Aluminum-Induced 1→3-β-d-Glucan Inhibits Cell-to-Cell Trafficking of Molecules through Plasmodesmata. A New Mechanism of Aluminum Toxicity in Plants

Abstract

Symplastic intercellular transport in plants is achieved by plasmodesmata (PD). These cytoplasmic channels are well known to interconnect plant cells to facilitate intercellular movement of water, nutrients, and signaling molecules including hormones. However, it is not known whether Al may affect this cell-to-cell transport process, which is a critical feature for roots as organs of nutrient/water uptake. We have microinjected the dye lucifer yellow carbohydrazide into peripheral root cells of an Al-sensitive wheat (Triticum aestivum cv Scout 66) either before or after Al treatment and followed the cell-to-cell dye-coupling through PD. Here we show that the Al-induced root growth inhibition is closely associated with the Al-induced blockage of cell-to-cell dye coupling. Immunofluorescence combined with immuno-electron microscopic techniques using monoclonal antibodies against 133-␤-d-glucan (callose) revealed circumstantial evidence that Al-induced callose deposition at PD may responsible for this blockage of symplastic transport. Use of 2-deoxy-d-glucose, a callose synthesis inhibitor, allowed us to demonstrate that a reduction in callose particles correlated well with the improved dye-coupling and reduced root growth inhibition. While assessing the tissue specificity of this Al effect, comparable responses were obtained from the dye-coupling pattern in tobacco (Nicotiana tabacum) mesophyll cells. Analyses of the Al-induced expression of PD-associated proteins, such as calreticulin and unconventional myosin VIII, showed enhanced fluorescence and co-localizations with callose deposits. These results suggest that Al-signal mediated localized alterations to calcium homeostasis may drive callose formation and PD closure. Our data demonstrate that extracellular Al-induced callose deposition at PD could effectively block symplastic transport and communication in higher plants.

Prospecting sugarcane genes involved in aluminum tolerance

“…Callose formation has been induced in the apical root cells of aluminum-sensitive maize cultivars (Sivaguru et al, 1999) and Arabidopsis mutants with increased sensitivity to aluminum (Larsen et al, 1996). A study using immuno-fluorescence and immuno-electron microscopic techniques combined with monoclonal antibodies against callose (Sivaguru et al, 2000) showed that aluminum-sensitive wheat root growth inhibition was closely associated with the blockage of plasmodesmata (cytoplasmic channels responsible for the intercellular movement of water, nutrients and for signaling) by callose deposition under aluminum stress, which could effectively block symplastic transport and communication in higher plants. One of the key enzymes acting in callose formation is callose synthase, which showed high similarity with genes in the SUCEST database.…”

RNAi-Mediated Tocopherol Deficiency Impairs Photoassimilate Export in Transgenic Potato Plants

“…In this respect, the formation of callose deposits at the neck region of PD leading to reduced size exclusion limits or PD closure has frequently been described as a specific response of plants to different abiotic and biotic stresses, including wounding, metal toxicity, and microbial infection (Enkerli et al, 1997;Iglesias and Meins, 2000;Sivaguru et al, 2000;Roberts and Oparka, 2003). For instance, enhanced callose accumulation was observed in membranes and PD of pea roots in response to aluminum treatment, leading to the blockage of symplastic transport and inhibition of root elongation (Sivaguru et al, 2000). Interestingly, callose formation was strongly correlated with aluminuminduced oxidative damage to membrane lipids and changes in intracellular calcium homeostasis, suggesting a mechanistic link between lipid peroxidation and callose synthesis (Jones et al, 1998;Yamamoto et al, 2001).…”

AnArabidopsisGPI-Anchor Plasmodesmal Neck Protein with Callose Binding Activity and Potential to Regulate Cell-to-Cell Trafficking

“…Callose deposition at Pds is stimulated by physical and physiological stresses (Hughes and Gunning, 1980;Beffa and Meins, 1996;Iglesias and Meins, 2000;Sivaguru et al, 2000;Rinne et al, 2005;Ueki and Citovsky, 2005;Maeda et al, 2006) and is proposed to provide a mechanism for regulating Pd flux (Botha and Cross, 2000;Iglesias and Meins, 2000;Levy et al, 2007a). Hence, for example, plants with reduced accumulation of the glycolytic enzyme 1,3-b-glucanase had increased callose accumulation and a reduction in the experimental molecular size exclusion limit.…”