Effects of soil organisms on aboveground multitrophic interactions are consistent between plant genotypes mediating the interaction

Kabouw, Patrick; Kos, Martine; Kleine, Sandra; Vockenhuber, Elke A.; Loon, Joop J. A. van; Putten, Wim H. van der; Dam, Nicole M. van; Biere, Arjen

doi:10.1111/j.1570-7458.2011.01123.x

Cited by 24 publications

(18 citation statements)

References 38 publications

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“…Similarly, it is unclear how the glucosinolate gluconapin, which was decreased by nematodes, affects aphid populations. Other studies that addressed effects of nematodes on leaf glucosinolates (Kabouw et al 2011; Kutyniok and Müller 2012; Lohmann et al 2009; Van Dam et al 2005; Wurst et al 2006) showed no clear pattern, but we can conclude that there was no increase in total glucosinolates after nematode infestation. In terms of specific glucosinolate classes, increases (Lohmann et al 2009), decreases (van Dam et al 2005; Wurst et al 2006), or no effects (Kutyniok and Müller 2012) have been found in aliphatic compounds.…”

Section: Discussioncontrasting

confidence: 54%

Heterodera schachtii Nematodes Interfere with Aphid-Plant Relations on Brassica oleracea

et al. 2013

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Aboveground and belowground herbivore species modify plant defense responses differently. Simultaneous attack can lead to non-additive effects on primary and secondary metabolite composition in roots and shoots. We previously found that aphid (Brevicoryne brassicae) population growth on Brassica oleracea was reduced on plants that were infested with nematodes (Heterodera schachtii) prior (4 weeks) to aphid infestation. Here, we examined how infection with root-feeding nematodes affected primary and secondary metabolites in the host plant and whether this could explain the increase in aphid doubling time from 3.8 to 6.7 days. We hypothesized that the effects of herbivores on plant metabolites would depend on the presence of the other herbivore and that nematode-induced changes in primary metabolites would correlate with reduced aphid performance. Total glucosinolate concentration in the leaves was not affected by nematode presence, but the composition of glucosinolates shifted, as gluconapin concentrations were reduced, while gluconapoleiferin concentrations increased in plants exposed to nematodes. Aphid presence increased 4-methoxyglucobrassicin concentrations in leaves, which correlated positively with the number of aphids per plant. Nematodes decreased amino acid and sugar concentrations in the phloem. Aphid population doubling time correlated negatively with amino acids and glucosinolate levels in leaves, whereas these correlations were non-significant when nematodes were present. In conclusion, the effects of an herbivore on plant metabolites were independent of the presence of another herbivore. Nematode presence reduced aphid population growth and disturbed feeding relations between plants and aphids.Electronic supplementary materialThe online version of this article (doi:10.1007/s10886-013-0338-4) contains supplementary material, which is available to authorized users.

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Section: Discussioncontrasting

confidence: 54%

Heterodera schachtii Nematodes Interfere with Aphid-Plant Relations on Brassica oleracea

et al. 2013

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“…M. persicae also showed a reduced growth rate and fecundity when feeding on M. incognita -infected Nicotiana tabacum (Kaplan et al, 2011). In contrast, no effect on the performance of B. brassicae was found by an infection of B. oleracea with a mix of different root parasitic nematode species (Kabouw et al, 2011). In A. thaliana , a simultaneous inoculation with the sedentary endoparasitic nematode H. schachtii and the aphid B. brassicae was performed (Kutyniok and Muller, 2012).…”

Section: Aboveground–belowground Interactions Between Nematodes and Imentioning

confidence: 94%

Plant systemic induced responses mediate interactions between root parasitic nematodes and aboveground herbivorous insects

Wondafrash¹,

Dam²,

Tytgat³

2013

Front. Plant Sci.

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Insects and nematodes are the most diverse and abundant groups of multicellular animals feeding on plants on either side of the soil–air interface. Several herbivore-induced responses are systemic, and hence can influence the preference and performance of organisms in other plant organs. Recent studies show that plants mediate interactions between belowground plant parasitic nematodes (PPNs) and aboveground herbivorous insects. Based on the knowledge of plant responses to pathogens, we review the emerging insights on plant systemic responses against root-feeding nematodes and shoot-feeding insects. We discuss the potential mechanisms of plant-mediated indirect interactions between both groups of organisms and point to gaps in our knowledge. Root-feeding nematodes can positively or negatively affect shoot herbivorous insects, and vice versa. The outcomes of the interactions between these spatially separated herbivore communities appear to be influenced by the feeding strategy of the nematodes and the insects, as well as by host plant susceptibility to both herbivores. The potential mechanisms for these interactions include systemic induced plant defense, interference with the translocation and dynamics of locally induced secondary metabolites, and reallocation of plant nutritional reserves. During evolution, PPNs as well as herbivorous insects have acquired effectors that modify plant defense responses and resource allocation patterns to their advantage. However, it is also known that plants under herbivore attack change the allocation of their resources, e.g., for compensatory growth responses, which may affect the performance of other organisms feeding on the plant. Studying the chemical and molecular basis of these interactions will reveal the molecular mechanisms that are involved. Moreover, it will lead to a better understanding of the ecological relevance of aboveground–belowground interactions, as well as support the development of sustainable pest management technologies.

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“…A number of studies have shown that soil organisms such as root herbivorous insects, nematodes, and bacteria and fungi can affect the concentrations of primary and secondary compounds in aboveground plant tissues and subsequently the performance of aboveground herbivores (Bezemer et al 2005, Erb et al 2009, Eisenhauer et al 2010, Kabouw et al 2011, Johnson et al 2012, Soler et al 2012. Changes in soil nutrient availability can also influence plant nutritional quality (Koricheva et al 1998, Hol 2011.…”

mentioning

confidence: 99%

Plant–soil feedback effects on plant quality and performance of an aboveground herbivore interact with fertilisation

Kos

Tuijl

Roo

et al. 2014

Oikos

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Plant–soil feedback (PSF) effects on plant performance can be influenced by the availability of nutrients in the soil. Recent studies have shown that PSF effects can also change aboveground plant–insect interactions via soil‐mediated changes in plant quality, but whether this is influenced by soil nutrient availability is unknown. We examined how fertilisation influences PSF effects on aboveground plant‐aphid interactions in ragwort Jacobaea vulgaris. We grew J. vulgaris in soil conditioned by conspecific plants and in unconditioned soil at two levels of fertilisation and measured soil fungal communities, plant biomass, concentrations of primary (amino acids) and secondary (pyrrolizidine alkaloids; PAs) metabolites in phloem exudates, performance of the specialist aphid Aphis jacobaeae and sequestration of PAs by the aphid. We observed a strong interaction between soil conditioning and fertilisation on amino acid and PA concentrations in phloem exudates of J. vulgaris and on aphid performance, with opposite effects of soil conditioning at the two fertilisation levels. Plant biomass was reduced by soil conditioning and increased by fertilisation. Aphids contained high PA concentrations, converted N‐oxides into tertiary amines and preferentially sequestered certain PA compounds, but PA sequestration was not affected by any of the treatments. We conclude that effects of PSF and fertilisation on plant chemistry and aphid performance are interdependent. Our study highlights the need to consider the importance of abiotic soil conditions on the outcome of PSF effects on aboveground plant–insect interactions.

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Effects of soil organisms on aboveground multitrophic interactions are consistent between plant genotypes mediating the interaction

Cited by 24 publications

References 38 publications

Heterodera schachtii Nematodes Interfere with Aphid-Plant Relations on Brassica oleracea

Heterodera schachtii Nematodes Interfere with Aphid-Plant Relations on Brassica oleracea

Plant systemic induced responses mediate interactions between root parasitic nematodes and aboveground herbivorous insects

Plant–soil feedback effects on plant quality and performance of an aboveground herbivore interact with fertilisation

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