Abstract
Lignin in Populus species is acylated with p-hydroxybenzoate. Monolignol p-hydroxybenzoyltransferase 1 (PHBMT1) mediates p-hydroxybenzoylation of sinapyl alcohol, eventually leading to the modification of syringyl lignin subunits. Angiosperm trees upon gravistimulation undergo the re-orientation of their growth along with the production of specialized secondary xylem, i.e., tension wood (TW), that generates tensile force to pull the inclined stem or leaning branch upward. Sporadic evidence suggests that angiosperm TW contains relatively a high percentage of syringyl lignin and lignin-bound p-hydroxybenzoate. However, whether such lignin modification plays a role in gravitropic response remains unclear. By imposing mechanical bending and/or gravitropic stimuli to the hybrid aspens in the wild type (WT), lignin p-hydroxybenzoate deficient, and p-hydroxybenzoate overproduction plants, we examined the responses of plants to gravitropic/mechanical stress and their cell wall composition changes. We revealed that mechanical bending or gravitropic stimulation not only induced the overproduction of crystalline cellulose fibers and increased the relative abundance of syringyl lignin, but also significantly induced the expression of PHBMT1 and the increased accumulation of p-hydroxybenzoates in TW. Furthermore, we found that although disturbing lignin-bound p-hydroxybenzoate accumulation in the PHBMT1 knockout and overexpression (OE) poplars did not affect the major chemical composition shifts of the cell walls in their TW as occurred in the WT plants, depletion of p-hydroxybenzoates intensified the gravitropic curving of the plantlets in response to gravistimulation, evident with the enhanced stem secant bending angle. By contrast, hyperaccumulation of p-hydroxybenzoates mitigated gravitropic response. These data suggest that PHBMT1-mediated lignin modification is involved in the regulation of poplar gravitropic response and, likely by compromising gravitropism and/or enhancing autotropism, negatively coordinates the action of TW cellulose fibers to control the poplar wood deformation and plant growth.
Highlights
As a sessile organism, the terrestrial plants evolve remarkable abilities in modulating their normal growth to cope with different environmental stresses
We discover that gravistimulation and mechanical bending strongly induce the expression of PHBMT1 and the accumulation of ligninbound pBAs in tension wood (TW) of poplar; whereas, paradoxically and interestingly, eliminating PHBMT1 and depleting lignin-bound pBAs appear to substantially enhance the stem curving of the plantlets upon gravistimulation; while the OE of PHBMT1 and hyperaccumulation of pBAs mitigate gravitropic response, evident with small stem secant bending angle
When 1-year-old hybrid aspen stems were bent for 10 days, qRT-PCR analysis with RNAs from the scrapped developing xylem revealed that the FLA9 transcripts were elevated approximately 800-fold in the developing xylem of the upper side of the bent stem, compared with that in the lower side of the bent stem, indicating the formation of TW at the upper side of the treated stem (Figure 2A)
Summary
The terrestrial plants evolve remarkable abilities in modulating their normal growth to cope with different environmental stresses. After the organ curves up, a phase of autotropic straightening or decurving starts at the tip and propagates downward, so that the curvature becomes concentrated at the base of the growth zone and steady (Stankovic et al, 1998b; Coutand et al, 2007; Bastien et al, 2013). This decurving process, i.e., the tendency of plants to recover straightness in the absence of any external stimulus is described as autotropism. The final set-point angle of an organ is achieved by a composite response of two tropisms, i.e., gravitropism and autotropism
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