Two citrate transporters coordinately regulate citrate secretion from rice bean root tip under aluminum stress

Abstract

Aluminum (Al)-induced organic acid secretion from the root apex is an important Al resistance mechanism. However, it remains unclear how plants fine-tune root organic acid secretion which can contribute significantly to the loss of fixed carbon from the plant. Here, we demonstrate that Al-induced citrate secretion from the rice bean root apex is biphasic, consisting of an early phase with low secretion and a later phase of large citrate secretion. We isolated and characterized VuMATE2 as a possible second citrate transporter in rice bean functioning in tandem with VuMATE1, which we previously identified. The time-dependent kinetics of VuMATE2 expression correlates well with the kinetics of early phase root citrate secretion. Ectopic expression of VuMATE2 in Arabidopsis resulted in increased root citrate secretion and Al resistance. Electrophysiological analysis of Xenopus oocytes expressing VuMATE2 indicated VuMATE2 mediates anion efflux. However, the expression regulation of VuMATE2 differs from VuMATE1. While a protein translation inhibitor suppressed Al-induced VuMATE1 expression, it releases VuMATE2 expression. Yeast one-hybrid assays demonstrated that a previously identified transcription factor, VuSTOP1, interacts with the VuMATE2 promoter at a GGGAGG cis-acting motif. Thus, we demonstrate that plants adapt to Al toxicity by fine-tuning root citrate secretion with two separate root citrate transport systems.

Rice bean: a lesser known pulse with well-recognized potential

“…Mechanism for aluminium tolerance in rice bean has been attributed to the release of citric acid on exposure of roots to aluminium (Yang et al 2006;Fan et al 2014). Two genes for aluminium-activated citrate transporter (VuMATE1 and VuMATE2) have been cloned from rice bean (Yang et al 2006;Liu et al 2018) and these are found to belong to multidrug and toxic compound extrusion family (MATE). Two types of patterns for organic acid efflux have been identified in aluminium-tolerant species.…”

Alleviation by abscisic acid of Al toxicity in rice bean is not associated with citrate efflux but depends on ABI5‐mediated signal transduction pathways

“…Sequence alignment established that CL3862.Contig1_All and Unigene20395_All are VuMATE1 and VuMATE2 , respectively, two previously identified Al tolerance genes responsible for Al‐stimulated citrate efflux (Liu et al ; ). In line with our previous work, ABA could slightly induce VuMATE1 expression, but both the intensity and localization of the expression differed from that induced by Al (Liu et al ).…”

Molecular cloning of TaMATE2 homoeologues potentially related to aluminium tolerance in bread wheat (Triticum aestivum L.)

“…Phylogenetic analysis also indicated differential functional behaviours between TaMATE1 and TaMATE2 of wheat, because TaMA-TE1B is closely clustered with ScFRDL1 of rye, HvAACT1 of barley and BdMATE of purple false brome that display constitutive citrate efflux, whereas TaMATE2 homoeologues are closer to ScFRDL2, ZmMATE1 and OsFRDL2 that require Al activation. These results suggest the 'activation' of MATE in planta is governed by a complex, yet unidentified, mechanism that may involve other interacting proteins (Liu et al 2018).…”

“…These results suggest the ‘activation’ of MATE in planta is governed by a complex, yet unidentified, mechanism that may involve other interacting proteins (Liu et al . ).…”