Aluminum-Dependent Root-Growth Inhibition in Arabidopsis Results from AtATR-Regulated Cell-Cycle Arrest

Abstract

Aluminum (Al) toxicity is a global problem severely limiting agricultural productivity in acid-soil regions comprising upwards of 50% of the world's arable land [1, 2]. Although Al-exclusion mechanisms have been intensively studied [3-9], little is known about tolerance to internalized Al, which is predicted to be mechanistically complex because of the plethora of predicted cellular targets for Al(3+)[2, 10]. An Arabidopsis mutant with Al hypersensitivity, als3-1, was found to represent a lesion in a phloem and root-tip-localized factor similar to the bacterial ABC transporter ybbm, with ALS3 likely responsible for Al transfer from roots to less-sensitive tissues [10-12]. To identify mutations that enhance mechanisms of Al resistance or tolerance, a suppressor screen for mutants that mask the Al hypersensitivity of als3-1 was performed [13]. Two allelic suppressors conferring increased Al tolerance were found to represent dominant-negative mutations in a factor required for monitoring DNA integrity, AtATR[14-17]. From this work, Al-dependent root-growth inhibition primarily arises from DNA damage coupled with AtATR-controlled blockage of cell-cycle progression and terminal differentiation because of loss of the root-quiescent center, with mutations that prevent response to this damage resulting in quiescent-center maintenance and sustained vigorous growth in an Al-toxic environment.