Down-regulation of plant defence in a resident spider mite species and its effect upon con- and heterospecifics

Godinho, Diogo Prino; Janssen, Arne; Dias, Teresa; Cruz, Cristina; Magalhães, Sara

doi:10.1007/s00442-015-3434-z

Cited by 67 publications

(77 citation statements)

References 67 publications

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“…Because all closely related competitors can exert indirect plant‐mediated effects on T. urticae (Kant et al ., , ; Sarmento et al ., ; Godinho et al ., ), we chose one that is known for a strong net negative effect (Sarmento et al ., ); the red spider mite T. evansi Baker and Pritchard, 1960. This species is mainly a specialist herbivore of Solanaceae and is considered an important agricultural pest.…”

Section: Methodsmentioning

confidence: 99%

Interspecific competition counteracts negative effects of dispersal on adaptation of an arthropod herbivore to a new host

Alzate

Bisschop

Etienne

et al. 2017

J of Evolutionary Biology

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Dispersal and competition have both been suggested to drive variation in adaptability to a new environment, either positively or negatively. A simultaneous experimental test of both mechanisms is however lacking. Here, we experimentally investigate how population dynamics and local adaptation to a new host plant in a model species, the two-spotted spider mite (Tetranychus urticae), are affected by dispersal from a stock population (no-adapted) and competition with an already adapted spider mite species (Tetranychus evansi). For the population dynamics, we find that competition generally reduces population size and increases the risk of population extinction. However, these negative effects are counteracted by dispersal. For local adaptation, the roles of competition and dispersal are reversed. Without competition, dispersal exerts a negative effect on adaptation (measured as fecundity) to a novel host and females receiving the highest number of immigrants performed similarly to the stock population females. By contrast, with competition, adding more immigrants did not result in a lower fecundity. Females from populations with competition receiving the highest number of immigrants had a significantly higher fecundity than females from populations without competition (same dispersal treatment) and than the stock population females. We suggest that by exerting a stronger selection on the adapting populations, competition can counteract the migration load effect of dispersal. Interestingly, adaptation to the new host does not significantly reduce performance on the ancestral host, regardless of dispersal rate or competition. Our results highlight that assessments of how species can adapt to changing conditions need to jointly consider connectivity and the community context.

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Section: Methodsmentioning

confidence: 99%

Interspecific competition counteracts negative effects of dispersal on adaptation of an arthropod herbivore to a new host

Alzate

Bisschop

Etienne

et al. 2017

J of Evolutionary Biology

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“…However, arthropod populations have adapted to suppress these defenses, including T. urticae populations (19,23,24,94), suggesting that effectors in their saliva are crucial determinants for success in colonizing host plants. To gain insight into the salivary proteome of T. urticae, spider mites were allowed to feed on small hemispheres filled with artificial diet.…”

Section: Identification Of Salivary Gland Proteinsmentioning

confidence: 99%

The Salivary Protein Repertoire of the Polyphagous Spider Mite Tetranychus urticae: A Quest for Effectors

Jonckheere

Dermauw

Zhurov

et al. 2016

Molecular & Cellular Proteomics

102

127

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The two-spotted spider mite Tetranychus urticae is an extremely polyphagous crop pest. Alongside an unparalleled detoxification potential for plant secondary metabolites, it has recently been shown that spider mites can attenuate or even suppress plant defenses. Salivary constituents, notably effectors, have been proposed to play an important role in manipulating plant defenses and might determine the outcome of plant-mite interactions.Here, the proteomic composition of saliva from T. urticae lines adapted to various host plants-bean, maize, soy, and tomato-was analyzed using a custom-developed feeding assay coupled with nano-LC tandem mass spectrometry. About 90 putative T. urticae salivary proteins were identified. Many are of unknown function, and in numerous cases belonging to multimembered gene families. RNAseq expression analysis revealed that many genes coding for these salivary proteins were highly expressed in the proterosoma, the mite body region that includes the salivary glands. A subset of genes encoding putative salivary proteins was selected for whole-mount in situ hybridization, and were found to be expressed in the anterior and dorsal podocephalic glands. Strikingly, host plant dependent expression was evident for putative salivary proteins, and was further studied in detail by micro-array based genome-wide expression profiling. This meta-analysis revealed for the first time the salivary protein repertoire of a phytophagous chelicerate. The availability of this salivary proteome will assist in unraveling the molecular interface between phytophagous mites and their host plants, and may ultimately facilitate the development of mite-resistant crops. Furthermore, the technique used in this study is a time-and resourceefficient method to examine the salivary protein composition of other small arthropods for which saliva or salivary glands cannot be isolated easily. The family of spider mites (Chelicerata: Acari: Tetranychidae) comprises well over 1000 species, including several that are important pests on crops, and about 0.9 billion euro is being spent annually for their control worldwide (1, 2). These minute herbivores-about 0.5 mm in size-use their stylets to pierce leaf mesophyll cells and to inject saliva, after which they suck out the cytoplasm. This results in cell death visible as chlorotic spots sometimes accompanied by necrosis, and ultimately in leaf abscission (3,4). Among the spider mites, the From the ‡Laboratory

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“…Several of the examples of suppression of plant defenses concern mites, which feed on host plants by piercing parenchyma cells and sucking out the contents. The feeding of some species or strains of species induces direct plant defenses of both the jasmonic acid and salicylic acid pathway, whereas other strains or species do not induce these defenses or even suppress them below constitutive levels (Kant et al ., , ; Alba et al ., ; Godinho et al ., ; Schimmel et al ., ). Unlike many other cases, T. evansi suppresses plant defenses of both the jasmonic acid and salicylic acid pathway, thus this suppression is independent of the antagonism between these two pathways (Sarmento et al ., ; Glas et al ., ; Alba et al ., ).…”

Section: Introductionmentioning

confidence: 99%

“…Plants are commonly attacked by different species of herbivores (Futuyma & Gould, 1979;Strauss, 1991;Rodriguez-Saona et al, 2010), and defenses induced by multiple species may differ from those induced by each species separately (Voelckel & Baldwin, 2004;Viswanathan et al, 2007;Poelman et al, 2008;Rodriguez-Saona et al, 2010). The defenses induced by an early-arriving herbivore affect the performance and colonization of other herbivores on the same plant (Karban & Carey, 1984;Karban & Baldwin, 1997;Stout et al, 1998;Viswanathan et al, 2005;Erb et al, 2011;Johnson et al, 2012;Soler et al, 2012;Erwin et al, 2014;Glas et al, 2014;Wang et al, 2014;Godinho et al, 2016). Hence, the order of arrival of different species on the same plant may determine the defense that is induced, and affect the outcome of interactions among herbivore species (Kessler & Baldwin, 2004;Voelckel & Baldwin, 2004;Viswanathan et al, 2007;Poelman et al, 2008;Erb et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Herbivore performance and plant defense after sequential attacks by inducing and suppressing herbivores

2017

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It is well known that herbivore-induced plant defenses alter host plant quality and can affect the behavior and performance of later arriving herbivores. Effects of sequential attacks by herbivores that either suppress or induce plant defenses are less well studied. We sequentially infested leaves of tomato plants with a strain of the phytophagous spider mite Tetranychus urticae that induces plant defenses and the closely related Tetranychus evansi, which suppresses plant defenses. Plant quality was quantified through oviposition of both spider mite species and by measuring proteinase inhibitor activity using plant material that had been sequentially attacked by both herbivore species. Spider-mite oviposition data show that T. evansi could suppress an earlier induction of plant defenses by T. urticae, and T. urticae could induce defenses in plants previously attacked by T. evansi in 1 day. Longer attacks by the second species did not result in further changes in oviposition. Proteinase inhibitor activity levels showed that T. evansi suppressed the high activity levels induced by T. urticae to constitutive levels in 1 day, and further suppressed activity to levels similar to those in plants attacked by T. evansi alone. Attacks by T. urticae induced proteinase inhibitor activity in plants previously attacked by T. evansi, eventually to similar levels as induced by T. urticae alone. Hence, plant quality and plant defenses were significantly affected by sequential attacks and the order of attack does not affect subsequent performance, but does affect proteinase inhibitor activity levels. Based on our results, we discuss the evolution of suppression of plant defenses.

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Down-regulation of plant defence in a resident spider mite species and its effect upon con- and heterospecifics

Cited by 67 publications

References 67 publications

Interspecific competition counteracts negative effects of dispersal on adaptation of an arthropod herbivore to a new host

Interspecific competition counteracts negative effects of dispersal on adaptation of an arthropod herbivore to a new host

The Salivary Protein Repertoire of the Polyphagous Spider Mite Tetranychus urticae: A Quest for Effectors

Herbivore performance and plant defense after sequential attacks by inducing and suppressing herbivores

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