Induced Jasmonate Signaling Leads to Contrasting Effects on Root Damage and Herbivore Performance

Abstract

Induced defenses play a key role in plant resistance against leaf feeders. However, very little is known about the signals that are involved in defending plants against root feeders and how they are influenced by abiotic factors. We investigated these aspects for the interaction between rice (Oryza sativa) and two root-feeding insects: the generalist cucumber beetle (Diabrotica balteata) and the more specialized rice water weevil (Lissorhoptrus oryzophilus). Rice plants responded to root attack by increasing the production of jasmonic acid (JA) and abscisic acid, whereas in contrast to in herbivore-attacked leaves, salicylic acid and ethylene levels remained unchanged. The JA response was decoupled from flooding and remained constant over different soil moisture levels. Exogenous application of methyl JA to the roots markedly decreased the performance of both root herbivores, whereas abscisic acid and the ethylene precursor 1-aminocyclopropane-1-carboxylic acid did not have any effect. JA-deficient antisense 13-lipoxygenase (asLOX) and mutant allene oxide cyclase hebiba plants lost more root biomass under attack from both root herbivores. Surprisingly, herbivore weight gain was decreased markedly in asLOX but not hebiba mutant plants, despite the higher root biomass removal. This effect was correlated with a herbivore-induced reduction of sucrose pools in asLOX roots. Taken together, our experiments show that jasmonates are induced signals that protect rice roots from herbivores under varying abiotic conditions and that boosting jasmonate responses can strongly enhance rice resistance against root pests. Furthermore, we show that a rice 13-lipoxygenase regulates root primary metabolites and specifically improves root herbivore growth.

Alteration of plant primary metabolism in response to insect herbivory

“…Such reallocation of primary metabolites may hamper herbivore performance by reducing the nutritive value of plant tissue. For example, both the generalist cucumber beetle (Diabrotica balteata) and the specialist rice water weevil (Lissorhoptrus oryzophilus) grew significantly slower on a jasmonate-deficient rice (Oryza sativa) mutant, despite the fact that these plants suffered greater loss of biomass than wild-type controls (Lu et al, 2015). This observation was correlated with herbivore-induced depletion of Suc in the infested tissue of the mutant rice line.…”

“…In support of contrasting hypotheses, herbivore attack or chemical elicitation of plant defenses can redirect primary metabolites away from treated tissues (Holland et al, 1996;Lu et al, 2015). Such reallocation of primary metabolites may hamper herbivore performance by reducing the nutritive value of plant tissue.…”

“…Lu et al (2015), for example, found that herbivore-induced carbohydrate sequestration can still occur in the roots of jasmonate signaling-deficient rice mutants, whereas reallocation of carbohydrates toward herbivore-attacked leaves and away from roots in N. attenuata is modulated by both jasmonate and auxin signaling (Machado et al, 2013(Machado et al, , 2015. Following this same line of investigation, concomitant with the incorporation of less-studied signaling networks, one would expect the eventual union of defense signaling networks that control herbivore-induced changes in both primary and secondary metabolism.…”

A Salivary Endo-β-1,4-Glucanase Acts as an Effector That Enables the Brown Planthopper to Feed on Rice

“…Plant hormones, namely, JA, JA-Ile, and SA, play major roles in rice defense against herbivores (Zhou Lu et al, 2011Lu et al, , 2015. To determine if the salivary protein NlEG1 influences the production of these phytohormones and thus modulates defense responses in rice, we investigated the levels of SA, JA, and JA-Ile in rice after the plant was either infested by fifthinstar BPH nymphs whose ability to produce NlEG1 had been silenced or treated with the recombination protein NlEG1.…”

“…The outer three leaf sheaths of stems were harvested at different time points (for details, see Fig. 7 ]JA-Ile) and then analyzed with HPLC-mass spectrometry/mass spectrometry following the method described by Lu et al (2015).…”