Low pH, Aluminum, and Phosphorus Coordinately Regulate Malate Exudation through GmALMT1 to Improve Soybean Adaptation to Acid Soils    

Abstract

Low pH, aluminum (Al) toxicity, and low phosphorus (P) often coexist and are heterogeneously distributed in acid soils. To date, the underlying mechanisms of crop adaptation to these multiple factors on acid soils remain poorly understood. In this study, we found that P addition to acid soils could stimulate Al tolerance, especially for the P-efficient genotype HN89. Subsequent hydroponic studies demonstrated that solution pH, Al, and P levels coordinately altered soybean (Glycine max) root growth and malate exudation. Interestingly, HN89 released more malate under conditions mimicking acid soils (low pH, +P, and +Al), suggesting that root malate exudation might be critical for soybean adaptation to both Al toxicity and P deficiency on acid soils. GmALMT1, a soybean malate transporter gene, was cloned from the Al-treated root tips of HN89. Like root malate exudation, GmALMT1 expression was also pH dependent, being suppressed by low pH but enhanced by Al plus P addition in roots of HN89. Quantitative real-time PCR, transient expression of a GmALMT1-yellow fluorescent protein chimera in Arabidopsis protoplasts, and electrophysiological analysis of Xenopus laevis oocytes expressing GmALMT1 demonstrated that GmALMT1 encodes a root cell plasma membrane transporter that mediates malate efflux in an extracellular pH-dependent and Al-independent manner. Overexpression of GmALMT1 in transgenic Arabidopsis, as well as overexpression and knockdown of GmALMT1 in transgenic soybean hairy roots, indicated that GmALMT1-mediated root malate efflux does underlie soybean Al tolerance. Taken together, our results suggest that malate exudation is an important component of soybean adaptation to acid soils and is coordinately regulated by three factors, pH, Al, and P, through the regulation of GmALMT1 expression and GmALMT1 function.

An InDel in the Promoter of Al-ACTIVATED MALATE TRANSPORTER9 Selected during Tomato Domestication Determines Fruit Malate Contents and Aluminum Tolerance

“…Both At-ALMT6 and At-ALMT9 play a role in vacuolar malate transport in guard cells; At-ALMT6 is a Ca 2+ -activated malate channel that does not function in regulating stoma movement and At-ALMT9 is a malate-activated vacuolar chloride channel that does control stomatal aperture and thereby stomatal conductance and drought tolerance. Other members of this family, e.g., Ta-ALMT1, At-ALMT1, Bn-ALMT1, Bn-ALMT2, and Gm-ALMT1, control leaf malate accumulation, malate exudation in root, and affect Al resistance Hurth et al, 2005;Hoekenga et al, 2006;Ligaba et al, 2006;Kobayashi et al, 2013;Liang et al, 2013). In this work, Sl-ALMT9 HMH accessions (e.g., TS40) and Sl-ALMT9 LMH accessions (e.g., TS66) showed significant differences in malate contents in fruits, but contained comparable amounts in leaves.…”

“…Following a 3-h incubation, the treatment solution was collected and dried, and the resulting residues were collected and analyzed for malate contents as described above. To characterize the role of Sl-ALMT9 in Al detoxification, tomato hairy roots were treated for 3 h with 1 mM CaCl 2 , pH 4.2, containing 100 mM Al, after which they were then stained with hematoxylin as described previously (Liang et al, 2013).…”

Physiological and molecular alterations in plants exposed to high [CO2] under phosphorus stress

“…The interactive effect of [CO 2 ] and P nutrition on root system remain inconclusive (discussed previously), on PEPCase activity in proteoid root suggests that high [CO 2 ] had no effect on total PEPCase activity in either P-deficient or sufficient leaves , and on organic anion transporters no studies have been carried out. However, a malate transporter (GmALMT1) identified from Glycine max was shown to be co-ordinately regulated by P stress, aluminum and low pH (Liang et al, 2013 A C C E P T E D M A N U S C R I P T…”

The ALMT Gene Family Performs Multiple Functions in Plants

“…Malate chelates the Al 3+ which reduces damage to the cell wall, membranes and other cellular components. Other members of the family perform similar functions in Arabidopsis [3,31], rape (Brassica napus L.) [4], rye (Secale cereale L.) [2], soybean (Glycine max L.) [32], alfalfa (Medicago sativa L.) [33], and Yorkshire fog (Holcus lanatus L.) [34]. Regulation of these vary and some show more complex interactions [35].…”

“…Regulation of these vary and some show more complex interactions [35]. For instance, AtALMT1 is not constitutively expressed in Arabidopsis roots but induced by low pH and Al 3+ [3] and GmALMT1 in soybean shows complex interactions with Al stress and phosphorus nutrition [32].…”