Abstract
Main conclusion
Our results indicate caterpillars and aphids cause similar levels of induced defences and resistance against caterpillars in wild cotton plants. These symmetrical effects are not consistent with patterns predicted by plant defensive signaling crosstalk and call for further work addressing the biochemical mechanisms underpinning these results.
Abstract
Plant-induced responses to attack often mediate interactions between different species of insect herbivores. These effects are predicted to be contingent on the herbivore’s feeding guild, whereby prior feeding by insects should negatively impact subsequent feeding by insects of the same guild (induced resistance) but may positively influence insects of a different guild (induced susceptibility) due to interfering crosstalk between plant biochemical pathways specific to each feeding guild. We compared the effects of prior feeding by leaf-chewing caterpillars (Spodoptera frugiperda) vs. sap-sucking aphids (Aphis gossypii) on induced defences in wild cotton (Gossypium hirsutum) and the consequences of these attacks on subsequently feeding caterpillars (S. frugiperda). To this end, we conducted a greenhouse experiment where cotton plants were either left undamaged or first exposed to caterpillar or aphid feeding, and we subsequently placed caterpillars on the plants to assess their performance. We also collected leaves to assess the induction of chemical defences in response to herbivory. We found that prior feeding by both aphids and caterpillars resulted in reductions in consumed leaf area, caterpillar mass gain, and caterpillar survival compared with control plants. Concomitantly, prior aphid and caterpillar herbivory caused similar increases in phenolic compounds (flavonoids and hydroxycinnamic acids) and defensive terpenoids (hemigossypolone) compared with control plants. Overall, these findings indicate that these insects confer a similar mode and level of induced resistance in wild cotton plants, calling for further work addressing the biochemical mechanisms underpinning these effects.


Data availability
The data generated or analysed during this study are not included in this article but can be made available as per request.
Change history
28 January 2024
A Correction to this paper has been published: https://doi.org/10.1007/s00425-024-04344-y
Abbreviations
- JA:
-
Jasmonic acid
- SA:
-
Salicylic acid
References
Abdala-Roberts L, Pérez Niño B, Moreira X, Parra-Tabla V, Grandi L, Glauser G, Benrey B, Turlings TCJ (2019a) Effects of early-season insect herbivory on subsequent pathogen infection and ant abundance on wild cotton (Gossypium hirsutum). J Ecol 107:1518–1529. https://doi.org/10.1111/1365-2745.13131
Abdala-Roberts L, Quijano-Medina T, Moreira X, Vázquez-González C, Parra-Tabla V, Berny Mier Y, Teran J, Grandi L, Glauser G, Turlings TCJ, Benrey B (2019b) Bottom-up control of geographic variation in insect herbivory on wild cotton (Gossypium hirsutum) by plant defenses and climate. Am J Bot 106:1059–1067. https://doi.org/10.1002/ajb2.1330
Agrawal AA, Karban R (2000) Specificity of constitutive and induced resistance: pigment glands influence mites and caterpillars on cotton plants. Entomol Exp Appl 9:39–49. https://doi.org/10.1046/j.1570-7458.2000.00677.x
Ali JG, Agrawal AA (2014) Asymmetry of plant-mediated interactions between specialist aphids and caterpillars on two milkweeds. Funct Ecol 28:1404–1412. https://doi.org/10.1111/1365-2435.12271
Appel HM (1993) Phenolics in ecological interactions: The importance of oxidation. J Chem Ecol 19:1521–1552. https://doi.org/10.1007/BF00984895
Arce CM, Besomi G, Glauser G, Turlings TCJ (2021) Caterpillar-induced volatile emissions in cotton: the relative importance of damage and insect-derived factors. Front Plant Sci 12:709858. https://doi.org/10.3389/fpls.2021.709858
Azcón R, Barea JM (1997) Mycorrhizal dependency of a representative plant species in Mediterranean shrublands (Lavandula spica L.) as a key factor to its use for revegetation strategies in desertification-threatened areas. Appl Soil Ecol 7:83–92. https://doi.org/10.1016/S0929-1393(97)00013-9
Bezemer TM, Wagenaar IR, van Dam NM, van der Putten WH, Wäckers FL (2004) Above- and below-ground terpenoid aldehyde induction in cotton, Gossypium herbaceum, following root and leaf injury. J Chem Ecol 30:53–67
Bi JL, Murphy JB, Felton GW (1997) Antinutritive and oxidative components as mechanisms of induced resistance in cotton to Helicoverpa zea. J Chem Ecol 23:97–117. https://doi.org/10.1023/B:JOEC.0000006348.62578.fd
Clancy MV, Mamine M, Flückinger G, Quijano-Medina T, Pérez-Niño B, Abdala-Roberts L, Turlings TCJ, Bustos-Segura C (2023) Terpene chemotypes in wild cotton (Gossypium hirsutum) from the Yucatan Peninsula. Phytochemistry 205:113454. https://doi.org/10.1016/j.phytochem.2022.113454
D’Eeckenbrugge G, Lacape JM (2014) Distribution and differentiation of wild, feral, and cultivated populations of perennial upland cotton (Gossypium hirsutum L.) in Mesoamerica and the Caribbean. PloS One 9:e107458. https://doi.org/10.1371/journal.pone.0107458
de Bobadilla MF, Weichen RV, Gort G, Poelman EH (2022) Plasticity in induced resistance to sequential attack by multiple herbivores in Brassica nigra. Oecologia 198:11–20. https://doi.org/10.1007/s00442-021-05043-1
Dixit G, Praveen A, Tripathi T, Yadav VK, Verma PC (2017) Herbivore-responsive cotton phenolics and their impact on insect performance and biochemistry. J Asia-Pac Entomol 20:341–351. https://doi.org/10.1016/j.aspen.2017.02.002
Dixit G, Srivastava A, Rai KM, Dubey RS, Srivastava R, Verma PC (2020) Distinct defensive activity of phenolics and phenylpropanoid pathway genes in different cotton varieties toward chewing pests. Plant Signal Behav 15:e1747689. https://doi.org/10.1080/15592324.2020.1747689
Eisenring M, Glauser G, Meissle M, Romeis J (2018) Differential impact of herbivores from three feeding guilds on systemic secondary metabolite induction, phytohormone levels and plant-mediated herbivore interactions. J Chem Ecol 44:1178–1189. https://doi.org/10.1007/s10886-018-1015-4
Ellinger D, Voigt CA (2014) Callose biosynthesis in Arabidopsis with a focus on pathogen response: what we have learned within the last decade. Ann Bot 114:1349–1358. https://doi.org/10.1093/aob/mcu120
Erb M, Meldau S, Howe GA (2012) Role of phytohormones in insect-specific plant reactions. Trends Plant Sci 17:250–259. https://doi.org/10.1016/j.tplants.2012.01.003
Gols R, Harvey JA (2023) Integrating chemical plant trait- and ecological-based approaches to better understand differences in insect herbivory between cultivated and natural systems. Agr Ecosyst Environ 356:108643. https://doi.org/10.1016/j.agee.2023.108643
Hagenbucher S, Olson DM, Ruberson JR (2013) Resistance mechanisms against arthropod herbivores in cotton and their interactions with natural enemies. Cr Rev Plant Sci 32:458–482. https://doi.org/10.1080/07352689.2013.809293
Hedin PA, Parrott WL, Jenkins JN, Mulrooney JE, Menn JJ (1988) Elucidating mechanisms of tobacco budworm resistance to allelochemicals by dietary tests with insecticide synergists. Pestic Biochem Physiol 32:55–61. https://doi.org/10.1016/0048-3575(88)90121-6
Hegde M, Oliveira JN, da Costa JG, Bleicher E, Santana AEG, Bruce TJA, Caulfield J, Dewhirst SY, Woodcock CM, Pickett JA, Birkett MA (2011) Identification of semiochemicals released by cotton, Gossypium hirsutum, upon infestation by the cotton aphid, Aphis gossypii. J Chem Ecol 37:741–750. https://doi.org/10.1007/s10886-011-9980-x
Hernández-Cumplido J, Glauser G, Benrey B (2016) Cascading effects of early-season herbivory on late-season herbivores and their parasitoids. Ecology 97:1283–1297. https://doi.org/10.1890/15-1293.1
Hosny MM, Topper CP, Moawad GM, El-Saadany GB (1986) Economic damage thresholds of Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae) on cotton in Egypt. Crop Prot 5:100–104. https://doi.org/10.1016/0261-2194(86)90088-8
Howe AG, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66. https://doi.org/10.1146/annurev.arplant.59.032607.092825
Huang X-Z, Chen J-Y, Xiao H-J, Xiao Y-T, Wu J, Wu J-X, Zhou J-J, Zhang Y-J, Guo Y-Y (2015) Dynamic transcriptome analysis and volatile profiling of Gossypium hirsutum in response to the cotton bollworm Helicoverpa armigera. Sci Rep 5:11867. https://doi.org/10.1038/srep11867
Kassambara A (2023) rstatix: Pipe-Friendly Framework for Basic Statistical Tests. R package version 0.7.2. Retrieved from https://rpkgs.datanovia.com/rstatix/
Koornneef A, Pieterse CMJ (2008) Cross talk in defense signaling. Plant Physiol 146:839–844. https://doi.org/10.1104/pp.107.112029
Kroes A, van Loon JJA, Dicke M (2015) Density-dependent interference of aphids with caterpillar-induced defenses in Arabidopsis: Involvement of phytohormones and transcription factors. Plant Cell Physiol 56:98–106. https://doi.org/10.1093/pcp/pcu150
Kroes A, Stam JM, David A, Boland W, van Loon JJA, Dicke M, Poelman EH (2016) Plant-mediated interactions between two herbivores differentially affect a subsequently arriving third herbivore in populations of wild cabbage. Plant Biol 18:981–991. https://doi.org/10.1111/plb.12490
Lenth R (2020) emmeans: Estimated marginal means, aka least-squares means. Package version 1.8.9. Retrieved from https://github.com/rvlenth/emmeans
Li J, Zhu L, Hull JJ, Liang S, Daniell H, Jin S, Zhang X (2016) Transcriptome analysis reveals a comprehensive insect resistance response mechanism in cotton to infestation by the phloem feeding insect Bemisia tabaci (whitefly). Plant Biotechnol 14:1956–1975. https://doi.org/10.1111/pbi.12554
Li B, Förster C, Robert CAM, Züst T, Hu L, Machado RAR, Berset J-D, Handrick V, Knauer T, Hensel G, Chen W, Kumlehn J, Yang P, Keller B, Gershenzon J, Jander G, Kölner TG, Erb M (2018) Convergent evolution of a metabolic switch between aphid and caterpillar resistance in cereals. Sci Adv 4:eaat6797. https://doi.org/10.1126/sciadv.aat6797
Mamin M, Vallat A, Turlings TCJ (2023) Cotton plants as ideal models for teaching and research on inducible direct plant defenses. Front Ecol Evol 11:1119472. https://doi.org/10.3389/fevo.2023.1119472
McAuslane HJ, Alborn HT, Toth JP (1997) Systemic induction of terpenoid aldehydes in cotton pigment glands by feeding of larval Spodoptera exigua. J Chem Ecol 23:2861–2879. https://doi.org/10.1023/A:1022575313325
Mertens D, Fernández de Bobadilla M, Rusman Q, Bloem J, Douma JC, Poelman EH (2021) Plant defence to sequential attack is adapted to prevalent herbivores. Nat Plants 7:1347–1353. https://doi.org/10.1038/s41477-021-00999-7
Moreira X, Abdala-Roberts L, Castagneyrol B (2018) Interactions between plant defence signalling pathways: Evidence from bioassays with insect herbivores and plant pathogens. J Ecol 106:2353–2364. https://doi.org/10.1111/1365-2745.12987
Morkunas I, Mai VC, Gabryś B (2011) Phytohormonal signaling in plant responses to aphid feeding. Acta Physiol Plant 33:2057–2073. https://doi.org/10.1007/s11738-011-0751-7
Mouradov A, Spangenberg G (2014) Flavonoids: A metabolic network mediating plants adaptation to their real estate. Front Plant Sci 5:620. https://doi.org/10.3389/fpls.2014.00620
Nykänen H, Koricheva J (2004) Damage-induced changes in woody plants and their effects on insect herbivore performance: a meta-analysis. Oikos 2:247–268. https://doi.org/10.1111/j.0030-1299.2004.12768.x
Opitz S, Kunert G, Gershenzon J (2008) Increased terpenoid accumulation in cotton (Gossypium hirsutum) foliage is a general wound response. J Chem Ecol 34:508–522. https://doi.org/10.1007/s10886-008-9453-z
Pieterse CMJ, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SCM (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Bi 28:489–521. https://doi.org/10.1146/annurev-cellbio-092910-154055
Poelman EH, Broekgaarden C, van Loon JJA, Dicke M (2008) Early season herbivore differentially affects plant defence responses to subsequently colonizing herbivores and their abundance in the field. Mol Ecol 17:3352–3365. https://doi.org/10.1111/j.1365-294X.2008.03838.x
Qin Q, Shi X, Liang P, Gao X (2005) Induction of phenylalanine ammonia-lyase and lipoxygenase in cotton seedlings by mechanical wounding and aphid infestation. Prog Nat Sci 15:419–423. https://doi.org/10.1080/10020070512331342330
Quijano-Medina T, Turlings TCJ, Sosenski P, Grandi L, Cervera JC, Moreira X, Abdala-Roberts L (2021) Effects of soil salinity on the expression of direct and indirect defences in wild cotton Gossypium hirsutum. J Ecol 109:354–3698. https://doi.org/10.1111/1365-2745.13483
Rodriguez-Saona C, Crafts-Brandner SJ, Canas LA (2003) Volatile emissions triggered by multiple herbivore damage: Beet armyworm and whitefly feeding on cotton plants. J Chem Ecol 29:2539–2550. https://doi.org/10.1023/A:1026314102866
Rodriguez-Saona C, Musser RO, Vogel H, Hum-Musser SM, Thaler JS (2010) Molecular, biochemical, and organismal analyses of tomato plants simultaneously attacked by herbivores from two feeding guilds. J Chem Ecol 36:1043–1057. https://doi.org/10.1007/s10886-010-9854-7
Rosenkranz M, Chen Y, Zhu P, Vlot AC (2021) Volatile terpenes – mediators of plant-to-plant communication. Plant J 108:617–631. https://doi.org/10.1111/tpj.15453
RStudioTeam (2016) RStudio: Integrated Development for R. RStudio, PBC, Boston, MA: RStudio, Inc. Retrieved from http://www.rstudio.com/
Salama HS, Dimetry NZ, Salem SA (1970) On the host preference and biology of the cotton leaf worm Spodoptera littoralis. Z Angew Entomol 67:261–266. https://doi.org/10.1111/j.1439-0418.1971.tb02122.x
Singh B, Sharma RA (2014) Plant terpenes: defence responses, phylogenetic analysis, regulation. 3 Biotech 5:129–151
Soler R, Badenes-Pérez FR, Broekgaarden C, Zheng S, David A, Boland W, Dicke M (2012) Plant-mediated facilitation between a leaf-feeding and a phloem-feeding insect in a brassicaceous plant: from insect performance to gene transcription. Funct Ecol 26:156–166. https://doi.org/10.1111/j.1365-2435.2011.01902.x
Stout MJ, Workman J, Duffey SS (1994) Differential induction of tomato foliar proteins by arthropod herbivores. J Chem Ecol 20:2575–2594. https://doi.org/10.1007/BF02036193
Su Q, Yang F, Yao Q, Peng Z, Tong H, Wang S, Wen X, Wu Q, Zhang Y (2020) A non-vector herbivore indirectly increases the transmission of a vector-borne virus by reducing plant chemical defences. Funct Ecol 34:1091–1101. https://doi.org/10.1111/1365-2435.13535
Tanatsiwa Mbiza NI, Hu Z, Zhang H, Zhang Y, Luo X, Wang Y, Wang Y, Liu T, Li J, Wang X, Zhang J, Yu Y (2022) GhCalS5 is involved in cotton response to aphid attack through mediating callose formation. Front Plant Sci 13:892630. https://doi.org/10.3389/fpls.2022.892630
Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:260–270. https://doi.org/10.1016/j.tplants.2012.02.010
Viswanathan DV, Lifchits OA, Thaler JS (2007) Consequences of sequential attack for resistance to herbivores when plants have specific induced responses. Oikos 116:1389–1399. https://doi.org/10.1111/j.0030-1299.2007.15882.x
Williams L, Rodriguez-Saon C, Castle SC (2017) Methyl jasmonate induction of cotton: a field test of the ‘ attract and reward ’ strategy of conservation biological control. AoB Plants 9:1–15. https://doi.org/10.1093/aobpla/plx032
Yuan D, Grover CE, Hu G, Pan M, Miller ER, Conover JL, Hunt SP, Udall JA, Wendel JF (2021) Parallel and intertwining threads of domestication in allopolyploid cotton. Adv Sci 8:2003634. https://doi.org/10.1002/advs.202003634
Zarate SI, Louisa A, Kempema LA, Walling LL (2007) Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol 143:866–875
Zebelo S, Disi J, Balusu R, Reeves B, Fadamiro H (2017) Spodoptera exigua modulates gossypol biosynthesis in cotton Gossypium hirsutum. J Plant Interact 12:121–127. https://doi.org/10.1080/17429145.2017.1298853
Zhang P, Zhu X, Huang F, Liu Y, Zhang J, Lu Y, Ruan Y (2011) Suppression of jasmonic acid-dependent defense in cotton plant by the mealybug Phenacoccus solenopsis. PLoS One 6:e22378. https://doi.org/10.1371/journal.pone.0022378
Zhang P-J, Xu C-X, Lu Y-B, Zhang J-M, Liu Y-Q, David A, Boland W, Turlings TCJ (2013) Phloem-feeding whiteflies can fool their host plants, but not their parasitoids. Funct Ecol 27:1304–1312. https://doi.org/10.1111/1365-2435.12132
Zhang P-J, Wei J-N, Zhao C, Zhang Y-F, Li C-Y, Liu S-S, Dicke M, Yu X-P, Turlings TCJ (2019) Airborne host-plant manipulation by whiteflies via an inducible blend of plant volatiles. Proc Natl Acad Sci USA 116:7387–7396. https://doi.org/10.1073/pnas.1818599116
Złotek U, Szymanowska U, Jakubczyk A, Sikora M, Świeca M (2019) Effect of arachidonic and jasmonic acid elicitation on the content of phenolic compounds and antioxidant and anti-inflammatory properties of wheatgrass (Triticum aestivum L.). Food Chem 288:256–261. https://doi.org/10.1016/j.foodchem.2019.02.124
Acknowledgements
We thank A. Vallat for help with running samples with the HPLC. In addition, Nicolás Salinas, Emiliano Sosa, Alexander Suárez, Biiniza Pérez, Martha Reyes, and Diego Angulo provided assistance in the field. The authors have no conflicts of interest to declare.
Funding
This study was in part supported by funds from the Swiss Science Foundation awarded to TCJT (315230_185319), two grants from the Spanish National Research Council (COOPA20477 and INCGL20004) to XM and LAR, and a grant from the Regional Government of Galicia (IN607D 2016/001) to XM.
Author information
Authors and Affiliations
Contributions
TQM, LAR, and XM conceived the ideas and designed the methodology; TQM collected the data; TQM and LAR analysed the data; TQM, USR, MM, MC, MF, and CBS performed the chemical analyses; and TQM, LAR, and XM wrote the manuscript. All authors contributed critically to the drafts and gave final approval for publication.
Corresponding author
Ethics declarations
Conflict of interest
The authors report no conflicts of interest in this work and have nothing to disclose.
Additional information
Communicated by Dorothea Bartels.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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
Quijano-Medina, T., Interian-Aguiñaga, J., Solís-Rodríguez, U. et al. Aphid and caterpillar feeding drive similar patterns of induced defences and resistance to subsequent herbivory in wild cotton. Planta 258, 113 (2023). https://doi.org/10.1007/s00425-023-04266-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-023-04266-1