Plant roots exude a diverse array of biologically active compounds, which have the capacity to shape the microbiome that is associated with roots. These exudates alter the chemistry of exposed soil, and can recruit beneficial disease-suppressing bacteria and fungi to the root surface (1). Some of these microbes, such as plant-growth promoting rhizobacteria and mycorrhizal fungi, have the ability to suppress plant disease through a range of mechanisms, including production of fungistatic secondary metabolites, competition for iron, and elicitation of induced systemic resistance (ISR), which is marked by priming of jasmonic acid-inducible genes in the leaves (2,3).
In cereals, benzoxazinoids (BXs), such as DIMBOA, represent an important class of secondary metabolites that influence belowground and aboveground plant-microbe interactions. Since their identification as defence metabolites, investigations have mostly focused on their role in defence against aboveground pests. BXs are typically produced during relatively early, vulnerable plant growth stages. After tissue damage, vacuole localised BX-glucosides become hydrolysed by plastid-localised β-glucosidases, causing rapid accumulation of aglycone BXs with biocidal activities.
BXs are also active against attackers that cause relatively minor tissue damage, such as aphids and pathogenic fungi. Previously, we discovered that this activity is based on increased accumulation of DIMBOA in the apoplast before the onset of large-scale tissue damage, where it signals increased deposition of callose-rich papillae (4). Thus, the role of BXs in aboveground cereal defence is not limited to their biocidal properties, but also includes a within-plant signalling function in the activation of plant innate immune responses against pests and diseases.
BXs have been implicated in plant defence belowground, where they are exuded from cereal roots as allelochemicals against microbes, insects or competing plants. We discovered an additional function of root-exuded maize BXs in recruitment of plant- beneficial rhizobacteria (5), where DIMBOA, or breakdown products therefor, act as the important allelochemicals to recruit disease-suppressing Pseudomonas putida to the rhizosphere of maize. Transcriptome analysis revealed that exposure of P. putida to DIMBOA induces bacterial genes involved in chemotactic responses. In vitro chemotaxis assays furthermore confirmed that P. putida displays positive taxis towards DIMBOA. The ecological relevance of this response was subsequently confirmed by root colonisation assays in soil, using maize mutant lines that impaired in BX biosynthesis, confirming that rhizosphere colonisation by P. putida is impaired by mutation affecting BX production (5). In a subsequent study, we also found that BX-deficient mutant plants failed to develop aboveground defence priming when grown in soils containing resistance-inducing P. putida bacteria (5).
More recently, we have investigated the impacts of different genetic mutations in the BX pathway on the maize root metabolome and the associated fungal and bacterial communities (6). This research also involves method development, to improve our analytical capability to study rhizosphere chemistry in non-sterile soil and further so elucidate the complex interplay between microbial rhizocommunities and rhizosphere chemistry (7).
This research component is particularly useful in the fight against cereal pests and diseases. By breeding cereal varieties that are better at defending themselves against below- and aboveground attackers through improved recruitment disease-suppressing soil bacteria, we can reduce our unsustianable reliance on chemical pesticides.
1. Rolfe, Griffith & Ton (2019) Curr Opin Microbiol 49:73-82. 2. Cameron D. et al. & Ton J. (2013) TIPS 10: 539-54. 3. Van der Ent, S. et al. & Ton J. (2009) New Phytol 183, 419-431. 4. Ahmad et al. & Ton (2011) Plant Physiol. 157, 317-327. 5. Neal A.L. et al. & Ton J. (2012) PLoS ONE 7, e35498. 5. Neal & Ton (2013) Plant Signal Behav e22655. 6. Cotton et al. Rolfe & Ton ISME J 13: 1647–1658. 7. Pétriacq et al. & Ton Plant J 92: 147-162.
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