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Plant defence to sequential attack is adapted to prevalent herbivores

Abstract

Plants have evolved plastic defence strategies to deal with the uncertainty of when, by which species and in which order attack by herbivores will take place1,2,3. However, the responses to current herbivore attack may come with a cost of compromising resistance to other, later arriving herbivores. Due to antagonistic cross-talk between physiological regulation of plant resistance to phloem-feeding and leaf-chewing herbivores4,5,6,7,8, the feeding guild of the initial herbivore is considered to be the primary factor determining whether resistance to subsequent attack is compromised. We show that, by investigating 90 pairwise insect–herbivore interactions among ten different herbivore species, resistance of the annual plant Brassica nigra to a later arriving herbivore species is not explained by feeding guild of the initial attacker. Instead, the prevalence of herbivore species that arrive on induced plants as approximated by three years of season-long insect community assessments in the field explained cross-resistance. Plants maintained resistance to prevalent herbivores in common patterns of herbivore arrival and compromises in resistance especially occurred for rare patterns of herbivore attack. We conclude that plants tailor induced defence strategies to deal with common patterns of sequential herbivore attack and anticipate arrival of the most prevalent herbivores.

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Fig. 1: Effect of herbivory by ten primary herbivores (inducers) on the performance of the same ten species as receiving herbivores relative to performance on an undamaged control plant.
Fig. 2: Optimal resistance strategies incorporate likelihood of subsequent attack.

Data availability

All data are available in the main text, the Supplementary Information and on the DRYAD public repository (https://doi.org/10.5061/dryad.pnvx0k6n3).

Code availability

All R code used in our analysis is made available on the DRYAD public repository (https://doi.org/10.5061/dryad.pnvx0k6n3).

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Acknowledgements

We thank A. Agrawal and M. Dicke for discussion of our results. We acknowledge funding by the European Research Council under the European Union’s Horizon 2020 research and innovation programme (grant no. 677139 to E.H.P.). J.C.D. was supported by NWO Earth and Life Sciences (NWO-ALW) through a VENI grant, project no. 863.14.018.

Author information

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Contributions

E.H.P., D.M. and M.F.B. planned and designed the study and developed the methodology. E.H.P., D.M., M.F.B., Q.R. and J.B. performed the experiments. M.F.B. and J.B. analysed gene expression. D.M. and B.D. analysed performance and field data. All authors contributed to writing of the manuscript.

Corresponding author

Correspondence to Erik H. Poelman.

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The authors declare no competing interests.

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Peer review information Nature Plants thanks Carolina Quintero and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Experimental setup for the performance experiment.

A, Brassica nigra plants were infested with one of ten insect species as primary herbivores (inducers). Five leaf chewers or ten phloem feeders were used as inducers. B, One and four days after plant infestation with herbivores, leaf samples for gene-expression analyses were taken (each plant was sampled only once). C, Seven days after plant infestation with herbivores, all remaining inducers were removed and plants were infested with receiving herbivores. Ten leaf chewers or 20 phloem feeders were used as receivers. D, Seven days after plant infestation with receivers, their performance was measured (leaf chewer weight or number of phloem feeders). We repeated this setup ten times, each time using a different insect as receiver, and preparing ten plant replicates per treatment (Supplementary Table S1).

Extended Data Fig. 2 Expression levels of the JA biosynthesis gene LOX2 and the SA responsive gene PR1 on Brassica nigra leaves after 96 h of herbivory.

Herbivores used were the leaf chewers Autographa gamma (Ag), Mamestra brassicae (Mb), Athalia rosae (Ar), Pieris brassicae (Pb), P. rapae (Pr) and Plutella xylostella (Px), and the phloem feeders Myzus persicae (Mp), M. persicae ssp. nicotianae (Mpn) Brevicoryne brassicae (Bb) and Lipaphis erysimi (Le). A, Effects of herbivory on the relative expression of LOX2 for each herbivore species. B, Effects of herbivory on the relative expression of LOX2 for herbivores grouped by feeding guild and diet breadth. C, Effects of herbivory on the relative expression of PR1 for each herbivore species. D, Effects of herbivory on the relative expression of PR1 for each herbivore species grouped by feeding guild and diet breadth. The boxes span from the first to the third quartiles, the centre lines represent the median values, and the whiskers show the data that lie within the 1.5 interquartile range of the lower and upper quartiles. The datapoints at the ends of the whiskers represent the outliers. Different letters refer to significant differences at P < 0.05 based on GLM and Tukey HSD tests adjusting for multiple comparisons (Supplementary Table 3–6), whereas n.s. indicates no significant difference in post-hoc comparisons was found. Each treatment in panels A and C is supported by n = 10 each, while bars in panels B and D are based on n = 40 for specialist chewing herbivores, or n = 20 for the other feeding guild by host specialization combinations.

Extended Data Fig. 3 Performance of secondary receiving herbivores on Brassica nigra plants induced by one of ten different herbivore species.

Larval mass or number of individuals on plants induced by herbivory from the leaf chewers Autographa gamma (Ag), Mamestra brassicae (Mb), Athalia rosae (Ar), Pieris brassicae (Pb), P. rapae (Pr) and Plutella xylostella (Px), and from the phloem feeders Myzus persicae (Mp), M. persicae ssp. nicotianae (Mpn) Brevicoryne brassicae (Bb) and Lipaphis erysimi (Le), and on non-treated plants (Ctrl). n = 4053. Panels correspond to the different receiving herbivores and the numbers below indicate the recapture rate for chewing herbivores, or the number of plants on which phloem feeder populations were assessed. The boxes span from the first to the third quartiles, the centre lines represent the median values, and the whiskers show the data that lie within the 1.5 interquartile range of the lower and upper quartiles. The datapoints at the ends of the whiskers identify the outliers.

Extended Data Fig. 4 Performance of herbivores is not explained by marker gene expression.

Performance of receiving herbivores (effect size; the natural logarithm of the ratio between individual performance on induced plant / average species performance on control plants) related to the relative expression of the JA-marker gene LOX2 (left panel) or the SA-marker gene PR1 (right panel). Colours and shapes correspond to the feeding guild of the receiving herbivore.

Extended Data Fig. 5 Resistance strategies are predicted by prevalence of the receiving herbivore.

Model predictions of performance of receiving herbivores (effect size; the natural logarithm of the ratio between individual performance on induced plant / average species performance on control plants) related to the prevalence of the receiving herbivore, separated for phloem-feeding herbivores (left panels) and leaf-chewing herbivores (right panels). Colours and shapes correspond to combinations of diet breadth of the inducing and receiving herbivores. A, Model predictions did not constrain the prevalence of the inducing herbivore. B) predictions were constrained in prevalence of the inducing herbivore at 2.5% of plants. C) predictions were constrained in prevalence of the inducing herbivore at 50% of plants.

Supplementary information

Supplementary information

Supplementary Tables 1–11, Results and Discussion.

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Mertens, D., Fernández de Bobadilla, M., Rusman, Q. et al. Plant defence to sequential attack is adapted to prevalent herbivores. Nat. Plants 7, 1347–1353 (2021). https://doi.org/10.1038/s41477-021-00999-7

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