The sorghum (Sorghum bicolor) Brown midrib 30 (Bmr30) gene encodes a chalcone isomerase required for cell wall lignification

Authors: Tetreault, Hannah; Gries, Tammy; LIU, SARAH - University Of Wisconsin; Toy, John; Xin, Zhanguo; VERMERRIS, WILFRED - University Of Wisconsin; RALPH, JOHN - University Of Florida; Funnell-Harris, Deanna; Sattler, Scott

Submitted to: Frontiers in Plant Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/19/2022
Publication Date: 10/19/2021
Citation: Tetreault, H.M., Gries, T.L., Liu, S., Toy, J.J., Xin, Z., Vermerris, W., Ralph, J., Funnell-Harris, D.L., Sattler, S.E. 2021. The sorghum (Sorghum bicolor) Brown midrib 30 (Bmr30) gene encodes a chalcone isomerase required for cell wall lignification. Frontiers in Plant Biology. 12:1-18. https://doi.org/10.3389/fpls.2021.732307.
DOI: https://doi.org/10.3389/fpls.2021.732307

Interpretive Summary: In the US, sorghum serves as an important forage crop for livestock, and it also is being developed as a bioenergy crop. Energy, biofuels and renewable chemicals can be produced from plant cell walls, which are composed of three main components, cellulose, hemicellulose and lignin. Lignin acts like glue holding the other cell wall components together, which makes the cellulose and the hemicellulose resistant to breakdown into their sugar subunits either in livestock digestive systems or cellulosic biofuel production. The brown midrib (bmr) mutants have long been associated with plants impaired in their ability to synthesize lignin. To understand how the bmr30 mutant affects lignin synthesis and cell walls, the Bmr30 gene was identified through next-generation sequencing and shown to encode an enzyme chalcone isomerase. This enzyme is involved in flavonoid synthesis, which is responsible for red and purple pigments of plants. Bmr30 showed the interconnection between plant pigmentation and lignin through a compound called tricin, which has recently been shown to be a component of lignin in grasses like sorghum. Overall, this study demonstrates an important link between two plant biochemical pathways, and provides a new way to reduce lignin in sorghum for improved forage, bioenergy and green chemistry utilization.

Technical Abstract: In sorghum (Sorghum bicolor) and other C4 grasses, brown midrib (bmr) mutants have long been associated with plants impaired in their ability to synthesize lignin. The Bmr30 gene, identified using a bulk segregant analysis and next-generation sequencing, was determined to encode a chalcone isomerase. Two independent mutations within this gene confirmed that loss of its function was responsible for the brown leaf midrib phenotype and reduced lignin concentration. Loss of the Bmr30 gene function, as shown by histochemical staining of leaf midrib and stalk sections, resulted in altered cell wall composition. Bmr30 mutations had reduced chalcone isomerase activity, inhibiting the conversion of hydroxychalcone to flavanone, consistent with its function in flavonoid biosynthesis. The stover of bmr30 mutant accumulated up to 20 times higher levels soluble p-coumaric acid than the levels in wild-type (WT) stover; p-coumaroyl-CoA is a key intermediate involved in both flavonoid and monolignol biosynthesis. The level of the flavone lignin monomer tricin was reduced 20-fold in the stem relative to WT, and to undetectable levels in the leaf tissue in which the novel flavone naringenin appeared to be incorporated. Bmr30 is therefore revealed to involve a mutation in a phenylpropanoid biosynthetic gene that is key to the interconnection between flavonoids and monolignols, both of which are utilized for lignin synthesis in the grasses.