Evidence map›Paper›PMID 23341359›Full record

ArticlePlant physiology2013

Low pH, aluminum, and phosphorus coordinately regulate malate exudation through GmALMT1 to improve soybean adaptation to acid soils.

Cuiyue Liang, Miguel A Piñeros, Jiang Tian, Zhufang Yao, Lili Sun, Jiping Liu, Jon Shaff, Alison Coluccio, Leon V Kochian, Hong Liao

Open access · hybridAbstract read
In one paragraph

Article in Plant physiology, 2013. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 99 papers.

0numbers the graph read from it
0cells of the map it votes in
99citing papers in PubMed
25.0field-weighted citation impact, top 1% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

99 citing papers in PubMed, 286 citations in OpenAlex.

  1. Overexpression ofInternational journal of molecular sciences · 2026
    Article
  2. Article
  3. Overexpression ofBiology · 2026
    Article
  4. Article
  5. Article
  6. Characterization of the Soybean (Plants (Basel, Switzerland) · 2025
    Article
  7. Article
  8. Root Exudates in Soilless Culture Conditions.Plants (Basel, Switzerland) · 2025
    Review
  9. Article
  10. Article
  11. Frontiers in plant science · 2025
    Article
  12. Article
  13. A Virulence Factor fromPlants (Basel, Switzerland) · 2024
    Article
  14. Article
  15. Review
  16. Article
  17. UnregulatedInternational journal of molecular sciences · 2024
    Article
  18. Article
  19. Investigating the involvement of potato (Frontiers in plant science · 2024
    Article
  20. Article

39 more citing papers are in PubMed but not listed here.

4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

10 authors at 4 institutions in 2 countries.

Cuiyue LiangState Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Root Biology Center, South China Agricultural University, Guangzhou 510642, People's Republic of China.
Miguel A Piñeros
Jiang Tian
Zhufang Yao
Lili Sun
Jiping Liu
Jon Shaff
Alison Coluccio
Leon V Kochian
Hong Liao
Tropical Crops Genetic Resources Institute · CNSouth China Agricultural University · CNRobert W. Holley Center for Agriculture & Health · USUnited States Department of Agriculture · US

Funding

No grant is acknowledged in the PubMed record.

6 · The paper itself

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.

Indexed as

AcidsAdaptation, PhysiologicalAluminumAnimalsArabidopsisBiomassCell MembraneGene Expression Regulation, PlantGenes, PlantGenotypeGlycine maxHydrogen-Ion ConcentrationMalatesMeristemOocytesOrganic Anion TransportersAcidsAluminumMalatesmalic acidOrganic Anion TransportersPhosphorusPlant ProteinsSoil

Identifiers

PMID23341359
PMCPMC3585601
OpenAlexW2116784531

What OpenQuestion holds

Textmetadata
Read underepoch 390

Registered trials

None linked

Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.