Abstract
Bast (phloem) fibers, tension wood fibers, and other cells with gelatinous-type secondary walls are rich in crystalline cellulose. In developing bast fibers of flax (Linum usitatissimum), a galactan-enriched matrix (Gn-layer) is gradually modified into a mature cellulosic gelatinous-layer (G-layer), which ultimately comprises most of the secondary cell wall. Previous studies have correlated this maturation process with expression of a putative β-galactosidase. Here, we demonstrate that β-galactosidase activity is in fact necessary for the dynamic remodeling of polysaccharides that occurs during normal secondary wall development in flax fibers. We found that developing stems of transgenic (LuBGAL-RNAi) flax with reduced β-galactosidase activity had lower concentrations of free Gal and had significant reductions in the thickness of mature cellulosic G-layers compared with controls. Conversely, Gn-layers, labeled intensively by the galactan-specific LM5 antibody, were greatly expanded in LuBGAL-RNAi transgenic plants. Gross morphology and stem anatomy, including the thickness of bast fiber walls, were otherwise unaffected by silencing of β-galactosidase transcripts. These results demonstrate a specific requirement for β-galactosidase in hydrolysis of galactans during formation of cellulosic G-layers. Transgenic lines with reduced β-galactosidase activity also had biochemical and spectroscopic properties consistent with a reduction in cellulose crystallinity. We further demonstrated that the tensile strength of normal flax stems is dependent on β-galactosidase-mediated development of the phloem fiber G-layer. Thus, the mechanical strength that typifies flax stems is dependent on a thick, cellulosic G-layer, which itself depends on β-galactosidase activity within the precursor Gn-layer. These observations demonstrate a novel role for matrix polysaccharides in cellulose deposition; the relevance of these observations to the development of cell walls in other species is also discussed.
Highlights
Bast fibers, tension wood fibers, and other cells with gelatinous-type secondary walls are rich in crystalline cellulose
A role for a tissue-specific b-galactosidase in fiber development was previously proposed based on transcript and protein expression patterns of a gene named LuBGAL1, whose expression coincides with the onset of fiber cell wall deposition in stems and hypocotyls (Roach and Deyholos, 2007, 2008; Hotte and Deyholos, 2008)
This expression pattern is correlated with a b-galactosidase that has been copurified with a tissuespecific galactan (i.e. rhamnogalacturonan I (RG-I) backbone with long galactan side chains) known to be deposited during secondary wall development in flax fibers (Gorshkova et al, 2004; Mikshina et al, 2009)
Summary
Bast (phloem) fibers, tension wood fibers, and other cells with gelatinous-type secondary walls are rich in crystalline cellulose. Gross morphology and stem anatomy, including the thickness of bast fiber walls, were otherwise unaffected by silencing of b-galactosidase transcripts These results demonstrate a specific requirement for b-galactosidase in hydrolysis of galactans during formation of cellulosic G-layers. The mechanical strength that typifies flax stems is dependent on a thick, cellulosic G-layer, which itself depends on b-galactosidase activity within the precursor Gn-layer These observations demonstrate a novel role for matrix polysaccharides in cellulose deposition; the relevance of these observations to the development of cell walls in other species is discussed. The galactan side chains undergo at least partial hydrolysis during fiber development; this is correlated with a high accumulation of free Gal in fiber-bearing tissues below the snap point (Mikshina et al, 2009). Partial hydrolysis of a tissue-specific galactan is closely correlated with the formation of the cellulose-rich cell wall of flax fibers. The expression of a b-galactosidase that acts on a tissuespecific galactan is closely correlated with fibers undergoing secondary wall thickening
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