Genetic analysis of the metabolome exemplified using a rice population

Abstract

Plant metabolites are crucial for both plant life and human nutrition. Despite recent advance in metabolomics, the genetic control of plant metabolome remains largely unknown. Here, we performed a genetic analysis of the rice metabolome that provided over 2,800 highly resolved metabolic quantitative trait loci for 900 metabolites. Distinct and overlapping accumulation patterns of metabolites were observed and complex genetic regulation of metabolism was revealed in two different tissues. We associated 24 candidate genes to various metabolic quantitative trait loci by data mining, including ones regulating important morphological traits and biological processes. The corresponding pathways were reconstructed by updating in vivo functions of previously identified and newly assigned genes. This study demonstrated a powerful tool and provided a vast amount of high-quality data for understanding the plasticity of plant metabolome, which may help bridge the gap between the genome and phenome.Oryza sativa | recombinant inbred line | metabolic profiling | gene function P lants are highly enriched in specific metabolites with extensive quantitative and qualitative variation both among and within different plant species (1, 2). Understanding the genes involved in metabolism and dissection of the metabolic pathway are essential to improve plant adaptation to environmental stresses, to improve food quality, and to increase crop yield. Recent advance in metabolomics together with transcriptomics and gene/metabolite coexpression networks analyses has proven to be powerful in functional gene elucidation, although it is specified for transcriptionally regulated genes with limited throughput so far.A large number of metabolic quantitative trait loci (mQTLs) have been identified based on linkage maps using low-density markers, such as restriction fragment length polymorphism and simple sequence repeat markers (3-5). However, the underlying genes remain elusive because of the relatively low resolution of the genetic maps associated with these markers. In addition to the species-specific accumulation of the metabolites in plant, tissue-specific accumulation of metabolites, especially secondary metabolites, are of special importance for the survival and adaptation of plant species. Although the genetics of tissue-specific regulation gene expression across the tissues as revealed by expression quantitative trait locus analysis is one of the major topics in animal and plant, the genetics of tissue-specific metabolome is somewhat overlooked (5, 6). Despite the advance in metabolomics (2), the genetic control of the plant metabolome is still largely unknown.Moreover, the elucidation of pathways for the biosyntheses of important metabolites such as amino acids, lysophosphatidylcholines (LPCs), and flavonoids, and the variation and the genetics control of them are vital for both basic research and breeding application. For example, flavonoids are one of the main groups of secondary metabolites that play important roles in a number of biolo...

Evolutionarily Distinct BAHD N-acyltransferases are Responsible for Natural Variation of Aromatic Amine Conjugates in Rice

“…Unlike complex quantitative traits (such as flowering time) for which little epistasis has been detected (Buckler et al, 2009;Morris et al, 2013;Zuo and Li, 2014), variation in levels of metabolites, especially specialized metabolites, is predominately controlled by epistasis in both RILs (Kliebenstein et al, 2002;Loudet et al, 2003;Calenge et al, 2006;Lisec et al, 2008;Rowe et al, 2008;Gong et al, 2013) and natural populations (Chan et al, 2011;Chen et al, 2014;Sauvage et al, 2014;Dong et al, 2015;Matsuda et al, 2015). Similar results were observed between some of the loci identified in our study (Supplemental Figure 5 and Supplemental Table 3).…”

“…Eleven rice phenolamides in this study refer to different combinations of CoA-thioesters and amine moieties. combined metabolite-based linkage and association studies have provided powerful forward-genetic strategies for dissecting the genetic and biochemical bases of metabolism in plants (Riedelsheimer et al, 2012;Gong et al, 2013;Chen et al, 2014;Wen et al, 2014Wen et al, , 2015Alseekh et al, 2015;Matsuda et al, 2015). As for the BAHD family of enzymes in rice, OsAT1 has been reported to be involved in responses to rice blight and blast (Mori et al, 2007).…”

Identification and Mode of Inheritance of Quantitative Trait Loci for Secondary Metabolite Abundance in Tomato

“…While only a handful of studies have used broad genetic crosses to identify mQTLs for a broad range of secondary metabolites (Kliebenstein et al, 2001a(Kliebenstein et al, , 2001bKeurentjes et al, 2006;Morreel et al, 2006;Khan et al, 2012;Matsuda et al, 2012;Routaboul et al, 2012;Gong et al, 2013;Wahyuni et al, 2014) and previous studies have largely been focused on Arabidopsis, considerable research has been focused on defining QTLs for volatile organic compounds from tomato fruit (Tieman et al, 2006;Mathieu et al, 2009;Mageroy et al, 2012;Rambla et al, 2014) and acyl-sugars in tomato leaf trichomes (Schilmiller et al, 2012(Schilmiller et al, , 2010. In addition, the levels of primary metabolites have been evaluated in multiple different breeding populations (Schauer et al, , 2008Do et al, 2010) as well as in association mapping panels (Sauvage et al, 2014).…”

Metabolomics as a Tool in Agriculture

“…Several studies have been carried out in this crop, where the main objective has been to characterize cultivars through the metabolic proiles obtained from several plant structures, mainly the leaf, using capillary electrophoresis coupled with mass spectrometry [28]. This crop has also been subject of studies where genetic and metabolic studies are combined using techniques such as GC-FID, GC-MS and GC-TOF-MS, in what is called functional genomics [29,30]. Naturally, in modern times, studies on transgenic individuals could not be absent, where their metabolic proiles have been determined [31].…”