Abstract
Maize lethal necrosis is one of the most devastating diseases of maize causing yield losses reaching up to 90% in sub-Saharan Africa. The disease is caused by a combination of maize chlorotic mottle virus (MCMV) and any one of cereal viruses in the Potyviridae group such as sugarcane mosaic virus. MCMV has been reported to be transmitted mainly by maize thrips (Frankliniella williamsi) and onion thrips (Thrips tabaci). To better understand the role of thrips vectors in the epidemiology of the disease, we investigated behavioral responses of F. williamsi and T. tabaci, to volatiles collected from maize seedlings infected with MCMV in a four-arm olfactometer bioassay. Volatile profiles from MCMV-infected and healthy maize plants were compared by gas chromatography (GC) and GC coupled mass spectrometry analyses. In the bioassays, both sexes of F. williamsi and male T. tabaci were significantly attracted to volatiles from maize plants infected with MCMV compared to healthy plants and solvent controls. Moreover, volatile analysis revealed strong induction of (E)-4,8-dimethyl-1,3,7-nonatriene, methyl salicylate and (E,E)-4,8,12-trimethyltrideca-1,3,7,11-tetraene in MCMV-infected maize seedlings. Our findings demonstrate MCMV induces changes in volatile profiles of host plants to elicit attraction of thrips vectors. The increased vector contact rates with MCMV-infected host plants could enhance virus transmission if thrips feed on the infected plants and acquire the pathogen prior to dispersal. Uncovering the mechanisms mediating interactions between vectors, host plants and pathogens provides useful insights for understanding the vector ecology and disease epidemiology, which in turn may contribute in designing integrated vector management strategies.
Similar content being viewed by others
References
Abdullah ZS, Greenfield BPJ, Ficken KJ, Taylor JWD, Wood M, Butt TM (2015) A new attractant for monitoring western flower thrips, Frankliniella occidentalis in protected crops. SpringerPlus 4:89
Abe H, Tomitaka Y, Shimoda T, Seo S, Sakurai T, Kugimiya S, Tsuda S, Kobayashi M (2011) Antagonistic plant defense system regulated by phytohormones assists interactions among vector insect, thrips and a tospovirus. Plant Cell Physiol 53(1):204–212
Adams IP, Harju VA, Hodges T, Hany U, Skelton A, Rai S, Deka MK, Smith J, Fox A, Uzayisenga B, Ngaboyisonga C (2014) First report of maize lethal necrosis disease in Rwanda. New Dis Rep 29:22
Aitchison J (1986) The statistical analysis of compositional data London; New York: Chapman and Hall xv, 416 p
Beale MH, Birkett MA, Bruce TJA, Chamberlain K, Field LM, Huttly AK, Martin JL, Parker R, Phillips AL, Pickett JA, Prosser IM, Shewry PR, Smart LE, Wadhams LJ, Woodcock CM, Zhang Y (2006) Aphid alarm pheromone produced by transgenic plants affects aphid and parasitoid behavior. Proc Natl Acad Sci U S A 103:10509–10513
Belliure B, Janssen A, Maris PC, Peters D, Sabelos MW (2005) Herbivore arthropods benefit from vectoring plant viruses. Ecol Lett 8:70–79
Blanc S, Michalakis Y (2016) Manipulation of hosts and vectors by plant viruses and impact of the environment. Curr Opin Insect Sci 16:36–43
Blua MJ, Perring TM (1992) Effects of zucchini yellow mosaic virus on colonization and feeding behavior of Aphis gossypii (Homoptera: Aphididae) Alatae. Environ Entomol 21:578–585
Braidwood L, Quito-Avila DF, Cabanas D, Bressan A, Wangai A, Baulcombe DC (2018) Maize chlorotic mottle virus exhibits low divergence between differentiated regional sub-populations. Sci Rep 8:1173
Bruce TJA, Pickett JA (2011) Perception of plant volatile blends by herbivorous insects – finding the right mix. Phytochemistry 72:1605–1611
Cabanas D, Watanabe S, Higashi CHV, Bressan A (2013) Dissecting the mode of maize chlorotic mottle virus transmission (Tombusviridae: Machlomovirus) by Frankliniella williamsi (Thysanoptera: Thripidae). J Econ Entomol 106:16–24
Cairns JE, Hellin J, Sonder K, Araus JL, Macrobert JF, Thierfelder C, Prasanna BM (2013) Adapting maize production to climate change in sub-Saharan Africa. Food Security 5:345–360
Chermenskaya TD, Burov VN, Maniar SP, Pow EM, Roditakis N, Selytskaya OG, Shamshev IV, Wadhams LJ, Woodcock CM (2001) Behavioural responses of western flower thrips, Frankliniella occidentalis (Pergande), to volatiles from three aromatic plants. Int J Trop Insect Sci 21(1):67–72
Cook SM, Khan ZR, Pickett JA (2007) The use of push-pull strategies in integrated pest management. Annu Rev Entomol 52:375–400
Degen T, Dillmann C, Marion-Poll F, Turlings TCJ (2004) High genetic variability of herbivoreinduced volatile emission within a broad range of maize inbred lines. Plant Physiol 135:1928–1938. https://doi.org/10.1104/pp.104.039891
De Boer JG, Dicke M (2004) The role of methyl salicylate in prey searching behavior of the predatory mite Phytoseiulus persimilis. J Chem Ecol 30:255–271
De Vos M, Jander G (2010) Volatile communication in plant-aphid interactions. Curr Opin Plant Biol 13:366–371
Eigenbrode SD, Ding H, Shiel P, Berger PH (2002) Volatiles from potato plants infected with potato leafroll virus attract and arrest the virus vector, Myzus persicae (Homoptera: Aphididae). Proc R Soc B 269:455–460
Isabirye BE, Rwomushana I (2016) Current and future potential distribution of Maize chlorotic mottle virus and risk of maize lethal necrosis disease in Africa. J Crop Prot 5:215–228
Kfir R, Overholt WA, Khan ZR, Polaszek A (2002) Biology and management of economically important lepidopteran cereal stem borers in Africa. Annu Rev Entomol 47:701–731
Koschier EH (2008) Essential oil compounds for thrips control – a review. Nat Prod Commun 3(7):1171–1182
Koschier EH, De Kogel WJ, Visser JH (2000) Assessing the attractiveness of volatile plant compounds to western flower thrips Frankliniella occidentalis. J Chem Ecol 26:2643–2655
Koschier EH, Hoffmann D, Riefler J (2007) Influence of salicylaldehyde and methyl salicylate on post-landing behaviour of Frankliniella occidentalis Pergande. J Appl Entomol 131(5):362–367
Kusia ES, Subramanian S, Nyasani JO, Khamis F, Villinger J, Ateka E, Pappu HR (2015) First report of lethal necrosis disease associated with co-infection of finger millet with Maize chlorotic mottle virus and Sugarcane mosaic virus in Kenya. Plant Dis 99:899–900
Lancashire PD, Bleiholder H, Langelüddecke P, Stauss R, Van Den Boom T, Weber E, Witzenberger A (1991) A uniform decimal code for growth stages of crops and weeds. Ann Appl Biol 119:561–601
Lukanda M, Owati A, Ogunsanya P, Valimunzigha K, Katsongo K, Ndemere H, Kumar PL (2014) First report of maize chlorotic mottle virus infecting maize in the Democratic Republic of Congo. Plant Dis 98:1448–1448
Mahuku G, Lockhart BE, Wanjala B, Jones MW, Kimunye JN, Stewart LR, Cassone BJ, Sevgan S, Nyasani JO, Kusia E, Kumar PL, Niblett CL, Kiggundu A, Asea G, Pappu HR, Wangai A, Prasanna BM, Redinbaugh MG (2015a) Maize lethal necrosis (MLN), an emerging threat to maize-based food security in sub-saharan africa. Phytopathol 105:956–965
Mahuku G, Wangai A, Sadessa K, Teklewold A, Wegary D, Ayalneh D, Adams I, Smith J, Bottomley E, Bryce S, Braidwood L, Feyissa B, Regassa B, Wanjala B, Kimunye JN, Mugambi C, Monjero K, Prasanna BM (2015b) First report of maize chlorotic mottle virus and maize lethal necrosis on maize in Ethiopia. Plant Dis 99:1870
Mallinger RE, Hogg DB, Gratton C (2011) Methyl salicylate attracts natural enemies and reduces populations of soybean aphids (Hemiptera: aphididae) in soybean agroecosystems. J Econ Entomol 104:115–124
Maris PC (2004) Evaluation of thrips resistance in pepper to control Tomato spotted wilt virus infection. PhD thesis, Wageningen University, Wageningen
Mauck KE, De Moraes CM, Mescher MC (2014) Biochemical and physiological mechanisms underlying effects of cucumber mosaic virus on host-plant traits that mediate transmission by aphid vectors. Plant Cell Environ 37:1427–1439
Mcelhany P, Real LA, Power AG (1995) Vector preference and disease dynamics: a study of barley yellow dwarf virus. Ecology 76:444–457
Mfuti DK, Niassy S, Subramanian S, Du Plessis H, Ekesi S, Maniania NK (2017) Lure and infect strategy for application of entomopathogenic fungus for the control of bean flower thrips in cowpea. Biol Control 107:70–76
Moritz G, Brandt S, Triapitsyn S, Subramanian S (2013) Identification and Information Tools for Pest Thrips in East Africa. QBIT, QAAFI, UQ. ISBN 978-1-74272-067-8 http://thripsnet.zoologie.unihalle.de/key-server-neu/data/ 03030c05-030b-4107-880b-0a0a0702060d/media/ Html/index.html
Nderitu JH, Wambua EM, Olubayo F, Kasina JM, Waturu CN (2007) Management of thrips (Thysanoptera: Thripdae) infestation on French beans (Phaseolus vulgaris L.) in Kenya by combination of insecticides and varietal resistance. J Entomol 4:469–473
Nelson S, Brewbaker J, Hu J (2011). Maize chlorotic mottle. Honolulu (HI): University of Hawaii. 6 p. (Plant disease; PD-79). http://hdl.handle.net/10125/32440
Niassy S, Maniania NK, Subramanian S, Gitonga LM, Ekesi S (2012) Performance of a semiochemical-baited autoinoculation device treated with Metarhizium anisopliae for control of Frankliniella occidentalis on French bean in field cages. Entomol Exp Applic 142:97–103
Nyasani JO, Meyhöfer R, Subramanian S, Poehling HM (2013) Seasonal abundance of western flower thrips and its natural enemies in different French bean agroecosystems in Kenya. J Pest Sci 86:515–523
Nyasani J, Kusia E, Subramanian S (2015) Thrips as pests and vectors of Maize chlorotic mottle virus in maize. In Proc. Xth international symposium on Thysanoptera and Tospoviruses, Asilomar conference grounds, may 16th–20th, 2015. 49 p
Oluwafemi S, Bruce TJ, Pickett JA, Ton J, Birkett MA (2011) Behavioral responses of the leafhopper, Cicadulina storeyi China, a major vector of maize streak virus, to volatile cues from intact and leafhopper-damaged maize. J Chem Ecol 37(1):40–48. https://doi.org/10.1007/s10886-010-9891-2 Epub 2010 Dec 30
R Development Core Team (2015) R: A Language and Environment for Statistical Computing R Foundation for Statistical Computing, Vienna, Austria
Rotenberg D, Kumar NKK, Ullman DE, Montero-Astúa M, Willis DK, German TL, Whitfield AE (2009) Variation in tomato spotted wilt virus titer in Frankliniella occidentalis and its association with frequency of transmission. Phytopathol 99:404–410
Saad KA, Roff MNM, Rebecca H, Hallett RH, Idris B, ABd-Ghani IB (2017) Effects of cucumber mosaic virus-infected chilli plants on non-vector Bemisia tabaci (Hemiptera: Aleyrodidae). https://doi.org/10.1111/1744-7917.12488
Seskar M, Shulaev V, Raskin I (1998) Endogenous methyl salicylate in pathogen-inoculated tobacco plants. Plant Physiol 116:387–392
Shalileh S, Ogada PA, Moualeu DP, Poehling HM (2016) Manipulation of Frankliniella occidentalis (Thysanoptera: Thripidae) by Tomato Spotted Wilt Virus (Tospovirus) via the host plant nutrients to enhance its transmission and spread. Environ Entomol 45:1235–1242
Shapiro L, De Moraes CM, Stephenson AG, Mescher MC (2012) Pathogen effects on vegetative and floral odours mediate vector attraction and host exposure in a complex pathosystem. Ecol Lett 15:1430–1438
Sileshi G, Akinnifesi FK, Debusho LK, Beedy T, Ajayi OC, Mong’omba S (2010) Variation in maize yield gaps with plant nutrient inputs, soil type and climate across sub-Saharan Africa. Field Crops Res 116:1–13
Silva R, Furlong MJ, Wilson LJ, Walter GH (2013) How predictable are the behavioral responses of insects to herbivore induced changes in plants? Responses of two congeneric thrips to induced cotton plants. PLoS One 8:e63611
Sisterson MS (2008) Effects of insect-vector preference for healthy or infected plants on pathogen spread. insights from a model J Econ Entomol 101:1–8
Stafford CA, Walker GP, Ullman DE (2011) Infection with a plant virus modifies vector feeding behavior. Proc Natl Acad Sci U S A 108:9350–9355
Tamiru A, Khan ZR (2017) Volatile semiochemical mediated plant defense in cereals: a novel strategy for crop protection. Agronomy 7(3):58
Tamiru A, Bruce TJA, Woodcock CM, Caulifield CJ, Midega CAO, Ogol CKPO, Mayon P, Birkett MA, Pickett JA, Khan ZR (2011) Maize landraces recruit egg and larval parasitoids in response to egg deposition by a herbivore. Ecol Lett 14:1075–1083
Tamiru A, Bruce TJA, Woodcock CM, Birkett MA, Midega CAO, Pickett JA, Khan ZR (2015) Chemical cues modulating electrophysiological and behavioral responses in the parasitic wasp Cotesia sesamiae. Can J Zool 93:281–287
Teulon DAJ, Castañé C, Nielsen M-C, El-Sayed AM, Davidson MM, Gardner-Gee R, Poulton J, Kean AM, Hall C, Butler RC, Sansom CE, Suckling DM, Perry NB (2014) Evaluation of new volatile compounds as lures for western flower thrips and onion thrips in New Zealand and Spain. N Z Plant Prot 67:175–183
Tomitaka Y, Abe H, Sakurai T, Tsuda S (2015) Preference of the vector thrips Frankliniella occidentalis for plants infected with thrips-non-transmissible tomato spotted wilt virus. J Appl Entomol 139:250–259
Turlings TCJ, Bernasconi M, Bertossa R, Bigler F, Caloz G, Dorn S (1998) The induction of volatile emissions in maize by three herbivore species with different feeding habits: possible consequences for their natural enemies. Biol Control 11:122–129
Uyemoto J (1983) Biology and control of maize chlorotic mottle virus. Plant Dis 67:7–10
Van De Wetering F, Van Der Hoek M, Goldbach R, Peters D (1999) Differences in Tomato spotted wilt virus vector competency between males and females of Frankliniella occidentalis. Entomol Exp Appl 93:105–112
Wang Q, Zhang C, Wang C, Qian Y, Li Z, Hong J, Zhou X (2017) Further characterization of maize chlorotic mottle virus and its synergistic interaction with sugarcane mosaic virus in maize. Sci Rep 7:39960
Wangai AW, Redinbaugh MG, Kinyua ZM, Miano DW, Leley PK, Kasina M, Mahuku G, Scheets K, Jeffers D (2012) First report of maize chlorotic mottle virus and maize lethal necrosis in Kenya. Plant Dis 96:1582–1583
Whitfield AE, Ullman DE, German TL (2005) Tospovirus-thrips interactions. Annu Rev Phytopathol 43:459–489
Xie L, Zhang J, Wang Q, Meng C, Hong J, Zhou X (2011) Characterization of maize chlorotic mottle virus associated with maize lethal necrosis disease in China. J Phytopathol 159:191–193
Acknowledgements
We gratefully acknowledge the financial support by the following organizations and agencies: BMZ (The German Federal Ministry for Economic Cooperation and Development) – Thrips Project, the European Union, Biovision Foundation, UK’s Department for International Development (DFID), Swedish International Development Cooperation Agency, the Swiss Agency for Development and Cooperation (SDC), and the Kenyan Government. The views expressed herein do not necessarily reflect the official opinion of these donors. The authors wish to thank icipe’s Thrips and ‘Push-Pull’ IPM projects staff for their technical assistance.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Ethical Approval
Experiments were performed in accordance with relevant guidelines and regulations on studies on live animals.
Rights and permissions
About this article
Cite this article
Mwando, N.L., Tamiru, A., Nyasani, J.O. et al. Maize Chlorotic Mottle Virus Induces Changes in Host Plant Volatiles that Attract Vector Thrips Species. J Chem Ecol 44, 681–689 (2018). https://doi.org/10.1007/s10886-018-0973-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-018-0973-x