The Sorghum (Sorghum bicolor) Brown Midrib 30 Gene Encodes a Chalcone Isomerase Required for Cell Wall Lignification.

Hannah M Tetreault,John Ralph,Deanna L Funnell-Harris,Wilfred Vermerris,Zhanguo Xin,Scott E Sattler,John Toy,Sarah Liu,Tammy Gries

doi:10.3389/fpls.2021.732307

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 brown midrib 30 (Bmr30) gene, identified using a bulk segregant analysis and next-generation sequencing, was determined to encode a chalcone isomerase (CHI). 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. In the bmr30 mutants, CHI activity was drastically reduced, and the accumulation of total flavonoids and total anthocyanins was impaired, which is consistent with its function in flavonoid biosynthesis. The level of the flavone lignin monomer tricin was reduced 20-fold in the stem relative to wild type, and to undetectable levels in the leaf tissue of the mutants. The bmr30 mutant, therefore, harbors 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.

Highlights

Sorghum bicolor is an economically important C4 grass, the fifth most important cereal crop in the world, which is grown as a grain, forage, sugar, and lignocellulosic bioenergy crop
This study demonstrated that the sorghum brown midrib 30 (Bmr30) locus encodes a chalcone isomerase (CHI), with loss of function affecting monolignol and flavonoid biosynthesis and lignin deposition
The brown midrib phenotype, which led to the isolation of the bmr30-1 mutant (Sattler et al, 2014), has long been linked to C4 grasses impaired in cell wall lignification (Jorgenson, 1931; Kuc and Nelson, 1964; Gee et al, 1968; Kuc et al, 1968)

Summary

Introduction

Sorghum bicolor is an economically important C4 grass, the fifth most important cereal crop in the world, which is grown as a grain, forage, sugar, and lignocellulosic bioenergy crop. Lignin is polymerized through radical coupling processes in which hydroxycinnamyl alcohols, mainly p-coumaryl, coniferyl, and sinapyl alcohols derived from monolignol biosynthesis, form radicals catalyzed by cell wall laccases and peroxidases. In addition to monolignol biosynthesis, the flavone tricin [5,7-dihydroxy-2-(4-hydroxy-3,5dimethoxyphenyl)-4H-chromen-4-one] was recently established as a lignin monomer in grass cell walls in which it potentially functions as a nucleation site for lignin polymerization (del Río et al, 2012; Lan et al, 2015, 2016a). This discovery linked together two branches of phenylpropanoid metabolism, monolignol and flavonoid biosynthesis, in grass lignification

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