Changes in "natural antibiotic" metabolite composition during tetraploid wheat domestication

Abstract

Gramineous plants protect their seeds from a variety of biotic stresses by producing toxic and deterrent secondary metabolites such as benzoxazinoids. It is unclear how the composition and abundance of these natural toxins has changed over the course of crop-plant domestication. To address this uncertainty, we characterized differences in metabolic levels of benzoxazinoids and their derivatives, between four lines of tetraploid wheat: wild emmer wheat (WEW), the direct progenitor of modern wheat; non-fragile domesticated emmer wheat (DEW), which was first domesticated about 11,000 years ago; the subsequently developed non-fragile and free-threshing durum landraces (LD); and modern durum (MD) varieties. Three-dimensional principal component analysis of mass spectrometry data of wheat metabolites showed with high resolution clear differences between metabolic profiles of WEW, DEW, and durum (LD + MD) and similarity in the metabolic profiles of the two durum lines (LD and MD) that is coherent with the phylogenetic relationship between the corresponding wheat lines. Moreover, our results indicated that some secondary metabolites involved in plant defense mechanisms became significantly more abundant during wheat domestication, while other defensive metabolites decreased or were lost. These metabolic changes reflect the beneficial or detrimental roles the corresponding metabolites might play during the domestication of three taxonomic subspecies of tetraploid wheat (Triticum turgidum).

Metabolome dynamics during wheat domestication

“…The primary domestication is the evolution of WEW to DEW, whereas the secondary domestication is the evolution of DEW to durum wheat 1 , which is also divided into two groups—LD (i.e., traditional) and MD (i.e., industrial). Three-dimensional (3D) principal component analyses (PCAs), run without a wheat category-bias, also demonstrated a clear separation among the WEW, DEW, and durum accessions in both the embryo and the endosperm tissues as describe here and elsewhere y Ben Abu and Itsko 25 (Fig. 1 ).…”

“…We next attempted to characterize which metabolites undergo changes in association with wheat domestication. For that purpose, we undertook used PCA analysis as we perform elsewhere 25 and appear in Fig. 1 A,B.…”

“…The plants were grown under the same conditions, in a net-house with three replicates per line; each replicate being grown in a separate block. All plants were grown in 3-L pots during the winter 25 .…”

“…Metabolite analysis was carried out using as described by Hanhineva et al (2008, 2011) and by Ben Abu et al (2021) 24 , 25 . This procedure used a UPLC-PDA-qTOF-MS system: a UPLC Waters Acquity instrument connected in-line to an Acquity PDA (photodiode array) detector and a Synapt HDMS detector (tandem quadrupole/time-of-flight mass spectrometer).…”

“…The identification of metabolites was performed as described previously on data obtained using the ESI-negative mode 24 . In short, the accurate mass and molecular formula predictions were screened for putative molecules from the Dictionary of Natural Products (Chapman and Hall/ CRC) and the SciFinder Scholar databases (SciFinder Scholar 2007) as described elsewhere 25 . The MS/MS fragmentation and UV-absorbability of the metabolites were compared with those of candidate molecules found in databases and verified with earlier literature on similar compounds 23 .…”