Differences in hormonal signaling triggered by two root-feeding nematode species result in contrasting effects on aphid population growth

Belowground feeding herbivores can affect their aboveground counterparts via systemic induced responses. Hormonal signaling pathways, such as the jasmonic acid (JA) and salicylic acid (SA) pathways, play a pivotal role in shaping such aboveground-belowground herbivore interactions. In this study, we analyzed the effects of two root-feeding nematode species, the cyst nematode Heterodera schachtii, and the root-knot nematode Meloidogyne hapla, on the preference and performance of cabbage aphid, Brevicoryne brassicae. The two sedentary nematodes differ in their feeding strategies and in which plant responses they trigger. We tested the hypothesis that differences in aphid preference and performance are governed by differences in systemic defense signaling triggered by the nematodes. When allowed to choose, aphids showed a lower preference for black mustard (Brassica nigra) plants infested with H. schachtii compared to uninfested plants. On these plants their population increase was reduced as well. Gene expression analyses revealed that aphid infestation on H. schachtii-infested plants strongly induced PR1, a marker gene for the SA-pathway. The expression of the JA marker genes VSP2 and MYC2 was repressed. On the other hand, M. hapla infestation increased aphid preference and population growth compared to those on control plants. Aphid feeding upregulated the expression of VSP2 and MYC2, whereas PR1 expression was not induced. Interestingly, aphid infestation on plants without nematodes did not activate any of the signaling pathways. This suggests that H. schachtii infestation systemically enhanced aphid induced-resistance via the SA pathway. In contrast, M. hapla infestation enhanced JA-pathway regulated responses. This may reduce SA-induced resistance to aphid infestation via negative JA-SA cross-talk. Based on our results, we conclude that the differences in the interactions of aphids with cyst and root-knot nematodes emerge from differences in the plant responses triggered by both nematodes. Our results show that aboveground herbivore performance on plants infested with different nematode species may be strongly associated with nematode feeding strategies.NvD gratefully acknowledges the support of the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig funded by the German Research Foundation (FZT 118). MW was supported by an Erasmus Mundus fellowship for the European Master of Science in Nematology (EUMAINE).http://www.frontiersin.org/Ecology_and_Evolutionam2018Forestry and Agricultural Biotechnology Institute (FABI)Zoology and Entomolog

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

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 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 defence, interference with the translocation and dynamics of locally induced secondary metabolites, and reallocation of plant nutritional reserves. During evolution, plant parasitic nematodes as well as herbivorous insects have acquired effectors that modify plant defence 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 pe

Amino acid concentrations in the shoots.

<p>Amino acid concentrations were measured by HPLC in the shoots after RJA, SJA and CON at day 1, 3, 7 and 14. The concentration of almost all amino acids was affected by JA treatment, whereby some (Arg, Asp, Gln, His, Phe) responded differently to RJA than SJA. Concentrations are expressed in nmol/mg dry plant material after RJA (dotted line, open circles), SJA (dashed line, squares) or control treatment (solid line, triangles). Error bars represent standard errors. Samples with a significantly different concentration compared to control are marked with an asterisk (p-value <0.05, t-test independent samples assuming unequal variances).</p

Gene expression in the glucosinolate synthesis pathway.

<p>The JA response of the genes involved in glucosinolate synthesis was weaker in the roots than in the shoots. In the shoots, RJA resulted in a stronger induction of several transcription factors and enzymes involved in the biosynthesis of aliphatic glucosinolates than SJA. In contrast, for the indole glucosinolate pathway, SJA lead to a stronger induction of the involved genes than RJA. Histograms represent the log₂ of the fold changes in expression after RJA or SJA compared CON for all genes that were significantly affected in at least one of the treatment groups (ANOVA, FDR corrected <i>P</i>-value <0.1). Samples showing a significantly different expression compared to CON are marked with an asterisk. RRJA, Root tissue RJA treatment; RSJA Root tissue SJA treatment, SRJA, Shoot tissue RJA treatment, SSJA, Shoot tissue SJA treatment.</p

Differential expression of JAZ genes depending on tissue as well as site of induction.

<p>In the shoots, <i>JAZ1, 2, 5, 6</i> and <i>12</i> were induced after JA treatment, while in the roots mainly <i>JAZ1, 2, 3 5, 6</i> and <i>10</i> responded. In the roots, a 10-fold induction was found of <i>JAZ10</i> after RJA, while only a two-fold after SJA. Gene expression is shown as log₂ of fold changes after RJA or SJA compared to CON. Samples in which the gene showed a significantly altered expression compared to CON are marked with an asterisk (ANOVA, FDR corrected <i>P</i>-value <0.1).</p

Average fold change analysis per gene functional classification bin.

<p>The average fold change per bin was analyzed with PageMan on all measured genes in roots and shoots at 6, 18 and 30 h after JA treatment. The shoots showed a more extensive JA response than the roots. In roots and shoots, the Amino Acid and Protein Synthesis bins were strongly induced, indicating large metabolic changes. In both tissues, several bins were only affected by one of the treatments. Fold changes were either RJA/CON, SJA/CON or SJA/RJA. Bins showing a significantly higher or lower average fold change compared to all other bins are highlighted with a red or green gradient, respectively, while bins that were not significantly affected in any of the treatment groups were omitted from the table (Wilcoxon test with Benjamini-Hochberg multiple testing correction).</p