Brittle stalk 2 encodes a putative glycosylphosphatidylinositol-anchored protein that affects mechanical strength of maize tissues by altering the composition and structure of secondary cell walls

Abstract

A spontaneous maize mutant, brittle stalk-2 (bk2-ref), exhibits dramatically reduced tissue mechanical strength. Reduction in mechanical strength in the stalk tissue was highly correlated with a reduction in the amount of cellulose and an uneven deposition of secondary cell wall material in the subepidermal and perivascular sclerenchyma fibers. Cell wall accounted for two-thirds of the observed reduction in dry matter content per unit length of the mutant stalk in comparison to the wildtype stalk. Although the cell wall composition was significantly altered in the mutant in comparison to the wildtype stalks, no compensation by lignin and cell wall matrix for reduced cellulose amount was observed. We demonstrate that Bk2 encodes a Cobra-like protein that is homologous to the rice Bc1 protein. In the bk2-ref gene, a 1 kb transposon-like element is inserted in the beginning of the second exon, disrupting the open reading frame. The Bk2 gene was expressed in the stalk, husk, root, and leaf tissues, but not in the embryo, endosperm, pollen, silk, or other tissues with comparatively few or no secondary cell wall containing cells. The highest expression was in the isolated vascular bundles. In agreement with its role in secondary wall formation, the expression pattern of the Bk2 gene was very similar to that of the ZmCesA10, ZmCesA11, and ZmCesA12 genes, which are known to be involved in secondary wall formation. We have isolated an independent Mutator-tagged allele of bk2, referred to as bk2-Mu7, the phenotype of which is similar to that of the spontaneous mutant. Our results demonstrate that mutations in the Bk2 gene affect stalk strength in maize by interfering with the deposition of cellulose in the secondary cell wall in fiber cells.

Silencing CHALCONE SYNTHASE in Maize Impedes the Incorporation of Tricin into Lignin and Increases Lignin Content

“…Similarly, the reduced cellulose content in mature stems of the spontaneous maize mutant brittle stalk2 (bk2), disrupted in a gene orthologous to the BC1 gene in rice, goes along with a marked enrichment in lignin deposition, resulting in brittleness of all aerial plant organs (Sindhu et al, 2007). In agreement with its corresponding mutant in rice, bk2 and wild-type plants were indistinguishable in all aspects of plant growth and development (Ching et al, 2006;Sindhu et al, 2007). In brachypodium, the dwarf spaghetti1 (spa1) mutant presents a unique phenotype combining brittleness with increased elasticity of the internodes (Timpano et al, 2015).…”

Molecular characterization, expression pattern, and function analysis of the OsBC1L family in rice

“…So far, several members of the COBRA gene family have been found to be involved in the synthesis of cellulose, which is responsible for the expansion and formation of the cell wall (Schindelman et al 2001;Li et al 2003;Brown et al 2005;Ching et al 2006). In addition, osbc1l4 shows similar mutant phenotype and expression pattern with some cellulose synthase genes (OsCESA4, OsCESA7, and OsCESA9; Tanaka et al 2003).…”

“…AtCOBL9 is required for tip-directed growth in root hair development in Arabidopsis (Parker et al 2000;Jones et al 2006). The rice brittle culm1 (bc1) mutant and the maize brittle stalk 2 (bk2) mutant were found to have mutations in the putative orthologs of AtCOBL4 that affected the mechanical strength of plant tissues and secondary cell wall biosynthesis Ching et al 2006;Sindhu et al 2007). Moreover, recent research has indicated that ZmBk2L1 is required for the root hair development in maize (Hochholdinger et al 2008).…”

Extent of genotypic variation for maize cell wall bioconversion traits across environments and among hybrid combinations

“…Specifically, hybrid genotypes displayed a greater accumulation of cell wall material (CW) in stem tissues and exhibited a higher proportion of lignin (Lig, Lig/CW) and cellulose (Cel/CW) in their cell walls. Presumably, these structural and constitutional adaptations would lead to improved stalk mechanical-strength; the latter deemed necessary to sustain the increased growth rates and yields typical of hybrid maize (Appenzeller et al 2004;Ching et al 2006). These compositional contrasts, however, did not appreciably alter the prevalent inter-relations that exist between cell wall compositional characters and biomass enzymatic convertibility.…”