Abstract
Main conclusion
VOC emissions increased with herbivore load, but this did not result in concomitant increases in resistance in neighbouring plants, suggesting that communication occurred independently of herbivore load in emitter plants.
Abstract
Herbivore-damaged plants emit volatile organic compounds (VOCs) that can alert neighbours and boost their resistance. While VOC-mediated plant communication has been shown to be herbivore-specific, we know little about its contingency on variation in herbivore load. To address this knowledge gap, we tested herbivore load effects on VOC-mediated communication between potato plants (Solanum tuberosum) using the generalist herbivore Spodoptera exigua. First, we tested whether herbivore load (three levels: undamaged control, low, and high load) affected total VOC emissions and composition. Second, we matched emitter and receiver plants and subjected emitters to the same herbivore load treatments. Finally, we performed a bioassay with S. exigua on receivers to test for induced resistance due to VOC-mediated communication. We found that herbivory significantly increased total VOC emissions relative to control plants, and that such increase was greater under high herbivore load. In contrast, we found no detectable effect of herbivory, regardless of the load, on VOC composition. The communication experiment showed that VOCs released by herbivore-induced emitters boosted resistance in receivers (i.e., lower leaf damage than receivers exposed to VOCs released by control emitters), but the magnitude of such effect was similar for both levels of emitter herbivore load. These findings suggest that changes in VOCs due to variation in herbivore load do not modify the outcomes of plant communication.
This is a preview of subscription content, log in via an institution to check access.
Data availability
All data generated or analysed during this study are included in this article [and its supplementary information files].
Abbreviations
- VOC:
-
Volatile organic compound
References
Abdala-Roberts L, Vázquez-González C, Rasmann S, Moreira X (2022) Test of communication between potato plants in response to herbivory by the Colorado potato beetle. Agric for Entomol 24:212–218
Brandoli Machado B, Orue JP, Arruda MS, Santos CV, Sarath DS, Goncalves WN, Silva GG, Pistori H, Roel AR, Rodrigues JF Jr (2016) BioLeaf: a professional mobile application to measure foliar damage caused by insect herbivory. Comput Electron Agric 129:44–55
Girling RD, Stewart-Jones A, Dherbecourt J, Staley JT, Wright DJ, Poppy GM (2011) Parasitoids select plants more heavily infested with their caterpillar hosts: a new approach to aid interpretation of plant headspace volatiles. Proc R Soc B 278(1718):2646–2653
Girón-Calva PS, Molina-Torres J, Heil M (2012) Volatile dose and exposure time impact perception in neighboring plants. J Chem Ecol 38(2):226–228
Heil M, Adame-Álvarez RM (2010) Short signalling distances make plant communication a soliloquy. Biol Lett 23:843–845
Heil M, Karban R (2010) Explaining evolution of plant communication by airborne signals. Trends Ecol Evol 25(3):137–144
Karban R (2011) The ecology and evolution of induced resistance against herbivores. Funct Ecol 25(2):339–347
Karban R (2015) Plant sensing and communication. University of Chicago Press
Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press
Karban R, Shiojiri K, Huntzinger M, McCall AC (2006) Damage-induced resistance in sagebrush: volatiles are key to intra- and interplant communication. Ecology 87:922–930
Karban R, Shiojiri K, Ishizaki S, Wetzel WC, Evans RY (2013) Kin recognition affects plant communication and defence. Proc R Soc B 280(1756):20123062
Karban R, Yang LH, Edwards KF (2014a) Volatile communication between plants that affects herbivory: a meta-analysis. Ecol Lett 17(1):44–52
Karban R, Wetzel WC, Shiojiri K, Ishizaki S, Ramirez SR, Blande JD (2014b) Deciphering the language of plant communication: volatile chemotypes of sagebrush. New Phytol 204(2):380–385
Karban R, Wetzel WC, Shiojiri K, Pezzola E, Blande JD (2016) Geographic dialects in volatile communication between sagebrush individuals. Ecology 97(11):2917–2924
Kariyat RR, Mauck KE, De Moraes CM, Stephenson AG, Mescher MC (2012) Inbreeding alters volatile signalling phenotypes and influences tri-trophic interactions in horsenettle (Solanum carolinense L.). Ecol Lett 15(4):301–309
Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82:1–16
Lenth RV (2016) Least-squares means: the R package lsmeans. J Stat Softw 69(1):1–33
Moreira X, Abdala-Roberts L (2019) Specificity and context-dependency of plant–plant communication in response to insect herbivory. Curr Opin Insect Sci 32:15–21
Moreira X, Nell CS, Katsanis A, Rasmann S, Mooney KA (2018) Herbivore specificity and the chemical basis of plant–plant communication in Baccharis salicifolia (Asteraceae). New Phytol 220(3):703–713
Moreira X, Granjel RR, de la Fuente M, Fernández-Conradi P, Pasch V, Soengas P, Turlings TC, Vázquez-González C, Abdala-Roberts L, Rasmann S (2021) Apparent inhibition of induced plant volatiles by a fungal pathogen prevents airborne communication between potato plants. Plant Cell Environ 44(4):1192–1201
Oksanen J, Blanchet FG, Kindt R, Legendre P, O’hara R, Simpson GL, Solymos P, Stevens MHH, Wagner H (2010) Vegan: community ecology package. R package version 1.17–4. URL http://CRAN.Rproject.org/package=vegan
Pinto-Zevallos DM, Bezerra RH, Souza SR, Ambrogi BG (2018) Species-and density-dependent induction of volatile organic compounds by three mite species in cassava and their role in the attraction of a natural enemy. Exp Appl Acarol 74(3):261–274
Rasmann S, Erwin AC, Halitschke R, Agrawal AA (2011) Direct and indirect root defences of milkweed (Asclepias syriaca): trophic cascades, trade-offs and novel methods for studying subterranean herbivory. J Ecol 99(1):16–25
Shiojiri K, Ozawa R, Kugimiya S, Uefune M, van Wijk M, Sabelis MW, Takabayashi J (2010) Herbivore-specific, density-dependent induction of plant volatiles: honest or “cry wolf” signals? PLoS ONE 5(8):e12161
Team RC (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org
Acknowledgements
We are grateful to Salvador Herrero for providing Spodoptera exigua eggs.
Funding
This research was supported by a grant from the Spanish Ministry of Science, Innovation and Universities (RTI2018-099322-B-I00) to XM, a grant from the Spanish National Research Council (2021AEP082) to XM, and a grant from the Regional Government of Galicia (IN607A 2021/03) to XM and CVG. CVG was supported by a postdoctoral fellowship from the Xunta de Galicia-GAIN/Fulbright (IN606B 2021/004). LMC was supported by a predoctoral fellowship from the Spanish Ministry of Science, Innovation and Universities (PRE2019-091096).
Author information
Authors and Affiliations
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.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Vázquez-González, C., Quiroga, V., Martín-Cacheda, L. et al. Effect of herbivore load on VOC-mediated plant communication in potato. Planta 257, 42 (2023). https://doi.org/10.1007/s00425-023-04075-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-023-04075-6