Abstract
Gln is a key player in plant metabolism. It is one of the major free amino acids that is transported into the developing seed and is central for nitrogen metabolism. However, Gln natural variation and its regulation and interaction with other metabolic processes in seeds remain poorly understood. To investigate the latter, we performed a metabolic genome-wide association study (mGWAS) of Gln-related traits measured from the dry seeds of the Arabidopsis (Arabidopsis thaliana) diversity panel using all potential ratios between Gln and the other members of the Glu family as traits. This semicombinatorial approach yielded multiple candidate genes that, upon further analysis, revealed an unexpected association between the aliphatic glucosinolates (GLS) and the Gln-related traits. This finding was confirmed by an independent quantitative trait loci mapping and statistical analysis of the relationships between the Gln-related traits and the presence of specific GLS in seeds. Moreover, an analysis of Arabidopsis mutants lacking GLS showed an extensive seed-specific impact on Gln levels and composition that manifested early in seed development. The elimination of GLS in seeds was associated with a large effect on seed nitrogen and sulfur homeostasis, which conceivably led to the Gln response. This finding indicates that both Gln and GLS play key roles in shaping the seed metabolic homeostasis. It also implies that select secondary metabolites might have key functions in primary seed metabolism. Finally, our study shows that an mGWAS performed on dry seeds can uncover key metabolic interactions that occur early in seed development.
Highlights
Glutamine (Gln) is a free amino acid (FAA) that belongs to the glutamate family, which includes glutamate (Glu), gamma-aminobutyric acid (GABA), proline (Pro), and arginine (Arg)(Skokut et al, 1978; Majumdar et al, 2016; Okumoto et al, 2016)
Our results strongly suggest that an interaction between Gln and GLS plays a key role in seed metabolic homeostasis
We used that data to assess the natural variation among only the proteogenic FAAs in the Glu family: i.e., Glu, Pro, Gln, and Arg
Summary
(Skokut et al, 1978; Majumdar et al, 2016; Okumoto et al, 2016) This amino acid family plays a key role in plant cell core metabolism by providing an entry point for inorganic nitrogen. Gln plays an important role in seed metabolism; as one of the main nitrogen carriers, it is transported via the xylem and phloem to sink tissues, including developing seeds (Zhang et al., 2010; Zhang et al, 2015; Besnard et al, 2016). A study of maturing Brassica napus seeds showed that embryos import nitrogen in the form of amino acids (mainly Gln and alanine) to synthesize other amino acids via transamination/deamination reactions and incorporation into seed storage proteins (SSP) (Schwender et al, 2006). Studies in Arabidopsis have shown that Gln levels are highly elevated prior to the onset of SSP synthesis (Baud et al., 2002; Fait et al, 2006) and drop substantially during seed maturation (Fait et al, 2006)
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