Resistance of Arabidopsis thaliana to the green peach aphid, Myzus persicae, involves camalexin and is regulated by microRNAs
Version of Record online: 25 MAR 2013
© 2013 The Authors. New Phytologist © 2013 New Phytologist Trust
Volume 198, Issue 4, pages 1178–1190, June 2013
How to Cite
Kettles, G. J., Drurey, C., Schoonbeek, H.-j., Maule, A. J. and Hogenhout, S. A. (2013), Resistance of Arabidopsis thaliana to the green peach aphid, Myzus persicae, involves camalexin and is regulated by microRNAs. New Phytologist, 198: 1178–1190. doi: 10.1111/nph.12218
- Issue online: 7 MAY 2013
- Version of Record online: 25 MAR 2013
- Manuscript Accepted: 31 JAN 2013
- Manuscript Received: 11 DEC 2012
- Biotechnology and Biological Sciences Research Council (BBSRC)
- John Innes Foundation
- 1999. EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284: 2148–2152. , , , , .
- 2005. Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs. Proceedings of the National Academy of Sciences, USA 102: 11928–11933. , .
- 1995. A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in Arabidopsis. Proceedings of the National Academy of Sciences, USA 92: 8675–8679. , , .
- 2000. Aphids on the World's crops: an identification and information guide. Chichester, UK: John Wiley & Sons. , .
- 1988. Insensitivity to ethylene conferred by a dominant mutation in Arabidopsis thaliana. Science 241: 1086–1089. , , , .
- 2003. HASTY, the Arabidopsis ortholog of exportin 5/MSN5, regulates phase change and morphogenesis. Development 130: 1493–1504. , , , , , .
- 2010. A functional genomics approach identifies candidate effectors from the aphid species Myzus persicae (Green Peach Aphid). PLoS Genetics 6: e1001216. , , , , , .
- 2008. Widespread translational inhibition by plant miRNAs and siRNAs. Science 320: 1185–1190. , , , , , , .
- 1994. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6: 1583–1592. , , , .
- 2004. Viral RNA silencing suppressors inhibit the microRNA pathway at an intermediate step. Genes & Development 18: 1179–1186. , , , , .
- 2008. Wounding of Arabidopsis leaves causes a powerful but transient protection against Botrytis infection. Plant Journal 55: 555–567. , , , , .
- 2007. Exploring plant responses to aphid feeding using a full Arabidopsis microarray reveals a small number of genes with significantly altered expression. Bulletin of Entomological Research 97: 523–532. , , , , .
- 2005. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiology 139: 5–17. , , , , .
- 2009. Myzus persicae (green peach aphid) salivary components induce defence responses in Arabidopsis thaliana. Plant, Cell & Environment 32: 1548–1560. , .
- 2005. Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Molecular Plant–Microbe Interactions 18: 923–937. , , , , , , , , , , et al.
- 2006. Hierarchical action and inhibition of plant Dicer-like proteins in antiviral defense. Science 313: 68–71. , , , , , .
- 2007. Antiviral immunity directed by small RNAs. Cell 130: 413–426. , .
- 2008. The RNA-binding proteins HYL1 and SE promote accurate in vitro processing of pri-miRNA by DCL1. Proceedings of the National Academy of Sciences, USA 105: 9970–9975. , , .
- 2004. Downstream divergence of the ethylene signaling pathway for harpin-stimulated Arabidopsis growth and insect defense. Plant Physiology 136: 3628–3638. , , , , , , , .
- 2006. Induction, suppression and requirement of RNA silencing pathways in virulent Agrobacterium tumefaciens infections. Nature Genetics 38: 258–263. , , .
- 2002. Volatiles from potato plants infected with potato leafroll virus attract and arrest the virus vector, Myzus persicae (Homoptera: Aphididae). Proceedings of the Royal Society B 269: 455–460. , , , .
- 2009. RNA silencing is required for Arabidopsis defence against Verticillium wilt disease. Journal of Experimental Botany 60: 591–602. , , , .
- 2005. A miRNA involved in phosphate-starvation response in Arabidopsis. Current Biology 15: 2038–2043. , , , , .
- 2010. Identification of potential early regulators of aphid resistance in Medicago truncatula via transcription factor expression profiling. New Phytologist 186: 980–994. , , , , , .
- 1994. Isolation of phytoalexin-deficient mutants of Arabidopsis thaliana and characterization of their interactions with bacterial pathogens. Proceedings of the National Academy of Sciences, USA 91: 8955–8959. , .
- 2006. Dissecting Arabidopsis thaliana DICER function in small RNA processing, gene silencing and DNA methylation patterning. Nature Genetics 38: 721–725. , , , , , , .
- 2008. Arabidopsis small RNAs and their targets during cyst nematode parasitism. Molecular Plant–Microbe Interactions 21: 1622–1634. , , , .
- 2008. Insect vector interactions with persistently transmitted viruses. Annual Review of Phytopathology, vol 46. Palo Alto: Annual Reviews, 327–359. , , , .
- 1999. Disruption of an RNA helicase/RNAse III gene in Arabidopsis causes unregulated cell division in floral meristems. Development 126: 5231–5243. , , .
- 2007. A novel class of bacteria-induced small RNAs in Arabidopsis. Genes & Development 21: 3123–3134. , , , .
- 2010. Role of small RNAs in host–microbe interactions. Annual Review of Phytopathology 48: 225–246. , .
- 2007. Myzus persicae (green peach aphid) feeding on Arabidopsis induces the formation of a deterrent indole glucosinolate. Plant Journal 49: 1008–1019. , .
- 2008. Identification of indole glucosinolate breakdown products with antifeedant effects on Myzus persicae (green peach aphid). Plant Journal 54: 1015–1026. , , , .
- 2005. Secondary metabolites influence Arabidopsis/Botrytis interactions: variation in host production and pathogen sensitivity. Plant Journal 44: 25–36. , , .
- 2004. Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proceedings of the National Academy of Sciences, USA 101: 12753–12758. , .
- 2008. Towards global understanding of plant defence against aphids – timing and dynamics of early Arabidopsis defence responses to cabbage aphid (Brevicoryne brassicae) attack. Plant, Cell & Environment 31: 1097–1115. , , , , , .
- 2007. Transcriptional responses of Arabidopsis thaliana ecotypes with different glucosinolate profiles after attack by polyphagous Myzus persicae and oligophagous Brevicoryne brassicae. Journal of Experimental Botany 58: 2537–2552. , , , , , .
- 2010. Identification of microRNAs involved in pathogen-associated molecular pattern-triggered plant innate immunity. Plant Physiology 152: 2222–2231. , , , , , .
- 2011. Transcription factor AtMYB44 regulates induced expression of the ETHYLENE INSENSITIVE2 gene in Arabidopsis responding to a harpin protein. Molecular Plant–Microbe Interactions 24: 377–389. , , , , , , .
- 2006. SERRATE: a new player on the plant microRNA scene. EMBO Reports 7: 1052–1058. , , , , .
- 2007. Targets of RNA-directed DNA methylation. Current Opinion in Plant Biology 10: 512–519. , , , , .
- 2010. Deceptive chemical signals induced by a plant virus attract insect vectors to inferior hosts. Proceedings of the National Academy of Sciences, USA 107: 3600–3605. , , .
- 1993. Ortho-anisic acid as internal standard for the simultaneous quantitation of salicylic acid and its putative biosynthetic precursors in cucumber leaves. Analytical Biochemistry 214: 500–505. , .
- 2005. Major signaling pathways modulate Arabidopsis glucosinolate accumulation and response to both phloem-feeding and chewing insects. Plant Physiology 138: 1149–1162. , , , , .
- 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. , , , , , .
- 2008. Specificity of ARGONAUTE7–miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133: 128–141. , , , , , , , , , .
- 2002. Gene expression profiling of Arabidopsis thaliana in compatible plant–aphid interactions. Archives of Insect Biochemistry and Physiology 51: 182–203. , , , .
- 2002. Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance. Plant Cell 14: 629–639. , , , , , , , .
- 2000. Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101: 533–542. , , , , , , , , , , et al.
- 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, USA 105: 9965–9969. , , , , , , , , , , et al.
- 2006. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312: 436–439. , , , , , , , .
- 2008. Suppression of the microRNA pathway by bacterial effector proteins. Science 321: 964–967. , , , , .
- 1999. Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell 11: 1393–1404. , .
- 2004. Transmission of plant viruses by aphid vectors. Molecular Plant Pathology 5: 505–511. , .
- 2007. RNA-directed RNA polymerase 1 (RdR1) mediates the resistance of Nicotiana attenuata to herbivore attack in nature. Plant Journal 50: 40–53. , .
- 2008. Herbivory-induced changes in the small-RNA transcriptome and phytohormone signaling in Nicotiana attenuata. Proceedings of the National Academy of Sciences, USA 105: 4559–4564. , , , .
- 2002. CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Current Biology 12: 1484–1495. , , , , .
- 2005. Nuclear processing and export of microRNAs in Arabidopsis. Proceedings of the National Academy of Sciences, USA 102: 3691–3696. , , , , .
- 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. , , , .
- 2009. The gene controlling the indole glucosinolate modifier1 quantitative trait locus alters indole glucosinolate structures and aphid resistance in Arabidopsis. Plant Cell 21: 985–999. , , .
- 2013. Aphid protein effectors promote aphid colonization in a plant species-specific manner. Molecular Plant–Microbe Interactions 26: 130–139. , .
- 2003. Genes and transposons are differentially methylated in plants, but not in mammals. Genome Research 13: 2658–2664. , , , , , , .
- 2011. The microRNA miR393 re-directs secondary metabolite biosynthesis away from camalexin and towards glucosinolates. Plant Journal 67: 218–231. , , , , , , .
- 1996. Mode of action of the Arabidopsis thaliana phytoalexin camalexin and its role in Arabidopsis–pathogen interactions. Molecular Plant–Microbe Interactions 9: 748–757. , , .
- 2009. Roles of plant small RNAs in biotic stress responses. Annual Review of Plant Biology 60: 485–510. , .
- 2012. Cucumis melo microRNA expression profile during aphid herbivory in a resistant and susceptible interaction. Molecular Plant–Microbe Interactions 25: 839–848. , , , , .
- 2006. CYP71B15 (PAD3) catalyzes the final step in camalexin biosynthesis. Plant Physiology 141: 1248–1254. , , , , , , , .
- 1992. Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proceedings of the National Academy of Sciences, USA 89: 6837–6840. , , .
- 2009. The ABC transporter BcatrB from Botrytis cinerea exports camalexin and is a virulence factor on Arabidopsis thaliana. Plant Journal 58: 499–510. , , , , , , , , .
- 2004. Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16: 2001–2019. , .
- 2008. Specific targeting of a plasmodesmal protein affecting cell-to-cell communication. PLoS Biology 6: e7. , , , , .
- 1995. Regulation of phloem sap feeding by aphids. In: Chapman RF, de Boer G. eds, Regulatory mechanisms in insect feeding. New York, NY, USA: Chapman & Hall, 190–209. .
- 2006. Salivary secretions by aphids interacting with proteins of phloem wound responses. Journal of Experimental Botany 57: 739–745. .
- 1993. Fine structure of aphid stylet routes in plant tissues in correlation with EPG signals. Physiological Entomology 18: 317–328. , .
- 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3: RESEARCH0034. , , , , , , .
- 2004a. The nuclear dsRNA binding protein HYL1 is required for microRNA accumulation and plant development, but not posttranscriptional transgene silencing. Current Biology 14: 346–351. , , , .
- 2010. The biosynthetic pathways and biological scopes of plant small RNAs. Trends in Plant Science 15: 337–345. , , .
- 2004b. Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Molecular Cell 16: 69–79. , , , , , , , , .
- 2009. Origin, biogenesis, and activity of plant microRNAs. Cell 136: 669–687. .
- 2007. Molecular sabotage of plant defense by aphid saliva. Proceedings of the National Academy of Sciences, USA 104: 10536–10541. , , , .
- 2005. DICER-LIKE 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 102: 12984–12989. , , , .
- 2004. Genetic and functional diversification of small RNA pathways in plants. PLoS Biology 2: e104. , , , , , , , .
- 2008. Activation of MAPK kinase 9 induces ethylene and camalexin biosynthesis and enhances sensitivity to salt stress in Arabidopsis. Journal of Biological Chemistry 283: 26996–27006. , , , , , , , .
- 2005. Methylation as a crucial step in plant microRNA biogenesis. Science 307: 932–935. , , , , , , , .
- 2011. Bacteria-responsive microRNAs regulate plant innate immunity by modulating plant hormone networks. Plant Molecular Biology 75: 93–105. , , , , , , , , , , et al.
- 2002. Trp-dependent auxin biosynthesis in Arabidopsis: involvement of cytochrome P450s CYP79B2 and CYP79B3. Genes & Development 16: 3100–3112. , , , , , , , , .
- 2003. ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299: 716–719. , , .