Coordination between Apoplastic and Symplastic Detoxification Confers Plant Aluminum Resistance

Abstract

Whether aluminum toxicity is an apoplastic or symplastic phenomenon is still a matter of debate. Here, we found that three auxin overproducing mutants, yucca, the recessive mutant superroot2, and superroot1 had increased aluminum sensitivity, while a transfer DNA insertion mutant, xyloglucan endotransglucosylase/hydrolases15 (xth15), showed enhanced aluminum resistance, accompanied by low endogenous indole-3-acetic acid levels, implying that auxin may be involved in plant responses to aluminum stress. We used yucca and xth15 mutants for further study. The two mutants accumulated similar total aluminum in roots and had significantly reduced cell wall aluminum and increased symplastic aluminum content relative to the wild-type ecotype Columbia, indicating that altered aluminum levels in the symplast or cell wall cannot fully explain the differential aluminum resistance of these two mutants. The expression of Al sensitive1 (ALS1), a gene that functions in aluminum redistribution between the cytoplasm and vacuole and contributes to symplastic aluminum detoxification, was less abundant in yucca and more abundant in xth15 than the wild type, consistent with possible ALS1 function conferring altered aluminum sensitivity in the two mutants. Consistent with the idea that xth15 can tolerate more symplastic aluminum because of possible ALS1 targeting to the vacuole, morin staining of yucca root tip sections showed more aluminum accumulation in the cytosol than in the wild type, and xth15 showed reduced morin staining of cytosolic aluminum, even though yucca and xth15 had similar overall symplastic aluminum content. Exogenous application of an active auxin analog, naphthylacetic acid, to the wild type mimicked the aluminum sensitivity and distribution phenotypes of yucca, verifying that auxin may regulate aluminum distribution in cells.Together, these data demonstrate that auxin negatively regulates aluminum tolerance through altering ALS1 expression and aluminum distribution within plant cells, and plants must coordinate exclusion and internal detoxification to reduce aluminum toxicity effectively.

TAA1-Regulated Local Auxin Biosynthesis in the Root-Apex Transition Zone Mediates the Aluminum-Induced Inhibition of Root Growth in Arabidopsis

“…The auxin accumulation in the TZ mimics the root growth inhibition induced by an external supply of auxin, much of which is taken up by the TZ . A recent report, which showed that auxin enhances Al toxicity via an alteration in ALUMINUM-SENSITIVE1-mediated Al distribution (Zhu et al, 2013), provides further support for our findings. Unfortunately, the study of Zhu et al (2013) made no attempt to define the spatial correlations between Al and auxin effects in the root apex during the Al-induced inhibition of root growth.…”

“…The importance of the properties of the cell wall in the context of Alinduced inhibition of root elongation and in Al tolerance has been emphasized . The binding of Al to the cell wall, and particularly to the pectic and hemicellulosic matrix in the most Al-sensitive zone of the root apex, has a major effect on cell wall properties and root growth in Arabidopsis (Yang et al, 2011a;Yang et al, 2011b;Zhu et al, 2012Zhu et al, , 2013. The binding of Al to pectins is known to be highly dependent on their degree of methylation: binding occurs preferentially to unmethylated pectin, catalyzed by the activity of pectin methylesterase (PME) Yang et al, 2011b).…”

Putrescine Alleviates Iron Deficiency via NO-Dependent Reutilization of Root Cell-Wall Fe in Arabidopsis

“…We previously demonstrated that hemicellulose contributes greatly to the metal binding in cell walls of rice and Arabidopsis (Yang et al, 2008(Yang et al, , 2011Zhu et al, 2012Zhu et al, , 2013. Here, we found that -Fe+Put treatment significantly decreased hemicellulose content compared with -Fe treatment alone (Fig.…”

“…The roots were then frozen at 280°C overnight. The root-cell sap solution was obtained by thawing the samples at room temperature, and then the liquid was collected after centrifuging at 20,600g for 10 min according to Zhu et al (2013). The soluble Fe, total Fe, and symplastic Fe content were determined by ICP-AES (IRIS/AP optical emission spectrometer).…”

“…As the first barrier to encounter the soil environment, the cell wall is a pivotal site for most cationic ions in plants (Lozano-Rodríguez et al, 1997;Carrier et al, 2003). Hemicellulose contributes to the overall Al/Cd accumulation in the cell wall of Arabidopsis (Zhu et al, 2012(Zhu et al, , 2013 and also acts as a Fe pool (Lei et al, 2014). Over 75% of Fe in the root is retained in the cell wall (Bienfait et al, 1985), especially in the hemicellulose fraction (Lei et al, 2014).…”