Abstract
Plant defense suppression is an offensive strategy of herbivores, in which they manipulate plant physiological processes to increase their performance. Paradoxically, defense suppression does not always benefit the defense‐suppressing herbivores, because lowered plant defenses can also enhance the performance of competing herbivores and can expose herbivores to increased predation. Suppression of plant defense may therefore entail considerable ecological costs depending on the presence of competitors and natural enemies in a community. Hence, we hypothesize that the optimal magnitude of suppression differs among locations. To investigate this, we studied defense suppression across populations of Tetranychus evansi spider mites, a herbivore from South America that is an invasive pest of solanaceous plants including cultivated tomato, Solanum lycopersicum, in other parts of the world. We measured the level of expression of defense marker genes in tomato plants after infestation with mites from eleven different T. evansi populations. These populations were chosen across a range of native (South American) and non‐native (other continents) environments and from different host plant species. We found significant variation at three out of four defense marker genes, demonstrating that T. evansi populations suppress jasmonic acid‐ and salicylic acid‐dependent plant signaling pathways to varying degrees. While we found no indication that this variation in defense suppression was explained by differences in host plant species, invasive populations tended to suppress plant defense to a smaller extent than native populations. This may reflect either the genetic lineage of T. evansi—as all invasive populations we studied belong to one linage and both native populations to another—or the absence of specialized natural enemies in invasive T. evansi populations.
Highlights
Plants and herbivores share a 420 million year history of antagonistic coevolution (Labandeira, 1998)
T. evansi was previously found to sometimes suppress tomato defense expression significantly below control levels (Godinho et al, 2016; de Oliveira, Pallini, & Janssen, 2016; Sarmento, Lemos, Bleeker, et al, 2011), we found expression levels to be similar to the levels in control plants or to be slightly higher for polyphenol oxidases (PPO)-D, proteinase inhibitors (PIs)-IIc, and protein 1a (PR-1a) and to be significantly higher for leucine aminopeptidase A1 (LAP-A1) (Figure S3)
Multiple arthropod herbivore species suppress the defenses of their host plants to prevent exposure to harmful plant defense and enhance herbivore performance (Kant et al, 2015; Musser et al, 2002)
Summary
Plants and herbivores share a 420 million year history of antagonistic coevolution (Labandeira, 1998). T. evansi suppress tomato defense downstream of plant hormone accumulation, such that the plant's expression of defense-associated genes is downregulated to the benefit of the herbivore (Alba et al, 2015; Ataide et al, 2016; Sarmento, Lemos, Bleeker, et al, 2011). Expression levels of defense-associated plant genes are an adequate measure of defense suppression by T. evansi, as long as timing is standardized and a benchmark treatment for defense induction is included (Alba et al, 2015; Sarmento, Lemos, Bleeker, et al, 2011; Schimmel, Ataide, Chafi, et al, 2017). We included a treatment where tomato plants were infested with a defense-inducing T. urticae genotype as a benchmark for defense induction For those genes where we observed different levels of expression among populations, we investigated if this variation was affected by host plant species or geographical range (invasive or native). To investigate the possibility that differences in suppression could be explained by differences in genetic lineage (Boubou et al, 2012; Gotoh et al, 2009), we sequenced a part of the mitochondrial cytochrome oxidase subunit 1 gene (CO1)
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