Evolution of the Crop Rhizosphere: Impact of Domestication on Root Exudates in Tetraploid Wheat (Triticum turgidum L.)

ORIGINAL RESEARCH published: 13 December 2017 doi: 10.3389/fpls.2017.02124 Evolution of the Crop Rhizosphere: Impact of Domestication on Root Exudates in Tetraploid Wheat (Triticum turgidum L.) Anna Iannucci 1† , Mariagiovanna Fragasso 1† , Romina Beleggia 1 , Franca Nigro 1 and Roberto Papa 1, 2* 1 Centro di Ricerca per la Cerealicoltura e le Colture Industriali , Consiglio per la Ricerca in Agricoltura e l’analisi dell’Economia Agraria (CREA-CI), Foggia, Italy, 2 Dipartimento di Scienze Agrarie, Alimentari e Ambientali, Università Politecnica delle Marche, Ancona, Italy Edited by: Marcelino Perez De La Vega, Universidad de León, Spain Reviewed by: Mark Chapman, University of Southampton, United Kingdom Dayakar Badri, Hill’s Pet nutrition Inc., United States *Correspondence: Roberto Papa † These authors have contributed equally to this work. Specialty section: This article was submitted to Plant Breeding, a section of the journal Frontiers in Plant Science Received: 16 August 2017 Accepted: 29 November 2017 Published: 13 December 2017 Citation: Iannucci A, Fragasso M, Beleggia R, Nigro F and Papa R (2017) Evolution of the Crop Rhizosphere: Impact of Domestication on Root Exudates in Tetraploid Wheat (Triticum turgidum L.). Front. Plant Sci. 8:2124. doi: 10.3389/fpls.2017.02124 Domestication has induced major genetic changes in crop plants to satisfy human needs and as a consequence of adaptation to agroecosystems. This adaptation might have affected root exudate composition, which can influence the interactions in the rhizosphere. Here, using two different soil types (sand, soil), we provide an original example of the impact of domestication and crop evolution on root exudate composition through metabolite profiling of root exudates for a panel of 10 wheat genotypes that correspond to the key steps in domestication of tetraploid wheat (wild emmer, emmer, durum wheat). Our data show that soil type can dramatically affect the composition of root exudates in the rhizosphere. Moreover, the composition of the rhizosphere metabolites is associated with differences among the genotypes of the wheat domestication groups, as seen by the high heritability of some of the metabolites. Overall, we show that domestication and breeding have had major effects on root exudates in the rhizosphere, which suggests the adaptive nature of these changes. Keywords: domestication, root exudates, wheat, tetraploid wheat, Triticum turgidum, metabolites, rhizosphere INTRODUCTION Domestication has shaped the genome of crop plants to satisfy human needs for adaptation to agroecosystems. Recent studies have shown that this process had profound phenotypic consequences far beyond the few traits of the domestication syndrome, which also involved genome-wide transcriptomic and metabolomic changes (Bellucci et al., 2014; Beleggia et al., 2016). Considering the crucial role of root-system and rhizosphere interactions for plant adaptation (in relation to the major changes in soil management associated with cultivation), one of the major questions is whether and how domestication and breeding have had any impact on these phenomena (Bulgarelli et al., 2015; Gioia et al., 2015; Kuijken et al., 2015). Indeed, a series of complex chemical, physical and biological interactions takes place between roots and their surrounding environment. Plants contribute to these interactions by secretion of an enormous range of metabolites from their roots into the surrounding soil (Badri and Vivanco, 2009). These root exudates are generally classified into two classes of metabolites: high molecular weight exudates, which contain polysaccharides and proteins; and low molecular weight metabolites, which include amino acids, organic acids, sugars, phenolics, and various secondary metabolites (Badri and Vivanco, 2009). Rhizosphere biology has recognized the biological importance of root exudates in the mediation of interactions with other plants and with microbes, in terms of competing roots Frontiers in Plant Science | www.frontiersin.org 1 December 2017 | Volume 8 | Article 2124 Iannucci et al. Domestication of Root Exudates in Tetraploid Wheat 1. Are there differences in root exudate composition that suggest genetic diversity of root exudates that is potentially relevant in the conditioning of the rhizosphere composition? 2. If there is indeed this diversity, are there any differences that suggest differential adaptation between subspecies that are known to have undergone different selection pressures associated with the diverse intensification between wild early wheat domesticates and modern durum wheat? and pathogenic and non-pathogenic microbes and invertebrates (Pangesti et al., 2013). Hence, root exudates provide a source of allelochemicals that can mediate plant-to-plant interactions (Fragasso et al., 2013), and as such, they represent chemical information that can influence vital physiological processes (e.g., respiration, protein biosynthesis, photosynthesis, cell division and elongation) (Field et al., 2007). At the same time, these allelochemicals provide the molecular basis for plant–microbe interactions in the rhizosphere (Bais et al., 2006) that are responsible for plant health and growth (e.g., defense against diseases, facilitation of nutrient acquisition) (Pérez-Jaramillo et al., 2016). The biological significance of these processes helps us to understand why plants sustain significant carbon costs to maintain the processes of root exudation (Uren, 2007). Furthermore, in Arabidopsis thaliana, possible connections have been highlighted between changes in root architecture and plantinfluenced chemical changes in the rhizosphere microbiome diversity (Micallef et al., 2009). Dissimilarities in root architecture between modern varieties and their wild relatives have been reported for several crops (Pérez-Jaramillo et al., 2016), and recently, Gioia et al. (2015) described the impact of domestication of tetraploid wheat on its shoot and root phenotypic architecture. Increasing evidence indicates the potential influence of soil type on growth investment and rhizosphere-associated metabolites (Kuijken et al., 2015). At the same time, several indications suggest that different genotypes of the same species can promote different rhizosphere compositions (Bulgarelli et al., 2015). Root exudates have a major role in the mobilization of soluble nutrients in the rhizosphere (Carvalhais et al., 2011), and the release into the rhizosphere of diverse organic materials that can influence the soil structure (Traoré et al., 2000). In addition, root exudates contain allelochemicals of biological significance to the rhizosphere (Bertin et al., 2003; Iannucci et al., 2013), and increasing evidence suggests that root exudates initiate and modulate the dialog between roots and soil microbes (Badri and Vivanco, 2009). A major question here is thus how much different plant genotypes and populations contribute to genetic d (...truncated)