Metabolomics approach to understand mechanisms of ß-N-Oxalyl-L-a,ß-diaminopropionic Acid (ß-ODAP) biosynthesis in grass pea (Lathyrus sativus L.)

Authors: LIU, FENGJUAN - Northwest Agricultural & Forestry University; JIAO, CHENGJIN - Tianshui Normal University; BI, CHUNXIAO - Northwest Agricultural & Forestry University; XU, QUANLE - Northwest Agricultural & Forestry University; CHEN, PENG - Northwest Agricultural University; HEUBERGER, ADAM - Colorado State University; Krishnan, Hari

Submitted to: Journal of Agricultural and Food Chemistry
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/7/2017
Publication Date: 11/7/2017
Publication URL: http://handle.nal.usda.gov/10113/5864301
Citation: Liu, F., Jiao, C., Bi, C., Xu, Q., Chen, P., Heuberger, A.L., Krishnan, H.B. 2017. Metabolomics approach to understand mechanisms of ß-N-Oxalyl-L-a,ß-diaminopropionic Acid (ß-ODAP) biosynthesis in grass pea (Lathyrus sativus L.). Journal of Agricultural and Food Chemistry. 65(47):10206-10213. https://doi.org/10.1021/acs.jafc.7b04037.

Interpretive Summary: Legumes are inexpensive source of highly nutritious and well-balanced human dietary protein. Among them, grass pea is widely cultivated as an edible and forage crop in arid and semi-arid regions. Consumption of grass pea as a main or sole diet for several months causes lathyrism, a neurodegenerative syndrome that results in the paralysis of lower limbs. The use of grass pea is limited by the presence of a neurotoxin (ß-ODAP) in the seeds. In this study we have performed systematic identification and quantification of the small molecule metabolic products of grass pea during a range of growth and development periods. Information provided in this manuscript should enable researchers to target key biological processes to lower the accumulation of the neurotoxin in grass pea seeds. Neurotoxin-free grass pea should drastically reduce the incidence of lathyrism encountered in people living in drought-prone areas of Asia and Africa and may open new markets in the U.S.

Technical Abstract: Grass pea (Lathyrus sativus L.) is an important food crop for human health and food security, however its seed contains high levels of the neurotoxin ß-ODAP. Previous work demonstrated that ß-ODAP content changes during early developmental stages of grass pea. Further, the regulation and mechanisms of ß-ODAP synthesis and accumulation have only been partially described. Here, a study was performed to identify metabolic processes associated with ß-ODAP synthesis using a metabolomics approach. GC-MS metabolomics was performed on seedlings at 2, 6, and 25 days after sowing. A total of 141 metabolites were detected among the three time points representing much of grass pea primary metabolism, including amino acids, carbohydrates, purines, and others. Principal component analysis revealed unique metabolite profiles of grass pea tissues among the three time points. Fold change, hierarchical clustering, and orthogonal projections to latent structures-discriminate analyses, and biochemical pathway ontologies were used to characterize co-variance of metabolites with ß-ODAP content. The data indicates that alanine and nitrogen metabolism, cysteine and sulfur metabolism, purine, pyrimidine and pyridine metabolism were associated with ß-ODAP metabolism. Further, the metabolite data was validated in two additional experiments that exogenously applied different amino acids and nitrogen metabolites to evaluate effects on ß-ODAP levels. All amine/amino acid foliar treatments reduced seedling ß-ODAP concentration, and purine/pyrimidine combinations also influenced ß-ODAP, whereby biosynthesis appears more sensitive to pyrimidine than purine content. Taken together, these data support that that cysteine and sulfur metabolism may regulate ß-ODAP biosynthesis, while nitrogen status, especially the ß-alanine group from uracil degradation, provides signals to determine ß-ODAP content. These results reveal the metabolite profiles in grass pea development and provide insights into mechanisms of ß-ODAP accumulation and degradation.