Towards sustainable use of acidic soils: Deciphering aluminum-resistant mechanisms in plants

Abstract

The widespread occurrence of acidic soils presents a major challenge for agriculture, as it hampers productivity via a combination of mineral toxicity, nutrient deficiency, and poor water uptake. Conventional remediation methods, such as amending the soil with lime, magnesium, or calcium, are expensive and not environmentally friendly. The most effective method to mitigate soil acidity is the cultivation of acid-tolerant cultivars. The ability of plants to tolerate acidic soils varies significantly, and a key factor influencing this tolerance is aluminum (Al) toxicity. Therefore, understanding the physiological, molecular, and genetic underpinnings of Al tolerance is essential for the successful breeding of acid-tolerant crops. Different tolerance mechanisms are regulated by various genes and quantitative trait loci in various plant species, and molecular markers have been developed to facilitate gene cloning and to support marker-assisted selection for breeding Al-tolerant cultivars. This study provides a comprehensive review of the current developments in understanding the physiological and molecular mechanisms underlying Al resistance. Through the application of genome-wide association methods, it is expected that new Al-resistant genes can be identified and utilized to cultivate Al-resistant varieties through intercrossing, backcrossing, and molecular marker-assisted selection, promoting the sustainable use of acidic soils.

Keywords: Acid-tolerant cultivars; Acidic soils; Agriculture; Aluminum toxicity; Remediation methods; Soil amendment.

Fig. 1

Model generalizing the plants’ Al resistant mechanisms of exclusion and internal detoxification with some modifications according to Kochian et al. . Upon the absorption of Al³⁺ by roots from the soil solution, a portion of the Al is subsequently transferred and accumulated in the shoots. The chelation of Al³⁺ by organic acids largely occurs in the upper root, where Al exclusion and internal Al tolerance processes are established. Root exudation of organic acid anions through multidrug and toxic compound extrusion (MATEs) or Al-activated malate transporters (ALMTs) localized in the plasma membrane are key components of root Al exclusion mechanisms. The influx of Al³⁺ into the cytosol occurs through nodulin 26-like intrinsic protein (NIP) Al transporters and/or natural resistance-associated macrophage proteins (Nramps). Finally, Al (either an Al-chelate complex or free Al³⁺ ion) is transported into the vacuole, possibly through the action of a vacuolar Al transporter (VALT) aquaporin transporter or an Al-sensitive 1-type ATP-binding cassette (ALS1-type ABC) transporter. Red arrows indicate Al influx into the cells, whereas green arrows indicate organic acid anion effluxes. The capacity of the cell wall to fix Al³⁺ is modulated by plant-mediated changes in cell-wall components, including hemicellulose rather than pectin, which constitutes an additional mechanism of Al tolerance. The translocation of Al organic acid compounds to the shoot occurs through an unidentified mechanism, in which, either Al or Al-chelate complexes are loaded to the xylem. This translocation, largely stored in leaf vacuoles, occurs in the Al accumulating plant species like Hydrangea macrophylla, through transport procedures involving permeases such as HmVALT, Hydrangea macrophylla plasma membrane Al transporter 1 (HmPALT1), and aquaporins. Abbreviations: Nrat1, Nramp Al transporter 1; OA, organic acid; TCA, tricarboxylic acid.

Fig. 2

Illustration of the involvement of a general signaling pathway in perception of Al stress in plant roots with some modifications according to Kochian et al. . Perception of Al stress (as indicated by purple arrows) can occur through various pathways, including the direct interaction of Al³⁺ ions with one or more putative plasma membrane Al receptors (upper right corner of the model), or indirectly through the increased cytoplasmic Al levels caused by Al³⁺ influx via plasma membrane Al transporters, such as NIPs and NRAMPs, and indirectly through plasma membrane signal transducers such as Ca²⁺ sensors (upper right) and hormones (upper left). Inhibition of membrane transport by Al may also play a role. These modifications potentially trigger signal transduction cascades leading to the activation of mechanisms resulting in Al resistance through two main processes. One is an Al-induced transcriptional activation of membrane transporters and biosynthetic enzymes, which underlie Al exclusion and internal Al resistance mechanisms (red arrows). This process is influenced by transcription factors such as AtSTOP1, AtWRKY46 (a WRKY domain-containing transcription factor), AtCAMTA2, AtCBL1, and AtCML24 in Arabidopsis, and OsART1, OsWRKY22, OsASR1/5, and OsMYB30 (an R2R3-MYB family transcription factor) in rice, which are involved in the relationship between Al perception and the control of their downstream genes. The other mechanism involves posttranslational Al activation and/or regulation at the protein functional level (blue arrows). This involves the activation of organic acid efflux transporters by Al, through direct binding to the transport protein, or indirectly, possibly through procedures such as protein phosphorylation and dephosphorylation and/or other protein-protein interactions that modify the activity of the transporter. Abbreviations: IAA, indole-3-acetic acid; VDCC, voltage-dependent calcium channel.

Fig. 3

General model illustrating the post-transcriptional and translational regulation of AtSTOP1 and OsART1. Despite the extensive studies on the post-transcriptional and translational regulation of AtSTOP1, a classical Al resistant transcription factor in Arabidopsis, little is known about the upstream regulatory mechanism of OsART1, a counterpart of classical Al resistant transcription factor in rice. Therefore, there is a need for further research to shed light on the post-transcriptional and translational regulation of OsART1.