Evolutionary Metabolomics Reveals Domestication-Associated Changes in Tetraploid Wheat Kernels

Abstract

Domestication and breeding have influenced the genetic structure of plant populations due to selection for adaptation from natural habitats to agro-ecosystems. Here, we investigate the effects of selection on the contents of 51 primary kernel metabolites and their relationships in three Triticum turgidum L. subspecies (i.e., wild emmer, emmer, durum wheat) that represent the major steps of tetraploid wheat domestication. We present a methodological pipeline to identify the signature of selection for molecular phenotypic traits (e.g., metabolites and transcripts). Following the approach, we show that a reduction in unsaturated fatty acids was associated with selection during domestication of emmer (primary domestication). We also show that changes in the amino acid content due to selection mark the domestication of durum wheat (secondary domestication). These effects were found to be partially independent of the associations that unsaturated fatty acids and amino acids have with other domestication-related kernel traits. Changes in contents of metabolites were also highlighted by alterations in the metabolic correlation networks, indicating wide metabolic restructuring due to domestication. Finally, evidence is provided that wild and exotic germplasm can have a relevant role for improvement of wheat quality and nutritional traits.

Adapting legume crops to climate change using genomic approaches

“…Recent decades witnessed a tremendous progress in DNA sequencing technologies; however, successful crop improvement plans are also dependant on accurately measuring plant traits to identify genetic loci associated with traits. Along with innovative and high throughout phenotyping strategies (such as near-infrared spectroscopy on agricultural harvesters and spectral reflectance of plant canopy), analysis can be extended to the molecular phenotype using transcriptomic, metabolomics, and proteomic approaches (Beleggia et al, 2016;Bitocchi, Rau, Benazzo, et al, 2017). Together, these will improve our capacity to explore the phenotypic space from large multilocation field trials (Fahlgren, Gehan, & Baxter, 2015;Montes, Melchinger, & Reif, 2007).…”

Multi‐tissue integration of transcriptomic and specialized metabolite profiling provides tools for assessing the common bean (Phaseolus vulgaris) metabolome

“…The structure of common bean populations, with its two independent domestication events and a rich repertoire of wild forms, land races and commercial varieties makes it a highly suitable candidate for forward genetic approaches based on natural variation. Such approaches represent a powerful method for investigation of mechanisms that underlie metabolic diversity and regulation, and ultimately in identifying candidates for the reintroduction of interesting genetic traits that were lost during domestication and breeding (Tanksley and McCouch, 1997;Paran and Zamir, 2003;McCouch, 2004;Fernie and Klee, 2011;Bellucci et al, 2014;Beleggia et al, 2016;Fernie and Tohge, 2017). An interesting target for such approaches that is particularly relevant both for plant fitness and human nutrition is specialized metabolism, which has been demonstrated to be one of the most affected traits by the loss of diversity occurring through the process of domestication (Meyer and Purugganan, 2013).…”

Shifts in plant functional strategies over the course of wheat domestication

“…Until recently, geneticists and plant breeders believed that only a few genes were involved in this domestication syndrome. However, recent papers on different species (Beleggia et al., ; Bellucci et al., ; Swanson‐Wagner et al., ) suggested that this syndrome has significantly affected the whole‐plant functioning as well as a larger part of the genome. Thus, the traits targeted by artificial selection may be more strongly correlated with other plant traits than previously thought, and considering whole‐plant phenotypic response to domestication becomes a critical avenue for both theoretical and applied questions.…”

“…Until recently, geneticists and plant breeders believed that only a few genes were involved in this domestication syndrome. However, recent papers on different species (Beleggia et al, 2016;Bellucci et al, 2014;Swanson-Wagner et al, 2012) suggested that this syndrome has significantly affected the whole-plant functioning as well as a larger part of the genome.…”