responses to the soybean aphid. New Phytologist 179, 185–195.
| Soybean defence responses to the soybean aphid.Crossref | GoogleScholarGoogle Scholar |
Liu J, Elmore JM, Fuglsang AT, Palmgren MG, Staskawicz BJ, Coaker G (2009) RIN4 functions with plasma membrane H+-ATPases to regulate stomatal apertures during pathogen attack. PLoS Biology 7, e1000139
| RIN4 functions with plasma membrane H+-ATPases to regulate stomatal apertures during pathogen attack.Crossref | GoogleScholarGoogle Scholar |
Liu S, Chougule NP, Vijayendran D, Bonning BC (2012) Deep sequencing of the transcriptomes of soybean aphid and associated endosymbionts. PLoS ONE 7, e45161
| Deep sequencing of the transcriptomes of soybean aphid and associated endosymbionts.Crossref | GoogleScholarGoogle Scholar |
Louis J, Lorenc-Kukula K, Singh V, Reese J, Jander G, Shah J (2010) Antibiosis against the green peach aphid requires the Arabidopsis thaliana MYZUS PERSICAE-INDUCED LIPASE1 gene. The Plant Journal 64, 800–811.
| Antibiosis against the green peach aphid requires the Arabidopsis thaliana MYZUS PERSICAE-INDUCED LIPASE1 gene.Crossref | GoogleScholarGoogle Scholar |
Louis J, Gobbato E, Mondal HA, Feys BJ, Parker JE, Shah J (2012) Discrimination of Arabidopsis PAD4 activities in defense against green peach aphid and pathogens. Plant Physiology 158, 1860–1872.
| Discrimination of Arabidopsis PAD4 activities in defense against green peach aphid and pathogens.Crossref | GoogleScholarGoogle Scholar |
Mackey D, Holt BF, Wiig A, Dangl JL (2002) RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108, 743–754.
| RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Martin GB, Bogdanove AJ, Sessa G (2003) Understanding the functions of plant disease resistance proteins. Annual Review of Plant Biology 54, 23–61.
| Understanding the functions of plant disease resistance proteins.Crossref | GoogleScholarGoogle Scholar |
Martinez De Ilarduya O, Moore AE, Kaloshian I (2001) The tomato Rme1 locus is required for Mi-1-mediated resistance to root-knot nematodes and the potato aphid. The Plant Journal 27, 417–425.
| The tomato Rme1 locus is required for Mi-1-mediated resistance to root-knot nematodes and the potato aphid.Crossref | GoogleScholarGoogle Scholar |
Martinez De Ilarduya O, Nombela G, Hwang C-F, Williamson VM, Muñiz M, Kaloshian I (2004) Rme1 is necessary for Mi-1-mediated resistance and acts early in the resistance pathway. Molecular Plant-Microbe Interactions 17, 55–61.
| Rme1 is necessary for Mi-1-mediated resistance and acts early in the resistance pathway.Crossref | GoogleScholarGoogle Scholar |
Mensah CC, Difonzo C, Nelson RL, Wang D (2005) Resistance to soybean aphid in early maturing soybean germplasm. Crop Science 45, 2228–2233.
| Resistance to soybean aphid in early maturing soybean germplasm.Crossref | GoogleScholarGoogle Scholar |
Mewis I, Appel HM, Hom A, Raina R, Schultz JC (2005) Major signaling pathways modulate Arabidopsis glucosinolate accumulation and response to both phloem-feeding and chewing insects. Plant Physiology 138, 1149–1162.
| Major signaling pathways modulate Arabidopsis glucosinolate accumulation and response to both phloem-feeding and chewing insects.Crossref | GoogleScholarGoogle Scholar |
Mewis I, Tokuhisa JG, Schultz JC, Appel HM, Ulrichs C, Gershenzon J (2006) Gene expression and glucosinolate accumulation in Arabidopsis thaliana in response to generalist and specialist herbivores of different feeding guilds and the role of defense signaling pathways. Phytochemistry 67, 2450–2462.
| Gene expression and glucosinolate accumulation in Arabidopsis thaliana in response to generalist and specialist herbivores of different feeding guilds and the role of defense signaling pathways.Crossref | GoogleScholarGoogle Scholar |
Moran PJ, Thompson GA (2001) Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiology 125, 1074–1085.
| Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways.Crossref | GoogleScholarGoogle Scholar |
Moran PJ, Cheng Y, Cassell JL, Thompson GA (2002) Gene expression profiling of Arabidopsis thaliana in compatible plant-aphid Interactions. Archives of Insect Biochemistry and Physiology 51, 182–203.
| Gene expression profiling of Arabidopsis thaliana in compatible plant-aphid Interactions.Crossref | GoogleScholarGoogle Scholar |
Mutti NS, Park Y, Reese JC, Reeck GR (2006) RNAi knockdown of a salivary transcript leading to lethality in the pea aphid, Acyrthosiphon pisum. Journal of Insect Science 6, 1–7.
| RNAi knockdown of a salivary transcript leading to lethality in the pea aphid, Acyrthosiphon pisum.Crossref | GoogleScholarGoogle Scholar |
Mutti NS, Louis J, Pappan LK, Begum K, Chen M-S, 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. Proceedings of the National Academy of Sciences of the United States of America 105, 9965–9969.
| A protein from the salivary glands of the pea aphid, Acyrthosiphon pisum, is essential in feeding on a host plant.Crossref | GoogleScholarGoogle Scholar |
Myers GO, Fatolun CA, Young ND (1996) RFLP mapping of an aphid resistance gene in cowpea (Vigna unguiculata L. Walp). Euphytica 91, 181–187.
Nombela G, Williamson VM, Muñiz M (2003) The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci. Molecular Plant-Microbe Interactions 16, 645–649.
| The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci.Crossref | GoogleScholarGoogle Scholar |
Ohnishi S, Miyake N, Takeuchi T, Kousaka F, Hiura S, Kanehira O, Saito M, Sayama T, Higashi A, Ishimoto M, Tanaka Y, Fujita S (2012) Fine mapping of foxglove aphid (Aulacorthum solani) resistance gene Raso1 in soybean and its effect on tolerance to Soybean dwarf virus transmitted by foxglove aphid. Breeding Science 61, 618–624.
| Fine mapping of foxglove aphid (Aulacorthum solani) resistance gene Raso1 in soybean and its effect on tolerance to Soybean dwarf virus transmitted by foxglove aphid.Crossref | GoogleScholarGoogle Scholar |
Ohta N, Mori N, Kuwahra Y, Nishida R (2006) A hemiterpene glucoside as a probing deterrent of the bean aphid, Megoura crassicauda, from a non-host vetch, Vicia hirsuta. Phytochemistry 67, 584–588.
| A hemiterpene glucoside as a probing deterrent of the bean aphid, Megoura crassicauda, from a non-host vetch, Vicia hirsuta.Crossref | GoogleScholarGoogle Scholar |
Pascal T, Pfeiffer F, Kervella J, Lacroze JP, Sauge MH (2002) Inheritance of green peach aphid resistance in the peach cultivar ‘Rubira’. Plant Breeding 121, 459–461.
Pathak RS (1988) Genetics of resistance to aphids in cowpea. Crop Science 28, 474–476.
| Genetics of resistance to aphids in cowpea.Crossref | GoogleScholarGoogle Scholar |
Pegadaraju V, Knepper C, Reese J, Shah J (2005) Premature leaf senescence modulated by the Arabidopsis PHYTOALEXIN DEFICIENT4 gene is associated with defense against the phloem-feeding green peach aphid. Plant Physiology 139, 1927–1934.
| Premature leaf senescence modulated by the Arabidopsis PHYTOALEXIN DEFICIENT4 gene is associated with defense against the phloem-feeding green peach aphid.Crossref | GoogleScholarGoogle Scholar |
Pegadaraju V, Louis J, Singh V, Reese JC, Bautor J, Feys BJ, Cook G, Parker JE, Shah J (2007) Phloem-based resistance to green peach aphid is controlled by Arabidopsis PHYTOALEXIN DEFICIENT4 without its signaling partner ENHANCED DISEASE SUSCEPTIBILITY1. The Plant Journal 52, 332–341.
| Phloem-based resistance to green peach aphid is controlled by Arabidopsis PHYTOALEXIN DEFICIENT4 without its signaling partner ENHANCED DISEASE SUSCEPTIBILITY1.Crossref | GoogleScholarGoogle Scholar |
Pichersky E, Lewinsohn E (2011) Convergent evolution in plant specialized metabolism. Annual Review of Plant Biology 62, 549–566.
| Convergent evolution in plant specialized metabolism.Crossref | GoogleScholarGoogle Scholar |
Pitino M, Hogenhout SA (2013) Aphid protein effectors promote aphid colonization in a plant species-specific manner. Molecular Plant-Microbe Interactions 26, 130–139.
| Aphid protein effectors promote aphid colonization in a plant species-specific manner.Crossref | GoogleScholarGoogle Scholar |
Ramsey JS, Wilson ACC, 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 Genomics 8, 423
| Genomic resources for Myzus persicae: EST sequencing, SNP identification, and microarray design.Crossref | GoogleScholarGoogle Scholar |
Ramsey JS, Rider DS, Walsh TK, De Vos M, Gordon KHJ, Ponnala L, Macmil SL, Roe BA, Jander G (2010) Comparative analysis of detoxification enzymes in Acrythosiphon pisum and Myzus persicae. Insect Molecular Biology 19, 155–164.
| Comparative analysis of detoxification enzymes in Acrythosiphon pisum and Myzus persicae.Crossref | GoogleScholarGoogle Scholar |
Rietz S, Stamm A, Malonek S, Wagner S, Becker D, Medina-Escobar N, Vlot AC, Feys BJ, Niefind K, Parker JE (2011) Different roles of enhanced disease susceptibility1 (EDS1) bound to and dissociated from phytoalexin deficient4 (PAD4) in Arabidopsis immunity. New Phytologist 191, 107–119.
| Different roles of enhanced disease susceptibility1 (EDS1) bound to and dissociated from phytoalexin deficient4 (PAD4) in Arabidopsis immunity.Crossref | GoogleScholarGoogle Scholar |
Roche P, Alston FH, Maliepaard C, Evans KM, Vrielink R, Dunemann F, Markussen T, Tartarini S, Brown LM, Ryder C, King GJ (1997) RFLP and RAPD markers linked to the rosy leaf curling aphid resistance gene (Sd1) in apple. Theoretical and Applied Genetics 94, 528–533.
| RFLP and RAPD markers linked to the rosy leaf curling aphid resistance gene (Sd1) in apple.Crossref | GoogleScholarGoogle Scholar |
Rossi M, Goggin F, Milligan SB, Kaloshian I, Ullman DE, Williamson VM (1998) The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proceedings of the National Academy of Sciences of the United States of America 95, 9750–9754.
| The nematode resistance gene Mi of tomato confers resistance against the potato aphid.Crossref | GoogleScholarGoogle Scholar |
Rouf Mian MA, Kang S-T, Beil SE, Hammond RB (2008) Genetic linkage mapping of the soybean aphid resistance gene in PI 243540. Theoretical and Applied Genetics 117, 955–962.
| Genetic linkage mapping of the soybean aphid resistance gene in PI 243540.Crossref | GoogleScholarGoogle Scholar |
Sargent DJ, Fernández-Fernández F, Rys A, Knight VH, Simpson DW, Tobutt KR (2007) Mapping of A1 conferring resistance to the aphid Amphorophora idaei and dw (dwarfing habit) in red raspberry (Rubus idaeus L.) using AFLP and microsatellite markers. BMC Plant Biology 7, 15
| Mapping of A1 conferring resistance to the aphid Amphorophora idaei and dw (dwarfing habit) in red raspberry (Rubus idaeus L.) using AFLP and microsatellite markers.Crossref | GoogleScholarGoogle Scholar |
Sattar S, Addo-Quaye C, Song Y, Anstead JA, Sunkar R, Thompson GA (2012a) Expression of small RNA in Aphis gossypii and its potential role in the resistance interaction with melon. PLoS ONE 7, e48579
Sattar S, Song Y, Anstead JA, Sunkar R, Thompson GA (2012b) Cucumis melo microRNA expression profile during aphid herbivory in a resistant and susceptible interaction. Molecular Plant-Microbe Interactions 25, 839–848.
| Cucumis melo microRNA expression profile during aphid herbivory in a resistant and susceptible interaction.Crossref | GoogleScholarGoogle Scholar |
Shakesby AJ, Wallace IS, Isaacs HV, Pritchard J, Roberts DM, Douglas AE (2009) A water-specific aquaporin involved in aphid osmoregulation. Insect Biochemistry and Molecular Biology 39, 1–10.
| A water-specific aquaporin involved in aphid osmoregulation.Crossref | GoogleScholarGoogle Scholar |
Shirasu K (2009) The HSP90–SGT1 chaperone complex for NLR immune sensors. Annual Review of Plant Biology 60, 139–164.
| The HSP90–SGT1 chaperone complex for NLR immune sensors.Crossref | GoogleScholarGoogle Scholar |
Skibbe M, Qu N, Galis I, Baldwin IT (2008) Induced plant defenses in the natural environment: Nicotiana attenuata WRKY3 and WRKY6 coordinate responses to herbivory. The Plant Cell 20, 1984–2000.
| Induced plant defenses in the natural environment: Nicotiana attenuata WRKY3 and WRKY6 coordinate responses to herbivory.Crossref | GoogleScholarGoogle Scholar |
Smith CM, Boyko EV (2007) The molecular bases of plant resistance and defense responses to aphid feeding: current status. Entomologia Experimentalis et Applicata 122, 1–16.
| The molecular bases of plant resistance and defense responses to aphid feeding: current status.Crossref | GoogleScholarGoogle Scholar |
Staudt M, Jackson B, El-Aouni H, Buatois B, Lacroze J-P, Poëssel J-L, Sauge M-H, Niinemets Ü (2010) Volatile organic compound emissions induced by the aphid Myzus persicae differ among resistant and susceptible peach cultivars and a wild relative. Tree Physiology 30, 1320–1334.
| Volatile organic compound emissions induced by the aphid Myzus persicae differ among resistant and susceptible peach cultivars and a wild relative.Crossref | GoogleScholarGoogle Scholar |
Stewart SA, Hodge S, Ismail N, Mansfield JW, Feys BJ, Prospéri J-M, Huguet T, Ben C, Gentzbittel L, Powell G (2009) The RAP1 gene confers effective, race-specific resistance to the pea aphid in Medicago truncatula independent of the hypersensitive reaction. Molecular Plant-Microbe Interactions 22, 1645–1655.
| The RAP1 gene confers effective, race-specific resistance to the pea aphid in Medicago truncatula independent of the hypersensitive reaction.Crossref | GoogleScholarGoogle Scholar |
Studham ME, Macintosh GC (2013) Multiple phytohormone signals control the transcriptional response to soybean aphid infestation in susceptible and resistant soybean plants. Molecular Plant-Microbe Interactions 26, 116–129.
| Multiple phytohormone signals control the transcriptional response to soybean aphid infestation in susceptible and resistant soybean plants.Crossref | GoogleScholarGoogle Scholar |
Tadege M, Ratet P, Mysore KS (2005) Insertional mutagenesis: a Swiss army knife for functional genomics of Medicago truncatula. Trends in Plant Science 10, 229–235.
| Insertional mutagenesis: a Swiss army knife for functional genomics of Medicago truncatula.Crossref | GoogleScholarGoogle Scholar |
Tagu D, Prunier-Leterme N, Legeai F, Gauthier J-P, Duclert A, Sabater-Muñoz B, Bonhomme J, Simon JC (2004) Annotated expressed sequence tags for studies of the regulation of reproductive modes in aphids. Insect Biochemistry and Molecular Biology 34, 809–822.
| Annotated expressed sequence tags for studies of the regulation of reproductive modes in aphids.Crossref | GoogleScholarGoogle Scholar |
Takemura M, Nishida R, Mori N, Kuwahara Y (2002) Acylated flavonol glycosides as probing stimulants of a bean aphid, Megoura crassicauda, from Vicia angustifolia. Phytochemistry 61, 135–140.
| Acylated flavonol glycosides as probing stimulants of a bean aphid, Megoura crassicauda, from Vicia angustifolia.Crossref | GoogleScholarGoogle Scholar |
Takken FLW, Albrecht M, Tameling WIL (2006) Resistance proteins: molecular switched of plant defence. Current Opinion in Plant Biology 9, 383–390.
| Resistance proteins: molecular switched of plant defence.Crossref | GoogleScholarGoogle Scholar |
Tameling WIL, Baulcombe DC (2007) Physical association of the NB-LRR resistance protein Rx with a Ran GTPase-activating protein is required for extreme resistance to potato virus X. The Plant Cell 19, 1682–1694.
| Physical association of the NB-LRR resistance protein Rx with a Ran GTPase-activating protein is required for extreme resistance to potato virus X.Crossref | GoogleScholarGoogle Scholar |
Tjallingii WF (2006) Salivary secretions by aphids interacting with proteins of phloem wound responses. Journal of Experimental Botany 57, 739–745.
| Salivary secretions by aphids interacting with proteins of phloem wound responses.Crossref | GoogleScholarGoogle Scholar |
Van Eck L, Schultz T, Leach JE, Scofield SR, Peairs FP, Botha A-M, Lapitan NLV (2010) Virus-induced gene silencing of WRKY53 and an inducible phenylalanine ammonia-lyase in wheat reduces aphid resistance. Plant Biotechnology Journal 8, 1023–1032.
| Virus-induced gene silencing of WRKY53 and an inducible phenylalanine ammonia-lyase in wheat reduces aphid resistance.Crossref | GoogleScholarGoogle Scholar |
van’t Slot KAE, Knogge W (2002) A dual role for microbial pathogen-derived effector proteins in plant disease and resistance. Critical Reviews in Plant Sciences 21, 229–271.
| A dual role for microbial pathogen-derived effector proteins in plant disease and resistance.Crossref | GoogleScholarGoogle Scholar |
Verheggen FJ, Arnaud L, Bartram S, Gohy M, Haubruge E (2008) Aphid and plant volatiles induce oviposition in an aphidophagous hoverfly. Journal of Chemical Ecology 34, 301–307.
| Aphid and plant volatiles induce oviposition in an aphidophagous hoverfly.Crossref | GoogleScholarGoogle Scholar |
Vos P, Simons G, Jesse T, Wijbrandi J, Heinen L, Hogers R, Frijters A, Groenendijk J, Diergaarde P, Reijans M, Fierens-Onstenk J, de Both M, Peleman J, Liharska T, Hontelez J, Zabeau M (1998) The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids. Nature Biotechnology 16, 1365–1369.
| The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids.Crossref | GoogleScholarGoogle Scholar |
Walling LL (2008) Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiology 146, 859–866.
| Avoiding effective defenses: strategies employed by phloem-feeding insects.Crossref | GoogleScholarGoogle Scholar |
Wang H, Hao J, Chen X, Hao Z, Wang X, Lou Y, Peng Y, Guo Z (2007) Overexpression of rice WRKY89 enhances ultraviolet B tolerance and disease resistance in rice plants. Plant Molecular Biology 65, 799–815.
| Overexpression of rice WRKY89 enhances ultraviolet B tolerance and disease resistance in rice plants.Crossref | GoogleScholarGoogle Scholar |
Will T, Tjallingii WF, Thonnessen A, Van Bel AJE (2007) Molecular sabotage of plant defense by aphid saliva. Proceedings of the National Academy of Sciences of the United States of America 104, 10 536–10 541.
| Molecular sabotage of plant defense by aphid saliva.Crossref | GoogleScholarGoogle Scholar |
Wroblewski T, Piskurewicz U, Tomczak A, Ochoa O, Michelmore RW (2007) Silencing of the major family of NBS-LRR encoding genes in lettuce results in the loss of multiple resistance specificities. The Plant Journal 51, 803–818.
| Silencing of the major family of NBS-LRR encoding genes in lettuce results in the loss of multiple resistance specificities.Crossref | GoogleScholarGoogle Scholar |
Zhang G, Gu C, Wang D (2009) Molecular mapping of soybean aphid resistance genes in PI 567541B. Theoretical and Applied Genetics 118, 473–482.
| Molecular mapping of soybean aphid resistance genes in PI 567541B.Crossref | GoogleScholarGoogle Scholar |
Zhang G, Gu C, Wang D (2010) A novel locus for soybean aphid resistance. Theoretical and Applied Genetics 120, 1183–1191.
| A novel locus for soybean aphid resistance.Crossref | GoogleScholarGoogle Scholar |
Zhu J, Park K-C (2005) Methyl salicylate, a soybean aphid-induced plant volatile attractive to the predator Coccinella septempunctata. Journal of Chemical Ecology 31, 1733–1746.
| Methyl salicylate, a soybean aphid-induced plant volatile attractive to the predator Coccinella septempunctata.Crossref | GoogleScholarGoogle Scholar |
