Polarized pectin accumulation regulates differential hypocotyl elongation at the dark-to-light transition.

Abstract

As one of the most influential environmental factors, light fundamentally shapes plant physiology and growth traits.^{1,2,3,4,5,6,7,8,9,10} The hypocotyl is critical for the morphological establishment of the seedling, and its length displays remarkable plasticity upon perception of changes in the light conditions.^{4,5,8,9,10,11,12,13,14,15} Although remodeling of the primary cell walls is well-documented to play an important role in hypocotyl growth, how the hypocotyl elongation rate is swiftly repressed at the dark-to-light transition remains elusive.^{16,17,18,19,20,21,22,23,24,25} Here, we show that expression of an Arabidopsis microRNA, miR775, is quickly inhibited at the dark-to-light transition by ELONGATED HYPOCOTYL 5 (HY5), an essential negative regulator of hypocotyl elongation that is degraded in the dark and accumulates in the light.²⁶ We found that this repression allows the miR775-targeted GALACTOSYLTRANSFERASE 9 (GALT9) to accumulate in the transverse walls of hypocotyl cells within 10 min of light exposure. Genetic analysis coupled with time-lapse photography demonstrates that GALT9 is both necessary and sufficient for controlling the differential hypocotyl growth rates at the dark-to-light transition. Immunohistochemical analysis and coherent Raman microscopy reveal that the polarized accumulation of GALT9 confers a rapid increase in the pectin content of the transverse walls. Atomic force microscopy (AFM) confirms that polarized pectin accumulation mediated by the HY5-miR775-GALT9 repression cascade correlates with rapid asymmetric increases in cell wall rigidity and hence decreases in cell elongation in the light. Together, these findings add new insights into the cellular mechanism governing differential hypocotyl growth at the dark-to-light transition and should also benefit the general understanding of polarized cell expansion in plants.