An exclusion mechanism is epistatic to an internal detoxification mechanism in aluminum resistance in Arabidopsis

Abstract

Background: In Arabidopsis, the aluminum (Al) exclusion mechanism is mainly facilitated by ALMT1mediated malate exudation and MATE-mediated citrate releases from the root. Recently, we have demonstrated that coordinated functioning between the ALMT1-mediated Al exclusion mechanism, via exudation of malate from the root tip, and a NIP1;2-facilitated internal detoxification mechanism, via removal of Al from the root cell wall and subsequent root-to-shoot Al translocation, plays critical roles in achieving overall Al resistance. However, the genetic relationship between ALMT1 and NIP1;2 in these processes remained unclear.Results: Through genetic and physiological analyses, we demonstrate that unlike ALMT1 and MATE, which function independently and additively, ALMT1 and NIP1;2 show an epistatic relationship in Al resistance. These results indicate that ALMT1 and NIP1;2 function in the same biochemical pathway, whereas ALMT1 and MATE in different ones. Conclusion:The establishment of the epistatic relationship and the coordinated functioning between the ALMT1 and NIP1;2-mediated exclusion and internal detoxification mechanisms are pivotal for achieving overall Al resistance in the non-accumulating Arabidopsis plant. We discuss and emphasize the indispensable roles of the root cell wall for the implementation of the Al exclusion mechanism and for the establishment of an epistatic relationship between the ALMT1-mediated exclusion mechanism and the NIP1;2-facilitated internal detoxification mechanism. Background Aluminum (Al) is the most abundant metal element in the earth crust [1]. Under neutral or alkalescent conditions, Al is present in the soil as forms that are non-toxic to plants [2]. However, at low pH (<5.0), aluminum ions (Al 3+ ) are dissolved and released from the soil clays into the soil solutions, which could interact with multiple sites of the plant root cell, including the cell wall, cell membrane and cytosol with toxic effects, resulting severe root growth inhibition, the most significant symptom of Al toxicity [1,3]. The impaired root system restricts root absorption of water and nutrients from the acid subsoil, leading to drought stresses and nutrient deficiencies and thus reduced yields for crops grown on acidic soils [1,4]. 4Physiologic studies indicated that the root apex, rather than the root elongation zone and the mature root region, is a major target of Al toxicity [5]. Cell wall loosening and synthesis of cell wall components are essential for sustained root cell elongation and water uptake [6,7]. However, Al 3+ ions severely inhibit root elongation through reducing cell wall cation binding, water permeability and cell wall enzyme activities [8][9][10][11]. As a result, the root cell wall in the root apical region is one of the major targets for Al toxicity [12,13].Plants have adopted several strategies to cope with Al stresses, including Al exclusion and internal detoxification mechanisms [14,15]. The exclusion mechanism relies on root releases of chemical exudates, including organic acids [1...