Abstract
Salinity is becoming a limiting factor for crop production, particularly in arid and semiarid areas all around the world. This phenomenon can adversely affect both plant integrity and herbivorous insects. Herein, we assessed the bottom-up effects of four salinity levels (3.1 [control], 6.0, 10 and 12.0 dS/m) on the life parameters of viruliferous bird cherry-oat aphid (Rhopalosiphum padi L.) and the aphid transmission of Barley yellow dwarf virus-PAV (BYDV-PAV) to wheat host. The results revealed that nymph longevity and adult pre-oviposition period of the aphids fed on salinity-stressed plants were significantly increased, while adult longevity, gross reproductive rate, net reproductive rate, intrinsic rate of increase and finite rate of increase of the aphids on plants challenged with salinity levels of 10 and 12.0 dS/m were significantly reduced. Also, survival rate and life expectancy of viruliferous R. padi remarkably decreased on wheat plants under 10 and 12.0 dS/m salinity. The R. padi-mediated transmission of BYDV-PAV to salinity-stressed (10 and 12.0 dS/m) wheat plants was significantly reduced. Moreover, the biochemical assays showed a significant increase in biosynthesis of phenolics and free proline within wheat plants challenged with salinity stress. Based on these findings, it can be concluded that salinity stress negatively influences life parameters of viruliferous R. padi, possibly through induction of phenolics and free proline within the salinity-stressed plants, and the aphid transmission of BYDV-PAV to wheat host.
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Abdel-Aal ES, Hucl P, Sosulski FW, Graf R, Gillott C, Pietrzak L (2001) Screening spring wheat for midge resistance in relation to ferulic acid content. J Agric Food Chem 49(8):3559–3566
Adachi S, Honma T, Yasaka R, Ohshima K, Tokuda M (2018) Effects of infection by Turnip mosaic virus on the population growth of generalist and specialist aphid vectors on turnip plants. PLoS ONE 13(7):e0200784
Akula R, Ravishankar GA (2011) Influence of abiotic stress signals on secondary metabolites in plants. Plant Signal Behav 6(11):1720–1731
Araya F, Abarca O, Zúñiga GE, Corcuera LJ (1991) Effects of NaCl on glycine-betaine and on aphids in cereal seedlings. Phytochemistry 30(6):1793–1795
Ashraf MA, Ashraf M, Ali Q (2010) Response of two genetically diverse wheat cultivars to salt stress at different growth stages: leaf lipid peroxidation and phenolic contents. Pak J Bot 42(1):559–565
Aucejo-Romero S, Gómez-Cadenas A, Jacas-Miret JA (2004) Effects of NaCl-stressed citrus plants on life-history parameters of Tetranychus urticae (Acari: Tetranychidae). Exp Appl Acarol 33(1–2):55
Ayers RS, Westcot DW (1985) Water quality for agriculture, vol 29. Food and Agriculture Organization of the United Nations, Rome
Azizpour K, Shakiba MR, Sima NKK, Alyari H, Mogaddam M, Esfandiari E, Pessarakli M (2010) Physiological response of spring durum wheat genotypes to salinity. J Plant Nutr 33(6):859–873
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39(1):205–207
Bennett RN, Wallsgrove RM (1994) Secondary metabolites in plant defence mechanisms. New Phytol 127(4):617–633
Berner J, Westhuizen A (2010) The selective induction of the phenylalanine ammonia-lyase pathway in the resistance response of wheat to the Russian wheat aphid. Cereal Res Commun 38(4):506–513
Cakmak I, Demiral MA (2007) Response of Tetranychus cinnabarinus feeding on NaCl-stressed strawberry plants. Phytoparasitica 35(1):37–49
Carr JP, Murphy AM, Tungadi T, Yoon JY (2019) Plant defense signals: players and pawns in plant-virus-vector interactions. Plant Sci 279:87–95
Chelli-Chaabouni A, Mosbah AB, Maalej M, Gargouri K, Gargouri-Bouzid R, Drira N (2010) In vitro salinity tolerance of two pistachio rootstocks: Pistacia vera L. and P. atlantica Desf. Environ Exp Bot 69(3):302–312
Cheraghi SAM (2004) Institutional and scientific profiles of organizations working on saline agriculture in Iran. In: Prospects of Saline Agriculture in the Arabian Peninsula: Proceedings of the International Seminar on Prospects of Saline Agriculture in the GCC Countries. pp 18–20
Chi H (2019) TWOSEX-MSChart: a computer program for the age-stage, two-sex life table analysis. Available onhttp://140.120, 197
Chi H, Getz WM (1988) Mass rearing and harvesting based on an age-stage, two-sex life table: a potato tuberworm (Lepidoptera: Gelechiidae) case study. Environ Entomol 17(1):18–25
Chi HSIN, Liu H (1985) Two new methods for the study of insect population ecology. Bull Inst Zool Acad Sin 24(2):225–240
Chrzanowski G, Leszczyński B, Czerniewicz P, Sytykiewicz H, Matok H, Krzyżanowski R, Sempruch C (2012) Effect of phenolic acids from black currant, sour cherry and walnut on grain aphid (Sitobion avenae F.) development. Crop Prot 35:71–77
Ciepiela A (1989) Biochemical basis of winter wheat resistance to the grain aphid, Sitobion avenae. Entomol Exp et Appl 51(3):269–275
Corcuera LJ, Argandona VH, Zuniga GE (1987) Resistance of cereal crops to aphids: role of allelochemicals. Allelochemicals: Role in agriculture and forestry. ACS Symposium Series, vol 330. ACS Publications, Washington, D.C, pp 129–135
Crowder DW, Li J, Borer ET, Finke DL, Sharon R, Pattemore D, Medlock J (2019) Species interactions affect the spread of vector-borne plant pathogens independent of transmission mode. Ecology 100:e02782
Davis TS, Bosque-Pérez NA, Foote NE, Magney T, Eigenbrode SD (2015) Environmentally dependent host–pathogen and vector–pathogen interactions in the Barley yellow dwarf virus pathosystem. J Appl Ecol 52(5):1392–1401
Dreyer DL, Jones KC (1981) Feeding deterrency of flavonoids and related phenolics towards Schizaphis graminum and Myzus persicae: aphid feeding deterrents in wheat. Phytochemistry 20(11):2489–2493
Dugasa MT, Cao F, Ibrahim W, Wu F (2019) Differences in physiological and biochemical characteristics in response to single and combined drought and salinity stresses between wheat genotypes differing in salt tolerance. Physiol Plant 165(2):134–143
Efron B, Tibshirani RJ (1994) An introduction to the bootstrap. CRC Press, Boca Raton
Foster WA, Treherne JE (1976) Insects of marine saltmarshes: problems and adaptations. Mar Insects 176:5–42
Goodman D (1982) Optimal life histories, optimal notation, and the value of reproductive value. Am Nat 119:803–823
Hajiboland R, Norouzi F, Poschenrieder C (2014) Growth, physiological, biochemical and ionic responses of pistachio seedlings to mild and high salinity. Trees 28(4):1065–1078
Han P, Wang ZJ, Lavoir AV, Michel T, Seassau A, Zheng WY et al (2016) Increased water salinity applied to tomato plants accelerates the development of the leaf miner Tuta absoluta through bottom-up effects. Sci Rep 6:32403
Harris KF, Maramorosch K (eds) (2014) Aphids as virus vectors. Elsevier, Amsterdam
Harris KF (2018) Aphid transmission of plant viruses. Plant viruses. CRC Press, Boca Raton, pp 177–204
Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Biol 51(1):463–499
Hernandez JA, Ferrer MA, Jimenez A, Barcelo AR, Sevilla F (2001) Antioxidant systems and O2−/H2O2 production in the apoplast of pea leaves. Its relation with salt-induced necrotic lesions in minor veins. Plant Physiol 127:817–831
Hull R (2014) Matthews’ plant virology, 5th edn. Academic Press, Cambridge
Hussain M, Ahmad S, Hussain S, Lal R, Ul-Allah S, Nawaz A (2018) Rice in saline soils: physiology, biochemistry, genetics, and management. Advances in agronomy, vol 148. Academic Press, Cambridge, pp 231–287
Isayenkov SV (2012) Physiological and molecular aspects of salt stress in plants. Cytol Genet 46:302–318
Isayenkov SV, Maathuis FJ (2019) Plant salinity stress: many unanswered questions remain. Front Plant Sci 10:80
James RA, von Caemmerer S, Condon AT, Zwart AB, Munns R (2008) Genetic variation in tolerance to the osmotic stress component of salinity stress in durum wheat. Funct Plant Biol 35(2):111–123
Jiménez-Martínez ES, Bosque-Pérez NA, Berger PH, Zemetra RS (2004) Life history of the bird cherry-oat aphid, Rhopalosiphum padi (Homoptera: Aphididae), on transgenic and untransformed wheat challenged with Barley yellow dwarf virus. J Econ Entomol 97(2):203–212
Kamangar SB, Taning CNT, De Jonghe K, Smagghe G (2019) Quantity and transmission efficiency of an isolate of the Potato virus Y-Wilga (PVY N−Wi) by aphid species reared on different host plants. J Plant Dis Prot 126:529–534
Khare T, Kumar V, Kishor PK (2015) Na+ and Cl− ions show additive effects under NaCl stress on induction of oxidative stress and the responsive antioxidative defense in rice. Protoplasma 252(4):1149–1165
Kumar S, Beena AS, Awana M, Singh A (2017) Physiological, biochemical, epigenetic and molecular analyses of wheat (Triticum aestivum) genotypes with contrasting salt tolerance. Front Plant Sci 8:1151
Laney AG, Chen P, Korth KL (2018) Interactive effects of aphid feeding and virus infection on host gene expression and volatile compounds in salt-stressed soybean, Glycinemax (L.) Merr. Arthropod-Plant Interact 12(3):401–413
Leszczyński B, Warchoł J, Niraz S (1985) The influence of phenolic compounds on the preference of winter wheat cultivars by cereal aphids. Int J Trop Insect Sci 6(2):157–158
Leszczynski B, Wright LC, Bakowski T (1989) Effect of secondary plant substances on winter wheat resistance to grain aphid. Entomol Exp Appl 52(2):135–139
Lim JH, Park KJ, Kim BK, Jeong JW, Kim HJ (2012) Effect of salinity stress on phenolic compounds and carotenoids in buckwheat (Fagopyrumesculentum M.) sprout. Food Chem 135(3):1065–1070
Malik CP, Singh MB (1980) Plant enzymology and histo-enzymology. Kalyani Publishers, Chennai
Mekawy AMM, Abdelaziz MN, Ueda A (2018) Apigenin pretreatment enhances growth and salinity tolerance of rice seedlings. Plant Physiol Biochem 130:94–104
Miller WA, Rasochová L (1997) Barley yellow dwarf viruses. Annu Rev Phytopathol 35:167–190
Mostefaoui H, Allal-Benfekih L, Djazouli ZE, Petit D, Saladin G (2014) Why the aphid Aphis spiraecola is more abundant on clementine tree than Aphis gossypii? CR Biol 337(2):123–133
Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25(2):239–250
Munns R, Gilliham M (2015) Salinity tolerance of crops–what is the cost? New Phytol 208(3):668–673
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Ann Rev Plant Biol 59:651–681
Nam KH, Kim YJ, Moon YS, Pack IS, Kim CG (2017) Salinity affects metabolomic profiles of different trophic levels in a food chain. Sci Total Environ 599:198–206
Pakdel A, Afsharifar A, Niazi A, Izadpanah K (2015) Molecular characterization of the complete genome of a barley yellow dwarf virus-PAV isolate from Iran. Iran J Plant Pathol 51(2):163–176 (in Persian)
Parihar P, Singh S, Singh R, Singh VP, Prasad SM (2015) Effect of salinity stress on plants and its tolerance strategies: a review. Environ Sci Pollut Res 22(6):4056–4075
Petridis A, Therios I, Samouris G, Tananaki C (2012) Salinity-induced changes in phenolic compounds in leaves and roots of four olive cultivars (Olea europaea L.) and their relationship to antioxidant activity. Environ Exp Bot 79:37–43
Polack LA, Pereyra PC, Sarandón SJ (2011) Effects of plant stress and habitat manipulation on Aphid control in greenhouse sweet peppers. J Sustain Agric 35(7):699–725
Qadir M, Qureshi AS, Cheraghi SAM (2008) Extent and characterisation of salt-affected soils in Iran and strategies for their amelioration and management. Land Degrad Dev 19(2):214–227
Quais MK, Ansari NA, Wang GY, Zhou WW, Zhu ZR (2019) Host plant salinity stress affects the development and population parameters of Nilaparvata lugens (Hemiptera: Delphacidae). Environ Entomol 48(5):1149–1161
Rahnama A, Fakhri S, Meskarbashee M (2019) Root growth and architecture responses of bread wheat cultivars to salinity stress. Agron J 111(6):1–8
Rattan RS (2010) Mechanism of action of insecticidal secondary metabolites of plant origin. Crop Prot 29(9):913–920
Renault S, Wolfe S, Markham J, Avila-Sakar G (2016) Increased resistance to a generalist herbivore in a salinity-stressed non-halophytic plant. AoB Plants 8:plw028
Rezvani Moghaddam P, Koocheki A (2001) Research history on salt affected lands of Iran: Present and future prospects—Halophytic ecosystem—International symposium on prospects of saline agriculture in the GCC Countries. Dubai, UAE
Safari M, Ferrari MJ, Roossinck MJ (2019) Manipulation of aphid behavior by a persistent plant virus. J Virol 93(9):e01781-e1818
Shabala S (ed) (2017) Plant stress physiology. CABI, Wallingford
Sienkiewicz-Paderewska D, Dmuchowski W, Baczewska AH, Brągoszewska P, Gozdowski D (2017) The effect of salt stress on lime aphid abundance on Crimean linden (Tilia ‘Euchlora’) leaves. Urban Forest Urban Green 21:74–79
Singh S (2016) Characterization of resistance in barley against corn leaf aphid Rhopalosiphum maidis (Fitch). Doctoral dissertation. Punjab Agricultural University, Ludhiana
Singh A, Bhushan B, Gaikwad K, Yadav OP, Kumar S, Rai RD (2015) Induced defence responses of contrasting bread wheat genotypes under differential salt stress imposition. Indian J Biochem Biophys 52:75–85
Srivastava PN, Auclair JL, Srivastava U (1983) Effect of nonessential amino acids on phagostimulation and maintenance of the pea aphid, Acyrthosiphon pisum. Can J Zool 61(10):2224–2229
Tiwari JK, Munshi AD, Kumar R, Pandey RN, Arora A, Bhat JS, Sureja AK (2010) Effect of salt stress on cucumber: Na+–K+ ratio, osmolyte concentration, phenols and chlorophyll content. Acta Physiol Plant 32(1):103–114
Trębicki P, Nancarrow N, Cole E, Bosque-Pérez NA, Constable FE, Freeman AJ et al (2015) Virus disease in wheat predicted to increase with a changing climate. Global Change Biol 21(9):3511–3519
Tsugane K, Kobayashi K, Niwa Y, Ohba Y, Wada K, Kobayashi H (1999) A recessive Arabidopsis mutant that grows photoautotrophically under salt stress shows enhanced active oxygen detoxification. Plant Cell 11:1195–1206
Van Emden HF, Harrington R (eds) (2017) Aphids as crop pests. CABI, Wallingford
Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35(4):753–759
Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218(1):1–14
Wang Q, Eneji AE, Kong X, Wang K, Dong H (2015) Salt stress effects on secondary metabolites of cotton in relation to gene expression responsible for aphid development. PLoS ONE 10(6):e0129541
Weimberg R (1987) Solute adjustments in leaves of two species of wheat at two different stages of growth in response to salinity. Physiol Plant 70(3):381–388
Wójcicka A (2010) Cereal phenolic compounds as biopesticides of cereal aphids. Pol J Environ Stud 19(6):1337–1343
Wojcicka A, Leszczynski B (2005) Secondary plant compounds may serve as biopesticides for the grain aphid Sitobion avenae F. PESTYCYDY-WARSZAWA- 4:163
Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–72
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The research was financially supported by Agricultural Sciences and Natural Resources University of Khuzestan [Grant No. 961.31].
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Ghodoum Parizipour, M.H., Rajabpour, A., Jafari, S. et al. Host-targeted salt stress affects fitness and vector performance of bird cherry-oat aphid (Rhopalosiphum padi L.) on wheat. Arthropod-Plant Interactions 15, 47–58 (2021). https://doi.org/10.1007/s11829-020-09795-0
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DOI: https://doi.org/10.1007/s11829-020-09795-0