Conserved nematode signalling molecules elicit plant defenses and pathogen resistance

Abstract

Plant-defense responses are triggered by perception of conserved microbe-associated molecular patterns (MAMPs), for example, flagellin or peptidoglycan. However, it remained unknown whether plants can detect conserved molecular patterns derived from plant-parasitic animals, including nematodes. Here we show that several genera of plant-parasitic nematodes produce small molecules called ascarosides, an evolutionarily conserved family of nematode pheromones. Picomolar to micromolar concentrations of ascr#18, the major ascaroside in plant-parasitic nematodes, induce hallmark defense responses including the expression of genes associated with MAMP-triggered immunity, activation of mitogen-activated protein kinases, as well as salicylic acid- and jasmonic acid-mediated defense signalling pathways. Ascr#18 perception increases resistance in Arabidopsis, tomato, potato and barley to viral, bacterial, oomycete, fungal and nematode infections. These results indicate that plants recognize ascarosides as a conserved molecular signature of nematodes. Using small-molecule signals such as ascarosides to activate plant immune responses has potential utility to improve economic and environmental sustainability of agriculture.

Pattern Recognition Receptors—Versatile Genetic Tools for Engineering Broad-Spectrum Disease Resistance in Crops

“…In addition, immunogenic molecular patterns have also been enriched from nematodes, insects, and parasitic plants [6,18,19]. Taken together, this demonstrates the central role of MAMP sensing for plant defense against different types of invaders.…”

Genetic architecture of wild soybean (Glycine soja) response to soybean cyst nematode (Heterodera glycines)

“…In our recent studies using transcriptome profiling to characterize the molecular mechanism of the soybean-SCN interaction, significant changes in the expression of genes participating in calcium and ethylene-related pathways were observed, suggesting that calcium and ethylene play important roles in soybean defense against or response to SCN infection (Klink et al 2007b; Klink et al 2007a; Kandoth et al 2011). Calcium- and ethylene-mediated plant defense signaling was recently verified conserved in the plant defenses against nematodes, as previously described (Manosalva et al 2015). …”

Combinatorial chemistry in nematodes: modular assembly of primary metabolism-derived building blocks

“…52 Ascarosides featuring short to medium length side chains (C 3 –C 11 ) are abundantly produced by the free-living C. elegans , 46 Panagrellus redivivus , 53 and many other nematode species, 52 whereas ascarosides incorporating longer side chains (C 11 –C 20 ) have been identified in the entomopathogenic Heterorhabditis bacteriophora , 52,54 the animal parasite Pelodera strongyloides , 52 and several plant-parasitic nematode species. 55 Ascarosides with very long-chain fatty acid residues (C 21 –C 33 ) have been identified in the metabolomes of C. elegans peroxisomal β-oxidation mutants 56 as well as in mammalian parasites of the genus Ascaris . 40,57 Considering that many nematode species share identical habitats, overlap in the production of putative ascaroside-based signalling molecules raises interesting questions regarding the maintenance of species-specific communication.…”