Paper · 2014 · PLANT PHYSIOLOGY

Malate Synthesis and Secretion Mediated by a Manganese-Enhanced Malate Dehydrogenase Confers Superior Manganese Tolerance in Stylosanthes guianensis

Zhijian Chen; Lili Sun; Pandao Liu; et al.

16
claims
24
verbatim quotes
134
citations
2
research areas
✓
Open access

Abstract

Manganese (Mn) toxicity is a major constraint limiting plant growth on acidic soils. Superior Mn tolerance in Stylosanthes spp. has been well documented, but its molecular mechanisms remain largely unknown. In this study, superior Mn tolerance in Stylosanthes guianensis was confirmed, as reflected by a high Mn toxicity threshold. Furthermore, genetic variation of Mn tolerance was evaluated using two S. guianensis genotypes, which revealed that the Fine-stem genotype had higher Mn tolerance than the TPRC2001-1 genotype, as exhibited through less reduction in dry weight under excess Mn, and accompanied by lower internal Mn concentrations. Interestingly, Mn-stimulated increases in malate concentrations and exudation rates were observed only in the Fine-stem genotype. Proteomic analysis of Fine-stem roots revealed that S. guianensis Malate Dehydrogenase1 (SgMDH1) accumulated in response to Mn toxicity. Western-blot and quantitative PCR analyses showed that Mn toxicity resulted in increased SgMDH1 accumulation only in Fine-stem roots, but not in TPRC2001-1. The function of SgMDH1-mediated malate synthesis was verified through in vitro biochemical analysis of SgMDH1 activities against oxaloacetate, as well as in vivo increased malate concentrations in yeast (Saccharomyces cerevisiae), soybean (Glycine max) hairy roots, and Arabidopsis (Arabidopsis thaliana) with SgMDH1 overexpression. Furthermore, SgMDH1 overexpression conferred Mn tolerance in Arabidopsis, which was accompanied by increased malate exudation and reduced plant Mn concentrations, suggesting that secreted malate could alleviate Mn toxicity in plants. Taken together, we conclude that the superior Mn tolerance of S. guianensis is achieved by coordination of internal and external Mn detoxification through malate synthesis and exudation, which is regulated by SgMDH1 at both transcription and protein levels.

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Claims 16

Observationobservedoriginal resultpositivemeasured

Claim · model-written summary

Stylosanthes guianensis had a high manganese toxicity threshold.

Taxon
Stylosanthes guianensisStylosanthes guianensise0
Outcome
high Mn toxicity thresholde0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Stylosanthes guianensis
Stylosanthes guianensis · TaxonHarry Rose from South West Rocks, Australia · CC BY 2.0 · Wikimedia Commons ↗

Verbatim

e0

“superior Mn tolerance in Stylosanthes guianensis was confirmed, as reflected by a high Mn toxicity threshold.”

✓ located verbatim in the source · abstract, characters 222–331 · show in text ↑
Observationobservedoriginal resultpositivemeasured

Claim · model-written summary

Fine-stem had higher manganese tolerance than TPRC2001-1.

Taxon
Stylosanthes guianensisStylosanthes guianensist0
Material
Fine-stem genotypee0
Outcome
Mn tolerancee0
Direction
highere0
Comparator
TPRC2001-1 genotypee0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Stylosanthes guianensis
Stylosanthes guianensis · TaxonHarry Rose from South West Rocks, Australia · CC BY 2.0 · Wikimedia Commons ↗

Verbatim

e0

“the Fine-stem genotype had higher Mn tolerance than the TPRC2001-1 genotype, as exhibited through less reduction in dry weight under excess Mn, and accompanied by lower internal Mn concentrations.”

✓ located verbatim in the source · abstract, characters 448–644 · show in text ↑
t0

“Stylosanthes guianensis”

✓ located verbatim in the source · title, characters 125–148 · show in text ↑
Observationobservedoriginal resultpositivemeasured

Claim · model-written summary

Under excess manganese, Fine-stem showed less dry-weight reduction than TPRC2001-1.

Taxon
Stylosanthes guianensisStylosanthes guianensist0
Material
Fine-stem genotypee0
Outcome
dry weighte0
Direction
less reductione0
Qualifier
under excess Mne0
Comparator
TPRC2001-1 genotypee0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Stylosanthes guianensis
Stylosanthes guianensis · TaxonHarry Rose from South West Rocks, Australia · CC BY 2.0 · Wikimedia Commons ↗

Verbatim

e0

“the Fine-stem genotype had higher Mn tolerance than the TPRC2001-1 genotype, as exhibited through less reduction in dry weight under excess Mn, and accompanied by lower internal Mn concentrations.”

✓ located verbatim in the source · abstract, characters 448–644 · show in text ↑
t0

“Stylosanthes guianensis”

✓ located verbatim in the source · title, characters 125–148 · show in text ↑
Observationobservedoriginal resultpositivemeasured

Claim · model-written summary

Fine-stem had lower internal manganese concentration than TPRC2001-1.

Taxon
Stylosanthes guianensisStylosanthes guianensist0
Material
Fine-stem genotypee0
Outcome
internal Mn concentrationse0
Direction
lowere0
Comparator
TPRC2001-1 genotypee0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Stylosanthes guianensis
Stylosanthes guianensis · TaxonHarry Rose from South West Rocks, Australia · CC BY 2.0 · Wikimedia Commons ↗

Verbatim

e0

“the Fine-stem genotype had higher Mn tolerance than the TPRC2001-1 genotype, as exhibited through less reduction in dry weight under excess Mn, and accompanied by lower internal Mn concentrations.”

✓ located verbatim in the source · abstract, characters 448–644 · show in text ↑
t0

“Stylosanthes guianensis”

✓ located verbatim in the source · title, characters 125–148 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Manganese increased malate concentration only in Fine-stem.

Taxon
Stylosanthes guianensisStylosanthes guianensist0
Material
Fine-stem genotypee0
Treatment
Mne0
Outcome
malate concentrationse0
Direction
increasese0

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Stylosanthes guianensis
Stylosanthes guianensis · TaxonHarry Rose from South West Rocks, Australia · CC BY 2.0 · Wikimedia Commons ↗

Verbatim

e0

“Mn-stimulated increases in malate concentrations and exudation rates were observed only in the Fine-stem genotype.”

✓ located verbatim in the source · abstract, characters 660–774 · show in text ↑
t0

“Stylosanthes guianensis”

✓ located verbatim in the source · title, characters 125–148 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Manganese increased malate exudation rate only in Fine-stem.

Taxon
Stylosanthes guianensisStylosanthes guianensist0
Material
Fine-stem genotypee0
Treatment
Mne0
Outcome
exudation ratese0
Direction
increasese0

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Stylosanthes guianensis
Stylosanthes guianensis · TaxonHarry Rose from South West Rocks, Australia · CC BY 2.0 · Wikimedia Commons ↗

Verbatim

e0

“Mn-stimulated increases in malate concentrations and exudation rates were observed only in the Fine-stem genotype.”

✓ located verbatim in the source · abstract, characters 660–774 · show in text ↑
t0

“Stylosanthes guianensis”

✓ located verbatim in the source · title, characters 125–148 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

SgMDH1 accumulated in Fine-stem roots during manganese toxicity.

Taxon
Stylosanthes guianensisStylosanthes guianensist0
Material
Fine-steme0
Organ / stage
rootse0
Treatment
Mn toxicitye0
Gene
S. guianensis Malate Dehydrogenase1 (SgMDH1)e0
Outcome
accumulatede0
Direction
accumulatede0

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Stylosanthes guianensis
Stylosanthes guianensis · TaxonHarry Rose from South West Rocks, Australia · CC BY 2.0 · Wikimedia Commons ↗

Verbatim

e0

“Proteomic analysis of Fine-stem roots revealed that S. guianensis Malate Dehydrogenase1 (SgMDH1) accumulated in response to Mn toxicity.”

✓ located verbatim in the source · abstract, characters 775–911 · show in text ↑
t0

“Stylosanthes guianensis”

✓ located verbatim in the source · title, characters 125–148 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Manganese toxicity increased SgMDH1 accumulation in Fine-stem roots.

Taxon
Stylosanthes guianensisStylosanthes guianensist0
Material
Fine-steme0
Organ / stage
rootse0
Treatment
Mn toxicitye0
Gene
SgMDH1e0
Outcome
SgMDH1 accumulatione0
Direction
increasede0

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Stylosanthes guianensis
Stylosanthes guianensis · TaxonHarry Rose from South West Rocks, Australia · CC BY 2.0 · Wikimedia Commons ↗

Verbatim

e0

“Mn toxicity resulted in increased SgMDH1 accumulation only in Fine-stem roots, but not in TPRC2001-1.”

✓ located verbatim in the source · abstract, characters 967–1068 · show in text ↑
t0

“Stylosanthes guianensis”

✓ located verbatim in the source · title, characters 125–148 · show in text ↑
Intervention effectobservedoriginal resultno effectmeasured

Claim · model-written summary

Manganese toxicity did not increase SgMDH1 accumulation in TPRC2001-1.

Taxon
Stylosanthes guianensisStylosanthes guianensist0
Material
TPRC2001-1e0
Treatment
Mn toxicitye0
Gene
SgMDH1e0
Outcome
SgMDH1 accumulatione0

Not reportedComparatorDirection

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Stylosanthes guianensis
Stylosanthes guianensis · TaxonHarry Rose from South West Rocks, Australia · CC BY 2.0 · Wikimedia Commons ↗

Verbatim

e0

“Mn toxicity resulted in increased SgMDH1 accumulation only in Fine-stem roots, but not in TPRC2001-1.”

✓ located verbatim in the source · abstract, characters 967–1068 · show in text ↑
t0

“Stylosanthes guianensis”

✓ located verbatim in the source · title, characters 125–148 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

SgMDH1 overexpression increased malate concentration in soybean hairy roots.

Taxon
soybean (Glycine max)Glycine maxe0
Organ / stage
hairy rootse0
Treatment
SgMDH1 overexpressione0
Gene
SgMDH1e0
Outcome
malate concentrationse0
Direction
increasede0

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Glycine max
Glycine max · TaxonPublic domain · Wikimedia Commons ↗

Verbatim

e0

“in vivo increased malate concentrations in yeast (Saccharomyces cerevisiae), soybean (Glycine max) hairy roots, and Arabidopsis (Arabidopsis thaliana) with SgMDH1 overexpression.”

✓ located verbatim in the source · abstract, characters 1223–1401 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

SgMDH1 overexpression increased malate concentration in Arabidopsis.

Taxon
Arabidopsis (Arabidopsis thaliana)Arabidopsis thalianae0
Treatment
SgMDH1 overexpressione0
Gene
SgMDH1e0
Outcome
malate concentrationse0
Direction
increasede0

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Arabidopsis thaliana
Arabidopsis thaliana · TaxonOriginal uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“in vivo increased malate concentrations in yeast (Saccharomyces cerevisiae), soybean (Glycine max) hairy roots, and Arabidopsis (Arabidopsis thaliana) with SgMDH1 overexpression.”

✓ located verbatim in the source · abstract, characters 1223–1401 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

SgMDH1 overexpression conferred manganese tolerance in Arabidopsis.

Taxon
ArabidopsisArabidopsise0
Treatment
SgMDH1 overexpressione0
Gene
SgMDH1e0
Outcome
Mn tolerancee0

Not reportedComparatorDirection

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Arabidopsis
Arabidopsis · Taxon · picture of the genus (one of its species)Original uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“SgMDH1 overexpression conferred Mn tolerance in Arabidopsis, which was accompanied by increased malate exudation and reduced plant Mn concentrations, suggesting that secreted malate could alleviate Mn toxicity in plants.”

✓ located verbatim in the source · abstract, characters 1415–1635 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

SgMDH1 overexpression increased malate exudation in Arabidopsis.

Taxon
ArabidopsisArabidopsise0
Treatment
SgMDH1 overexpressione0
Gene
SgMDH1e0
Outcome
malate exudatione0
Direction
increasede0

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Arabidopsis
Arabidopsis · Taxon · picture of the genus (one of its species)Original uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“SgMDH1 overexpression conferred Mn tolerance in Arabidopsis, which was accompanied by increased malate exudation and reduced plant Mn concentrations, suggesting that secreted malate could alleviate Mn toxicity in plants.”

✓ located verbatim in the source · abstract, characters 1415–1635 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

SgMDH1 overexpression reduced plant manganese concentration in Arabidopsis.

Taxon
ArabidopsisArabidopsise0
Treatment
SgMDH1 overexpressione0
Gene
SgMDH1e0
Outcome
plant Mn concentrationse0
Direction
reducede0

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Arabidopsis
Arabidopsis · Taxon · picture of the genus (one of its species)Original uploader was Brona at en.wikipedia . User:Roepers at nl.wikipedia · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“SgMDH1 overexpression conferred Mn tolerance in Arabidopsis, which was accompanied by increased malate exudation and reduced plant Mn concentrations, suggesting that secreted malate could alleviate Mn toxicity in plants.”

✓ located verbatim in the source · abstract, characters 1415–1635 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

Secreted malate was proposed to alleviate manganese toxicity in plants.

Taxon
plantsViridiplantaee0
Compound
secreted malatee0
Outcome
alleviate Mn toxicitye0

Verbatim

e0

“SgMDH1 overexpression conferred Mn tolerance in Arabidopsis, which was accompanied by increased malate exudation and reduced plant Mn concentrations, suggesting that secreted malate could alleviate Mn toxicity in plants.”

✓ located verbatim in the source · abstract, characters 1415–1635 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

SgMDH1-regulated malate synthesis and exudation were proposed to coordinate internal and external manganese detoxification in S. guianensis.

Taxon
S. guianensisStylosanthes guianensise0
Gene
SgMDH1e0
Outcome
superior Mn tolerancee0
Qualifier
coordination of internal and external Mn detoxification through malate synthesis and exudatione0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Stylosanthes guianensis
Stylosanthes guianensis · TaxonHarry Rose from South West Rocks, Australia · CC BY 2.0 · Wikimedia Commons ↗

Verbatim

e0

“the superior Mn tolerance of S. guianensis is achieved by coordination of internal and external Mn detoxification through malate synthesis and exudation, which is regulated by SgMDH1 at both transcription and protein levels.”

✓ located verbatim in the source · abstract, characters 1669–1893 · show in text ↑

manganese atom · molecular: metabolites · Stylosanthes guianensis (stylo)Results agree

2 papers: 2 positive, 0 negative or no effect

1 paper in the same direction as this paper

  1. positive
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Claims are grouped by organism, treatment and what was measured or targeted. A paper counts as positive when any of its claims in the group is positive.