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

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 ci...

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Published in:Plant, cell and environment cell and environment, 2018-04, Vol.41 (4), p.809-822
Main Authors: Liu, Mei Ya, Lou, He Qiang, Chen, Wei Wei, Piñeros, Miguel A., Xu, Jia Meng, Fan, Wei, Kochian, Leon V., Zheng, Shao Jian, Yang, Jian Li
Format: Article
Language:English
Subjects:
Aluminum
Citric acid
Ectopic expression
Efflux
Kinetics
Oocytes
Secretion
Toxicity
Vigna umbellata
Yeast
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Summary: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. Although Al‐induced organic acid secretion from the root apex is an important Al resistance mechanism, it remains unclear how plants maximize carbon utilization efficiency. We found that Al‐induced citrate secretion from root apex of rice bean consists of an early and a late phase which is cooperatively regulated by two MATE‐type citrate transporters, VuMATE2 and VuMATE1. Furthermore, a previously identified C2H2‐type zinc finger transcription factor VuSTOP1 plays differential roles in the expression regulation of VuMATE1 and VuMATE2 in response to Al stress. Our results reveal the mechanism by which plants cope with Al toxicity by fine‐tuning root citrate secretion.
ISSN:0140-7791
1365-3040
DOI:10.1111/pce.13150