Cellulose Deficiency Is Enhanced on Hyper Accumulation of Sucrose by a H⁺-Coupled Sucrose Symporter

Abstract

(C.R.S.).In order to understand factors controlling the synthesis and deposition of cellulose, we have studied the Arabidopsis (Arabidopsis thaliana) double mutant shaven3 shaven3-like1 (shv3svl1), which was shown previously to exhibit a marked cellulose deficiency. We discovered that exogenous sucrose (Suc) in growth medium greatly enhances the reduction in hypocotyl elongation and cellulose content of shv3svl1. This effect was specific to Suc and was not observed with other sugars or osmoticum. Live-cell imaging of fluorescently labeled cellulose synthase complexes revealed a slowing of cellulose synthase complexes in shv3svl1 compared with the wild type that is enhanced in a Suc-conditional manner. Solid-state nuclear magnetic resonance confirmed a cellulose deficiency of shv3svl1 but indicated that cellulose crystallinity was unaffected in the mutant. A genetic suppressor screen identified mutants of the plasma membrane Suc/H + symporter SUC1, indicating that the accumulation of Suc underlies the Suc-dependent enhancement of shv3svl1 phenotypes. While other cellulose-deficient mutants were not specifically sensitive to exogenous Suc, the feronia (fer) receptor kinase mutant partially phenocopied shv3svl1 and exhibited a similar Suc-conditional cellulose defect. We demonstrate that shv3svl1, like fer, exhibits a hyperpolarized plasma membrane H + gradient that likely underlies the enhanced accumulation of Suc via Suc/H + symporters. Enhanced intracellular Suc abundance appears to favor the partitioning of carbon to starch rather than cellulose in both mutants. We conclude that SHV3-like proteins may be involved in signaling during cell expansion that coordinates proton pumping and cellulose synthesis.

Transient alkalinization of the leaf apoplast stiffens the cell wall during onset of chloride salinity in corn leaves

“…Maize cell walls were prepared and analyzed essentially as described (56). Samples (1 mg of lyophilized grinded powder) were hydrolyzed in diluted H2SO4 for one hour at 121°C.…”

A dual mechanism of cellulose deficiency in shv3svl1

“…Our recent work with the double mutant shv3svl1 has shown that intracellular sucrose can regulate carbon partitioning between cellulose and starch. 3 We found that shv3svl1 exhibits a sucrose-conditional cellulose deficiency that is due to enhanced sucrose uptake in the mutant (Fig. 1A).…”

“…3 However, assigning a biochemical function to SHV3-like proteins has been challenging. While they exhibit sequence similarity to glycerophosphodiester phosphodiesterase (GDPD) and phosphatidylinositol-specific phospholipase C (PI-PLC) enzymes, they lack several conserved active site amino acids of these enzymes, and attempts to demonstrate either activity have been unsuccessful.…”

“…While they exhibit sequence similarity to glycerophosphodiester phosphodiesterase (GDPD) and phosphatidylinositol-specific phospholipase C (PI-PLC) enzymes, they lack several conserved active site amino acids of these enzymes, and attempts to demonstrate either activity have been unsuccessful. 3,13 The localization of SHV3-like proteins may provide a general hint as to their function. SHV3-like proteins possess glycosylphosphatidylinositol (GPI) anchors that direct their localization to the outer leaflet of the PM.…”

Inter‐relationships between the heterotrimeric Gβ subunit AGB1, the receptor‐like kinase FERONIA, and RALF1 in salinity response

“…This discrepancy is likely attributable to the different growth conditions, particularly sucrose concentrations used in the growth media in different experiments. The fer mutant is hypersensitive to growth inhibition by external sucrose and shows decreased cellulose content when grown under high sucrose concentrations (Yeats, Sorek, Wemmer, & Somerville, ) that may contribute to loss of cell wall integrity. We observed that at the low sucrose concentration used in our assays (0.5 mM sucrose), the fer mutant is able to grow some elongated root hairs (Figure S7) whereas at 1% (29.2 mM) sucrose, only burst root hairs were observed in fer (Figure S1).…”