The role of plant silicon (Si) in the alleviation of abiotic and biotic stress is now widely recognised and researched. Amongst the biotic stresses, Si is known to increase resistance to herbivores through biomechanical and chemical mechanisms, although the latter are indirect and remain poorly characterised. Chemical defences are principally regulated by several antiherbivore phytohormones. The jasmonic acid (JA) signalling pathway is particularly important and has been linked to Si supplementation, albeit with some contradictory findings. In this Perspectives article, we summarise existing knowledge of how Si affects JA in the context of herbivory and present a conceptual model for the interactions between Si and JA signalling in wounded plants. Further, we use novel information from the model grass Brachypodium distachyon to underpin aspects of this model. We show that Si reduces JA concentrations in plants subjected to chemical induction (methyl jasmonate) and herbivory (Helicoverpa armigera) by 34% and 32%, respectively. Moreover, +Si plants had 13% more leaf macrohairs than −Si plants. From this study and previous work, our model proposes that Si acts as a physical stimulus in the plant, which causes a small, transient increase in JA. When +Si plants are subsequently attacked by herbivores, they potentially show a faster induction of JA due to this priming. +Si plants that have already invested in biomechanical defences (e.g. macrohairs), however, have less utility for JA-induced defences and show lower levels of JA induction overall.
1. Elevated atmospheric CO 2 (eCO 2 ) not only increases plant growth but can also interfere with defence against insect herbivory through the disruption of the jasmonic acid (JA) pathway. Silicon (Si) plays an important role in plant stress tolerance and resistance to herbivory, particularly in grasses, many of which accumulate high amounts of Si. Activation of the JA pathway has been reported to stimulate Si uptake, while Si supplementation can alter both constitutive and induced phytohormone levels. A reduction in JA concentration under eCO 2 has the potential to reduce Si uptake in plants. Using both Si supplemented (Si+) and control (Si−) plants (Brachypodium distachyon)grown under ambient (400 ppm) and elevated (640 ppm) CO 2 concentrations, we tested how plant growth, foliar Si concentration and endogenous JA responded to methyl jasmonate (MeJA) application and the subsequent effects on insect herbivore performance (Helicoverpa armigera). Elevated CO2 reduced Si concentration by 19% and endogenous JA by 70% on average. MeJA significantly increased Si concentration in Si+ plants. Si+ plants had higher baseline JA levels compared to Si− plants under control conditions (i.e. no stress), however, when plants were chemically induced with MeJA, the JA response was on average 84% lower in Si+ plants compared to Si− plants. Plants without MeJA treatment showed the opposite response, that is, Si+ plants had higher baseline JA levels compared to Si− plants. Si significantly reduced herbivore consumption and growth rate. Despite eCO 2 significantly reducing both Si and endogenous JA, no effect was seen on herbivores feeding on eCO 2 plants. 4. Collectively our results suggest that Si alters the JA response of plants. We show that JA induces Si uptake, however, Si then reduces the JA response of plants under induced stress conditions. However, predicted increases in CO 2 levels within this century may significantly reduce Si-based mechanical defences against herbivory via a reduction of endogenous JA. K E Y W O R D S elevated CO 2 , herbivory, jasmonic acid, plant defence, silica S U PP O RTI N G I N FO R M ATI O N Additional supporting information may be found online in the Supporting Information section. How to cite this article: Hall CR, Mikhael M, Hartley SE, Johnson SN. Elevated atmospheric CO 2 suppresses jasmonate and silicon-based defences without affecting herbivores. Funct
Plants deploy an arsenal of chemical and physical defenses against arthropod herbivores, but it may be most cost efficient to produce these only when attacked. Herbivory activates complex signaling pathways involving several phytohormones, including jasmonic acid (JA), which regulate production of defensive compounds. The Poaceae also have the capacity to take up large amounts of silicon (Si) which accumulates in plant tissues. Si accumulation has anti-herbivore properties, but it is poorly understood how Si defenses relate to defense hormone signaling. Here we show that Si enrichment causes the model grass Brachypodium distachyon to show lower levels of JA induction when attacked by chewing herbivores. Triggering this hormone even at lower concentrations, however, prompts Si uptake and physical defenses (e.g. leaf hairs) which negatively impact chewing herbivores. Removal of leaf hairs restored performance. Crucially, activation of such Si-based defense is herbivore-specific and occurred only in response to chewing and not fluid-feeding (aphid) herbivores. This aligned with our meta-analysis of 88 studies that showed Si defenses were more effective against chewing herbivores than fluid-feeders. Our results suggest integration between herbivore defenses in a model Si-accumulating plant, which potentially allows it to avoid unnecessary activation of other costly defenses.
The role of silicon (Si) in alleviating the effects of biotic and abiotic stresses, including defence against insect herbivores, in plants is widely reported. Si defence against insect herbivores is overwhelmingly studied in grasses (especially the cereals), many of which are hyper-accumulators of Si. Despite being neglected, legumes such as soybean (Glycine max) have the capacity to control Si accumulation and benefit from increased Si supply. We tested how Si supplementation via potassium, sodium or calcium silicate affected a soybean pest, the native budworm Helicoverpa punctigera Wallengren (Lepidoptera: Noctuidae). Herbivory reduced leaf biomass similarly in Si-supplemented (+Si) and non-supplemented (–Si) plants (c. 29 and 23%, respectively) relative to herbivore-free plants. Both Si supplementation and herbivory increased leaf Si concentrations. In relative terms, herbivores induced Si uptake by c. 19% in both +Si and –Si plants. All Si treatments reduced H. punctigera relative growth rates (RGR) to a similar extent for potassium (−41%), sodium (−49%) and calcium (−48%) silicate. Moreover, there was a strong negative correlation between Si accumulation in leaves and herbivore RGR. To our knowledge, this is only the second report of Si-based herbivore defence in soybean; the rapid increase in leaf Si following herbivory being indicative of an induced defence. Taken together with the other benefits of Si supplementation of legumes, Si could prove an effective herbivore defence in legumes as well as grasses.
Grasses accumulate large amounts of silicon (Si) which is deposited in trichomes, specialised silica cells and cell walls. This may increase leaf toughness and reduce cell rupture, palatability and digestion. Few studies have measured leaf mechanical traits in response to Si, thus the effect of Si on herbivores can be difficult to disentangle from Si-induced changes in leaf surface morphology. We assessed the effects of Si on Brachypodium distachyon mechanical traits (specific leaf area (SLA), thickness, leaf dry matter content (LDMC), relative electrolyte leakage (REL)) and leaf surface morphology (macrohairs, prickle, silica and epidermal cells) and determined the effects of Si on the growth of two generalist insect herbivores (Helicoverpa armigera and Acheta domesticus). Si had no effect on leaf mechanical traits; however, Si changed leaf surface morphology: silica and prickle cells were on average 127% and 36% larger in Si supplemented plants, respectively. Prickle cell density was significantly reduced by Si, while macrohair density remained unchanged. Caterpillars were more negatively affected by Si compared to crickets, possibly due to the latter having a thicker and thus more protective gut lining. Our data show that Si acts as a direct defence against leaf-chewing insects by changing the morphology of specialised defence structures without altering leaf mechanical traits.
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