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Journal of Integrative Agriculture  2020, Vol. 19 Issue (6): 1464-1474    DOI: 10.1016/S2095-3119(19)62786-3
Special Focus: Physiology and interaction of insects with environmental factors Advanced Online Publication | Current Issue | Archive | Adv Search |
Physiology and defense responses of wheat to the infestation of different cereal aphids
LIU Fang-hua1, 2, 3*, KANG Zhi-wei1, 2*, TAN Xiao-ling4, FAN Yong-liang1, 2, TIAN Hong-gang1, 2, LIU Tong-xian1, 2  
1 State Key Laboratory of Crop Stress Biology for Arid Areas, Northwest A&F University, Yangling 712100, P.R.China
2 Key Laboratory of Northwest Loess Plateau Crop Pest Management, Ministry of Agriculture and Rural Affairs, Northwest A&F University, Yangling 712100, P.R.China
3 State Key Laboratory of Integrated Management of Pest and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, P.R.China
4 State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R.China
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Abstract  Cereal aphids are major insect pests of wheat, which cause significant damages to wheat production.  Previous studies mainly focused on the resistance of different wheat varieties to one specific aphid species.  However, reports on the physiology and defense responses of wheat to different cereal aphids are basically lacking.  In this work, we studied the feeding behavior of three cereal aphids: the grain aphid, Sitobion avenae (Fabricius), the greenbugs, Schizaphis graminum (Rondani), and the bird cherry-oat aphid, Rhopalosiphum padi (Linnaeus) on winter wheat, and the physiology and defense responses of wheat to the infestation of these cereal aphids with focus on how these cereal aphids utilize divergent strategies to optimize their nutrition requirement from wheat leaves.  Our results indicated that S. graminum and R. padi were better adapted to penetrating phloem tissue and to collect more nutrition than S. avenae.  The harm on wheat physiology committed by S. graminum and R. padi was severer than that by S. avenae, through reducing chlorophyll concentration and interfering metabolism genes.  Furthermore, cereal aphids manipulated the plant nutrition metabolism by increasing the relative concentration of major amino acids and percentage of essential amino acids.  In addition, different cereal aphids triggered specific defense response in wheat.  All of these results suggested that different cereal aphids utilize divergent strategies to change the physiological and defense responses of their host plants in order to optimize their nutrition absorption and requirement.  These findings not only extend our current knowledge on the insect–plant interactions but also provide useful clues to develop novel biotechnological strategies for enhancing the resistance and tolerance of crop plants against phloem-feeding insects.
Keywords:  cereal aphids        feeding behavior        nutrition        physiology        defense response  
Received: 23 May 2019   Accepted:
Fund: This work was supported by the earmarked fund of China Agriculture Research System (CARS-23-D06).
Corresponding Authors:  Correspondence TIAN Hong-gang, E-mail:; LIU Tong-xian, E-mail:   
About author:  * These authors contributed equally to this study.

Cite this article: 

LIU Fang-hua, KANG Zhi-wei, TAN Xiao-ling, FAN Yong-liang, TIAN Hong-gang, LIU Tong-xian . 2020. Physiology and defense responses of wheat to the infestation of different cereal aphids. Journal of Integrative Agriculture, 19(6): 1464-1474.

Adams J B, McAllan J W. 1958. Pectinases in certain insects. Canadian Journal of Zoology, 36, 305–308.
Ajayi B O, Dewar A M. 1983. The effect of barley yellow dwarf virus on field populations of the cereal aphids, Sitobion avenae and Metopolophium dirhodum. Annals of Applied Biology, 103, 1–11.
Al-Mousawi A H, Richardson P E, Burton R L. 1983. Ultrastructural studies of greenbug (Homoptera: Aphididae) feeding damage to susceptible and resistant wheat cultivars. Annals of the Entomological Society of America, 16, 964–971.
Arnon D I. 1949. Copper enzymes in isolated chloroplasts. Phenoloxidae in Beta vulgaris. Plant Physiology, 24, 1–15.
Baumann P. 2005. Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annual Review of Microbiology, 59, 155–189.
Bos J I, Prince D, Pitino M, Maffei M E, Win J, Hogenhout S A. 2010. A functional genomics approach identifies candidate effectors from the aphid species Myzus persicae (green peach aphid). PLoS Genetics, 6, e1001216.
Botha A M, Lacock L, van Niekerk C, Matsioloko M T, du Preez F B, Loots S, Venter E, Kunert K J, Cullis C A. 2006. Is photosynthetic transcriptional regulation in Triticum aestivum L. cv. ‘TugelaDN’ a contributing factor for tolerance to Diuraphis noxia? Plant Cell Reports, 25, 41–54.
Boyko E V, Smith C M, Thara V K, Bruno J M, Deng Y, Starkey S R, Klaahsen D L. 2006. 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, 1430–1445.
Burd, J D, Burton R L. 1992. Characterization of plant damage caused by Russian wheat aphid (Homoptera: Aphididae). Journal of Economic Entomology, 85, 2017–2022.
Caillaud C M, Pierre J S, Chaubet B, Pietro J P. 1995. Analysis of wheat resistance to the cereal aphid Sitobion avenae using electrical penetration graphs and flow charts combined with correspondence analysis. Entomologia Experimentalis et Applicata, 75, 9–18.
Cao H H, Liu H R, Zhang Z F, Liu T X. 2016. The green peach aphid Myzus persicae perform better on pre-infested Chinese cabbage Brassica pekinensis by enhancing host plant nutritional quality. Scientific Reports, 6, 21954.
Cooper W R, Dillwith J W, Puterka G J. 2011. Comparisons of salivary proteins from five aphid (Hemiptera: Aphididae) species. Environmental Entomology, 40, 151–156.
Cui F, Michael Smith C, Reese J, Edwards O, Reeck G. 2012. Polymorphisms in salivary-gland transcripts of Russian wheat aphid biotypes 1 and 2. Insect Science, 19, 429–440.
Deng Y, Chen S, Lu A, Chen F, Tang F, Guan Z, Teng N. 2010. Production and characterisation of the intergeneric hybrids between Dendranthema morifolium and Artemisia vulgaris exhibiting enhanced resistance to chrysanthemum aphid (Macrosiphoniella sanbourni). Planta, 231, 693–703.
Dorschner K W, Ryan J D, Johnson R C, Eikenbary R D. 1987. Modification of host nitrogen levels by the greenbug (Homoptera: Aphididae): Its role in resistance of winter wheat to aphids. Environmental Entomology, 16, 1007–1011.
Douglas A E. 2003. The nutritional physiology of aphids. Advances in Insect Physiology, 31, 73–140.
Elzinga D A, Jander G. 2013. The role of protein effectors in plant–aphid interactions. Current Opinion in Plant Biology, 16, 451–456.
Van Emden H F, Harrington R. 2007. Aphids as Crop Pests. CABI Press, Wallingford, United Kingdom.
Febvay G, Delobel B, Rahbé Y. 1988. Influence of the amino acid balance on the improvement of an artificial diet for a biotype of Acyrthosiphon pisum (Homoptera: Aphididae). Canadian Journal of Zoology, 66, 2449–2453.
Feldhaar H. 2011. Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecological Entomology, 36, 533–543.
Forrest J M S. 1971. The growth of Aphis fabae as an indicator of the nutritional advantage of galling to the apple aphid Dysaphis devecta. Entomologia Experimentalis et Applicata, 14, 477–483.
Fouché A, Verhoeven R L, Hewitt P H, Walters M C, Kriel C F, De Jager J. 1984. Russian aphid (Diuraphis noxia) feeding damage on wheat, related cereals and Bromus grass species. In: Walters M C, ed., Progress in Russian Wheat Aphid (D. Noxia) Research in the Republic of South Africa. Technical Communication from the Department of Agriculture, Republic of South Africa. pp. 22–33.
Garzo E, Soria C, Gomez-Guillamon M L, Fereres A. 2002. Feeding behavior of Aphis gossypii on resistant accessions of different melon genotypes (Cucumis melo). Phytoparasitica, 30, 129–140.
Goggin F L. 2007. Plant–aphid interactions: molecular and ecological perspectives. Current Opinion in Plant Biology, 10, 399–408.
Goldasteh S, Talebi A A, Rakhshani E, Goldasteh S. 2012. Effect of four wheat cultivars on life table parameters of Schizaphis graminum (Hemiptera: Aphididae). Journal of Crop Protection, 1, 121–129.
Hu X S, Keller M A, Liu X F, Hu Z Q, Zhao H Y, Liu T X. 2013. The resistance and correlation analysis to three species of cereal aphids (Hemiptera: Aphididae) on 10 wheat varieties or lines. Journal of Economic Entomology, 106, 1894–1901.
Hu X S, Liu X F, Thieme T, Zhang G S, Liu T X, Zhao H Y. 2015. Testing the fecundity advantage hypothesis with Sitobion avenae, Rhopalosiphum padi, and Schizaphi graminum (Hemiptera: Aphididae) feeding on ten wheat accessions. Scientific Reports, 5, 18549.
Ingwell L L, Eigenbrode S D, Bosque-Pérez N A. 2012. Plant viruses alter insect behaviour to enhance their spread. Scientific Reports, 2, 1–6.
Kang Z W, Liu F H, Pang R P, Yu W B, Tan X L, Zheng Z Q, Tian H G, Liu T X. 2018a. The identification and expression analysis of candidate chemosensory genes in the bird cherry-oat aphid Rhopalosiphum padi (L.). Bulletin of Entomological Research, 108, 645–657.
Kang Z W, Liu F H, Tan X L, Zhang Z F, Zhu J Y, Tian H G, Liu T X. 2018b. Infection of powdery mildew reduces the fitness of grain aphids (Sitobion avenae) through restricted nutrition and induced defense response in wheat. Frontiers in Plant Science, 9, 778.
Kang Z W, Liu F H, Zhang Z F, Tian H G, Liu T X. 2018c. Volatile β-ocimene can regulate developmental performance of peach aphid Myzus persicae through activation of defense responses in Chinese cabbage Brassica pekinensis. Frontiers in Plant Science, 9, 708.
Kawano T. 2003. Roles of the reactive oxygen species-generating peroxidase reactions in plant defense and growth induction. Plant Cell Reports, 21, 829–837.
Kehr J. 2006. Phloem sap proteins: their identities and potential roles in the interaction between plants and phloem-feeding insects. Journal of Experimental Botany, 57, 167–774.
Koyama Y, Yao I, Akimoto S I. 2004. Aphid galls accumulate high concentrations of amino acids: A support for the nutrition hypothesis for gall formation. Entomologia Experimentalis et Applicata, 113, 35–44.
Kutchan T M. 1995. Alkaloid biosynthesis: the basis for metabolic engineering of medicinal plants. The Plant Cell, 7, 1059–1070.
Liang L Y, Liu L F, Yu X P, Han B Y. 2012. Evaluation of the resistance of different tea cultivars to tea aphids by EPG technique. Journal of Integrative Agriculture, 11, 2028–2034.
Liu F H, Kang Z W, Hu X S, Zhang Z F, Liu T X. 2017. Effects of foliage nutrients of different wheat cultivars on the grain aphid, Sitobion avenae (Hemiptera: Aphididae). Journal of Plant Protection, 44, 305–311. (in Chinese)
Liu Y H, Kang Z W, Guo Y, Zhu G S, Rahman Shah M M, Song Y, Fan Y L, Jing X F, Liu T X. 2016. Nitrogen hurdle of host alternation for a polyphagous aphid and the associated changes of endosymbionts. Scientific Reports, 6, 24781.
Ma R, Reese J C, Black IV W C, Bramel-Cox P. 1990. Detection of pectinesterase and polygalacturonase from salivary secretions of living greenbugs, Schizaphis graminum (Homoptera: Aphididae). Journal of Insect Physiology, 36, 507–512.
Ma R Z, Reese J C, Black IV W C, Bramel-Cox P. 1998. Chlorophyll loss in a greenbug-susceptible sorghum due to pectinases and pectin fragments. Journal of the Kansas Entomological Society, 71, 51–60.
Markkula M, Laurema S. 1964. Changes in the concentration of free amino acids in plants induced by virus diseases and the reproduction of aphids. Annales Agriculturae Fenniae, 3, 265–271.
Miles P W. 1990. Aphid salivary secretions and their involvement in plant toxicoses. In: Campbell R K and Eikenbary R D, eds., Aphid–Plant Genotype Interactions, Elsevier, New York, NY. pp. 131–147.
Mittler R, Vanderauwera S, Suzuki N, Miller G A D, Tognetti V B, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F. 2011. ROS signaling: The new wave? Trends in Plant Science, 16, 300–309.
Mutti N S, Louis J, Pappan L K, Pappan K, Begum K, Chen M S, Park Y S, Dittmer N, Marshall J, Reese J C, Reeck G R. 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.
Mutti N S, Park Y, J C, Reese J C, Reeck G R. 2006. RNAi knockdown of a salivary transcript leading to lethality in the pea aphid, Acyrthosiphon pisum, Journal of Insect Science, 6, 1–7.
Ni X, Quisenberry S S. 1997. Effect of wheat leaf epicuticular structure on host selection and probing rhythm of Russian wheat aphid (Homoptera: Aphididae). Journal of Economic Entomology, 90, 1400–1407.
Park S J, Huang Y, Ayoubi P. 2005. Identification of expression profiles of sorghum genes in response to greenbug phloem feeding using cDNA subtraction and microarray analysis. Planta, 223, 932–947.
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.
Pike K S, Allison D. 1991. Russian Wheat Aphid-Biology, Damage and Management. Washington, Oregon, Idaho Pacific Northwest Extension Publication. PNW371. Pullman, WA.
Powell G, Tosh C R, Hardie J. 2006. Host plant selection by aphids: Behavioral, evolutionary, and applied perspectives. Annual Review of Entomology, 51, 309–330.
Prado E, Tjallingii W F. 1994 Aphid activities during sieve element punctures. Entomologia Experimentalis et Applicata, 72, 157–165.
Radwanski E R, Last R L. 1995. Tryptophan biosynthesis and metabolism: Biochemical and molecular genetics. The Plant Cell, 7, 921–934.
Reese J C, Schwenke J R, Lamont P S, Zehr D D. 1994. Importance and quantification of plant tolerance in crop pest management programs for aphids: greenbug resistance in sorghum. Journal of Agricultural Entomology, 11, 255–270.
Riedell W E. 1989. Effect of Russian wheat aphid infestation on barley plant response to drought stress. Physiologia Plantarum, 77, 587–592.
Sarria E, Cid M, Garzo E, Fereres A. 2009. Excel Workbook for automatic parameter calculation of EPG data. Computers and Electronics in Agriculture, 67, 35–42.
Sandström J, Telang A, Moran N A. 2000. Nutritional enhancement of host plants by aphids - a comparison of three aphid species on grasses. Journal of Insect Physiology, 46, 33–40.
Slansky F, Scriber J M. 1985. Food consumption and utilization. In: Kerkut G A, Gilbert L I, eds., Comprehensive Insect Physiology, Biochemistry and Pharmacology. Vol. 4. Pergamon Press, Oxford, United Kingdom. pp. 87–163.
Smith C M, Liu X, Wang L J, Liu X, Chen M S, Starkey S, Bai J. 2010. Aphid feeding activates expression of a transcriptome of oxylipin-based defense signals in wheat involved in resistance to herbivory. Journal of Chemical Ecology, 36, 260–216.
Srivastava P N, Auclair J L, Srivastava U. 1983. Effect of nonessential amino acids on phagostimulation and maintenance of the pea aphid, Acyrthosiphon pisum. Canadian Journal of Zoology, 61, 2224–2229.
Thiele B, Füllner K, Stein N, Oldiges M, Kuhn A J, Hofmann D. 2008. Analysis of amino acids without derivatization in barley extracts by LC-MS-MS. Analytical and Bioanalytical Chemistry, 391, 2663–2672.
Tjallingii W F. 1978. Electronic recording of penetration behaviour by aphids. Entomologia Experimentalis et Applicata, 24, 721–730.
Voelckel C, Weisser W W, Baldwin I T. 2004. An analysis of plant–aphid interactions by different microarray hybridization strategies. Molecular Ecology, 13, 3187–3195.
Vogt T. 2010. Phenylpropanoid biosynthesis. Molecular Plant, 3, 2–20.
Wang T, Quisenberry S S, Ni X, Tolmay V. 2004. Aphid (Hemiptera: Aphidae) resistance in wheat near-isogenic lines. Journal of Economic Entomology, 96, 475–481.
Will T, Kornemann S R, Furch A C, Tjallingii W F, van Bel A J. 2009. Aphid watery saliva counteracts sieve-tube occlusion: a universal phenomenon? Journal of Experimental Biology, 212, 3305–3312.
Wille B D, Hartman G L. 2008. Evaluation of artificial diets for rearing Aphis glycines (Hemiptera: Aphididae). Journal of Economic Entomology, 101, 1228–1232.
Zhang Y, Fan J, Fu Y, Francis F, Chen J L. 2019. Plant-mediated interactions between two cereal aphid species: Promotion of aphid performance and attraction of more parasitoids by infestation of phytotoxic aphid Schizaphis graminum. Journal of Agricultural and Food Chemistry, 67, 2763−2773.
Zytynska S E, Jourdie V, Naseeb S, Delneri D, Preziosi R F. 2016. Induced expression of defence-related genes in barley is specific to aphid genotype. Biological Journal of the Linnean Society, 117, 672–685.
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