[en] BACKGROUND: Plants are constantly exposed to a wide range of herbivores at both aboveground (AG) and belowground (BG) levels, involving multiple constitutive defenses in leaves and roots. However, the Optimal Defense Theory predicts that the energy cost of defenses prevents plants from defending all organs equally. In an agroeconomic context, selecting genotypes for their root-specific resistance may therefore create trade-offs in the allocation of constitutive defenses, potentially leaving leaves more vulnerable to aerial herbivores. To test this hypothesis, we assessed the resistance to the root-feeding aphid Pemphigus bursarius (BG) and the foliar aphids Myzus persicae and Nasonovia ribisnigri (AG) in two chicory (Cichorium intybus var foliosum) genotypes: AX, considered susceptible, and B18, considered resistant to P. bursarius. Aphids' survival and fecundity were measured, and their feeding behavior was evaluated using the electrical penetration graph (EPG) technique. RESULTS: Only the root-feeding aphid P. bursarius exhibited reduced survival, fecundity and feeding activity on the B18 genotype, compared with the susceptible AX genotype, confirming the root-level resistance for which this line was originally selected. In contrast, the foliar aphid N. ribisnigri showed enhanced feeding activity and fecundity on B18, whereas M. persicae displayed only increased feeding activity, suggesting increased foliar susceptibility relative to AX. CONCLUSION: Selection for root resistance may promote a shift in resource allocation toward root defenses, potentially reducing constitutive defenses in leaves. These results highlight potential trade-offs in plant defense allocation and underline the importance of considering multi-organ herbivory when breeding for resistance traits.
Disciplines :
Entomology & pest control
Author, co-author :
Cochenille, Thomas; UMR CNRS 7058 EDYSAN (Écologie et Dynamique des Systèmes Anthropisés), Université de Picardie Jules Verne, Amiens, France ; Ecologie des Interactions et Changements Globaux, Research Institute for Bio-sciences, Université de Mons, Mons, Belgium
Baracchini, Clément; UMR CNRS 7058 EDYSAN (Écologie et Dynamique des Systèmes Anthropisés), Université de Picardie Jules Verne, Amiens, France
Doury, Géraldine; UMR CNRS 7058 EDYSAN (Écologie et Dynamique des Systèmes Anthropisés), Université de Picardie Jules Verne, Amiens, France
Six, Audrey; Association des Producteurs d'Endives de France, Arras, France
Tougeron, Kévin ✱; Université de Mons - UMONS > Faculté des Sciences > Service Écologie des Interactions et Changements Globaux
Ameline, Arnaud ✱; UMR CNRS 7058 EDYSAN (Écologie et Dynamique des Systèmes Anthropisés), Université de Picardie Jules Verne, Amiens, France
✱ These authors have contributed equally to this work.
Language :
English
Title :
Testing optimal defense theory: Root resistance selection in chicory (Cichorium intybus) reduces foliar defense and alters aphid performance and feeding behavior
Publication date :
30 April 2026
Journal title :
Pest Management Science
ISSN :
1526-498X
eISSN :
1526-4998
Publisher :
John Wiley & Sons, Hoboken, United States - New Jersey
Peer reviewed :
Peer Reviewed verified by ORBi
Development Goals :
2. Zero hunger 15. Life on land
Research unit :
S850 - Ecologie des Interactions et Changements Globaux
Bezemer TM, Wagenaar R, Van Dam NM and Wäckers FL, Interactions between above- and belowground insect herbivores as mediated by the plant defense system. Oikos 101:555–562 (2003). https://doi.org/10.1034/j.1600-0706.2003.12424.x.
Kafle D, Hänel A, Lortzing T, Steppuhn A and Wurst S, Sequential above- and belowground herbivory modifies plant responses depending on herbivore identity. BMC Ecol 17:5 (2017). https://doi.org/10.1186/s12898-017-0115-2.
Kaplan I, Halitschke R, Kessler A, Sardanelli S and Denno RF, Constitutive and induced defenses to herbivory in above- and belowground plant tissues. Ecology 89:392–406 (2008). https://doi.org/10.1890/07-0471.1.
War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S et al., Mechanisms of plant defense against insect herbivores. Plant Signal Behav 7:1306–1320 (2012). https://doi.org/10.4161/psb.21663 PubMed PMID: 22895106.
Agrawal AA, Fishbein M, Jetter R, Salminen JP, Goldstein JB, Freitag AE et al., Phylogenetic ecology of leaf surface traits in the milkweeds (asclepias spp.): chemistry, ecophysiology, and insect behavior. New Phytol 183:848–867 (2009). https://doi.org/10.1111/j.1469-8137.2009.02897.x.
Chen A, Liu T, Wang Z and Chen X, Plant root suberin: a layer of defence against biotic and abiotic stresses. Front Plant Sci 13:1056008 (2022). https://doi.org/10.3389/fpls.2022.1056008.
Hanley ME, Lamont BB, Fairbanks MM and Rafferty CM, Plant structural traits and their role in anti-herbivore defence. Perspect Plant Ecol Evol Syst 8:157–178 (2007). https://doi.org/10.1016/j.ppees.2007.01.001.
Mithöfer A and Boland W, Plant defense against herbivores: chemical aspects. Annu Rev Plant Biol 63:431–450 (2012). https://doi.org/10.1146/annurev-arplant-042110-103854.
Gebretsadik KG, Liu Z, Yang J, Liu H, Qin A, Zhou Y et al., Plant-aphid interactions: recent trends in plant resistance to aphids. Stress Biol 5:28 (2025). https://doi.org/10.1007/s44154-025-00214-z.
Tjallingii WF, Electrical recording of stylet penetration activities, in Aphids, their Biology, Natural Enemies and Control. Elsevier, Amsterdam, pp. 95–108 (1988) Available from: https://research.wur.nl/en/publications/electrical-recording-of-stylet-penetration-activities.
Van Dam NM, Belowground herbivory and plant defenses. Annu Rev Ecol Evol Syst 40:373–391 (2009). https://doi.org/10.1146/annurev.ecolsys.110308.120314.
Erb M, The role of roots in plant Defence, in Plant Defence: Biological Control, ed. by Mérillon JM and Ramawat KG. Springer Netherlands, Dordrecht, pp. 291–309 (2012). https://doi.org/10.1007/978-94-007-1933-0_12.
Erb M, Lenk C, Degenhardt J and Turlings TCJ, The underestimated role of roots in defense against leaf attackers. Trends Plant Sci 14:653–659 (2009). https://doi.org/10.1016/j.tplants.2009.08.006 PubMed PMID: 19736036.
Kaplan I, Halitschke R, Kessler A, Rehill BJ, Sardanelli S and Denno RF, Physiological integration of roots and shoots in plant defense strategies links above- and belowground herbivory. Ecol Lett 11:841–851 (2008). https://doi.org/10.1111/j.1461-0248.2008.01200.x.
Nalam VJ, Shah J and Nachappa P, Emerging role of roots in plant responses to aboveground insect herbivory. Insect Sci 20:286–296 (2013). https://doi.org/10.1111/1744-7917.12004.
Rasmann S and Agrawal AA, In defense of roots: a research agenda for studying plant resistance to belowground herbivory. Plant Physiol 146:875–880 (2008). https://doi.org/10.1104/pp.107.112045.
Züst T and Agrawal AA, Trade-offs between plant growth and defense against insect herbivory: an emerging mechanistic synthesis. Annu Rev Plant Biol 68:513–534 (2017). https://doi.org/10.1146/annurev-arplant-042916-040856 PubMed PMID: 28142282.
McKey D, Adaptive patterns in alkaloid physiology. Am Nat 108:305–320 (1974). https://doi.org/10.1086/282909.
Hunziker P, Lambertz SK, Weber K, Crocoll C, Halkier BA and Schulz A, Herbivore feeding preference corroborates optimal defense theory for specialized metabolites within plants. Proc Natl Acad Sci 118:e2111977118 (2021). https://doi.org/10.1073/pnas.2111977118.
Touw AJ and Van Dam NM, Optimal chemical defence allocation in roots: where, why and how? Phytochem Rev 24:27–36 (2023). https://doi.org/10.1007/s11101-023-09872-1.
Tsunoda T, Krosse S and van Dam NM, Root and shoot glucosinolate allocation patterns follow optimal defence allocation theory. J Ecol 105:1256–1266 (2017). https://doi.org/10.1111/1365-2745.12793.
Alba C, Bowers MD and Hufbauer R, Combining optimal defense theory and the evolutionary dilemma model to refine predictions regarding plant invasion. Ecology 93:1912–1921 (2012). https://doi.org/10.1890/11-1946.1.
Ali JG and Agrawal AA, Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci 17:293–302 (2012). https://doi.org/10.1016/j.tplants.2012.02.006.
Barrett LG and Heil M, Unifying concepts and mechanisms in the specificity of plant–enemy interactions. Trends Plant Sci 17:282–292 (2012). https://doi.org/10.1016/j.tplants.2012.02.009.
Herms DA and Mattson WJ, The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335 (1992). https://doi.org/10.1086/417659.
Gaillard MDP, Glauser G, Robert CAM and Turlings TCJ, Fine-tuning the ‘plant domestication-reduced defense’ hypothesis: specialist vs generalist herbivores. New Phytol 217:355–366 (2018). https://doi.org/10.1111/nph.14757.
Draga S, Gabelli G, Palumbo F and Barcaccia G, Genome-wide datasets of chicories (Cichorium intybus L.) for marker-assisted crop breeding applications: a systematic review and meta-analysis. Int J Mol Sci 24:14 (2023). https://doi.org/10.3390/ijms241411663.
Moreno A, Bertolini E, Olmos A, Cambra M and Fereres A, Estimation of vector propensity for Lettuce mosaic virus based on viral detection in single aphids. Span J Agric Res 5:376–384 (2007). https://doi.org/10.5424/SJAR/2007053-5343.
Nebreda M, Moreno A, Pérez N, Palacios I, Seco-Fernández V and Fereres A, Activity of aphids associated with lettuce and broccoli in Spain and their efficiency as vectors of Lettuce mosaic virus. Virus Res 100:83–88 (2004). https://doi.org/10.1016/j.virusres.2003.12.016.
Szwejda JH, Diptera pests occurring on vegetable crops in Poland. J Hortic Res 31:169–188 (2023). https://doi.org/10.2478/johr-2023-0030.
Verbeek M, Dullemans AM and van der Vlugt RAA, Aphid transmission of lettuce necrotic leaf curl virus, a member of a tentative new subgroup within the genus Torradovirus. Virus Res 241:125–130 (2017). https://doi.org/10.1016/J.VIRUSRES.2017.02.008 PubMed PMID: 28223184.
Benigni M, Cassan L, Leignez S, Durlin L and Oste S, Control of root aphid (Pemphigus bursarius L.) in witloof chicory culture (Cichorium intybus L. var. foliosum). Crop Prot 89:209–215 (2016). https://doi.org/10.1016/j.cropro.2016.07.027.
Vandegehuchte ML, de la Peña E and Bonte D, Contrasting covariation of above- and belowground invertebrate species across plant genotypes. J Anim Ecol 80:148–158 (2011). https://doi.org/10.1111/j.1365-2656.2010.01766.x.
Dunn JA, The biology of lettuce root aphid. Ann Appl Biol 47:475–491 (1959). https://doi.org/10.1111/j.1744-7348.1959.tb07280.x.
Hough GL, Biology and Control of Currant Lettuce Aphid Nasonovia Ribisnigri [phd] [Internet]. University of Warwick, Coventry, (2013) Available from: http://webcat.warwick.ac.uk/record=b2691453~S1.
Baudry X, Doury G, Couty A, Fourdrain Y, van Havermaet R, Lateur M et al., Antagonist effects of the leek Allium porrum as a companion plant on aphid host plant colonization. Sci Rep 11:4032 (2021). https://doi.org/10.1038/s41598-021-83580-8.
Diaz BM and Fereres A, Life table and population parameters of Nasonovia ribisnigri (Homoptera: Aphididae) at different constant temperatures. Environ Entomol 34:527–534 (2005). https://doi.org/10.1603/0046-225X-34.3.527.
Ameline A, Denoirjean T, Casati M, Dorland J and Decocq G, How generalist insect herbivores respond to alien plants? The case of Aphis fabae–Myzus persicae–Rhododendron ponticum. Pest Manag Sci 80:1795–1801 (2023). https://doi.org/10.1002/ps.7908.
Shrestha G, Skovgård H, Reddy GVP, Steenberg T and Enkegaard A, Role of the aphid species and their feeding locations in parasitization behavior of Aphelinus abdominalis, a parasitoid of the lettuce aphid Nasonovia ribisnigri. PLoS One 12:e0184080 (2017). https://doi.org/10.1371/journal.pone.0184080.
Tjallingii, WF, Electronic recording of penetration behaviour by aphids. Entomologia experimentalis et applicata 24:721–730 (1978). https://doi.org/10.1111/j.1570-7458.1978.tb02836.x.
Cole RA, Riggall W and Morgan A, Electronically monitored feeding behaviour of the lettuce root aphid (Pemphigus bursarius) on resistant and susceptible lettuce varieties. Entomol Exp Appl 68:179–185 (1993). https://doi.org/10.1111/j.1570-7458.1993.tb01701.x.
Sarria E, Cid M, Garzo E and Fereres A, Excel workbook for automatic parameter calculation of EPG data. Comput Electron Agric 67:35–42 (2009). https://doi.org/10.1016/j.compag.2009.02.006.
Thompson GA and Goggin FL, Transcriptomics and functional genomics of plant defence induction by phloem-feeding insects. J Exp Bot 57:755–766 (2006). https://doi.org/10.1093/jxb/erj135.
R Core Team, R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria (2025) Available from: https://www.r-project.org/.
Posit Team, RStudio: Integrated Development Environment for R [Internet]. Posit Software, PBC, Boston, MA (2025) Available from: http://www.posit.co/.
Palial S, Kumar S, Atri C, Sharma S and Banga SS, Antixenosis and antibiosis mechanisms of resistance to turnip aphid, Lipaphis erysimi (Kaltenbach) in Brassica juncea-fruticulosa introgression lines. J Pest Sci 95:749–760 (2022). https://doi.org/10.1007/s10340-021-01418-8.
Gebretsadik KG, Zhang Y and Chen J, Screening and evaluation for antibiosis resistance of the spring wheat accessions to the grain aphid, Sitobion miscanthi (Takahashi) (Hemiptera: Aphididae). J Integr Agric 21:2329–2344 (2022). https://doi.org/10.1016/S2095-3119(21)63716-4.
Stenberg JA and Muola A, How should plant resistance to herbivores be measured? Front Plant Sci 8:663 (2017). https://doi.org/10.3389/fpls.2017.00663.
Le Roux V, Dugravot SB, Campan E, Dubois FO, Vincent C and Giordanengo P, Wild solanum resistance to aphids: antixenosis or antibiosis? J Econ Entomol 101:584–591 (2014).
Yang X, Zhang L, Li Y, Liu X, Chen C, Deng Y et al., Fortifying crop defenses: unraveling the molecular arsenal against aphids. Hortic Adv 2:22 (2024). https://doi.org/10.1007/s44281-024-00038-3.
Smith CM and Clement SL, Molecular bases of plant resistance to arthropods. Annu Rev Entomol 57:309–328 (2012). https://doi.org/10.1146/annurev-ento-120710-100642.
Awmack CS and Leather SR, Host plant quality and fecundity in herbivorous insects. Annu Rev Entomol 47:817–844 (2002). https://doi.org/10.1146/annurev.ento.47.091201.145300.
Wetzel WC, Kharouba HM, Robinson M, Holyoak M and Karban R, Variability in plant nutrients reduces insect herbivore performance. Nature 539:425–427 (2016). https://doi.org/10.1038/nature20140.
ten Broeke CJM, Dicke M and van Loon JJA, Performance and feeding behaviour of two biotypes of the black currant-lettuce aphid, Nasonovia ribisnigri, on resistant and susceptible Lactuca sativa near-isogenic lines. Bull Entomol Res 103:511–521 (2013). https://doi.org/10.1017/S0007485312000880.
Yang M, Wu C, Zhang T, Shi L, Li J, Liang H et al., Chicoric acid: natural occurrence, chemical synthesis, biosynthesis, and their bioactive effects. Front Chem 10:888673 (2022). https://doi.org/10.3389/fchem.2022.888673.
Frey M, Vahabi K, Cankar K, Lackus ND, Padilla-Gonzalez F, Ro DK et al., Sesquiterpene lactones – insights into biosynthesis, regulation and Signalling roles. Crit Rev Plant Sci 43:131–157 (2024). https://doi.org/10.1080/07352689.2024.2307240.
Bogdanović M, Cankar K, Todorović S, Dragicević M, Simonović A, Van Houwelingen A et al., Tissue specific expression and genomic organization of bitter sesquiterpene lactone biosynthesis in Cichorium intybus L. (Asteraceae). Ind Crop Prod 129:253–260 (2019). https://doi.org/10.1016/j.indcrop.2018.12.011.
Padilla-Gonzalez GF, Dos Santos FA and Da Costa FB, Sesquiterpene lactones: more than protective plant compounds with high toxicity. Crit Rev Plant Sci 35:18–37 (2016). https://doi.org/10.1080/07352689.2016.1145956.
Jurgoński A, Milala J, Juśkiewicz J, Zduńczyk Z and Król B, Composition of chicory root, peel, seed and leaf ethanol extracts and biological properties of their non-inulin fractions (2011).
Jaiswal R, Kiprotich J and Kuhnert N, Determination of the hydroxycinnamate profile of 12 members of the Asteraceae family. Phytochemistry 72:781–790 (2011). https://doi.org/10.1016/j.phytochem.2011.02.027.
Kundu A and Vadassery J, Chlorogenic acid-mediated chemical defence of plants against insect herbivores. Plant Biol 21:185–189 (2019). https://doi.org/10.1111/plb.12947.
Leiss KA, Maltese F, Choi YH, Verpoorte R and Klinkhamer PGL, Identification of chlorogenic acid as a resistance factor for thrips in chrysanthemum. Plant Physiol 150:1567–1575 (2009). https://doi.org/10.1104/pp.109.138131.
Cole RA, Phenolic acids associated with the resistance of lettuce cultivars to the lettuce root aphid. Ann Appl Biol 105:129–145 (1984). https://doi.org/10.1111/j.1744-7348.1984.tb02809.x.
Beharav A, Ben-David R, Malarz J, Stojakowska A, Michalska K, Doležalová I et al., Variation of sesquiterpene lactones in Lactuca aculeata natural populations from Israel, Jordan and Turkey. Biochem Syst Ecol 38:602–611 (2010). https://doi.org/10.1016/j.bse.2010.07.007.
Lankau RA, Specialist and generalist herbivores exert opposing selection on a chemical defense. New Phytol 175:176–184 (2007). https://doi.org/10.1111/j.1469-8137.2007.02090.x.
Landau I, Müller-Schärer H and Ward PI, Influence of cnicin, a sesquiterpene lactone ofCentaurea maculosa (Asteraceae), on specialist and generalist insect herbivores. J Chem Ecol 20:929–942 (1994). https://doi.org/10.1007/BF02059588.
Sharma M, Oraon PK, Srivastava R, Chongtham R, Goel S, Agarwal M et al., Comparative transcriptomics of a generalist aphid, Myzus persicae and a specialist aphid, Lipaphis erysimi reveals molecular signatures associated with diversity of their feeding behaviour and other attributes. Front Plant Sci 15:1415628 (2024). https://doi.org/10.3389/fpls.2024.1415628.
Jhou YS, Poovendhan S, Huang LH and Tsai CW, Host acceptance and plant resistance: a comparative behavioral study of Myzus persicae and Acyrthosiphon pisum. Insects 12:975 (2021). https://doi.org/10.3390/insects12110975.
Wang Y, Ma Y, Zhou DS, Gao SX, Zhao XC, Tang QB et al., Higher plasticity in feeding preference of a generalist than a specialist: experiments with two closely related Helicoverpa species. Sci Rep 7:17876 (2017). https://doi.org/10.1038/s41598-017-18244-7.
Tooker JF and Frank SD, Genotypically diverse cultivar mixtures for insect pest management and increased crop yields. J Appl Ecol 49:974–985 (2012). https://doi.org/10.1111/j.1365-2664.2012.02173.x.