Silicon or symbionts? Grasses use both types of anti-herbivore defences

Ximena Cibils-Stewart recently submitted her doctoral dissertation at The Hawkesbury Institute for the Environment, Western Sydney University, and is currently an adjunct scientist at the Instituto Nacional de Investigación Agropecuaria (http://www.inia.uy/en) in Uruguay. In her doctoral work her main focus was to evaluate how silicon-supplementation in combination with beneficial symbionts (i.e. endophytes) enhances grass resistance to insect pests. In this Behind the Paper, she talks about her recent paper “Interactions between silicon and alkaloid defences in endophyte-infected grasses and consequences for a folivore

About the paper

Ximena and Juan (husband) preparing samples for carbon nitrogen analysis at HIE. Image courtesy of Ximena Cibils-Stewart
Ximena and Juan (husband) preparing samples for carbon nitrogen analysis at HIE. Image courtesy of Ximena Cibils-Stewart

Plants deploy an arsenal of physical and chemical defences to naturally defend themselves against insect herbivory. Grasses, in particular, accumulate a large amount of silicon (Si) in tissue as a physical defence; specifically, plant roots uptake dissolved Si from the soil and it is subsequently deposited in foliage as solid silica, making the plant very unpalatable for herbivores, particularly chewers (i.e. caterpillars). Additionally, many grasses associate symbiotically with foliar Epichloë-endophytes that provide chemical defence via antiherbivore alkaloids that are toxic and poisonous upon ingestion.

Despite Si and Epichloë-endophytes being universally present in most temperate grasses, their antiherbivore properties have mostly been studied separately. In fact, only two studies have looked at their interaction (Cibils-Stewart et al., 2020; Huitu et al., 2014). Both studies reported that the presence of endophytes increases Si accumulation in foliar grass tissue. However, until this paper, the consequences of such interactions for chewing insect herbivores remained unknown.

The present paper therefore explores this research gap utilising the two most sown pasture grasses worldwide, tall fescue and perennial ryegrass, associated with different native and commercial endophyte strains and supplied with Si through irrigation. To achieve this all plants were grown in the glasshouse in soil with low levels of Si and exposed to in-situ feeding by the global pest caterpillar, Helicoverpa armigera. Our main objectives were to evaluate how Si supply and Epichloë-endophytes in interaction with herbivory affected foliar Si and mutualist-derived alkaloid concentrations. Subsequently, their combined effects on H. armigera growth were evaluated.

We found that the presence of endophytes in both grasses generally increased Si concentrations in Si supplied plants. Additionally, for the two most used commercial endophyte strains (one in each grass species) Si concentrations were also induced (herbivore-inoculated) by at least 25%. Surprisingly and contrary to what we expected, Si supply did not affect alkaloids produced by most endophytes tested. In other words, Si did not affect the production of chemical defences by endophytes.

For the caterpillar, however, we report that the effects of both Si and endophytes were species and endophyte specific.  Specifically, for tall fescue, Si supply reduced caterpillar growth significantly, with endophyte-alkaloids playing a secondary role in plant defence. Conversely, in perennial ryegrass, both Si and endophyte-alkaloids (regardless of Si supply) reduced herbivore growth independently, although not synergised.

About the research

Experimental plants were grown in the glasshouse in soil in the absence/presence of: 1) Si supply (through water), 2) endophytes, and 3) cages with and without herbivores in a factorial combination. Image courtesy of Ximena Cibils-Stewart.
Experimental plants were grown in the glasshouse in soil in the absence/presence of: 1) Si supply (through water), 2) endophytes, and 3) cages with and without herbivores in a factorial combination. Image courtesy of Ximena Cibils-Stewart.

We believe that understanding how Si- and endophyte-based defences operate in grasses is important to increase resistance to herbivory while reducing the use of insecticides.

Our novel findings regarding the combined antiherbivore effects of both Si and endophytes for the two grass species suggest that these natural strategies do not antagonize each other. In a more applied sense, both Si and endophytes can be artificially incorporated into productive pastures as either manufactured or naturally occurring Si fertilisers, or though the insertion of novel endophytes into productive cultivars.

Lastly, endophytic alkaloids have been shown to be an effective defence against other insects such as piercing-sucking aphids, for which Si defences are proven to be less effective. Thus, the nature of the protective interaction between Si and grass endophytes may depend on the feeding guild of the insect herbivore.

About the author

 Scanning electron microscope image of the abaxial leaf surface of a tall fescue leaf grown in soil supplied with Si through irrigation. Note solid silica crystals as white structures in the leaf surface; Image courtesy of Ximena Cibils-Stewart taken at the Advanced Materials Characterisation Facility, Western Sydney University.
Scanning electron microscope image of the abaxial leaf surface of a tall fescue leaf grown in soil supplied with Si through irrigation. Note solid silica crystals as white structures in the leaf surface; Image courtesy of Ximena Cibils-Stewart taken at the Advanced Materials Characterisation Facility, Western Sydney University.

Born and raised in Uruguay SA, Ximena has always been fascinated with entomology. In fact entomology has been the cause of her professional experience across different continents (USA –NZA–Australia), as well as, the reason why Ximena returned home (Uruguay). Specifically, Ximena earned a double B.S. in Biology and Entomology at Iowa State University (ISU-2010) and an MSc in Entomology at Kansas State University (KSU-2014).

During her BSc she worked with corn rootworm resistance management specifically testing pathogen susceptibility, and associated fitness costs. Her MSc contributions helped to fill knowledge gaps regarding the effects of within-plant distribution of prey on predator communities in winter canola and helped determine whether winter canola is acting as a source or as a sink (ecological trap) to beneficial insects and pollinators.

Whilst obtaining a permanent position as an associate scientist in entomology at INIA, Uruguay´s National Institute of Agricultural Research (http://www.inia.uy/en) in 2014; she recently finished her PhD in Australia at the Hawkesbury Institute for the Environment (HIE) at Western Sydney University (2021). At INIA, Ximena’s work has been majorly linked to the breeding programs of legumes and forage crops; specifically disentangling interactions between Epichloë-endophyte and insect-pests in Uruguay. Epichloë-endophytes are symbionts that produce antiherbivore-alkaloids (natural insecticides).

Her PhD project extends this and focused on how interactions between silicon (physical defense), Epichloë-endophytes, and arbuscular mycorrhizal fungi might increase plant resistance against herbivorous pests. Her career goal is to undertand natural available defenses in plants to better incorporate them into insect management programs.

https://orcid.org/0000-0003-0296-5554  https://www.researchgate.net/profile/Ximena-Cibils-Stewart

Ximena and Juan (husband) preparing samples for carbon nitrogen analysis at HIE. Image courtesy of Ximena Cibils-Stewart

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