The THO/TREX Complex Component RAE2/TEX1 Is Involved in the Regulation of Aluminum Resistance and Low Phosphate Response in Arabidopsis.

Yi-Fang Zhu,Yang Zhang,Jinliang Guo,Chao-Feng Huang

doi:10.3389/fpls.2021.698443

Abstract

The C2H2-type zinc finger transcription factor SENSITIVE TO PROTON RHIZOTOXICITY 1 (STOP1) plays a critical role in aluminum (Al) resistance and low phosphate (Pi) response mainly through promoting the expression of the malate transporter-encoding gene ARABIDOPSIS THALIANA ALUMINUM ACTIVATED MALATE TRANSPORTER 1 (AtALMT1). We previously showed that REGULATION OF ATALMT1 EXPRESSION 3 (RAE3/HPR1), a core component of the THO/TREX complex, is involved in the regulation of nucleocytoplasmic STOP1 mRNA export to modulate Al resistance and low Pi response. Here, we report that RAE2/TEX1, another core component of the THO complex, is also involved in the regulation of Al resistance and low Pi response. Mutation of RAE2 reduced the expression of STOP1-downstream genes, including AtALMT1. rae2 was less sensitive to Al than rae3, which was consistent with less amount of malate secreted from rae3 roots than from rae2 roots. Nevertheless, low Pi response was impaired more in rae2 than in rae3, suggesting that RAE2 also regulates AtALMT1-independent pathway to modulate low Pi response. Furthermore, unlike RAE3 that regulates STOP1 mRNA export, mutating RAE2 did not affect STOP1 mRNA accumulation in the nucleus, although STOP1 protein level was reduced in rae2. Introduction of rae1 mutation into rae2 mutant background could partially recover the deficient phenotypes of rae2. Together, our results demonstrate that RAE2 and RAE3 play overlapping but distinct roles in the modulation of Al resistance and low Pi response.

Highlights

Aluminum (Al) toxicity represents a major constraint for crop production on acid soils, which comprise more than 30% of the world’s arable land (von Uexkull and Mutert, 1995)
We recently discovered that F-box proteins REGULATION OF ATALMT1 EXPRESSION 1 (RAE1) and RAE1 HOMOLOG 1 (RAH1) can facilitate SENSITIVE TO PROTON RHIZOTOXICITY 1 (STOP1) ubiquitination and promote its degradation via the ubiquitin26S proteasome pathway, which is important for balancing Al resistance and plant growth (Zhang et al, 2019; Fang et al, 2021b)
The expression of ALS1 not targeted by STOP1 was slightly reduced in rae2 but not in rae3 (Figure 1I)

Summary

Introduction

Aluminum (Al) toxicity represents a major constraint for crop production on acid soils, which comprise more than 30% of the world’s arable land (von Uexkull and Mutert, 1995). The model plant Arabidopsis (Arabidopsis thaliana) secretes both malate and citrate for the Al detoxification, albeit malate plays a more important role in Al resistance than citrate (Hoekenga et al, 2003, 2006; Liu et al, 2009). Genes involved in the exudation of malate and citrate were first identified in crops, which encode anion transporters belonging to the Al-activated malate transporter (ALMT) family and the multidrug and toxic compound extrusion (MATE) family, respectively (Sasaki et al, 2004; Furukawa et al, 2007; Magalhaes et al, 2007).

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Conclusion