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ARS Home » Northeast Area » Ithaca, New York » Robert W. Holley Center for Agriculture & Health » Plant, Soil and Nutrition Research » Research » Publications at this Location » Publication #346643
Title: Two citrate transporters coordinately regulate citrate secretion from rice bean root tip under aluminum stress

Author
item LIU, MEI - Zheijiang University
item LOU, HE - Zhejiang University
item CHEN, WEI - Hangzhou Normal University
item Pineros, Miguel
item XU, JIA - Zhejiang University
item FAN, WEI - Yunnan Agricultural University
item KOCHIAN, LEON - University Of Saskatchewan
item YANG, JIAN - Zhejiang University
item ZHENG, SHAO - Zhejiang University

Submitted to: Plant, Cell & Environment
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/9/2018
Publication Date: 1/18/2018
Citation: Liu, M., Lou, H., Chen, W., Pineros, M., Xu, J., Fan, W., Kochian, L., Yang, J., Zheng, S. 2018. Two citrate transporters coordinately regulate citrate secretion from rice bean root tip under aluminum stress. Plant, Cell & Environment. 41:809-822. https://doi.org/10.1111/pce.13150.
DOI: https://doi.org/10.1111/pce.13150

Interpretive Summary: Over 20% of the US land area and approximately 50% of the world's arable lands are acidic (pH < 5). In acidic soils, aluminum (Al) toxicity is the primary factor limiting agricultural productivity, as toxic Al results in damaged and stunted plant root systems, ultimately resulting in a reduction of crop yields. Given that a large proportion of the acid soils are found in the tropics/subtropics regions where many developing countries are located, Al toxicity limits agricultural productivity in the very areas where food security is most tenuous. This worldwide agriculture problem has led research efforts at universities, government agencies, and international agriculture organizations to identifying genes that provide tolerance to Al toxicity, as means to improve crop Al tolerance via molecular breeding and biotechnology. The release of organic acid from the root apex in response to Al-stress constitutes a widespread Al-resistance mechanism by which plant roots are able to ameliorate the toxic levels of Al surrounding the growing root. Several genes encoding for membrane proteins involved in the transport and the release of these organic acids from root cells have been identified and cloned. In rice bean, VuMATE1 and VuMATE2 constitute two proteins that mediate these processes, thereby releasing the organic acid citrate. In this study we examine how plants adapt to Al-toxicity by fine-tuning root citrate secretion, using two separate root citrate transport pathways that operate at different times during the onset of the stress response. Our findings highlight the importance of understanding the various mechanism and factors dictating their expression at a given point time, as they represent key targets for future improvements in Al-resistance in cereals via molecular breeding approaches.

Technical Abstract: 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.