Chemical defence in Brassicaceae against pollen beetles revealed by metabolomics and flower bud manipulation approaches

Abstract

Divergence of chemical plant defence mechanisms within the Brassicaceae can be utilized to identify means against specialized pest insects. Using a bioassay‐driven approach, we (a) screened 24 different Brassica napus cultivars, B. napus resyntheses and related brassicaceous species for natural plant resistance against feeding adults of the pollen beetle (Brassicogethes aeneus), (b) tested for gender‐specific feeding resistance, (c) analysed the flower bud metabolomes by a non‐targeted approach and (d) tested single candidate compounds for their antifeedant activity. (a) In no‐choice assays, beetles were allowed to feed on intact plants. Reduced feeding activity was mainly observed on Sinapis alba and Barbarea vulgaris but not on B. napus cultivars. (b) Males fed less and discriminated more in feeding than females. (c) Correlation of the metabolite abundances with the beetles' feeding activity revealed several glucosinolates, phenylpropanoids, flavonoids and saponins as potential antifeedants. (d) These were tested in dual‐bud‐choice assays developed for medium‐throughput compound screening. Application of standard compounds on single oilseed rape flower buds revealed highly deterrent effects of glucobarbarin, oleanolic acid and hederagenin. These results help to understand chemical plant defence in the Brassicaceae and are of key importance for further breeding strategies for insect‐resistant oilseed rape cultivars.

Chemodiversity in flowers of Tanacetum vulgare has consequences on a florivorous beetle

“…However, plants also incorporate deterrent or toxic compounds, including terpenoids, in these tissues to defend against over-exploitation by pollinators or florivores (Palmer-Young et al 2019;Rivest & Forrest 2020;Sasidharan et al 2023). For example, a glucosinolate and saponins deter feeding of the pollen beetle Brassicogethes aeneus (Coleoptera: Nitidulidae) on oilseed rape (Austel et al 2021). The nutrient content in pollen may be correlated with its specialized metabolite diversity (Sasidharan et al 2023), but differences in nutrient composition among plants of different chemotypes have rarely been investigated (Eilers et al 2021).…”

Perspectives for integrated insect pest protection in oilseed rape breeding

“…Unfortunately, these genomes are also less likely to contain useful resistances that are not present in rapeseed already than more distantly related species, due to the high level of gene conservation between the Brassica subgenomes present in the different species (Chalhoub et al 2014 ). So far, some evidence suggests this also applies to insect resistance traits (Austel et al 2021 ). Thus, we may need to also consider the wider relatives when breeding for insect resistance (Table 1 ).…”

“…Ahuja et al 2010 ). Terpenoids including triterpene saponins play a role in specialist insect resistance in the Brassicaceae genera Lunaria (honesty), Thlaspi (pennycress) and Barbarea (winter cress) for resistance against the striped flea beetle ( Pyllotetra striolata ), the diamondback moth , the cabbage butterfly ( P. rapae ) (reviewed in Hussain et al 2019 ) and pollen beetles (Austel et al 2021 ). Tetracyclic triterpene steroids from Iberis species (candytuft) are involved in resistance against several species of flea beetles (Nielsen 1978 ) as well.…”

Floral volatiles evoke partially similar responses in both florivores and pollinators and are correlated with non-volatile reward chemicals

“…Some of these may act as toxins when present in sufficiently high concentrations (Palmer-Young et al, 2019, Rivest and Forrest, 2020). Toxins in floral tissue deter florivores and can thus reduce floral damage (Adler et al, 2001, Austel et al, 2021, Irwin and Adler, 2006, Strauss et al, 2004). In many of these cases, such compounds simultaneously deter beneficial pollinators (de Mesquita et al, 2010, Irwin and Adler, 2006, Irwin et al, 2014).…”

“…Likewise, the consumption of nectar alkaloids can reduce the protozoan pathogen load in bumblebees (Manson et al, 2010). Although toxins in pollen are believed to be largely targeted against florivores (Adler et al, 2001, Austel et al, 2021, Irwin and Adler, 2006, Strauss et al, 2004), pollinators may nonetheless also be affected by pollen and nectar toxins at certain concentrations, leading to deterrence, impaired development or even death (de Mesquita et al, 2010, Irwin and Adler, 2006, Irwin et al, 2014, Stevenson, 2020). Thus, a similar trade-off as found in FVOCs may exist in pollen traits, namely, the need to protect nutrients serving as rewards for pollinators with toxins to deter florivores and excessive pollen consumers.…”