|Liang, Cuiyue -|
|Tian, Jiang -|
|Yao, Zhufang -|
|Sun, Lili -|
|Shaff, Jon -|
|Liao, Hong -|
Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: January 18, 2013
Publication Date: March 1, 2013
Repository URL: http://DOI: 10.1104/pp.112.208934
Citation: Liang, C., Pineros, M., Tian, J., Yao, Z., Sun, L., Liu, J., Shaff, J., Liao, H., Kochian, L.V. 2013. Low pH, aluminum and phosphorus coordinately regulate malate exudation through GmALMT1 to improve soybean adaptation to acid soils. Plant Physiology. 161:1347-1361. Interpretive Summary: Large areas of land within the U.S. and over 40% of the world’s arable lands are acidic. In these acid soils, aluminum (Al) toxicity and phosphorous (P) deficiency are the two factors limiting crop production. The physiological and molecular basis for acid soil tolerance is still poorly understood. Thus, we need a more complete understanding of the mechanisms underlying both Al tolerance and tolerance to low P (P efficiency) if we are going to be able to develop more improved crops for agriculture on acid soils. In this paper, we used molecular and physiological methods to study both Al tolerance and P efficiency in two soybean lines differing in P efficiency. We had previously shown that Al activates the efflux of the Al-detoxifying organic acid malate from soybean roots, and here we show that this response is inhibited by low pH, and enhanced by both P in addition to roots as well as Al exposure. We then cloned the gene that encodes the root transporter of malic acid, GmALMT1, and showed via electrophysiological techniques that it indeed mediates the release of malic acid from root cells. Also, we found that expression of the GmALMT1 gene is inhibited by low pH and enhanced by P addition. These findings show that this mechanism of tolerance to acid soils is coordinately regulated by 3 factors; Al, P and changes in soil pH. This research is providing a deeper understanding of the strategies plants use to tolerate toxic Al and low P on acid soils and will help us in developing more acid soil tolerant crops for agriculture on acid soils that are widespread both in the US and also in developing countries.
Technical Abstract: Low pH, aluminum (Al) toxicity and low phosphorus (P) often coexist in acid soils where crops need to cope with these multiple limiting factors. In this study we found that P addition to acid soils alleviates Al toxicity and enhanced soybean adaptation to acid soils, especially for the P-efficient genotype, HN89. Further studies in hydroponics showed that both internal root malate content and malate exudation were suppressed by low pH, and interestingly, compared to the P-inefficient genotype HN112, HN89 released more malate from its roots under hydroponic conditions that mimic the primary aspects of acid soils - low pH, high Al, and low P supply, suggesting that root malate exudation might be critical for soybean adaptation to more than Al toxicity on acid soils. A soybean malate transporter gene, GmALMT1, was functionally characterization in Xenopus laevis oocytes and found to encode a membrane transporter that mediates malate efflux in a pH-dependent manner. GmALMT1 expression was also pH-dependent, being suppressed by low pH, but enhanced by Al plus P addition to the solution bathing the roots of HN89, which correlated with the enhanced malate exudation from roots under the same conditions. Also, overexpression and knockdown of GmALMT1 in transgenic soybean hairy roots and GmALMT1 overexpression in transgenic Arabidopsis indicated that GmALMT1 mediates malate efflux and could help to detoxify Al. Taken together, our results suggest that malate exudation might be the critical mechanism of soybean adaptation to acid soils, which is coordinately regulated by three factors, low pH, Al and P supply, through regulation of GmALMT1.