A tonoplast‐localized half‐size ABC transporter is required for internal detoxification of aluminum in rice

Abstract

SUMMARYToxic aluminum enters the root cells rapidly, therefore internal detoxification is required. However, the molecular mechanisms underlying this process are poorly understood. Here we functionally characterized a rice gene, Os03g0755100 (OsALS1), that is regulated by ART1, a C2H2-type zinc finger transcription factor. OsALS1 encodes a half-size ABC transporter that is a member of the TAP (transporter associated with antigen processing) sub-group. Expression of OsALS1 was rapidly and specifically induced by Al in the roots, but not by other metals or low pH. OsALS1 was localized at all cells of the roots. Furthermore, OsALS1 is localized to the tonoplast. These expression patterns and cell specificity of localization are different from those of the homologous gene AtALS1 in Arabidopsis. Knockout of OsALS1 in three independent lines resulted in significant increased sensitivity to Al, but did not affect the sensitivity to other metals and low pH. Comparison of Al accumulation patterns between wild-type and osals1 mutants showed that there was no difference in Al levels in the cell sap of root tips between wild-type and the mutants, but the mutants accumulated more Al in the cytosol and nucleus than the wild-type. Expression of OsALS1 in yeast resulted in increased Al sensitivity due to mis-localization. These results indicate that OsALS1 localized at the tonoplast is responsible for sequestration of Al into the vacuoles, which is required for internal detoxification of Al in rice.

Coordination between Apoplastic and Symplastic Detoxification Confers Plant Aluminum Resistance

“…Morin can detect aluminum in the cytosol but not cell wall-bound aluminum or vacuole-compartmentalized aluminum (Eticha et al, 2005b;Huang et al, 2012). The lack of morin staining in vacuole may be attributed to two reasons according to Huang et al (2012): (1) morin is not permeable to the tonoplast, and (2) vacuolar aluminum is chelated by organic reagents, such as malic and citric acids, and morin cannot detect complexed aluminum forms, similar to cell wall-bound aluminum (Eticha et al, 2005b). Therefore, strong aluminumdependent green fluorescence represents aluminum present in the cytosol and nucleus.…”

“…In addition, ALS1, which encodes a transporter localized to the root tip and the vasculature, has been implicated in aluminum sequestration to more tolerant tissues (Larsen et al, 2007). Recently, Huang et al (2012) identified that OsALS1, which is expressed ubiquitously in rice, with the encoded protein localizing to the tonoplast, is responsible for sequestration of aluminum into the vacuoles and is required for internal detoxification of aluminum in rice. Although both ALS1 and ALS3 have critical roles in aluminum resistance, ALS3 is a plasma membrane transporter that moves aluminum away from the root tip and is not involved in redistribution between the cytoplasm and vacuole.…”

“…In Arabidopsis (Arabidopsis thaliana), the tonoplast-localized ATP-binding cassette (ABC) transporter Al sensitive1 (ALS1), which is involved in Al tolerance in Arabidopsis (Larsen et al, 2007), while ALS3 is responsible for movement of aluminum away from sensitive tissues for sequestration in more tolerant tissues (Larsen et al, 2005(Larsen et al, , 2007. Huang et al (2012) identified a rice (Oryza sativa) tonoplast-localized aluminum transporter, encoded by OsALS1, which is responsible for sequestration of aluminum into vacuoles and thus contributes to the internal detoxification of aluminum in rice. In addition, some plants have been found to harbor multiple strategies for aluminum detoxification.…”

Natural variation underlies alterations in Nramp aluminum transporter ( NRAT1 ) expression and function that play a key role in rice aluminum tolerance

“…Second, it is possible that in addition to sequestration in the vacuole of the Al transported across the plasma membrane from the cell wall, some of the transported Al could move radially into the root where it is loaded into the xylem and then transported to the shoot for storage in a manner similar to what occurs in the Al accumulators, hydrangea and buckwheat (4,5). It has been suggested that the tonoplast-localized ABC transporter aluminum sensitive 1 (OsALS1) might be responsible for the sequestration of Al 3+ from the cytosol into the rice root vacuole (5).…”

“…Al tolerance involves internal mechanisms that allow plants to deal with Al toxicity in the root cell wall and/or to detoxify Al 3+ that enters root cells by forming nontoxic organic acid (OA)-Al complexes in the cytosol and/or by sequestering the Al in subcellular compartments, such as vacuoles (3)(4)(5). The primary Al avoidance mechanism involves exclusion of Al from the growing root tip via the exudation of Al-chelating OAs into the rhizosphere, where the OAs form nontoxic OA-Al complexes which do not enter the root.…”