Abstract
Plant tissues that require structural rigidity synthesize a thick, strong secondary cell wall of lignin, cellulose and hemicelluloses in a complicated bridged structure. Master regulators of secondary wall synthesis were identified in dicots, and orthologs of these regulators have been identified in monocots, but regulation of secondary cell wall formation in monocots has not been extensively studied. Here we demonstrate that the rice transcription factors SECONDARY WALL NAC DOMAIN PROTEINs (SWNs) can regulate secondary wall formation in rice (Oryza sativa) and are potentially useful for engineering the monocot cell wall. The OsSWN1 promoter is highly active in sclerenchymatous cells of the leaf blade and less active in xylem cells. By contrast, the OsSWN2 promoter is highly active in xylem cells and less active in sclerenchymatous cells. OsSWN2 splicing variants encode two proteins; the shorter protein (OsSWN2S) has very low transcriptional activation ability, but the longer protein (OsSWN2L) and OsSWN1 have strong transcriptional activation ability. In rice, expression of an OsSWN2S chimeric repressor, driven by the OsSWN2 promoter, resulted in stunted growth and para-wilting (leaf rolling and browning under normal water conditions) due to impaired vascular vessels. The same OsSWN2S chimeric repressor, driven by the OsSWN1 promoter, caused a reduction of cell wall thickening in sclerenchymatous cells, a drooping leaf phenotype, reduced lignin and xylose contents and increased digestibility as forage. These data suggest that OsSWNs regulate secondary wall formation in rice and manipulation of OsSWNs may enable improvements in monocotyledonous crops for forage or biofuel applications.
Highlights
The secondary wall is a plant-specific, stiff and thick cell wall composed of lignin, cellulose and hemicelluloses in a complicated bridged structure
OsSWN PROMOTERS ARE ACTIVE IN RICE XYLEM CELLS To analyze how secondary wall formation in rice is regulated and to determine which promoter is most suitable for the manipulation of rice secondary walls, we surveyed rice NAC transcription factor genes that are similar to Arabidopsis NSTs, which act as master regulators of secondary wall formation
The OsSWN2 promoter was active in bundle sheath, including vascular vessels in the xylem (Figures 1C,E,G) and the OsSWN1 promoter was preferentially active in several layers of sclerenchymatous cells beneath the epidermis in addition to the bundle sheath (Figures 1B,D,F)
Summary
The secondary wall is a plant-specific, stiff and thick cell wall composed of lignin, cellulose and hemicelluloses in a complicated bridged structure. Monocots are traditionally important forage crops; high lignin content results in poor digestibility. Several monocot plants, such as miscanthus and switchgrass, have recently emerged as potential feedstock crops for cellulosic biofuels (Schmer et al, 2008); high lignin can adversely affect the conversion of cellulose to fermentable sugars. High arabinoxylan and xylan contents in primary and secondary cell walls of monocots may require an additional xylose fermentation after saccharification. Pyrolytic biofuels applications may benefit from high lignin content, which increases energy density. Elucidation of the mechanisms regulating secondary wall biosynthesis in monocots has the potential to improve crops for multiple important applications
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