Abstract
This study examined the induction of the defence-related hormones jasmonic acid (JA), salicylic acid (SA) and abscisic acid (ABA) and the phytoalexin medicarpin in Medicago truncatula when challenged by the pea aphid Acyrthosiphon pisum. There was some induction of hormones in the compatible interaction between A. pisum clone N116 and M. truncatula cultivar DZA315, whereas JA, SA and medicarpin exhibited more significant increases in foliage concentration during the incompatible interaction between A. pisum clone PS01 and M. truncatula cultivar Jemalong A17. Foliar concentration of JA, SA and medicarpin exhibited a positive relationship with aphid density after 3-day feeding, whereas ABA was not affected by the presence of aphids. When aphids were restricted to a single leaf using plastic tubes, JA, SA and medicarpin displayed strong local induction, whereas there were no significant systemic increases in uninfested leaves. Medicarpin and SA appeared to increase with duration of aphid feeding, whereas JA showed a more transient increase in concentration 24 h after challenge commenced. Results suggest that increases in JA, SA and medicarpin are associated with M. truncatula resistance to particular clones of A. pisum. The variation in concentration of the defence-related compounds recorded with regard to aphid density, duration of challenge, genotypes of plant and aphids, and between locally challenged and distant leaves reinforces the need for consideration of these experimental factors when generalizing about the plant defence processes that occur during aphid–plant interactions.
Similar content being viewed by others
References
Ahuja I, Kissen R, Bones AM (2012) Phytoalexins in defense against pathogens. Trends Plant Sci 17:73–90
Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488
Bennett RN, Wallsgrove RM (1994) Secondary metabolites in plant defence mechanisms. New Phytol 127:617–633
Berger S (2002) Jasmonate-related mutants of Arabidopsis as tools for studying stress signaling. Planta 214:497–504
Bostock RM (1999) Signal conflicts and synergies in induced resistance to multiple attackers. Physiol Mol Plant Pathol 55:99–109
Bostock RM, Karban R, Thaler JS, Weyman PD, Gilchrist D (2001) Signal interactions in induced resistance to pathogens and insect herbivores. Eur J Plant Pathol 107:103–111
Brunissen L, Vincent C, Le Roux V, Giordanengo P (2010) Effects of systemic potato response to wounding and jasmonate on the aphid Macrosiphum euphorbiae (Sternorryncha: Aphididae). J Appl Entomol 134:562–571
Chen M-S (2008) Inducible direct plant defense against insect herbivores: a review. Insect Sci 15:101–114
Cruickshank IAM, Spencer K, Mandryk M (1979) Nitrogen nutrition and the net accumulation of medicarpan in infection-droplets on excised leaves of white clover. Physiol Plant Pathol 14:71–76
de Ilarduya OM, Xie QG, Kaloshian I (2003) Aphid-induced defense responses in Mi-1-mediated compatible and incompatible tomato interactions. Mol Plant Microbe Interact 16:699–708
de Vos M, Jander G (2009) Myzus persicae (green peach aphid) salivary components induce defence responses in Arabidopsis thaliana. Plant Cell Environ 32:1548–1560
de Vos M, van Oosted VR, van Poecke RMP, van Pelt JA, Pozo MJ, Mueller MJ, Buchala AJ, Metraux J-P, van Loon LC, Dicke M, Pieterse CMJ (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant-Microbe Interact 18:923–937
de Vos M, Kim JH, Jander G (2007) Biochemistry and molecular biology of Arabidopsis–aphid interactions. BioEssays 29:871–883
Divol F, Vilaine F, Thibivilliers S, Amselem J, Palauqui J-C, Kusiak K, Dinant S (2005) Systemic response to aphid infestation by Myzus persicae in the phloem of Apium graveolens. Plant Mol Biol 57:517–540
Donovan MP, Nabity PD, DeLucia EH (2013) Salicylic acid-mediated reductions in yield in Nicotiana attenuate challenged by aphid herbivory. Arthropod Plant Interact 7:45–52
Dugravot S, Brunissen L, Letocart E, Tjallingii WF, Vincent C, Giordanengo P, Cherqui A (2007) Local and systemic responses induced by aphids on Solanum tuberosum plants. Entomol Exp Appl 123:271–277
Erb M, Meldau S, Howe GA (2012) Role of phytohormones in insect-specific plant reactions. Trends Plant Sci 17:250–259
Ferrari J, Via S, Godfray HCJ (2008) Population differentiation and genetic variation in performance on eight hosts in the pea aphid complex. Evolution 62:2508–2524
Ferry N, Stavroulakis S, Guan W, Davison GM, Bell HA, Weaver RJ, Down RE, Gatehouse JA, Gatehouse AMR (2011) Molecular interactions between wheat and cereal aphid (Sitobion avenae): analysis of changes to the wheat proteome. Proteomics 11:1985–2002
Forcat S, Bennett MH, Mansfield JW, Grant MR (2008) A rapid and robust method for simultaneously measuring changes in the phytohormones ABA, JA and SA in plants following biotic and abiotic stress. Plant Methods 4:16
Gao L-L, Anderson JP, Klingler JP, Nair RM, Edwards OR, Singh KB (2007) Involvement of the octadecanoid pathway in bluegreen aphid resistance in Medicago truncatula. Mol Plant Microbe Interact 20:82–93
Gao L-L, Klingler JP, Anderson JP, Edwards OR, Singh KB (2008) Characterization of pea aphid resistance in Medicago truncatula. Plant Physiol 146:96–109
Guo S, Kamphuis LG, Gao 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 Signal Behav 4:328–331
Guo SM, Kamphuis LG, Gao LL, Klingler JP, Lichtenzveig J, Edwards O, Singh KB (2012) Identification of distinct quantitative trait loci associated with defence against the closely related aphids Acyrthosiphon pisum and A. kondoi in Medicago truncatula. J Exp Bot 63:3913–3922
Guo H, Sun Y, Li Y, Liu X, Wang P, Zhu-Salzman K, Ge F (2014) Elevated CO2 alters the feeding behaviour of the pea aphid by modifying the physical and chemical resistance of Medicago truncatula. Plant Cell Environ 37:2158–2168
Hebert SL, Jia L, Goggin FL (2007) Quantitative differences in aphid virulence and foliar symptom development on tomato plants carrying the Mi resistance gene. Environ Entomol 36:458–467
Hodge S, Powell G, Thompson GA (2005) Application of DL-β-aminobutyric acid (BABA) as a root drench to legumes inhibits the growth and reproduction of the pea aphid Acyrthosiphon pisum Harris. Bull Entomol Res 95:449–455
Hodge S, Ward JL, Beale MH, Bennett M, Mansfield JW, Powell G (2013) Aphid-induced accumulation of trehalose in Arabidopsis thaliana is systemic and dependent upon aphid density. Planta 237:1057–1064
Jacobo-Velázquez DA, González-Agüero M, Cisneros-Zevallos L (2015) Cross-talk between signaling pathways: the link between plant secondary metabolite production and wounding stress response. Sci Rep 5:8608. doi:10.1038/srep08608
Jasinksi M, Kachlicki P, Rodziewicz M, Stobiecki M (2009) Changes in the profile of flavonoid accumulation in Medicago truncatula leaves during infection with fungal pathogen Phoma medicaginis. Plant Physiol Biochem 47:847–853
Kamphuis LG, Gao L-L, Singh KB (2012) Identification and characterization of resistance to cowpea aphid (Aphis craccivora Koch) in Medicago truncatula. BMC Plant Biol 12:101
Kamphuis LG, Lichtenzveig J, Peng K, Guo S-M, Klingler JP, Siddique KHM, Gao L-L, Singh KB (2013) Characterization and genetic dissection of resistance to spotted alfalfa aphid (Therioaphis trifoli) in Medicago truncatula. Exp Bot 64:5157–5172
Kanvil S, Powell G, Turnbull C (2014) Pea aphid biotype performance on diverse Medicago host genotypes indicates highly specific virulence and resistance functions. Bull Entomol Res 104:689–701
Kersch-Becker MF, Thaler JS (2014) Virus strains differentially induce plant susceptibility to aphid vectors and chewing herbivores. Oecologia 174:883–892
Kettles GJ, Drurey C, Schoonbeek H, Maule AJ, Hogenhaut S (2013) Resistance of Arabidopsis thaliana to the green peach aphid, Myzus persicae, involves camalexin and is regulated by microRNAs. New Phytol 198:1178–1190
Klingler JP, Creasy R, Gao L, Nair RM, Calix AS, Spafford Jacob H, 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 Physiol 137:1445–1455
Klingler JP, Edwards OR, Singh KB (2007) Independent action and contrasting phenotypes of resistance genes against spotted alfalfa aphid and blue-green aphid in Medicago truncatula. New Phytol 173:630–640
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. J Exp Bot 60:4115–4127
Kombrink E, Somssich IE (1997) Pathogenesis-related proteins and plant defense. In: Carrol GC, Tudzynski P (eds) The mycota V part A, plant relationships. Springer, Berlin, pp 107–128
Kroes A, van Loon JJ, Dicke M (2015) Density-dependent interference of aphids with caterpillar-induced defenses in Arabidopsis: involvement of phytohormones and transcription factors. Plant Cell Physiol 56:98–106
Kuśnierczyk A, Winge PER, Jørstad TS, Troczyńska J, Rossiter JT, Bones AM (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 Environ 31:1097–1115
Kutyniok M, Müller M (2012) Crosstalk between above- and belowground herbivores is mediated by minute metabolic responses of the host Arabidopsis thaliana. J Exp Botany 63:6199–6210
Legendre P, Legendre L (1998) Numerical ecology. Elsevier, Amsterdam
Li Y, Zou J, Li M, Bilgin DD, Vodkin LO, Hartman GL, Clough SJ (2008) Soybean defense responses to the soybean aphid. New Phytol 179:185–195
Louis J, Shah J (2013) Arabidopsis thaliana—Myzus persicae interaction: shaping the understanding of plant defense against phloem-feeding aphids. Front Plant Sci. doi:10.3389/fpls.2013.00213
Mai VC, Drzewiecka K, Jelen H, Narozna D, Rucinska-Sobkowiak R, Kesy J, Floryszak-Wieczorek J, Gabrys B, Morkunas I (2014) Differential induction of Pisum sativum defense signaling molecules in response to pea aphid infestation. Plant Sci 221(222):1–12
Mewis I, Appel HM, Hom A, Raina R, Schultz JC (2005) Major signalling pathways modulate Arabidopsis glucosinolate accumulation and response to both phloem-feeding and chewing insects. Plant Physiol 138:1149–1162
Mewis I, Khan MAM, Glawischnig E, Schreiner M, Ulrichs C (2012) Water stress and aphid feeding differentially influence metabolite composition in Arabidopsis thaliana (L.). PLoS One 7(11):e48661. doi:10.1371/journal.pone.0048661
Mohase L, van der Westhuizen AJ (2002) Salicylic acid is involved in resistance responses in the Russian wheat aphid–wheat interaction. J Plant Physiol 159:585–590
Moran P, Thompson GA (2001) Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiol 125:1074–1085
Moran PJ, Cheng Y, Cassell JL, Thompson GA (2002) Gene expression profiling of Arabidopsis thaliana in compatible plant–aphid interactions. Arch Insect Biochem Physiol 51:182–203
Naoumkina M, Farag MA, Sumner LW, Tang YH, Liu CJ, Dixon RA (2007) Different mechanisms for phytoalexin induction by pathogen and wound signals in Medicago truncatula. Proc Natl Acad Sci 104:17909–17915
Paul ND, Hatcher PE, Taylor JE (2000) Coping with multiple enemies: an integration of molecular and ecological perspectives. Trends Plant Sci 5:220–225
Pegadaraju V, Knepper C, Reese J, Shah J (2005) Premature leaf senescence modulated by the PHYTOALEXIN DEFICIENT4 gene is associated with defense against the phloem-feeding green peach aphid. Plant Physiol 139:1927–1934
Piepho H-P, Williams ER, Fleck M (2006) A note on the analysis of designed experiments with complex treatment structure. HortScience 41:446–452
Pieterse CMJ, VanWees SCM, Van Pelt JA, Knoester M, Laan R, Gerrits H, Weisbeek PJ, Van Loon LC (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571–1580
Reymond P, Farmer EE (1998) Jasmonate and salicylate as global signals for defense gene expression. Curr Opin Plant Biol 1:404–411
Rosa-Gomes MF, Salvadori JR, Schons J (2008) Damage of Rhopalosiphum padi (L.) (Hemiptera: Aphididae) on wheat plants related to duration time and density of infestation. Neotrop Entomol 37:577–581
Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner H-Y, Hunt MD (1996) Systemic acquired resistance. Plant J 8:1809–1819
Smith CM, Clement SL (2012) Molecular bases of plant resistance to arthropods. Annu Rev Entomol 57:309–328
Smith JL, De Moraes CM, Mescher MC (2009) Jasmonate- and salicylate mediated plant defense responses to insect herbivores, pathogens and parasitic plants. Pest Manag Sci 65:497–503
Stewart SA, Hodge S, Ismail N, Mansfield JM, Feys BJ, Prosperi J-M, Huguet T, Ben C, Gentzbittel L, Powell G (2009) The RAP1 gene confers extreme, race-specific resistance to the pea aphid in Medicago truncatula independent of the hypersensitive reaction. Mol Plant- Microbe Interact 12:1645–1655
Studham ME, MacIntosh GC (2013) Multiple phytohormone signals control the transcriptional response to soybean aphid infestation in susceptible and resistant soybean plants. Mol Plant Microbe Interact 26:116–129
Takemoto H, Uefune M, Ozawa R, Arimura G-I, Takabayashi J (2013) Previous infestation of pea aphids Acyrthosiphon pisum on broad bean plants resulted in the increased performance of conspecific nymphs on the plants. J Plant Interact 8:370–374
Thompson GA, Goggin FL (2006) Transcriptomics and functional genomics of plant defence induction by nphloem feeding insects. J Exp Bot 57:755–766
Tretner C, Hut U, Hause B (2008) Mechanostimulation of Medicago truncatula leads to enhanced levels of jasmonic acid. J Exp Bot 59:2847–2856
Truman W, Bennett MH, Kubigstelig I, Turnbull C, Grant M (2007) Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proc Natl Acad Sci 104:1075–1080
Truong D-H, Delory BM, Vanderplanck M, Brostaux Y, Vandereycken A, Heuskin S, Delaplace P, Francis F, Lognay G (2014) Temperature regimes and aphid density interactions differentially influence VOC emissions in Arabidopsis. Arthropod Plant Interact 8:317–327
van der Westhuizen AJ, Qian XM, Botha AM (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
Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216
Zhang P-J, Huang F, Zhang J-M, Wei J-N, Lu Y-B (2015) The mealybug Phenacoccus solenopsis suppresses plant defense responses by manipulating JA–SA crosstalk. Sci Rep 5:9354. doi:10.1038/srep09354
Zhu-Salzman K, Salzman RA, Ahn JE, Koiwa H (2004) Transcriptional regulation of sorghum defense determinants against a phloem-feeding aphid. Plant Physiol 134:420–431
Zhu-Salzman K, Bi J-L, Liu T-X (2005) Molecular strategies of plant defense and insect counter defense. Insect Sci 12:3–15
Acknowledgments
This work was funded by a Ph.D. studentship (to S. A. S.) and research grant (to G. P.) from the Biotechnology and Biological Sciences Research Council, UK. Our thanks go to Dr Martin Selby for technical support.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Robert Glinwood.
Rights and permissions
About this article
Cite this article
Stewart, S.A., Hodge, S., Bennett, M. et al. Aphid induction of phytohormones in Medicago truncatula is dependent upon time post-infestation, aphid density and the genotypes of both plant and insect. Arthropod-Plant Interactions 10, 41–53 (2016). https://doi.org/10.1007/s11829-015-9406-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11829-015-9406-8