Research Advances in the Mutual Mechanisms Regulating Response of Plant Roots to Phosphate Deficiency and Aluminum Toxicity

Abstract

Low phosphate (Pi) availability and high aluminum (Al) toxicity constitute two major plant mineral nutritional stressors that limit plant productivity on acidic soils. Advances toward the identification of genes and signaling networks that are involved in both stresses in model plants such as Arabidopsis thaliana and rice (Oryza sativa), and in other plants as well have revealed that some factors such as organic acids (OAs), cell wall properties, phytohormones, and iron (Fe) homeostasis are interconnected with each other. Moreover, OAs are involved in recruiting of many plant-growth-promoting bacteria that are able to secrete both OAs and phosphatases to increase Pi availability and decrease Al toxicity. In this review paper, we summarize these mutual mechanisms by which plants deal with both Al toxicity and P starvation, with emphasis on OA secretion regulation, plant-growth-promoting bacteria, transcription factors, transporters, hormones, and cell wall-related kinases in the context of root development and root system architecture remodeling that plays a determinant role in improving P use efficiency and Al resistance on acidic soils.

Keywords: acidic soil; aluminum toxicity; organic acids; phosphate deficiency; signal crosstalk; stress response.

Figure 1

Schematic illustration of the roles of organic acid anions (OAs) and their metabolism regulation in Al detoxification and P solubilization on acidic soils. The OAs are produced mainly through mitochondria tricarboxylic acid (TCA) cycle. Under stress conditions, stress signals trigger the transcription factor STOP1 via SUMOylation and ubiquitination regulation to induce the transcription of transporter genes that are responsible for OAs exudation, Pi uptake, and Al complexation and uptake. The OAs that are secreted from roots function in against Al toxicity and P deficiency when grown on acid soils. OAs form complexes with Al³⁺ to protect the roots from Al toxicity in the rhizosphere, and solubilize rhizosphere Pi via complexation with Al, Fe, and Ca oxides and hydroxides on mineral surfaces. ALMT: Aluminum-activated malate transporter; ESD4: EARLY IN SHORT DAYS 4; MATE: Multidrug and toxic compound extrusion; NIP1;2: nodulin 26-like intrinsic protein 1;2; Nrat1: NRAMP-type Al transporter1; PHTs: Phosphate transporters; SIZ1: a SUMO E3 ligase; RAE1: REGULATION OF ATALMT1 EXPRESSION 1; RAH1: RAE1 HOMOLOG 1; VPE: vacuolar Pi efflux transporter.

Figure 2

Phylogenetic and motif analysis for the 20 plant metal transporters of the Nramp family. (A) An unrooted phylogenetic tree was built by MEGA7. (B) Sequence alignment of the two signature motifs of the 20 plant Nramp transporters. The 20 Nramp transporters are rice OsNrat1 (XP_015625418), Sorghum SbNrat1 (XP_002451480), Maize ZmNrat1 (NP_001334019), six Arabidopsis Nramp proteins, five tomato Nramp proteins, and six Brachypodium distachyon Nramp proteins.

Figure 3

A simplified model for the relationship among different hormones in response to both Al toxicity and low P. Al stress and P deficiency induce the local up-regulation of TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS 1 (TAA1) and YUCCA (YUC) in the root transition zone through an ethylene-dependent pathway, which contributes to auxin accumulation in the root transition zone (TZ), suppressing primary root growth. Local cytokinin (CK) accumulation acts downstream of auxin signaling through ARF7/9, synergistically regulating the stress-induced inhibition of root growth. COI1-mediated jasmonate (JA) signaling is involved in stress-induced root growth inhibition through ALMT1-mediated malate exudation from roots to affect ROS production. In addition, the production of melatonin under stress conditions is able to reduce the ROS production and induce cell wall expansion to promote root growth. JA: jasmonic acid; COI1: F-box protein CORONATINE INSENSITIVE 1; ALMT1: aluminum-activated malate transporter1; LPR1: low phosphate-resistant root1; TIR1: transport inhibitor response 1; ARF: auxin responsive factor; RAM: root apical meristem; NO: nitric oxide; ROS: reactive oxygen species; ETR1: ethylene receptor1; EIN2: ETHYLENE INSENSITIVE2.