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Characterization of Arabidopsis thaliana regrowth patterns suggests a trade-off between undamaged fitness and damage tolerance

  • Plant-microbe-animal interactions - original research
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Abstract

Herbivory is a fundamental type of plant–animal interaction that presents substantial selection pressure on plants to replace lost tissues and to prevent subsequent losses in fitness. Apical herbivory, which entails removal or damage to the apical meristem, causes a change in plant architecture by disrupting the balance of hormones produced in part by the apical meristem. Therefore, for an annual semelparous plant, the ability to preserve reproductive success following damage (i.e., to tolerate damage) is largely dependent on the plant’s pre-damage investment into fitness and its regrowth pattern following damage. Using multiple regression analyses, we assessed the relationship of developmental and architectural traits of experimentally damaged plants relative to undamaged plants of 33 Arabidopsis thaliana genotypes that display a wide range of undamaged fitness and damage tolerance. Our analyses revealed evidence for an evolutionary bet-hedging strategy within a subset of genotypes to presumably maximize fitness under natural herbivory—genotypes with the greatest seed production when undamaged exhibited a significant reduction in seed yield when damaged, while genotypes with low undamaged seed production were the only genotypes whose seed yield increased when damaged. Patterns of endopolyploidy paralleled those of seed production, such that the increase in whole-plant ploidy by genome re-replication during growth/regrowth contributes to undamaged fitness, damage tolerance, and their trade-off. Overall, this study provides the first large-scale characterization of A. thaliana regrowth patterns and suggests that investment into fitness and endopolyploidy when undamaged may come at a cost to tolerance ability once damaged.

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Acknowledgements

Flow cytometry was performed by the Iowa State University Flow Cytometry Facility. Seeds were obtained from the Arabidopsis Biological Resource Center at The Ohio State University.

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Authors and Affiliations

Authors

Contributions

DRS conducted plant growth, maintenance, and measurement. DRS, ENR, and KNP conducted study design, data analysis, and writing.

Corresponding author

Correspondence to Daniel R. Scholes.

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Funding

This research was supported by awards from the National Science Foundation (DEB1146085 and associated REU) and the University of Illinois Campus Research Board to KNP.

Conflict of interest

The authors declare that they have no conflict of interest.

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This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Communicated by Merijn Kant.

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442_2017_3897_MOESM1_ESM.pdf

Online Resource 1 (ESM1.pdf): Model iterations of LASSO regression of all traits and only architectural and developmental traits regressed against tolerance (Table 1), and regression of undamaged seed production vs. percent change in seed production for all genotypes combined and global ecotypes alone (Fig. 1)

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Scholes, D.R., Rasnick, E.N. & Paige, K.N. Characterization of Arabidopsis thaliana regrowth patterns suggests a trade-off between undamaged fitness and damage tolerance. Oecologia 184, 643–652 (2017). https://doi.org/10.1007/s00442-017-3897-1

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  • DOI: https://doi.org/10.1007/s00442-017-3897-1

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