ANAC050 confers aluminium resistance by cooperating with the secretion of organic acids and the accumulation of cell wall hemicelluloses

Abstract

Aluminium (Al) toxicity is one of the key factors limiting crop output in acidic soils, but until now little has been known about how Al is regulated transcriptionally in plants. This study identified Arabidopsis NAC transcription factor ANAC050 in the regulation of Al tolerance. NAC is composed of NO APICAL MERISTEM (NAM), ARABIDOPSIS TRANSCRIPTION ACTIVATION FACTOR1/2 (ATAF1/2), and CUP-SHAPED COTYLEDON 2 (CUC2). ANAC050 was located in the nucleus and displayed constitutive expression in the silique, flower, leaf, stem and root, despite the fact that Al stress decreased its expression and protein accumulation. When compared with their wild-type Col-0 (WT), anac050 mutants that lacked function of ANAC050 exhibited Al sensitivity phenotype, while transgenic lines that overexpressedANAC050 showed an Al-resistant phenotype, indicating the favorable influence of ANAC050 on preserving the Al tolerance in plants. Further analysis indicated that anac050 mutants’ roots accumulated more Al, implying that ANAC050 may confer a potential operation of an Al exclusion mechanism. Interestingly, anac050 mutants had down-regulated the expression of the MULTIDRUG AND TOXIC COMPOUND EXTRUSION (MATE) and AL-ACTIVATED MALATE TRANSPORTER (ALMT1), which were involved in the secretion of citrate and malate, even though there was no evidence of a direct interaction between them, suggesting ANAC050 may mediate the secretion of citrate and malate indirectly. Together with the decreased hemicellulose content, lower Al content was also discovered in anac050 mutants’ roots cell walls and hemicellulose, pointing to a potential interaction between ANAC017 and xyloglucanendotransglucosylase/hydrolase (XTH). Although there was no evidence of a direct interaction between ANAC050 and XTH31, it is worth mentioning that the expression of XTH31, which is essential for xyloglucan modification, was down-regulated in anac050 mutants irrespective of the amount of Al given. In conclusion, our findings showed that ANAC050 contributed to Al resistance by indirectly control of the release of organic acids and the accumulation of cell wall hemicelluloses.