Abstract Carmine spider mites (Tetranychus cinnabarinus) and cotton aphids (Aphis gossypii) are both serious pests of cotton, and cause reductions in yields of this key agricultural crop. In order to gain insights into how plant defense responses induced by one herbivore species affect the behavior and performance of another, we examined how infestation with T. cinnabarinus influences the development of A. gossypii using cotton as a model. In this study, we measured the activities of several important biochemical markers and secondary metabolites in the leaves of cotton seedlings responding to infestation by T. cinnabarinus. Furthermore, the influences of T. cinnabarinus infestation on the development of A. gossypii in cotton were also examined. Our data showed that the activities of several key defense enzymes, including phenylalanine ammonia-lyase (PAL), peroxidase (POD), lipoxygenase (LOX), and polyphenol oxidase (PPO), were substantially increased in cotton seedlings responding to spider mite infestation. Further, the contents of gossypol and condensed tannins, key defensive compounds, were significantly enhanced in leaves of cotton seedlings following T. cinnabarinus infestation. Moreover, the T. cinnabarinus-induced production of defense enzymes and secondary metabolites was correlated with infestation density. The developmental periods of A. gossypii on cotton seedling leaves infested with T. cinnabarinus at densities of 10 and 15 individuals cm–2 were 1.16 and 1.18 times that of control, respectively. Meanwhile, the mean relative growth rates of A. gossypii on cotton leaves infested with T. cinnabarinus at densities of 8, 10 and 15 individuals cm–2 were significantly reduced. Therefore, these data suggested that the developmental periods of A. gossypii were significantly lengthened and the mean relative growth rates were markedly reduced when cotton aphids were reared on plants infested with high densities of spider mites. This research sheds light on the role that inducible defense responses played in plant-mediated interspecific interactions between T. cinnabarinus and A. gossypii.
About author: MA Guang-min, Tel: +86-10-62732974, E-mail: firstname.lastname@example.org;
Cite this article:
MA Guang-min, SHI Xue-yan, KANG Zhi-jiao, GAO Xi-wu. The influence of Tetranychus cinnabarinus-induced plant defense responses on Aphis gossypii development[J]. Journal of Integrative Agriculture,
2018, 17(01): 164-172.
Adams J B, van Emden H F. 1972. The biological properties of aphids and their host plant relationships. In: van Emden H F, ed., Aphid Technology. Academic Press, London. pp. 47-104.
Ali J G, Agrawal A A. 2014. Asymmetry of plant-mediated interactions between specialist aphids and caterpillars on two milkweeds. Functional Ecology, 28, 1404-1412.
Axelrod B, Cheesbrough T M, Laakso S. 1981. Lipoxygenase from soybeans. Methods in Enzymology, 7, 411-451.
Bezemer T M, Wagenaar R, Van Dam N M, Wäckers F L. 2003. Interactions between above- and belowground insect herbivores as mediated by the plant defense system. OIKOS, 101, 555-562.
Bradford M M. 1976. A rapid and sensitive method for the quantification of microgram quantities of protein using the principle of protein dye binding. Analytical Biochemistry, 72, 248-254.
Chaman M E, Corcuera L J, Zuniga G E, Cardemil L, Argandona V H. 2001. Induction of soluble and cell wall peroxidases by aphid infestation in barley. Journal of Agricultural and Food Chemistry, 49, 2249-2253.
Chen C, Bélanger R, Benhamou N, Paulitz T C. 2000. Defense enzymes induced in cucumber roots by treatment with plant growth-promoting rhizobacteria (PGPR) and Pythium aphanidermatum. Physiological and Molecular Plant Pathology, 56, 13-23.
Chen M S, Wu J X, Zhang G H. 2009. Inducible direct plant defense against insect herbivores. Chinese Bulletin of Entomology, 46, 175-186. (in Chinese)
Dicke M, Gols R, Ludeking D, Posthumus M A. 1999. Jasmonic acid and herbivory differentially induce carnivore-attracting plant volatiles in lima bean plants. Journal of Chemical Ecology, 25, 1907-1922.
Duan W C,Duan L Q,Li H P,Feng S J,Zhang Y, Zhang L N. 2012. Defense responses in wolfberry (Lycium barbarum) induced by exogenous jasmonic acid and gallmite Aceria pallida(Acari: Eriophyidae). Acta Entomologica Sinica, 55, 804-809. (in Chinese)
Dubery I A, Smit F. 1994. Phenylalanine ammonia-lyase from cotton (Gossypium hirsutum) hypocotyls: Properties of the enzyme induced by a Verticillium dahliae phytotoxin. Biochimica et Biophysica Acta, 1207, 24-30.
Gershenzon J. 1994. Metabolic costs of terpenoid accumulation in higher plants. Journal of Chemical Ecology, 20, 1281-1328.
Gianoli E, Niemeyer H M. 1998. Allocation of herbivory-induced hydroxamic acids in the wild wheat Triticum uniaristatum. Chemoecology, 8, 19-23.
Hagenbucher S, Olson D M, Ruberson J R, Wackers F L, Romeis J. 2013a. Resistance mechanisms against arthropod herbivores incottonand their interactions with natural enemies.Critical Reviews in Plant Sciences, 32, 458-482.
Hagenbucher S, Wäckers F L, Wettestein F E, Olson D M, Ruberson J R, Romeis J. 2013b. Pest tradeoffs in technology: Reduced damage by caterpillars in Bt cotton benefits aphids. Proceedings of the Royal Society (B: Biological Sciences), 280, 20130042.
Hagerman A E, Butler L G. 1989. Choosing appropriate methods and standards for assaying tannin. Journal of Chemical Ecology, 15, 1795-1810.
Han Y, Wang Y, Bi J, Yang X, Huang Y, Zhao X, Hu Y, Cai Q N. 2009. Constitutive and induced activities of defense-related enzymes in aphid-resistant and aphid-susceptible cultivars of wheat. Journal Chemical Ecology, 35, 176-182.
Heitz T, Bergey D R, Ryan C A. 1997. A gene encoding a chloroplast targeted lipoxygenase in tomato leaves is transiently induced by wounding, systemin, and methyl jasmonate. Plant Physiology, 114, 1085-1093.
Hildebrand D F,Rodriguez J G, Legg C S, Brown G C, Bookjans G. 1989. The effects of wounding andmiteinfestation on soybean leaf lipoxygenase levels.Zeitschrift für Naturforschung (C: Biosciences), 44, 655-659.
Hodge S, Thompson G A, Powell G. 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 (Hemiptera: Aphididae). Bulletin of Entomological Research, 95, 449-455.
Kielkiewicz M. 2001. Influence of carmine spider mite Tetranychus cinnabarinus Boisd. (Acarida: Tetranychidae) feeding on ethylene production and the activity of oxidative enzymes in damaged tomato plants. In: Bernini F, Nannelli R, Nuzzaci G, Lillo E E, eds., Acarid Phylogeny and Evolution: Adaptation in Mites and Ticks. Springer Netherlands, Berlin. pp. 389-392.
Inbar M, Doostdar H, Leibee G L, Mayer R T. 1999a. The role of plant rapidly induced responses in asymmetric interspecific interactions among insect herbivores. Journal of Chemical Ecology, 25, 1961-1979.
Inbar M, Doostdar H, Mayer R T. 1999b. Effects of sessile whitefly nymphs (Homoptera: Aleyrodidae) on leaf-chewing larvae (Lepidoptera: Noctuidae). Environmental Entomology, 28, 353-357.
Karban R, Myers J H. 1989. Induced plant responses to herbivory. Annual Review of Ecology and Systematics, 20, 331-348.
Kessler A, Halitschke R, Baldwin I T. 2004. Silencing the jasmonate cascade: Induced plant defenses and insect populations. Science, 305, 665-668.
Koukol J, Conn E E. 1961. Metabolism of aromatic compounds in higher plants. IV. Purification and properties of phenylalanine deaminase of Horden vulgare. Journal of Biological Chemistry, 236, 2692-2698.
Liu Y, Zhang P T,Chen B L,Guo W Q, Zhang H Y. 2013. Analysis on changes of physiological indices of young leaves infected byLygus lucorumof transgenic Bt cotton. CottonScience, 25, 51-56. (in Chinese)
MacDonald M J, D’Cunha G B. 2007. A modern view of phenylalanine ammonia lyase. Biochemistry and Cell Biology, 85, 273-282.
Mayer A M. 1987. Polyphenol oxidase in plants-recent progress. Phytochemistry, 26, 11-20.
Patykowski J, Urbanek H, Kaczorowska T. 1988. Peroxidase activity in leaves of wheat cultivars differing in resistance to Erysiphe graminis DC. Journal of Phytopathology, 122, 126-134.
Qin Q J, Gao X W. 2005. Plant defense responses induced by insect herbivory. Acta Entomologica Sinica, 48, 125-134. (in Chinese)
Qin Q J, Shi X Y, Liang P, Gao X W. 2005. Induction of phenylalanine ammonia-lyase and lipoxygenase in cotton seedlings by mechanical wounding and aphid infestation. Progress in Natural Science, 15, 419-423.
Ralph J, Bunzel M, Marita J M, Hatfield R D, Lu F C, Kim H, Schatz P F, Grabber J H, Steinhart H. 2004. Peroxidase-dependent cross-linking reactions of p-hydroxycinnamates in plant cell walls. Phytochemistry Reviews, 3, 79-96.
Roseleen S S J, Ramaraju K. 2010. Host-plant resistance in okra against the two-spotted spidermite,Tetranychus urticaeKoch. Pest Management and Economic Zoology, 18, 179-187.
Sabelis M W, van Baalen M, Bakker F M, Bruin J, Drukker B, Egas M, Janssen A R M, Lesna I K, Pels B, van Rijn P, Scutareanu P. 1999. The evolution of direct and indirect plant defence against herbivorous arthropods. In: Olff H, Brown V K, Drent R H, eds., Herbivores: Between Plants and Predators. Blackwell Science, Oxford. pp. 109-166.
Sha P J, Fan Y J, Wang Z C, Shi X Y. 2015. Response dynamics of three defense related enzymes in cotton leaves to the interactive stress of Helicoverpa armigera (Hübner) herbivory and omethoate application. Journal of Integrative Agriculture, 14, 355-364.
Spence K O, Bicocca V T, Rosenheim J A. 2007. Friend or foe?: A plant’s induced response to an omnivore.Environmental Entomology, 36, 623-630.
Stipanovic R D，Altman D W，Begin D L, Greenblatt G A, Benedict J H. 1988. Terpenoid aldehydes in upland cottons: Analysis by aniline and HPLC methods. Journal of Agricultural and Food Chemistry, 36, 509-515．
wi?tek M, Kielkiewicz M, Zagdanska B. 2014. Insect-resistant Bt-maize response to the short-term non-target mite-pest infestation and soil drought. Acta Physiologiae Plantarum, 36, 2705-2715.
Wang H B, Tao Y, Jin S. 1994. Chitinase in Vicia faba leaves:induction by Aphis craccivora - A convergent plant physiological stress reaction. Chinese Journal of Applied Ecology, 5, 68-71. (in Chinese)
Wang H B, Wu Q H, Gao W D. 1993. Studies on Tetranychus cinnabarinus-Solanum melongena interaction system 1. Relationship between population dynamics of red spider and tannic acid fluctuation in plant leaves. Chinese Journal of Applied Ecology, 4, 174-177. (in Chinese)
Wang M Y, Wang D S, Hong X Y, Yuan Y D, Gan J H. 2008. Relationship between physical and chemical differences of tomato leaf and the resistance to Aculops lycopersici. Chinese Bulletin of Entomology, 45, 904-908. (in Chinese)
Wang Z S. 1997. Effects of gossypol and tannic acid on the growth and digestion physiology of cotton bollworm larvae. Acta Phytophylacica Sinica, 24, 13-18. (in Chinese)
War A R, Paulraj M G, Ahmad T, Buhroo A A, Hussain B, Ignacimuthu S, Sharma H C. 2012. Mechanisms of plant defense against insect herbivores. Plant Signaling & Behavior, 7, 1306-1320.
Williams J L, Ellers-Kirk C, Orth R G, Gassmann A J, Head G, Tabashnik B E, Carrière Y. 2011. Fitness cost of resistance to Bt cotton linked with increased gossypol content in pink bollworm larvae. PLoS One, 6, e21863.
Wu Y Q, Guo Y Y. 2000. Determination of tannin in cotton plant. Chinese Journal of Applied Ecology, 11, 243-245. (in Chinese)
Zangerl A R, Bazzaz F A. 1992. Theory and pattern in plant defense allocation. In: Fritz R, Simms E L, eds., Plant Resistance to Herbivores and Pathogens. University of Chicago Press, Chicago. pp. 363-392.
Zhou M L, Zhang C C, Wu Y M, Tang Y X. 2013. Metabolic engineering of gossypol in cotton. Applied Microbiology and Biotechnology, 97, 6159-6165.