Benzoxazinoids in wheat allelopathy - from discovery to application for sustainable weed management

Authors: SÁNCHEZ-MOREIRAS, ADELA - University Of Vigo; SCHULZ, MARGOT - University Of Bonn; Baerson, Scott; WESTON, LESLIE - Charles Sturt University; HUSSAIN, M. IFTIKHAR - University Of Vigo; ARANITI, FABRIZIO - University Of Reggio Calabria; BILSBORROW, PAUL - University Of Newcastle; MACÍAS, FRANCISCO - University Of Cadiz; REIGOSA, MANUEL - University Of Vigo

Submitted to: Environmental and Experimental Botany
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/11/2022
Publication Date: 7/19/2022
Citation: Sánchez-Moreiras, A.M., Schulz, M., Baerson, S.R., Weston, L.A., Hussain, M., Araniti, F., Bilsborrow, P., Macías, F.A., Reigosa, M.J. 2022. Benzoxazinoids in wheat allelopathy - from discovery to application for sustainable weed management. Environmental and Experimental Botany. https://doi.org/10.1016/j.envexpbot.2022.104997.
DOI: https://doi.org/10.1016/j.envexpbot.2022.104997

Interpretive Summary: Many native species produce specialized compounds referred to as allelochemicals, which interfere with the growth and development of neighboring plants. This type of chemical interference confers a competitive advantage to plants which release these compounds (allelopaths), since they must compete for potentially limiting resources such as light, water, and nutrients with their neighbors. Modern crop species in some cases are derived from ancestral allelopaths, and thus have retained the ability to release allelochemicals. One of the most extensively-studied allelopathic crop species is wheat, which also represents one of the most important crops produced world-wide. This article reviews the current state of knowledge concerning the allelochemicals produced by wheat, their biological activities, and their known roles in natural and agricultural systems. Emphasis is also placed on the biochemistry and potential biotechnological applications of benzoxazinoids, a highly potent class of allelochemicals produced by wheat as well as by other grass species. Evolutionary aspects of allelochemical production are also discussed, within the context of their impact on the evolution of organisms which must adapt to their presence in natural ecosystems.

Technical Abstract: Allelopathic activity of wheat (Triticum aestivum L.) has previously been associated with the production of phenolic acids and flavonoids (PAF), benzoxazinones (BXZs) and phenoxazinones (PXZs). The biosynthesis of BXZs is closely regulated during cereal growth, with the greatest accumulation in young tissues and dependence on wheat genotypes and environmental conditions. Allelochemicals from wheat are mainly released through living plants via root exudation and tissue disruption of plant residues. A diverse group of allelochemicals, including simple phenolics (p-hydroxybenzoic, cis-ferulic, vanillic, cis-p-coumaric, trans-ferulic, protocatechuic, syringic, trans-p-coumaric acid, and flavonoids (luteolin, quercetin, vanillin), and hydroxamic acids have been isolated and quantified in recent years from wheat shoots, roots, and root exudates. In this review, we mainly focus on the benzoxazinones (DIMBOA, BOA, MBOA, HBOA, HMBOA, DIBOA) and phenoxazinones (APO, AMPO, AAPO, AAMPO) derived from wheat tissues and their impact on the germination, seedling growth, physiological, biochemical transcriptional, and proteome traits of surrounding plants and weeds. The major pathways known to be employed by plants for benzoxazinoid detoxication involve hydroxylation and glucosylation reactions, and the polymerization of intermediates occurring within these pathways. Allelochemicals from different wheat genotypes have been shown to inhibit the growth of various weed species including Bromus japonicus, Chenopodium album, Portulaca oleraceae, Avena fatua and Lolium rigidum. Wheat allelopathy can potentially be exploited from the standpoint of crop mulches, soil incorporation of crop residues, tissue disruption, intercropping with allelopathic cultivars and application of aqueous wheat extracts. Many native plants, fungi and insect herbivores inherently possess varying levels of tolerance towards benzoxazinoids, however other BXZ- susceptible species could be adversely impacted by elevated BXZ levels in crop plants. In the soil, BXZs undergo a cascade of transformations and their concentrations may vary both qualitatively and quantitatively from one gentoype to another. The further transformation of BXZs to more potent bioherbicidal metabolites by soil microbiota has also been characterized in recent years. BXZs have been shown to suppress the growth and development of certain agricultural pests, including insects, fungal pathogens and weeds, thus considerations for the selection and breeding of novel wheat genotypes possessing enhanced defensive ability via elevated BXZ contents are discussed in the present review. Here, we reconsider these objectives with a focus on co-evolutionary aspects, as well as their potential impacts on biodiversity. It will be important for future breeding efforts to take such potential adverse environmental impacts into account, in combination with an increased focus on the enhancement of beneficial allelopathic interactions between species within agricultural systems.