An Arabidopsis quiescin-sulfhydryl oxidase regulates cation homeostasis at the root symplast–xylem interface

Abstract

A genetic screen of Arabidopsis 'activation-tagging' mutant collection based on tolerance to norspermidine resulted in a dominant mutant (par1-1D) with increased expression of the QSO2 gene (At1g15020), encoding a member of the quiescin-sulfhydryl oxidase (QSO) family. The par1-1D mutant and transgenic plants overexpressing QSO2 cDNA grow better than wild-type Arabidopsis in media with toxic cations (polyamines, Li þ and Na þ ) or reduced K þ concentrations. This correlates with a decrease in the accumulation of toxic cations and an increase in the accumulation of K þ in xylem sap and shoots. Conversely, three independent loss-of-function mutants of QSO2 exhibit phenotypes opposite to those of par1-1D. QSO2 is mostly expressed in roots and is upregulated by K þ starvation. A QSO2HGFP fusion ectopically expressed in leaf epidermis localized at the cell wall. The recombinant QSO2 protein, produced in yeast in secreted form, exhibits disulfhydryl oxidase activity. A plausible mechanism of QSO2 action consists on the activation of root systems loading K þ into xylem, but different from the SKOR channel, which is not required for QSO2 action. These results uncover QSOs as novel regulators of ion homeostasis.

Diversification of Quiescin sulfhydryl oxidase in a preserved framework for redox relay

“…Though disulfide catalysts are conserved components of the endoplasmic reticulum (ER), QSOX is localized outside the ER. In particular, plant QSOX is found in the cell wall [3], and mammalian QSOX is localized to the Golgi apparatus [4,5] or secreted from cells [6]. The importance of oxidative protein folding in the early secretory pathway for production of cell-surface and secreted proteins is well-appreciated, but the role of an additional disulfide catalyst downstream of the ER is poorly understood.…”

Oxidative Protein-Folding Systems in Plant Cells

“…Mammalian QSOX proteins are localized to the Golgi in the post-ER secretory pathways or secreted from cells [136–138], and Arabidopsis AtQSOX1, when expressed in the leaf epidermis, is found in the cell wall rather than the plasma membrane (Table 1) [139]. QSOX, in which the Erv domain has been linked with a redox-active TRX domain during evolution, catalyzes both de novo disulfide generation and disulfide transfer.…”

“…AtQSOX1 contains a CxxC motif in the TRX domain, and this motif exhibits sulfhydryl oxidase activity on the small-molecule substrate dithiothreitol but not electron transfer activity from the TRX domain to the Erv domain [143]. The expression of AtQSOX1 in leaves is upregulated by K + starvation, and AtQSOX1 plays a role in regulating cation homeostasis by activating root systems that load K + into the xylem [139]. This K + efflux system may be regulated by AtQSOX1-mediated oxidation of sulfhydryl groups of the transporter at the external side of the plasma membrane [139].…”

“…The expression of AtQSOX1 in leaves is upregulated by K + starvation, and AtQSOX1 plays a role in regulating cation homeostasis by activating root systems that load K + into the xylem [139]. This K + efflux system may be regulated by AtQSOX1-mediated oxidation of sulfhydryl groups of the transporter at the external side of the plasma membrane [139]. …”

Ion homeostasis: plants feel better with proper control

“…The domain structure of QSOs was originally identified in human fibroplasts, but their physiological functions remain only poorly defined. Although the precise mode of action of the plant enzyme is not yet known, the recent report by Alejandro et al (2007) indicates an important role in adjusting ion homeostasis. Experimental evidence suggests that QSO2 regulates ion transport at the root symplast-xylem loading interface; however, the well-known xylem parenchyma-expressed outward-rectifying K + channel SKOR (Gaymard et al, 1998) is not required for this mechanism.…”