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Previous herbivory modulates aphid population growth and plant defense responses in a non-model plant, Carthamus tinctorius (Asteraceae)

Published online by Cambridge University Press:  17 September 2021

Motahareh Amiri Domari
Affiliation:
Department of Biodiversity, Institute of Science and High Technology and Environmental Sciences, Graduate University of Advanced Technology, Kerman, Iran
Seyed Mozaffar Mansouri*
Affiliation:
Department of Biodiversity, Institute of Science and High Technology and Environmental Sciences, Graduate University of Advanced Technology, Kerman, Iran
Mohsen Mehrparvar
Affiliation:
Department of Biodiversity, Institute of Science and High Technology and Environmental Sciences, Graduate University of Advanced Technology, Kerman, Iran
*
Author for correspondence: Seyed Mozaffar Mansouri, Email: [email protected]

Abstract

Plants have a variety of defense mechanisms that are often induced following attacks by herbivores; this benefits those plants by decreasing performance or preference of herbivores that attack the plants later. We investigated the effects of previous exposure of plants to the safflower aphid, Uroleucon carthami, cotton bollworm, Helicoverpa armigera, and mechanical wounding on subsequent safflower aphid infestations using commercial safflower (Carthamus tinctorius) cultivars and wild safflower species (C. oxyacantha). The experiments were conducted in a greenhouse with two treatments: previously induced plants via direct herbivory or mechanical wounding, and control plants that had never experienced herbivory. To test the performance of safflower aphid on different plant treatments, five unwinged aphids were placed on each plant and allowed to reproduce for 14 days. Finally, the total numbers of aphids on each plant were counted and the percentage of produced winged individuals was calculated. The number of aphids on plants that were previously infested or injured was significantly lower than in control plants. Percentage of winged aphids was significantly higher on induced plants, which is an indicator for unsuitable conditions. Also, significant increase in total phenolic content and hydrogen peroxide was observed in induced plants, showing that the levels of these compounds were either treatment, cultivar and/or genotype × treatment dependent, highlighting the specificity of these interactions. Overall, among the safflower cultivars the lowest number of aphids and the highest percentage of winged aphid individuals were observed on Mahali-Isfahan cultivar and wild safflower, showing that this cultivar is more sensitive to herbivory and/or responds to it more than other cultivars. These findings could contribute to a better utilization of induced defense in the integrated pest management of safflower fields.

Type
Research Paper
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Agrawal, AA, Tuzun, S and Bent, E (1999) Induced Plant Defenses Against Pathogens and Herbivores: Biochemistry, Ecology, and Agriculture. Minnesota, USA: American Phytopathological Society.Google Scholar
Ali, JG and Agrawal, AA (2014) Asymmetry of plant-mediated interactions between specialist aphids and caterpillars on two milkweeds. Functional Ecology 28, 14041412.CrossRefGoogle Scholar
Apel, K and Hirt, H (2004) Reactive oxygen Species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373379.CrossRefGoogle ScholarPubMed
Bergvinson, DJ, Arnason, JT and Pietrzak, LN (1994) Localization and quantification of cell wall phenolics in European corn borer resistant and susceptible maize inbreds. Canadian Journal of Botany 72, 12431249.CrossRefGoogle Scholar
Bi, JL and Felton, GW (1995) Foliar oxidative stress and insect herbivory: primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance. Journal of Chemical Ecology 21, 15111530.CrossRefGoogle ScholarPubMed
Boyko, EV, Smith, CM, Thara, VK, Bruno, JM, Deng, Y, Starkey, SR and Klaahsen, DL (2006) The molecular basis of plant gene expression during aphid invasion: wheat Pto- and Pti-like sequences are involved in interactions between wheat and Russian wheat aphid (Homoptera: Aphididae). Journal of Economic Entomology 99, 14301445.CrossRefGoogle Scholar
Braendle, C, Davis, GK, Brisson, JA and Stern, DL (2006) Wing dimorphism in aphids. Heredity 97, 192199.CrossRefGoogle ScholarPubMed
Brisson, JA (2010) Aphid wing dimorphisms: linking environmental and genetic control of trait variation. Philosophical Transactions of the Royal Society B-Biological Sciences 365, 605616.CrossRefGoogle ScholarPubMed
Cheeseman, JM (2007) Hydrogen peroxide and plant stress: a challenging relationship. Plant Stress 1, 415.Google Scholar
Ciepiela, A (1989) Biochemical basis of winter wheat resistance to the grain aphid, Sitobion avenae. Entomologia Experimentalis et Applicata 51, 269275.CrossRefGoogle Scholar
Dicke, M, Takabayashi, J and Posthumus, MA (1998) Plant phytoseiid interactions mediated by herbivore induced plant volatiles: variation in production of cues and in responses of predatory mites. Experimental and Applied Acarology 22, 311333.CrossRefGoogle Scholar
Engelberth, J (2012) Plant resistance to insect herbivory. In Witzany, G and Baluska, F (eds), Biocommunication of Plants. Berlin Heidelberg: Springer, pp. 303327.CrossRefGoogle Scholar
Fürstenberg-Hägg, J, Zagrobelny, M and Bak, S (2013) Plant defense against insect herbivores. International Journal of Molecular Sciences 14, 1024210279.CrossRefGoogle ScholarPubMed
Gatehouse, JA (2002) Plant resistance towards insect herbivores: a dynamic interaction. New Phytologist 156, 145169.CrossRefGoogle ScholarPubMed
Golan, K, Sempruch, C, Górska-Drabik, E, Czerniewicz, P, Łagowska, B, Kot, I, Kmieć, K, Magierowicz, K and Leszczyński, B (2017) Accumulation of amino acids and phenolic compounds in biochemical plant responses to feeding of two different herbivorous arthropod pests. Arthropod-Plant Interactions 11, 675682.CrossRefGoogle Scholar
Hartley, SE and Lawton, JH (1987) The effects of different types of damage on the chemistry of birch foliage and the responses of birch feeding insects. Oecologia 74, 432437.CrossRefGoogle ScholarPubMed
Havlickova, H, Cvikrova, M and Eder, J (1996) Phenolic acids in wheat cultivars in relation to plant suitability for and response to cereal aphids. Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz 103, 535542.Google Scholar
Havlickova, H, Cvikrová, M, Eder, J and Hrubcová, M (1998) Alterations in the levels of phenolics and peroxidase activities induced by Rhopalosiphum padi (L.) in two winter wheat cultivars. Journal of Plant Diseases and Protection 105, 140148.Google Scholar
Heil, M and Kost, C (2006) Priming of indirect defences. Ecology Letters 9, 813817.CrossRefGoogle ScholarPubMed
Hille Ris Lambers, D (1966) Polymorphism in Aphididae. Annual Review of Entomology 11, 4778.CrossRefGoogle Scholar
Junglee, S, Urban, L, Sallanon, H and Lopez-Lauri, F (2014) Optimized assay for hydrogen peroxide determination in plant tissue using potassium iodide. American Journal of Analytical Chemistry 5, 730736.CrossRefGoogle Scholar
Kanchiswamy, CN and Maffei, ME (2015) Calcium signaling preceding the emission of plant volatiles in plant–insect interactions. Journal of the Indian Institute of Science 95, 1523.Google Scholar
Kant, MR, Jonckheere, W, Knegt, B, Lemos, F, Liu, J, Schimmel, BCJ, Villarroel, CA, Ataide, LMS, Dermauw, W, Glas, JJ, Egas, M, Janssen, A, Van Leeuwen, T, Schuurink, RC, Sabelis, MW and Alba, JM (2015) Mechanisms and ecological consequences of plant defense induction and suppression in herbivore communities. Annals of Botany 115, 10151051.CrossRefGoogle Scholar
Karban, R and Baldwin, IT (1997) Induced Responses to Herbivory. Chicago, USA: University of Chicago Press.CrossRefGoogle Scholar
Kaur, R, Gupta, AK and Taggar, GK (2014) Role of catalase, H2O2 and phenolics in resistance of pigeonpea towards Helicoverpa armigera (Hubner). Acta Physiologiae Plantarum 36, 15131527.CrossRefGoogle Scholar
Kaur, H, Salh, PK and Singh, B (2017) Role of defense enzymes and phenolics in resistance of wheat crop (Triticum aestivum L.) towards aphid complex. Journal of Plant Interactions 12, 304311.CrossRefGoogle Scholar
Kessler, A and Baldwin, IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annual Review of Plant Biology 53, 299328.CrossRefGoogle ScholarPubMed
Kuźniak, E and Urbanek, H (2000) The involvement of hydrogen peroxide in plant responses to stresses. Acta Physiologiae Plantarum 22, 195203.CrossRefGoogle Scholar
Lee, JE, Vogt, T, Hause, B and Lëbler, M (1997) Methyl jasmonate induces an O-methyltransferase in barley. Plant Cell Physiology 38, 851862.CrossRefGoogle ScholarPubMed
Leszczynski, B (1985) Changes in phenols content and metabolism in leaves of susceptible and resistant winter wheat cultivars infested by Rhopalosiphum padi (L.) (Hom., Aphididae). Journal of Applied Entomology 100, 343348.Google Scholar
Maffei, ME, Miyhofer, A and Boland, W (2007) Insects feeding on plants: rapid signals and responses preceding the induction of phytochemical release. Phytochemistry 68, 29462959.CrossRefGoogle ScholarPubMed
Mehrparvar, M, Mansouri, SM and Weisser, WW (2014) Mechanisms of species-sorting: effect of habitat occupancy on aphids' host plant selection. Ecological Entomology 39, 281289.CrossRefGoogle Scholar
Messina, FJ, Taylor, R and Karren, ME (2002) Divergent responses of two cereal aphids to previous infestation of their host plant. Entomologia Experimentalis et Applicata 16, 4350.CrossRefGoogle Scholar
Mittler, TE and Sutherland, ORW (1969) Dietary influences on aphid polymorphism. Entomologia Experimentalis et Applicata 12, 703713.CrossRefGoogle Scholar
Mittler, R, Vanderauwera, S, Gollery, M and Van Breusegem, F (2004) Reactive oxygen gene network of plants. Trends in Plant Science 9, 490498.CrossRefGoogle Scholar
Moloi, MJ and van der Westhuizen, AJ (2008) Antioxidative enzymes and the Russian wheat aphid (Diuraphis noxia) resistance response in wheat (Triticum aestivum). Plant Biology 10, 403407.CrossRefGoogle Scholar
Morkunas, I, Mai, VC and Gabrys, B (2011) Phytohormonal signaling in plant responses to aphid feeding. Acta Physiologiae Plantarum 33, 20572073.CrossRefGoogle Scholar
Müller, CB, Williams, IS and Hardie, J (2001) The role of nutrition, crowding and interspecific interactions in the development of winged aphids. Ecological Entomology 26, 330340.CrossRefGoogle Scholar
Pollard, DG (1972) Plant penetration by feeding aphids (Hemiptera. Aphidoidea): a review. Bulletin of Entomological Research 62, 631714.Google Scholar
Saltveit, ME (2017) Synthesis and metabolism of phenolic compounds. In Yahia, EM (ed.), Fruit and Vegetable Phytochemicals. West Sussex, UK: Wiley & Sons, Ltd, pp. 115124.CrossRefGoogle Scholar
Schaller, A (ed.) (2008) Induced Plant Resistance to Herbivory. Berlin, Germany: Springer.CrossRefGoogle Scholar
Sharma, P, Jha, AB, Dubey, RS and Pessarakli, M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Journal of Botany 2012, 126.CrossRefGoogle Scholar
Singleton, VL and Rossi, JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. American Journal of Enology and Viticulture 16, 144158.Google Scholar
Smirnoff, N and Arnaud, D (2019) Hydrogen peroxide metabolism and functions in plants. New Phytologist 221, 11971214.CrossRefGoogle ScholarPubMed
Smith, CM (2005) Plant Resistance to Arthropods: Molecular and Conventional Approaches. Dordrecht, The Netherlands: Springer Press.CrossRefGoogle Scholar
Stout, MJ, Workman, KV, Bostock, RM and Duffey, SS (1998) Specificity of induced resistance in the tomato, Lycopersicon esculentum. Oecologia 113, 7481.CrossRefGoogle Scholar
Tibebu, B (2018) Defense mechanisms of plants to insect pests: from morphological to biochemical approach. Trends in Technical & Scientific Research 2, 555584.Google Scholar
Walling, LL (2001) Induced resistance: from the basic to the applied. Trends in Plant Science 6, 445447.CrossRefGoogle Scholar
War, AR, Paulraj, MG, War, MY and Ignacimuthu, S (2011) Herbivore- and elicitor-induced resistance in groundnut to asian armyworm, Spodoptera litura (Fab.) (Lepidoptera: Noctuidae). Plant Signaling & Behavior 6, 17691777.CrossRefGoogle Scholar
War, AR, Paulraj, MG, War, MY and Ignacimuthu, S (2012) Herbivore-induced resistance in different groundnut germplasm lines to Asian armyworm, Spodoptera litura (Fab.) (Lepidoptera: Noctuidae). Acta Physiologiae Plantarum 34, 343352.CrossRefGoogle Scholar
Will, T, Furch, ACU and Zimmermann, MR (2013) How phloem-feeding insects face the challenge of phloem-located defenses. Frontiers in Plant Science 4, 112.CrossRefGoogle ScholarPubMed
Wise, MJ and Weinburg, AM (2002) Prior flea beetle herbivory affects oviposition preference and larval performance of a potato beetle on their shared host plant. Ecological Entomology 27, 115122.CrossRefGoogle Scholar
Wool, D and Hales, DF (1996) Previous infestation affects recolonization of cotton by Aphis gossypii: induced resistance or plant damage? Phytoparasitica 24, 3948.CrossRefGoogle Scholar
Zhang, SZ, Hau, BZ and Zhang, F (2008) Induction of the activities of antioxidative enzymes and the levels of malondialdehyde in cucumber seedlings as a consequence of Bemisia tabaci (Hemiptera: Aleyrodidae) infestation. Arthropod-Plant Interactions 2, 209213.CrossRefGoogle Scholar
Züst, T and Agrawal, AA (2016) Mechanisms and evolution of plant resistance to aphids. Nature Plants 2, 19.CrossRefGoogle ScholarPubMed