UV-induced reactive oxygen species and transcriptional control of 3-deoxyanthocyanidin biosynthesis in black sorghum pericarp

Authors: SCHUMAKER, BROOKLYN - Texas A&M University; FEDENIA, LAUREN - Texas A&M University; Klein, Robert; MANDAL, SABYASACHI - Texas A&M University; Dykes, Linda; Gladman, Nicholas; ROONEY, WILLIAMS - Texas A&M University; Burson, Byron; KLEIN, PATRICIA - Texas A&M University

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/10/2024
Publication Date: 10/7/2024
Citation: Schumaker, B., Fedenia, L., Klein, R.R., Mandal, S., Dykes, L., Gladman, N.P., Rooney, W., Burson, B.L., Klein, P. 2024. UV-induced reactive oxygen species and transcriptional control of 3-deoxyanthocyanidin biosynthesis in black sorghum pericarp. Frontiers in Plant Science. 15. Article 1451215. https://doi.org/10.3389/fpls.2024.1451215.
DOI: https://doi.org/10.3389/fpls.2024.1451215

Interpretive Summary: The black grain trait in sorghum has notable value in the specialty food and nutraceutical industries. The black coloration of the grain is associated with a group of rare compounds valued for use as natural food colorants, food preservatives, antioxidant food additives, and as compounds cytotoxic to cancer cells. In the present study, we found that UV light increases reactive oxygen species in the grain which leads to the accumulation of these health-associated compounds in the seed. Based on the unique upregulation of a suite of genes in black seed, we postulate that UV light produces a stress in black sorghum grain tissue, which triggers the seed to turn black providing a sunscreen to the harmful effects of UV light. This study is critical for breeders and sorghum growers to pick the best environment for growing the blackest sorghum with the highest level of the health-associated compounds in the black seed.

Technical Abstract: Black pericarp sorghum has notable value due to the biosynthesis of 3-deoxyanthocyanidins (3-DOAs), a rare class of bioactive polyphenols valued as antioxidant food additives and as bioactive compounds with cytotoxicity to human cancer cells. In this study, a metabolic and transcriptomic study of black sorghum pericarp was conducted to ascertain the cascade of cellular events leading to the activation of 3-DOA biosynthesis in black sorghum pericarp. Prolonged exposure of pericarp during grain maturation to high-fluence ultraviolet (UV) light resulted in elevated levels of reactive oxygen species (ROS) and the activation of 3-DOA biosynthesis in pericarp tissues directly exposed to UV. Associated with 3-DOA biosynthesis was the transcriptional activation of specific family members of early and late flavonoid biosynthesis pathway genes. A working model of UV-induced 3-DOA biosynthesis in black pericarp shared features of plant immunity associated with pathogen attack or mechanical wounding, which included ROS biosynthesis/signaling, and the transcriptional activation of receptor kinases leading to expression of transcription factors (TFs) including NAC, WRKY, bHLH, AP2, and C2H2 Zinc finger domain. The cascade signaling resulted in downstream activation of defense-related pathways and the biosynthesis of secondary metabolites including the 3-DOAs. Promoter analysis of genes highly correlated with 3-DOA biosynthesis in black pericarp were enriched in MYB and HHO5/ ARR-B motifs. Light microscopy studies of black pericarp tissues suggest that 3-DOAs are predominantly localized in the epicarp and are associated with the cell wall.