Mechanisms and ecological implications of plant‐mediated interactions between belowground and aboveground insect herbivores

Abstract

Plant-mediated interactions between belowground (BG) and aboveground (AG) herbivores have received increasing interest recently. However, the molecular mechanisms underlying ecological consequences of BG-AG interactions are not fully clear yet. Herbivore-induced plant defenses are complex and comprise phytohormonal signaling, gene expression and production of defensive compounds (defined here as response levels), each with their own temporal dynamics. Jointly they shape the response that will be expressed. However, because different induction methods are used in different plant-herbivore systems, and only one or two response levels are measured in each study, our ability to construct a general framework for BG-AG interactions remains limited. Here we aim to link the mechanisms to the ecological consequences of plant-mediated interactions between BG and AG insect herbivores. We first outline the molecular mechanisms of herbivore-induced responses involved in BG-AG interactions. Then we synthesize the literature on BG-AG interactions in two well-studied plant-herbivore systems, Brassica spp. and Zea mays, to identify general patterns and specific differences. Based on this comprehensive review, we conclude that phytohormones can only partially mimic induction by real herbivores. BG herbivory induces resistance to AG herbivores in both systems, but only in maize this involves drought stress responses. This may be due to morphological and physiological differences between monocotyledonous (maize) and dicotyledonous (Brassica) species, and differences in the feeding strategies of the herbivores used. Therefore, we strongly recommend that future studies explicitly account for these basic differences in plant morphology and include additional herbivores while investigating all response levels involved in BG-AG interactions.

Foliar herbivory by caterpillars and aphids differentially affects phytohormonal signalling in roots and plant defence to a root herbivore

“…Most research on insect–plant interactions focusses on what is visible above ground (Kaplan & Denno, , Papadopoulou & van Dam, , Poelman, Broekgaarden, van Loon, & Dicke, , Poelman, Van Loon, Van Dam, Vet, & Dicke, , Stam et al, ), yet there is a hidden world beneath our feet, with its own organisms, ecological interactions, food webs, and abiotic environment (Erb, Robert, Hibbard & Turlings, ; Johnson et al, ; Johnson & Rasmann, ; Rasmann et al, ). What happens below ground often has major impacts on what we see above ground.…”

“…Defence responses occur not only locally, but throughout the plant. Although most studies on systemic responses focus on above ground tissues, in response to induction in either another leaf or in the roots (Papadopoulou & van Dam, ; Soler et al, ), there is an increasing body of literature showing that roots respond to leaf herbivory as well (Gulati, Baldwin, & Gaquerel, ; Huang, Siemann, Xiao, Yang, & Ding, ; Kim, Song, & Ryu, ; Kong, Kim, Song, Lee, & Ryu, ; Machado et al, ; Machado, Arce, McClure, Baldwin, & Erb, ; Soler, Erb, & Kaplan, ).…”

Aboveground herbivory induced jasmonates disproportionately reduce plant reproductive potential by facilitating root nematode infestation

“…Jasmonates have been suggested to regulate plant‐mediated interactions between above and below ground herbivores (Erb, Lenk, Degenhardt, & Turlings, ; Erb, Ton, Degenhardt, & Turlings, ; Papadopoulou & van Dam, ; van Dam & Heil, ; van Dam & Oomen, ). Foliar jasmonate treatments reduce gall formation by root parasitic nematodes in tomato (Bhattarai et al, ; Cooper, Jia, & Goggin, ; Fan et al, ; Fujimoto et al, ; Zinovieva, Vasyukova, Udalova, & Gerasimova, ), rice (Kyndt et al, ; Nahar, Kyndt, de Vleesschauwer, Höfte, & Gheysen, ), soybean (Hu, You, Li, Hua, & Wang, ), oat (Soriano, Asenstorfer, Schmidt, & Riley, ), and thale cress (Gleason, Leelarasamee, Meldau, & Feussner, ; Ozalvo et al, ).…”

The 30th anniversary of Ecological Research: past, present, and future

“…To remain competitive, ER has increased the proportion of open access articles published in the journal, which accounted for 16.8% of papers published in 2016. The ESJ has so far borne the open access costs for its ER award articles (e.g., Nakazawa 2016; Suzuki 2016) and for ER symposium papers (e.g., Papadopoulou and van Dam 2017). Further promotion of open access is under discussion with the journal's publisher.…”