Understanding the chemical foundation and genetic mechanism of the black grain trait in quinoa by integrating metabolome and transcriptome analyses

Abstract

Quinoa (Chenopodium quinoa Willd.) cultivars that produce black grains are thought to be more nutritious and contain powerful antioxidant properties, but little is known about the chemical foundation and the genetic mechanism behind this trait. In this research, widely-targeted metabolome and transcriptome analyses were employed to unveil the chemical and genetic differences between black and white quinoa cultivars. A total of 157 differentially expressed metabolites were found in the black and white quinoa cultivars. The tannins and flavonoids were present at high levels in the black quinoa grains. The tannins comprised 13 proanthocyanins, all of which could barely be detected in white grains. Proanthocyanidins are suggested to cause the black grain trait in Arabidopsis thaliana and Brassica species and are thought to produce the black grain trait, while contributing to antioxidant activity, in black grain quinoa. A total of 4620 differentially expressed unigenes were identified in the black and white quinoa grains. Structural genes associated with proanthocyanin biosynthesis, particularly DFR, LAR, LDOX and ANR, were more highly expressed in black than white grains. Genes involved in the betalain biosynthetic pathway, which competes with anthocyanin biosynthesis, showed relatively lower levels of expression in black grains. Two MYB and one MYC transcription factor related to the phenylpropane metabolic pathway displayed higher expression levels in black grains, while BvMYB1, associated with betalain biosynthesis, was not detected. This study suggested that the accumulation of proanthocyanins produces the black grain trait in quinoa, and the activation of transcription factors triggers the proanthocyanidin biosynthesis pathway.