Abstract
Plants produce a range of volatile organic compounds (VOCs) that mediate vital ecological interactions between herbivorous insects, their natural enemies, plants, and soil dwelling organisms including arbuscular mycorrhizal fungi (AMF). The composition, quantity, and quality of the emitted VOCs can vary and is influenced by numerous factors such as plant species, variety (cultivar), plant developmental stage, root colonization by soil microbes, as well as the insect developmental stage, and level of specialization of the attacking herbivore. Understanding factors shaping VOC emissions is important and can be leveraged to enhance plant health and pest resistance. In this greenhouse study, we evaluated the influence of plant variety, mycorrhizal colonization, herbivory, and their interactions on the composition of emitted volatiles in tomato plants (Solanum lycopersicum L.). Four tomato varieties from two breeding histories (two heirlooms and two hybrids), were used. Tomato plants were inoculated with a commercial inoculum blend consisting of four species of AMF. Plants were also subjected to herbivory by Manduca sexta (Lepidoptera: Sphingidae L.) five weeks after transplanting. Headspace volatiles were collected from inoculated and non-inoculated plants with and without herbivores using solid phase-microextraction. Volatile profiles consisted of 21 different volatiles in detectable quantities. These included monoterpenes, sesquiterpenes, and alkane hydrocarbons. We documented a strong plant variety effect on VOC emissions. AMF colonization and herbivory suppressed VOC emissions. Plant biomass was improved by colonization of AMF. Our results show that mycorrhization, herbivory and plant variety can alter tomato plant VOC emissions and further shape volatile-mediated insect and plant interactions.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
Available upon request
Code Availability
Available upon request
References
Adesemoye AO, Kloepper JW (2009) Plant–microbes interactions in enhanced fertilizer-use efficiency. Appl Microbiol Biotechnol 85(1):1–12. https://doi.org/10.1007/s00253-009-2196-0
Anastasaki E, Balayannis G, Papanikolaou NE, Michaelakis AN, Milonas PG (2015) Oviposition induced volatiles in tomato plants. Phytochem Lett 13:262–266. https://doi.org/10.1016/j.phytol.2015.07.007
Arce CCM, Machado RAR, Ribas NS, Cristaldo PF, Ataíde LMS, Pallini Â, Carmo FM, Freitas LG, Lima E (2017) Nematode root herbivory in tomato increases leaf defenses and reduces leaf miner oviposition and performance. J Chem Ecol 43(2):120–128. https://doi.org/10.1007/s10886-016-0810-z
Asensio D, Rapparini F, Peñuelas J (2012) AM fungi root colonization increases the production of essential isoprenoids vs. Nonessential isoprenoids especially under drought stress conditions or after jasmonic acid application. Phytochemistry 77:149–161. https://doi.org/10.1016/j.phytochem.2011.12.012
Ayelo PM, Yusuf AA, Pirk CWW, Mohamed SA, Chailleux A, Deletre E (2021) The role of trialeurodes vaporariorum-infested tomato plant volatiles in the attraction of encarsia formosa (Hymenoptera: Aphelinidae). J Chem Ecol 47(2):192–203. https://doi.org/10.1007/s10886-021-01245-2
Babikova Z, Gilbert L, Bruce T, Dewhirst SY, Pickett JA, Johnson D (2014a) Arbuscular mycorrhizal fungi and aphids interact by changing host plant quality and volatile emission. Funct Ecol 28(2):375–385. https://doi.org/10.1111/1365-2435.12181
Babikova Z, Gilbert L, Randall KC, Bruce TJA, Pickett JA, Johnson D (2014b) Increasing phosphorus supply is not the mechanism by which arbuscular mycorrhiza increase attractiveness of bean (Vicia faba) to aphids. J Exp Bot 65(18):5231–5241. https://doi.org/10.1093/jxb/eru283
Babikova Z, Johnson D, Bruce T, Pickett J, Gilbert L (2014c) Underground allies: How and why do mycelial networks help plants defend themselves? BioEssays 36(1):21–26. https://doi.org/10.1002/bies.201300092
Bauer JT, Kleczewski NM, Bever JD, Clay K, Reynolds HL (2012) Nitrogen-fixing bacteria, arbuscular mycorrhizal fungi, and the productivity and structure of prairie grassland communities. Oecologia 170(4):1089–1098. https://doi.org/10.1007/s00442-012-2363-3
Bennett AE, Bever JD (2007) Mycorrhizal species differentially alter plant growth and response to herbivory. Ecology 88(1):210–218. https://doi.org/10.1890/0012-9658(2007)88[210:MSDAPG]2.0.CO;2
Bennett AE, Bever JD, Bowers MD (2009) Arbuscular mycorrhizal fungal species suppress inducible plant responses and alter defensive strategies following herbivory. Oecologia 160(4):771–779. https://doi.org/10.1007/s00442-009-1338-5
Blanca J, Montero-Pau J, Sauvage C, Bauchet G, Illa E, Díez MJ, Francis D, Causse M, van der Knaap E, Cañizares J (2015) Genomic variation in tomato, from wild ancestors to contemporary breeding accessions. BMC Genomics 16(1):257. https://doi.org/10.1186/s12864-015-1444-1
Bleeker PM, Diergaarde PJ, Ament K, Guerra J, Weidner M, Schütz S, de Both MTJ, Haring MA, Schuurink RC (2009) The role of specific tomato volatiles in tomato-whitefly interaction. Plant Physiol 151(2):925–935. https://doi.org/10.1104/pp.109.142661
Bona E, Scarafoni A, Marsano F, Boatti L, Copetta A, Massa N, Gamalero E, D’Agostino G, Cesaro P, Cavaletto M, Berta G (2016) Arbuscular mycorrhizal symbiosis affects the grain proteome of Zea mays: a field study. Sci Rep 6(1):26439. https://doi.org/10.1038/srep26439
Bruce TJA, Wadhams LJ, Woodcock CM (2005) Insect host location: a volatile situation. Trends Plant Sci 10(6):269–274. https://doi.org/10.1016/j.tplants.2005.04.003
Campo S, Martín-Cardoso H, Olivé M, Pla E, Catala-Forner M, Martínez-Eixarch M, San Segundo B (2020) Effect of root colonization by arbuscular mycorrhizal fungi on growth, productivity and blast resistance in rice. Rice 13(1):42. https://doi.org/10.1186/s12284-020-00402-7
Chen YH, Gols R, Benrey B (2015) Crop domestication and its impact on naturally selected trophic interactions. Ann Rev Entomol 60:35–58. https://doi.org/10.1146/annurev-ento-010814-020601
Chitarra W, Pagliarani C, Maserti B, Lumini E, Siciliano I, Cascone P, Schubert A, Gambino G, Balestrini R, Guerrieri E (2016) Insights on the impact of arbuscular mycorrhizal symbiosis on tomato tolerance to water stress. Plant Physiol 171(2):1009–1023. https://doi.org/10.1104/pp.16.00307
Core Team R (2023) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. v4.2.3. https://www.R-project.org/. Accessed 25 Jul 2023
Damodaram KJP, Gadad HS, Parepally SK, Vaddi S, Hunashikatti LR, Bhat RM (2021) Low moisture stress influences plant volatile emissions affecting herbivore interactions in tomato, Solanum lycopersicum. Ecol Entomol 46(3):637–650. https://doi.org/10.1111/een.13012
Darshanee HLC, Ren H, Ahmed N, Zhang Z-F, Liu Y-H, Liu T-X (2017) Volatile-mediated attraction of greenhouse whitefly trialeurodes vaporariorum to tomato and eggplant. Front Plant Sci. https://doi.org/10.3389/fpls.2017.01285
de Lange ES, Farnier K, Gaudillat B, Turlings TCJ (2016) Comparing the attraction of two parasitoids to herbivore-induced volatiles of maize and its wild ancestors, the teosintes. Chemoecology 26(1):33–44. https://doi.org/10.1007/s00049-015-0205-6
de Lange ES, Laplanche D, Guo H, Xu W, Vlimant M, Erb M, Ton J, Turlings TCJ (2020) Spodoptera frugiperda Caterpillars Suppress Herbivore-Induced Volatile Emissions in Maize. J Chem Ecol 46(3):344–360. https://doi.org/10.1007/s10886-020-01153-x
Degen T, Bakalovic N, Bergvinson D, Turlings TCJ (2012) Differential performance and parasitism of caterpillars on maize inbred lines with distinctly different herbivore-induced volatile emissions. PLoS ONE 7:e47589. https://doi.org/10.1371/journal.pone.0047589
Degen T, Dillmann C, Marion-Poll F, Turlings TCJ (2004) High genetic variability of herbivore-induced volatile emission within a broad range of maize inbred lines. Plant Physiol 135(4):1928–1938. https://doi.org/10.1104/pp.104.039891
Dehimeche N, Buatois B, Bertin N, Staudt M (2021) Insights into the intraspecific variability of the above and belowground emissions of volatile organic compounds in tomato. Molecules 26(1):237. https://doi.org/10.3390/molecules26010237
Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the cry for help. Trends Plant Sci 15(3):167–175. https://doi.org/10.1016/j.tplants.2009.12.002
Doebley JF, Gaut BS, Smith BD (2006) The molecular genetics of crop domestication. Cell 127(7):1309–1321. https://doi.org/10.1016/j.cell.2006.12.006
Du Y-J, Poppy GM, Powell W (1996) Relative importance of semiochemicals from first and second trophic levels in host foraging behavior ofAphidius ervi. J Chem Ecol 22(9):1591–1605. https://doi.org/10.1007/BF02272400
Dudareva N, Negre F, Nagegowda DA, Orlova I (2006) Plant volatiles: recent advances and future perspectives. CRC Crit Rev Plant Sci 25(5):417–440. https://doi.org/10.1080/07352680600899973
Dudareva N, Pichersky E, Gershenzon J (2004) Biochemistry of plant volatiles. Plant Physiol 135(4):1893–1902. https://doi.org/10.1104/pp.104.049981
Dumas-Gaudot E, Gollotte A, Cordier C, Gianinazzil S, Gianinazzi-Pearson V (2000) Modulation of Host Defence Systems. In: Kapulnik Y, Douds DD (eds) Arbuscular Mycorrhizas: Physiology and Function. Springer, Netherlands, pp 173–200. https://doi.org/10.1007/978-94-017-0776-3_9
Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH (2004) Airborne signals prime plants against insect herbivore attack. Proc Natl Acad Sci 101(6):1781–1785. https://doi.org/10.1073/pnas.0308037100
Ezawa T, Saito K (2018) How do arbuscular mycorrhizal fungi handle phosphate? New insight into fine-tuning of phosphate metabolism. New Phytol 220(4):1116–1121. https://doi.org/10.1111/nph.15187
Fellbaum CR, Gachomo EW, Beesetty Y, Choudhari S, Strahan GD, Pfeffer PE, Kiers ET, Bücking H (2012a) Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci 109(7):2666–2671. https://doi.org/10.1073/pnas.1118650109
Fellbaum CR, Mensah JA, Pfeffer PE, Kiers ET, Bücking H (2012b) The role of carbon in fungal nutrient uptake and transport. Plant Signal Behav 7(11):1509–1512. https://doi.org/10.4161/psb.22015
Fontana A, Reichelt M, Hempel S, Gershenzon J, Unsicker SB (2009) The effects of arbuscular mycorrhizal fungi on direct and indirect defense metabolites of plantago lanceolata L. J Chem Ecol 35(7):833–843. https://doi.org/10.1007/s10886-009-9654-0
Gershenzon J (1994a) The cost of plant chemical defense against herbivory: A biochemical perspective. In EA Bernays (ed) Insect-Plant Interactions, 5th edn. (pp 105–173). CRC Press, Boca Raton, FL
Gershenzon J (1994b) Metabolic costs of terpenoid accumulation in higher plants. J Chem Ecol 20(6):1281–1328. https://doi.org/10.1007/BF02059810
Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84(3):489–500. https://doi.org/10.1111/j.1469-8137.1980.tb04556.x
Goldman A (2008) The Heirloom Tomato: From Garden to Table: Recipes, Portraits, and History of the World’s Most Beautiful Fruit. Bloomsbury, New York, NY, USA
Gouinguené SP, Turlings TCJ (2002) The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiol 129(3):1296–1307. https://doi.org/10.1104/pp.001941
Hart MM, Aleklett K, Chagnon P-L, Egan C, Ghignone S, Helgason T, Lekberg Y, Öpik M, Pickles BJ, Waller L (2015) Navigating the labyrinth: A guide to sequence-based, community ecology of arbuscular mycorrhizal fungi. New Phytol 1(207):235–247. https://doi.org/10.1111/nph.13340
Harvey JA, van Dam NM, Raaijmakers CE, Bullock JM, Gols R (2011) Tri-trophic effects of inter- and intra-population variation in defence chemistry of wild cabbage (Brassica oleracea). Oecologia 166(2):421–431. https://doi.org/10.1007/s00442-010-1861-4
Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67(3):283–335. https://doi.org/10.1086/417659
Hodge A, Storer K (2015) Arbuscular mycorrhiza and nitrogen: Implications for individual plants through to ecosystems. Plant Soil 386(1):1–19. https://doi.org/10.1007/s11104-014-2162-1
Holopainen JK, Gershenzon J (2010) Multiple stress factors and the emission of plant VOCs. Trends Plant Sci 15(3):176–184. https://doi.org/10.1016/j.tplants.2010.01.006
Jacobi VG, Fernandez PC, Barriga LG, Almeida-Trapp M, Mithöfer A, Zavala JA (2021) Plant volatiles guide the new pest Dichelops furcatus to feed on corn seedlings. Pest Manag Sci 77(5):2444–2453. https://doi.org/10.1002/ps.6273
Johnson NC, Graham JH (2013) The continuum concept remains a useful framework for studying mycorrhizal functioning. Plant Soil 363(1):411–419. https://doi.org/10.1007/s11104-012-1406-1
Junker RR, Tholl D (2013) Volatile organic compound mediated interactions at the plant-microbe interface. J Chem Ecol 39(7):810–825. https://doi.org/10.1007/s10886-013-0325-9
Kant MR, Sabelis MW, Haring MA, Schuurink RC (2008) Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defences. Proc Royal Soc B: Biol Sci 275(1633):443–452. https://doi.org/10.1098/rspb.2007.1277
Karban R, Yang LH, Edwards KF (2014) Volatile communication between plants that affects herbivory: a meta-analysis. Ecol Lett 17(1):44–52. https://doi.org/10.1111/ele.12205
Kempel A, Schädler M, Chrobock T, Fischer M, van Kleunen M (2011) Tradeoffs associated with constitutive and induced plant resistance against herbivory. Proc Natl Acad Sci 108(14):5685–5689. https://doi.org/10.1073/pnas.1016508108
Khaosaad T, Vierheilig H, Nell M, Zitterl-Eglseer K, Novak J (2006) Arbuscular mycorrhiza alter the concentration of essential oils in oregano (Origanum sp., Lamiaceae). Mycorrhiza 16(6):443–446. https://doi.org/10.1007/s00572-006-0062-9
Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A, Palmer TM, West SA, Vandenkoornhuyse P, Jansa J, Bücking H (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333(6044):880–882. https://doi.org/10.1126/science.1208473
Kigathi RN, Weisser WW, Reichelt M, Gershenzon J, Unsicker SB (2019) Plant volatile emission depends on the species composition of the neighboring plant community. BMC Plant Biol 19:58. https://doi.org/10.1186/s12870-018-1541-9
Kleczewski NM, Herms DA, Bonello P (2010) Effects of soil type, fertilization and drought on carbon allocation to root growth and partitioning between secondary metabolism and ectomycorrhizae of Betula papyrifera. Tree Physiol 30(7):807–817. https://doi.org/10.1093/treephys/tpq032
Knegt B, Meijer TT, Kant MR, Kiers ET, Egas M (2020) Tetranychus evansi spider mite populations suppress tomato defenses to varying degrees. Ecol Evol 10(10):4375–4390. https://doi.org/10.1002/ece3.6204
Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23(2):95–103. https://doi.org/10.1016/j.tree.2007.10.008
Larimer AL, Bever JD, Clay K (2010) The interactive effects of plant microbial symbionts: a review and meta-analysis. Symbiosis 2(51):139–148. https://doi.org/10.1007/s13199-010-0083-1
Leitner M, Kaiser R, Hause B, Boland W, Mithöfer A (2010) Does mycorrhization influence herbivore-induced volatile emission in Medicago truncatula? Mycorrhiza 2(20):89–101. https://doi.org/10.1007/s00572-009-0264-z
Liaw A, Wiener M (2002) Classification and regression by randomforest. R News 2(3):18–22 (https://CRAN.R-project.org/doc/Rnews/)
Loreto F, Dicke M, Schnitzler J-P, Turlings TCJ (2014) Plant volatiles and the environment. Plant Cell Environ 37(8):1905–1908. https://doi.org/10.1111/pce.12369
Loughrin JH, Potter DA, Hamilton-Kemp TR (1995) Volatile compounds induced by herbivory act as aggregation kairomones for the Japanese beetle (Popillia japonica Newman). J Chem Ecol 21(10):1457–1467. https://doi.org/10.1007/BF02035145
McCormick AC, Gershenzon J, Unsicker SB (2014a) Little peaks with big effects: Establishing the role of minor plant volatiles in plant–insect interactions. Plant Cell Environ 37(8):1836–1844. https://doi.org/10.1111/pce.12357
McCormick AC, Irmisch S, Reinecke A, Boeckler GA, Veit D, Reichelt M, Hansson BS, Gershenzon J, Köllner TG, Unsicker SB (2014b) Herbivore-induced volatile emission in black poplar: regulation and role in attracting herbivore enemies. Plant Cell Environ 37(8):1909–1923. https://doi.org/10.1111/pce.12287
McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular—Arbuscular mycorrhizal fungi. New Phytol 115(3):495–501. https://doi.org/10.1111/j.1469-8137.1990.tb00476.x
Meier AR, Hunter MD (2018) Arbuscular mycorrhizal fungi mediate herbivore-induction of plant defenses differently above and belowground. Oikos 127(12):1759–1775. https://doi.org/10.1111/oik.05402
Meier AR, Hunter MD (2019) Mycorrhizae alter constitutive and herbivore-induced volatile emissions by milkweeds. J Chem Ecol 45(7):610–625. https://doi.org/10.1007/s10886-019-01080-6
Michereff MFF, Magalhães DM, Hassemer MJ, Laumann RA, Zhou J-J, Ribeiro PE, de Viana A, Guimarães PA, de Schimmelpfeng PE, Borges PHC, Pickett M, Birkett JA, Blassioli-Moraes MA (2019) Variability in herbivore-induced defence signalling across different maize genotypes impacts significantly on natural enemy foraging behaviour. J Pest Sci 92(2):723–736. https://doi.org/10.1007/s10340-018-1033-6
Milla R, Osborne CP, Turcotte MM, Violle C (2015) Plant domestication through an ecological lens. Trends Ecol Evol 30(8):463–469. https://doi.org/10.1016/j.tree.2015.06.006
Mumm R, Dicke M (2010) Variation in natural plant products and the attraction of bodyguards involved in indirect plant defense. Can J Zool 88:628–277. https://doi.org/10.1139/Z10-032
Musser R, Hum-Musser SM, Eichenseer H, Peiffer M, Ervin G, Murphy JB, Felton GW (2002) Caterpillar saliva beats plant defences. Nature 416(6881):599–600. https://doi.org/10.1038/416599a
Ngumbi E, Chen L, Fadamiro HY (2009) Comparative GC-EAD responses of a specialist (Microplitis croceipes) and a generalist (Cotesia marginiventris) parasitoid to cotton volatiles induced by two caterpillar species. J Chem Ecol 35(9):1009–1020. https://doi.org/10.1007/s10886-009-9700-y
Ngumbi E, Dady E, Calla B (2022) Flooding and herbivory: The effect of concurrent stress factors on plant volatile emissions and gene expression in two heirloom tomato varieties. BMC Plant Biol 22(1):536. https://doi.org/10.1186/s12870-022-03911-3
Ngumbi EN, Ugarte CM (2021) Flooding and herbivory interact to alter volatile organic compound emissions in two maize hybrids. J Chem Ecol 47(7):707–718. https://doi.org/10.1007/s10886-021-01286-7
Ninkovic V, Markovic D, Rensing M (2021) Plant volatiles as cues and signals in plant communication. Plant Cell Environ 44(4):1030–1043. https://doi.org/10.1111/pce.13910
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MH, Wagner H (2019) Community Ecology Package – Package ‘vegan’
Paran I, van der Knaap E (2007) Genetic and molecular regulation of fruit and plant domestication traits in tomato and pepper. J Exp Bot 58(14):3841–3852. https://doi.org/10.1093/jxb/erm257
Paudel S, Lin P-A, Foolad MR, Ali JG, Rajotte EG, Felton GW (2019) Induced plant defenses against herbivory in cultivated and wild tomato. J Chem Ecol 45(8):693–707. https://doi.org/10.1007/s10886-019-01090-4
Peñuelas J, Asensio D, Tholl D, Wenke K, Rosenkranz M, Piechulla B, Schnitzler JP (2014) Biogenic volatile emissions from the soil. Plant Cell Environ 37(8):1866–1891. https://doi.org/10.1111/pce.12340
Pineda A, Zheng S-J, van Loon J, Pieterse C, Dicke M (2010) Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci 15:507–514. https://doi.org/10.1016/j.tplants.2010.05.007
Pozo MJ, Azcón-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10(4):393–398. https://doi.org/10.1016/j.pbi.2007.05.004
Proffit M, Birgersson G, Bengtsson M, Reis R, Witzgall P, Lima E (2011) Attraction and oviposition of Tuta absoluta females in response to tomato leaf volatiles. J Chem Ecol 37(6):565–574
Raghava T, Ravikumar P, Hegde R, Kush A (2010) Spatial and temporal volatile organic compound response of select tomato cultivars to herbivory and mechanical injury. Plant Sci 179(5):520–526. https://doi.org/10.1016/j.plantsci.2010.07.020
Ranganathan Y, Borges RM (2010) Reducing the babel in plant volatile communication: using the forest to see the trees. Plant Biol 12(5):735–742. https://doi.org/10.1111/j.1438-8677.2009.00278.x
Rapparini F, Llusia J, Penuelas J (2008) Effect of arbuscular mycorrhizal (AM) colonization on terpene emission and content of Artemisia annua L. Plant Biol (Stuttgart Germany) 10:108–122. https://doi.org/10.1055/s-2007-964963
Rodriguez-Saona C, Vorsa N, Singh AP, Johnson-Cicalese J, Szendrei Z, Mescher MC, Frost CJ (2011) Tracing the history of plant traits under domestication in cranberries: potential consequences on anti-herbivore defences. J Exp Bot 62(8):2633–2644. https://doi.org/10.1093/jxb/erq466
Rowen E, Kaplan I (2016) Eco-evolutionary factors drive induced plant volatiles: a meta-analysis. New Phytol 210(1):284–294. https://doi.org/10.1111/nph.13804
RStudio Team (2023) RStudio: Integrated Development for R. RStudio. PBC, Boston, MA
Saia S, Benítez E, García-Garrido JM, Settanni L, Amato G, Giambalvo D (2014) The effect of arbuscular mycorrhizal fungi on total plant nitrogen uptake and nitrogen recovery from soil organic material. J Agricultural Sci 152(3):370–378. https://doi.org/10.1017/S002185961300004X
Sarmento RA, Lemos F, Bleeker PM, Schuurink RC, Pallini A, Oliveira MGA, Lima ER, Kant M, Sabelis MW, Janssen A (2011) A herbivore that manipulates plant defence. Ecol Lett 14(3):229–236. https://doi.org/10.1111/j.1461-0248.2010.01575.x
Schausberger P, Peneder S, Jürschik S, Hoffmann D (2012) Mycorrhiza changes plant volatiles to attract spider mite enemies. Funct Ecol 26(2):441–449. https://doi.org/10.1111/j.1365-2435.2011.01947.x
Schulz-Bohm K, Gerards S, Hundscheid M, Melenhorst J, de Boer W, Garbeva P (2018) Calling from distance: attraction of soil bacteria by plant root volatiles. ISME J 12(5):1252–1262. https://doi.org/10.1038/s41396-017-0035-3
Shimoda T, Ozawa R, Sano K, Yano E, Takabayashi J (2005) The Involvement of volatile infochemicals from spider mites and from food-plants in prey location of the generalist predatory Mite Neoseiulus californicus. J Chem Ecol 31(9):2019–2032. https://doi.org/10.1007/s10886-005-6075-6
Shrivastava G, Ownley BH, Augé RM, Toler H, Dee M, Vu A, Köllner TG, Feng C (2015) Colonization by arbuscular mycorrhizal and endophytic fungi enhanced terpene production in tomato plants and their defense against a herbivorous insect. Symbiosis 65(2):65–74
Silva DB, Weldegergis BT, van Loon JJA, Bueno VHP (2017) Qualitative and quantitative differences in herbivore-induced plant volatile blends from tomato plants infested by either Tuta absoluta or Bemisia tabaci. J Chem Ecol 43(1):53–65. https://doi.org/10.1007/s10886-016-0807-7
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, London
Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250. https://doi.org/10.1146/annurev-arplant-042110-103846
Snoeren TAL, Kappers IF, Broekgaarden C, Mumm R, Dicke M, Bouwmeester HJ (2010) Natural variation in herbivore-induced volatiles in Arabidopsis thaliana. J Exp Bot 61(11):3041–3056. https://doi.org/10.1093/jxb/erq127
Tamiru A, Bruce TJA, Woodcock CM, Caulfield JC, 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(11):1075–1083. https://doi.org/10.1111/j.1461-0248.2011.01674.x
Tanksley SD, McCouch SR (1997) Seed banks and molecular maps: unlocking genetic potential from the wild. Science 277(5329):1063–1066. https://doi.org/10.1126/science.277.5329.1063
Tieman D, Zhu G, Resende MFR, Lin T, Nguyen C, Bies D, Rambla JL, Beltran KSO, Taylor M, Zhang B, Ikeda H, Liu Z, Fisher J, Zemach I, Monforte A, Zamir D, Granell A, Kirst M, Huang S, Klee H (2017) A chemical genetic roadmap to improved tomato flavor. Science 355(6323):391–394. https://doi.org/10.1126/science.aal1556
Vannette RL, Hunter MD (2009) Mycorrhizal fungi as mediators of defence against insect pests in agricultural systems. Agric For Entomol 11(4):351–358. https://doi.org/10.1111/j.1461-9563.2009.00445.x
Vannette RL, Hunter MD, Rasmann S (2013) Arbuscular mycorrhizal fungi alter above- and below-ground chemical defense expression differentially among Asclepias species. Front Plant Sci. https://doi.org/10.3389/fpls.2013.00361
Veluchamy S, Hind SR, Dunham DM, Martin GB, Panthee DR (2014) Natural variation for responsiveness to flg22, flgII-28, and csp22 and Pseudomonas syringae pv. tomato in heirloom tomatoes. PLoS ONE 9(9):e106119. https://doi.org/10.1371/journal.pone.0106119
Volpe V, Chitarra W, Cascone P, Volpe MG, Bartolini P, Moneti G, Pieraccini G, di Serio C, Maserti B, Guerrieri E, Balestrini R (2018) The association with two different arbuscular mycorrhizal fungi differently affects water stress tolerance in tomato. Front Plant Sci 9. https://doi.org/10.3389/fpls.2018.01480
Wang E, Yu N, Bano SA, Liu C, Miller AJ, Cousins D, Zhang X, Ratet P, Tadege M, Mysore KS, Downie JA, Murray JD, Oldroyd GED, Schultze M (2014) A H+-ATPase that energizes nutrient uptake during mycorrhizal symbioses in rice and Medicago truncatula. Plant Cell 26(4):1818–1830. https://doi.org/10.1105/tpc.113.120527
Weinblum N, Cna’ani A, Yaakov B, Sadeh A, Avraham L, Opatovsky I, Tzin V (2021) Tomato cultivars resistant or susceptible to spider mites differ in their biosynthesis and metabolic profile of the monoterpenoid pathway. Front Plant Sci 12:630155. https://doi.org/10.3389/fpls.2021.630155
Whitehead SR, Turcotte MM, Poveda K (2017) Domestication impacts on plant–herbivore interactions:a meta-analysis. Philosophical Trans Royal Soc B: Biol Sci 372(1712):20160034. https://doi.org/10.1098/rstb.2016.0034
Wickham H, Averick M, Bryan J, Chang W, McGowan LD, François R, Grolemund G, Hayes A, Henry L, Hester J, Kuhn M, Pedersen TL, Miller E, Bache SM, Müller K, Ooms J, Robinson D, Seidel DP, Spinu V, Yutani H (2019) Welcome to the tidyverse. J Open Source Softw 4(43):1686. https://doi.org/10.21105/joss.01686
Yamamoto RT (1969) Mass rearing of the tobacco hornworm. II. Larval rearing and pupation12. J Econ Entomol 62(6):1427–1431. https://doi.org/10.1093/jee/62.6.1427
Yasmin H, Rashid U, Hassan MN, Nosheen A, Naz R, Ilyas N, Sajjad M, Azmat A, Alyemeni MN (2021) Volatile organic compounds produced by Pseudomonas pseudoalcaligenes alleviated drought stress by modulating defense system in maize (Zea mays L). Physiol Plant 172(2):896–911. https://doi.org/10.1111/ppl.13304
Yeom H-J, Kang JS, Kim G-H, Park I-K (2012) Insecticidal and acetylcholine esterase inhibition activity of Apiaceae plant essential oils and their constituents against adults of German Cockroach (Blattella germanica). J Agric Food Chem 60(29):7194–7203. https://doi.org/10.1021/jf302009w
Züst T, Agrawal AA (2017) Trade-offs between plant growth and defense against insect herbivory: an emerging mechanistic synthesis. Annu Rev Plant Biol 68:513–534. https://doi.org/10.1146/annurev-arplant-042916-040856
Acknowledgements
We thank: Jim and Joyce Nardi, Larry Hanks, Anna Grommes, and Kim Leigh; Department of Entomology at University of Illinois Urbana-Champaign.
Guirong Zhang of Crop Sciences at University of Illinois Urbana-Champaign.
Rosalie Metallo, Heather Lash and Montgomery W. Flack; Plant Care Facility University of Illinois Urbana-Champaign.
Lily Wilcock and Aaron Mleziva for statistical consulting at University of Illinois Urbana-Champaign.
Funding
This research was funded by the University of Illinois Urbana-Champaign.
Author information
Authors and Affiliations
Contributions
Erinn Dady, Nathan Kleczewski, Carmen Ugarte and Esther Ngumbi contributed to the study conception and design. Material preparation, and data collection and analysis were performed by Erinn Dady and Esther Ngumbi. Data analyses were performed by Erinn Dady and Carmen Ugarte. The first draft of the manuscript was written by Erinn Dady and Esther Ngumbi and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics Approval
Not Applicable.
Consent to Participate
Not applicable.
Consent for Publication
Co-authors consent to the submission of this manuscript.
Competing Interests
The authors declare no competing interests.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material
Table S1
Excel table of individual VOC emissions among tomato varieties, averaged and identified by class. Compounds are arranged in order of elution during gas chromatography. (XLSX 18.4 KB)
Table S2
Excel table of total VOC emissions among tomato varieties that were not significant by interaction. Data are averages of eight replicates (n = 8) ± SE. (XLSX 10.1 KB)
Table S3
Excel table of biomass and root architecture among tomato varieties. Data are averages of eight replicates (n = 8) ± SE. (XLSX 11.9 KB)
Table S4
Excel table of mycorrhization data among tomato varieties. Each individual plant had eight slides prepared to contain five root sections each, for a total of 64 slides per treatment group. Data are averages of percent of roots colonized for eight replicates (n = 8) ± SE. (XLSX 11.3 KB)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Dady, E.R., Kleczewski, N., Ugarte, C.M. et al. Plant Variety, Mycorrhization, and Herbivory Influence Induced Volatile Emissions and Plant Growth Characteristics in Tomato. J Chem Ecol 49, 710–724 (2023). https://doi.org/10.1007/s10886-023-01455-w
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-023-01455-w