Volatiles and hormones mediated root-knot nematode induced wheat defense response to foliar herbivore aphid

Plant root-leaf communication signals are critical for plant defense. Numerous studies show that belowground organisms can alter systemically resistance traits in aboveground parts against herbivores. However, there are limited studies on root-knot nematode-aphid interaction. Moreover, the impact of nematode's initial density and infection time on plant defense is poorly understood. Here we aim to examine the induced defense responses by root-knot nematode Meloidogyne incognita against aboveground feeding aphid Sitobion avenae in wheat. Further, we investigated the influence of the nematode infection density as well as the length of infection in these interactions. We tested the direct and indirect defense responses triggered by M. incognita against S. avenae as well as how the responses affect the preference of Harmonia axyridis. Plant volatiles and hormones were determined to explore plant defense mechanisms that mediate aboveground-belowground defense. The photosynthetic rate was tested to examine plant tolerance strategy. We found that, both low and high densities M. incognita root infection at 7 days post inoculation (dpi) reduced the feeding of the aphid S. avenae. Behavioral assay showed that H. axyridis preferred plants co-damaged by both M. incognita and S. avenae at 7 dpi. M. incognita infection induced the changes of jasmonic acid, salicylic acid and volatile content, which mediated plant response to S. avenae. Furthermore, photosynthetic rate in wheat increased at 5 dpi under 300 M. incognita or 1000 M. incognita infection. These results suggest that plant roots induced multiple defense strategies against foliar herbivores as damages increased. Our study provides evidence of a complex dynamic response of wheat aboveground defense against aphids in response to belowground nematode damage on a temporal scale.