Paper · 2025 · Frontiers in Plant Science

The involvement of arbuscular mycorrhizal fungi in modulating polyamine metabolism and low-temperature tolerance enhancement in white clover

Songyuan Yao; Lin Li; Haitang Xiong; et al.

11
claims
29
verbatim quotes
3
citations
3
research areas
✓
Open access · cc-by

Abstract

Sustained low temperatures can prevent white clover ( Trifolium repens L.) from overwintering and regreening, making it difficult to revive the plants in the spring. Arbuscular mycorrhizal fungi (AMF) are widely known for their ability to enhance host stress tolerance. It is unclear whether AMF can enhance the low-temperature tolerance of white clover, which is associated with polyamines. The purpose of this study was to examine how inoculating white clover with an arbuscular mycorrhizal fungus Funneliformis mosseae affected the biomass, leaf chlorophyll and gas exchange, levels of root polyamines (putrescine, spermidine, and spermine), activities of key polyamine-related enzymes, and the expression level of the S-adenosyl-L-methionine decarboxylase ( TrSAMDC1 ) gene at low temperatures (4°C for four days). The low-temperature treatment inhibited the root mycorrhizal colonization rate. Mycorrhizal inoculation significantly increased shoot, root, and total biomass, with greater increases found at optimal temperatures (22°C/18°C, 16 h/8 h, day/night temperature) than at low temperatures. Similarly, AMF inoculation significantly improved leaf gas exchange parameters, with larger increases observed at optimal temperatures than at low temperatures. Low temperatures caused a considerable increase in putrescine and spermidine levels, while simultaneously decreasing spermine levels. Mycorrhizal inoculation elevated putrescine, spermidine, and spermine levels regardless of temperature conditions, along with a significant rise in the (spermidine+spermine)/putrescine ratio. Mycorrhizal plants also exhibited considerably increased activities of arginine decarboxylase and polyamine oxidase, but not ornithine decarboxylase, in response to low temperatures. Mycorrhizal inoculation, together with low temperatures, elevated TrSAMDC1 expression. The observed alterations in mycorrhiza-mediated polyamines were primarily attributed to increased arginine decarboxylase activity and TrSAMDC1 expression. This study demonstrated the role of mycorrhizal fungi in modulating polyamine metabolism and enhancing plant tolerance to low-temperature stress.

Abstract from the paper’s OpenAlex record; open copy licensed cc-by. Read at the source ↗

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Claims 11

Intervention effectobservedoriginal resultpositivesignificant (as stated)measured

Claim · model-written summary

Funneliformis mosseae inoculation significantly increased shoot, root and total biomass of white clover, with greater increases at optimal than at low temperatures.

Taxon
white cloverTrifolium repense0
Treatment
Mycorrhizal inoculatione1
Interactor
Funneliformis mosseaeFunneliformis mosseaee4symbiont
Outcome
shoot, root, and total biomasse1
Direction
increasede1
Qualifier
greater increases found at optimal temperaturese2

Not reportedComparator

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

Trifolium repens
Trifolium repens · TaxonIvar Leidus · CC BY-SA 4.0 · Wikimedia Commons ↗
Funneliformis mosseae
Funneliformis mosseae · Interactor · picture from its Wikimedia Commons categorySamson90 · CC0 · Wikimedia Commons ↗

Verbatim

e0

“Sustained low temperatures can prevent white clover ( Trifolium repens L.) from overwintering and regreening”

✓ located verbatim in the source · abstract, characters 0–108 · show in text ↑
e1

“Mycorrhizal inoculation significantly increased shoot, root, and total biomass”

✓ located verbatim in the source · abstract, characters 899–977 · show in text ↑
e2

“with greater increases found at optimal temperatures (22°C/18°C, 16 h/8 h, day/night temperature) than at low temperatures”

✓ located verbatim in the source · abstract, characters 979–1101 · show in text ↑
e4

“inoculating white clover with an arbuscular mycorrhizal fungus Funneliformis mosseae”

✓ located verbatim in the source · abstract, characters 437–521 · show in text ↑
Intervention effectobservedoriginal resultpositivesignificant (as stated)measured

Claim · model-written summary

AMF inoculation significantly improved leaf gas exchange parameters of white clover, with larger increases at optimal than at low temperatures.

Taxon
white cloverTrifolium repense0
Treatment
AMF inoculatione3
Interactor
Funneliformis mosseaeFunneliformis mosseaee4symbiont
Outcome
leaf gas exchange parameterse3
Direction
improvede3
Qualifier
larger increases observed at optimal temperaturese3

Not reportedComparator

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

Trifolium repens
Trifolium repens · TaxonIvar Leidus · CC BY-SA 4.0 · Wikimedia Commons ↗
Funneliformis mosseae
Funneliformis mosseae · Interactor · picture from its Wikimedia Commons categorySamson90 · CC0 · Wikimedia Commons ↗

Verbatim

e0

“Sustained low temperatures can prevent white clover ( Trifolium repens L.) from overwintering and regreening”

✓ located verbatim in the source · abstract, characters 0–108 · show in text ↑
e3

“AMF inoculation significantly improved leaf gas exchange parameters, with larger increases observed at optimal temperatures than at low temperatures”

✓ located verbatim in the source · abstract, characters 1114–1262 · show in text ↑
e4

“inoculating white clover with an arbuscular mycorrhizal fungus Funneliformis mosseae”

✓ located verbatim in the source · abstract, characters 437–521 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Low temperature increased putrescine and spermidine levels in white clover roots.

Taxon
white cloverTrifolium repense0
Treatment
Low temperaturese4
Outcome
putrescine and spermidine levelse4
Direction
increasee4

Not reportedComparator

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

Trifolium repens
Trifolium repens · TaxonIvar Leidus · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“Sustained low temperatures can prevent white clover ( Trifolium repens L.) from overwintering and regreening”

✓ located verbatim in the source · abstract, characters 0–108 · show in text ↑
e4

“Low temperatures caused a considerable increase in putrescine and spermidine levels, while simultaneously decreasing spermine levels”

✓ located verbatim in the source · abstract, characters 1264–1396 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Low temperature decreased spermine levels in white clover.

Taxon
white cloverTrifolium repense0
Treatment
Low temperaturese4
Outcome
spermine levelse4
Direction
decreasinge4

Not reportedComparator

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

Trifolium repens
Trifolium repens · TaxonIvar Leidus · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“Sustained low temperatures can prevent white clover ( Trifolium repens L.) from overwintering and regreening”

✓ located verbatim in the source · abstract, characters 0–108 · show in text ↑
e4

“Low temperatures caused a considerable increase in putrescine and spermidine levels, while simultaneously decreasing spermine levels”

✓ located verbatim in the source · abstract, characters 1264–1396 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Funneliformis mosseae inoculation elevated putrescine, spermidine and spermine levels in white clover regardless of temperature.

Taxon
white cloverTrifolium repense0
Treatment
Mycorrhizal inoculatione5
Interactor
Funneliformis mosseaeFunneliformis mosseaee4symbiont
Outcome
putrescine, spermidine, and spermine levelse5
Direction
elevatede5
Qualifier
regardless of temperature conditionse5

Not reportedComparator

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

Trifolium repens
Trifolium repens · TaxonIvar Leidus · CC BY-SA 4.0 · Wikimedia Commons ↗
Funneliformis mosseae
Funneliformis mosseae · Interactor · picture from its Wikimedia Commons categorySamson90 · CC0 · Wikimedia Commons ↗

Verbatim

e0

“Sustained low temperatures can prevent white clover ( Trifolium repens L.) from overwintering and regreening”

✓ located verbatim in the source · abstract, characters 0–108 · show in text ↑
e5

“Mycorrhizal inoculation elevated putrescine, spermidine, and spermine levels regardless of temperature conditions”

✓ located verbatim in the source · abstract, characters 1398–1511 · show in text ↑
e4

“inoculating white clover with an arbuscular mycorrhizal fungus Funneliformis mosseae”

✓ located verbatim in the source · abstract, characters 437–521 · show in text ↑
Intervention effectobservedoriginal resultsignificant (as stated)measured

Claim · model-written summary

Mycorrhizal inoculation significantly raised the (spermidine+spermine)/putrescine ratio in white clover.

Taxon
white cloverTrifolium repense0
Treatment
Mycorrhizal inoculatione5
Outcome
(spermidine+spermine)/putrescine ratioe6
Direction
risee6

Not reportedComparator

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

Trifolium repens
Trifolium repens · TaxonIvar Leidus · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“Sustained low temperatures can prevent white clover ( Trifolium repens L.) from overwintering and regreening”

✓ located verbatim in the source · abstract, characters 0–108 · show in text ↑
e5

“Mycorrhizal inoculation elevated putrescine, spermidine, and spermine levels regardless of temperature conditions”

✓ located verbatim in the source · abstract, characters 1398–1511 · show in text ↑
e6

“along with a significant rise in the (spermidine+spermine)/putrescine ratio”

✓ located verbatim in the source · abstract, characters 1513–1588 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Under low temperature, mycorrhizal white clover showed considerably increased arginine decarboxylase and polyamine oxidase activities.

Taxon
white cloverTrifolium repense0
Treatment
low temperaturese7
Interactor
Funneliformis mosseaeFunneliformis mosseaee4symbiont
Outcome
activities of arginine decarboxylase and polyamine oxidasee7
Direction
considerably increasede7

Not reportedComparator

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

Trifolium repens
Trifolium repens · TaxonIvar Leidus · CC BY-SA 4.0 · Wikimedia Commons ↗
Funneliformis mosseae
Funneliformis mosseae · Interactor · picture from its Wikimedia Commons categorySamson90 · CC0 · Wikimedia Commons ↗

Verbatim

e0

“Sustained low temperatures can prevent white clover ( Trifolium repens L.) from overwintering and regreening”

✓ located verbatim in the source · abstract, characters 0–108 · show in text ↑
e7

“Mycorrhizal plants also exhibited considerably increased activities of arginine decarboxylase and polyamine oxidase, but not ornithine decarboxylase, in response to low temperatures”

✓ located verbatim in the source · abstract, characters 1590–1771 · show in text ↑
e4

“inoculating white clover with an arbuscular mycorrhizal fungus Funneliformis mosseae”

✓ located verbatim in the source · abstract, characters 437–521 · show in text ↑
Intervention effectobservedoriginal resultno effectmeasured

Claim · model-written summary

Under low temperature, mycorrhizal white clover showed no increase in ornithine decarboxylase activity.

Taxon
white cloverTrifolium repense0
Treatment
low temperaturese7
Interactor
Funneliformis mosseaeFunneliformis mosseaee4symbiont
Outcome
ornithine decarboxylasee7
Direction
but note7

Not reportedComparator

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

Trifolium repens
Trifolium repens · TaxonIvar Leidus · CC BY-SA 4.0 · Wikimedia Commons ↗
Funneliformis mosseae
Funneliformis mosseae · Interactor · picture from its Wikimedia Commons categorySamson90 · CC0 · Wikimedia Commons ↗

Verbatim

e0

“Sustained low temperatures can prevent white clover ( Trifolium repens L.) from overwintering and regreening”

✓ located verbatim in the source · abstract, characters 0–108 · show in text ↑
e7

“Mycorrhizal plants also exhibited considerably increased activities of arginine decarboxylase and polyamine oxidase, but not ornithine decarboxylase, in response to low temperatures”

✓ located verbatim in the source · abstract, characters 1590–1771 · show in text ↑
e4

“inoculating white clover with an arbuscular mycorrhizal fungus Funneliformis mosseae”

✓ located verbatim in the source · abstract, characters 437–521 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Mycorrhizal inoculation together with low temperature elevated TrSAMDC1 expression in white clover.

Taxon
white cloverTrifolium repense0
Treatment
Mycorrhizal inoculation, together with low temperaturese1
Gene
TrSAMDC1e1
Outcome
expressione1
Direction
elevatede1

Not reportedComparator

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

Trifolium repens
Trifolium repens · TaxonIvar Leidus · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“Sustained low temperatures can prevent white clover ( Trifolium repens L.) from overwintering and regreening”

✓ located verbatim in the source · abstract, characters 0–108 · show in text ↑
e1

“Mycorrhizal inoculation, together with low temperatures, elevated TrSAMDC1 expression”

✓ located verbatim in the source · abstract, characters 1773–1858 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

The mycorrhiza-mediated polyamine changes are attributed mainly to higher arginine decarboxylase activity and TrSAMDC1 expression.

Taxon
white cloverTrifolium repense0
Gene
TrSAMDC1e1
Outcome
mycorrhiza-mediated polyaminese1
Qualifier
primarily attributed to increased arginine decarboxylase activitye1

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

Trifolium repens
Trifolium repens · TaxonIvar Leidus · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“Sustained low temperatures can prevent white clover ( Trifolium repens L.) from overwintering and regreening”

✓ located verbatim in the source · abstract, characters 0–108 · show in text ↑
e1

“The observed alterations in mycorrhiza-mediated polyamines were primarily attributed to increased arginine decarboxylase activity and TrSAMDC1 expression”

✓ located verbatim in the source · abstract, characters 1860–2013 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Low temperature inhibited root mycorrhizal colonization in white clover.

Taxon
white cloverTrifolium repense0
Treatment
low-temperature treatmente1
Outcome
root mycorrhizal colonization ratee1
Direction
inhibitede1

Not reportedComparator

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

Trifolium repens
Trifolium repens · TaxonIvar Leidus · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“Sustained low temperatures can prevent white clover ( Trifolium repens L.) from overwintering and regreening”

✓ located verbatim in the source · abstract, characters 0–108 · show in text ↑
e1

“The low-temperature treatment inhibited the root mycorrhizal colonization rate”

✓ located verbatim in the source · abstract, characters 819–897 · show in text ↑

mycorrhiza · Funneliformis mosseae · Trifolium repens (white clover)Positive and negative results

3 papers: 2 positive, 1 negative or no effect

1 paper in the same direction as this paper · 1 in the opposite direction

  1. negative
  2. positive
See all 3 papers →

inoculation · Funneliformis mosseae · Trifolium repens (white clover)Results agree

2 papers: 2 positive, 0 negative or no effect

1 paper in the same direction as this paper

  1. positive
See all 2 papers →

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.