Paper · 2020 · Frontiers in Plant Science

Synergisms of Microbial Consortia, N Forms, and Micronutrients Alleviate Oxidative Damage and Stimulate Hormonal Cold Stress Adaptations in Maize

Narges Moradtalab; Aneesh Ahmed; Joerg Geistlinger; et al.

15
claims
26
verbatim quotes
53
citations
3
research areas
✓
Open access · cc-by

Abstract

Aims: Low soil temperature in spring is a major constraint for the cultivation of tropical crops in temperate climates. This study aims at the exploitation of synergistic interactions of micronutrients, consortia of plant growth-promoting microorganisms and N forms as cold-stress protectants. Methods: Maize seedlings were exposed for two weeks to low root zone temperatures at 8-14 °C under controlled conditions on a silty clay-loam soil (pH 6.9) collected from a maize field cultivation site. A pre-selection trial with fungal and bacterial PGPM strains revealed superior cold-protective performance for a microbial consortium of Trichoderma harzianum OMG16 and Bacillus spp. with Zn/Mn supplementation (CombiA+), particularly combined with N-ammonium as a starting point for the characterization of the underlying physiological and molecular mechanisms. Results: In maize nitrate-treated plants, the cold stress treatment increased oxidative leaf damage by 133% and reduced the shoot biomass by 25%, explained by the reduced acquisition of phosphate (P), zinc (Zn) and manganese (Mn). The supplying of N as ammonium improved the Zn and Mn maize nutritional status and increased the ABA shoot concentration by 33%, as well as moderately increased detoxification of reactive oxygen species (ROS). Moreover, use of N as ammonium also increased the root auxin (IAA) concentration (+76%), with increased expression of auxin-responsive genes, involved in IAA synthesis (ZmTSA), transport (ZmPIN1a), and perception (ZmARF12). Additional inoculation with the microbial consortium promoted root colonization with the inoculant strain T. harzianum OMG16 in combination with ammonium fertilization (+140%). An increased ABA/cytokinin ratio and increased concentrations of jasmonic (JA) and salicylic acids (SA) were related to a further increase in enzymatic and non-enzymatic ROS detoxification. Additional supplementation with Zn and Mn further increased shoot IAA, root length and total antioxidants, resulting in the highest shoot biomass production and the lowest leaf damage by oxidative chemical species. Conclusions: Our results suggest the mitigation of cold stress and reduction of stress priming effects on maize plants due to improved ROS detoxification and induction of hormonal stress adaptations rely on the strategic combination of stress-protective nutrients with selected microbial inoculants.

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Claims 15

Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Cold stress increased oxidative leaf damage by 133% in nitrate-treated maize.

Taxon
maizeZea mayse1
Treatment
the cold stress treatmente1
Outcome
oxidative leaf damagee1
Direction
increasede1
Value
133%e1
Qualifier
nitrate-treated plantse1

Not reportedComparator

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

Zea mays
Zea mays · TaxonAkwugo · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e1

“In maize nitrate-treated plants, the cold stress treatment increased oxidative leaf damage by 133% and reduced the shoot biomass by 25%”

✓ located verbatim in the source · abstract, characters 868–1003 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Cold stress reduced shoot biomass by 25% in nitrate-treated maize.

Taxon
maizeZea mayse1
Treatment
the cold stress treatmente1
Outcome
shoot biomasse1
Direction
reducede1
Value
25%e1
Qualifier
nitrate-treated plantse1

Not reportedComparator

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

Zea mays
Zea mays · TaxonAkwugo · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e1

“In maize nitrate-treated plants, the cold stress treatment increased oxidative leaf damage by 133% and reduced the shoot biomass by 25%”

✓ located verbatim in the source · abstract, characters 868–1003 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

The shoot biomass reduction under cold stress is explained by reduced acquisition of phosphate, zinc and manganese.

Taxon
maizeZea mayse1
Outcome
shoot biomasse1
Qualifier
reduced acquisition of phosphate (P), zinc (Zn) and manganese (Mn)e2

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

Zea mays
Zea mays · TaxonAkwugo · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e1

“In maize nitrate-treated plants, the cold stress treatment increased oxidative leaf damage by 133% and reduced the shoot biomass by 25%”

✓ located verbatim in the source · abstract, characters 868–1003 · show in text ↑
e2

“explained by the reduced acquisition of phosphate (P), zinc (Zn) and manganese (Mn)”

✓ located verbatim in the source · abstract, characters 1005–1088 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Supplying N as ammonium improved the zinc and manganese nutritional status of maize.

Taxon
maizeZea mayse3
Treatment
supplying of N as ammoniume3
Outcome
nutritional statuse3
Direction
improvede3

Not reportedComparator

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

Zea mays
Zea mays · TaxonAkwugo · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e3

“The supplying of N as ammonium improved the Zn and Mn maize nutritional status and increased the ABA shoot concentration by 33%, as well as moderately increased detoxification of reactive oxygen species (ROS)”

✓ located verbatim in the source · abstract, characters 1090–1298 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Supplying N as ammonium increased shoot ABA concentration by 33% in maize.

Taxon
maizeZea mayse3
Treatment
supplying of N as ammoniume3
Compound
ABAe3
Outcome
ABA shoot concentratione3
Direction
increasede3
Value
33%e3

Not reportedComparator

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

Zea mays
Zea mays · TaxonAkwugo · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e3

“The supplying of N as ammonium improved the Zn and Mn maize nutritional status and increased the ABA shoot concentration by 33%, as well as moderately increased detoxification of reactive oxygen species (ROS)”

✓ located verbatim in the source · abstract, characters 1090–1298 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Supplying N as ammonium moderately increased detoxification of reactive oxygen species in maize.

Taxon
maizeZea mayse3
Treatment
supplying of N as ammoniume3
Outcome
detoxification of reactive oxygen species (ROS)e3
Direction
increasede3
Qualifier
moderatelye3

Not reportedComparator

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

Zea mays
Zea mays · TaxonAkwugo · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e3

“The supplying of N as ammonium improved the Zn and Mn maize nutritional status and increased the ABA shoot concentration by 33%, as well as moderately increased detoxification of reactive oxygen species (ROS)”

✓ located verbatim in the source · abstract, characters 1090–1298 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Use of N as ammonium increased root auxin (IAA) concentration by 76% in maize.

Taxon
MaizeZea mayst0
Treatment
use of N as ammoniume4
Outcome
root auxin (IAA) concentratione4
Direction
increasede4
Value
+76%e4

Not reportedComparator

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

Zea mays
Zea mays · TaxonAkwugo · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

t0

“Hormonal Cold Stress Adaptations in Maize”

✓ located verbatim in the source · title, characters 104–145 · show in text ↑
e4

“use of N as ammonium also increased the root auxin (IAA) concentration (+76%)”

✓ located verbatim in the source · abstract, characters 1310–1387 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Use of N as ammonium increased expression of the auxin-responsive genes ZmTSA, ZmPIN1a and ZmARF12 in maize.

Taxon
MaizeZea mayst0
Treatment
use of N as ammoniume4
Gene
ZmTSAe5
Outcome
expression of auxin-responsive genese5
Direction
increasede5
Qualifier
transport (ZmPIN1a), and perception (ZmARF12)e5

Not reportedComparator

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

Zea mays
Zea mays · TaxonAkwugo · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e4

“use of N as ammonium also increased the root auxin (IAA) concentration (+76%)”

✓ located verbatim in the source · abstract, characters 1310–1387 · show in text ↑
t0

“Hormonal Cold Stress Adaptations in Maize”

✓ located verbatim in the source · title, characters 104–145 · show in text ↑
e5

“with increased expression of auxin-responsive genes, involved in IAA synthesis (ZmTSA), transport (ZmPIN1a), and perception (ZmARF12)”

✓ located verbatim in the source · abstract, characters 1389–1522 · show in text ↑
Associationobservedoriginal resultmeasured

Claim · model-written summary

An increased ABA/cytokinin ratio and higher jasmonic and salicylic acid levels were associated with increased ROS detoxification in maize.

Taxon
MaizeZea mayst0
Compound
jasmonic (JA) and salicylic acids (SA)e6
Outcome
enzymatic and non-enzymatic ROS detoxificatione6
Direction
increasee6

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

Zea mays
Zea mays · TaxonAkwugo · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

t0

“Hormonal Cold Stress Adaptations in Maize”

✓ located verbatim in the source · title, characters 104–145 · show in text ↑
e6

“An increased ABA/cytokinin ratio and increased concentrations of jasmonic (JA) and salicylic acids (SA) were related to a further increase in enzymatic and non-enzymatic ROS detoxification”

✓ located verbatim in the source · abstract, characters 1701–1889 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Additional supplementation with Zn and Mn increased shoot IAA, root length and total antioxidants in maize.

Taxon
MaizeZea mayst0
Treatment
Additional supplementation with Zn and Mne7
Outcome
shoot IAA, root length and total antioxidantse7
Direction
increasede7

Not reportedComparator

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

Zea mays
Zea mays · TaxonAkwugo · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

t0

“Hormonal Cold Stress Adaptations in Maize”

✓ located verbatim in the source · title, characters 104–145 · show in text ↑
e7

“Additional supplementation with Zn and Mn further increased shoot IAA, root length and total antioxidants, resulting in the highest shoot biomass production and the lowest leaf damage by oxidative chemical species”

✓ located verbatim in the source · abstract, characters 1891–2104 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Additional supplementation with Zn and Mn gave the highest shoot biomass production in maize.

Taxon
MaizeZea mayst0
Treatment
Additional supplementation with Zn and Mne7
Outcome
shoot biomass productione7
Direction
higheste7

Not reportedComparator

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

Zea mays
Zea mays · TaxonAkwugo · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

t0

“Hormonal Cold Stress Adaptations in Maize”

✓ located verbatim in the source · title, characters 104–145 · show in text ↑
e7

“Additional supplementation with Zn and Mn further increased shoot IAA, root length and total antioxidants, resulting in the highest shoot biomass production and the lowest leaf damage by oxidative chemical species”

✓ located verbatim in the source · abstract, characters 1891–2104 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Additional supplementation with Zn and Mn gave the lowest leaf damage in maize.

Taxon
MaizeZea mayst0
Treatment
Additional supplementation with Zn and Mne7
Outcome
leaf damagee7
Direction
loweste7

Not reportedComparator

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

Zea mays
Zea mays · TaxonAkwugo · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

t0

“Hormonal Cold Stress Adaptations in Maize”

✓ located verbatim in the source · title, characters 104–145 · show in text ↑
e7

“Additional supplementation with Zn and Mn further increased shoot IAA, root length and total antioxidants, resulting in the highest shoot biomass production and the lowest leaf damage by oxidative chemical species”

✓ located verbatim in the source · abstract, characters 1891–2104 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Inoculation with the microbial consortium promoted root colonization by T. harzianum OMG16 in combination with ammonium fertilization (+140%) in maize.

Taxon
MaizeZea mayst0
Treatment
inoculation with the microbial consortiume1
Interactor
T. harzianum OMG16Trichoderma harzianume1symbiont
Outcome
root colonizatione1
Direction
promotede1
Value
+140%e1
Qualifier
in combination with ammonium fertilizatione1

Not reportedComparator

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

Zea mays
Zea mays · TaxonAkwugo · CC BY-SA 4.0 · Wikimedia Commons ↗
Trichoderma harzianum
Trichoderma harzianum · InteractorUS Department of Agriculture, Agricultural Research Service, Systematic Botany and Mycology Laboratory, [1] · Public domain · Wikimedia Commons ↗

Verbatim

t0

“Hormonal Cold Stress Adaptations in Maize”

✓ located verbatim in the source · title, characters 104–145 · show in text ↑
e1

“Additional inoculation with the microbial consortium promoted root colonization with the inoculant strain T. harzianum OMG16 in combination with ammonium fertilization (+140%)”

✓ located verbatim in the source · abstract, characters 1524–1699 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

A pre-selection trial found superior cold-protective performance for a consortium of Trichoderma harzianum OMG16 and Bacillus spp. with Zn/Mn supplementation.

Taxon
MaizeZea mayst0
Treatment
a microbial consortium of Trichoderma harzianum OMG16 and Bacillus spp. with Zn/Mn supplementation (CombiA+)e1
Interactor
Trichoderma harzianum OMG16Trichoderma harzianume1symbiont
Second interactor
Bacillus spp.e1symbiont
Outcome
cold-protective performancee1
Direction
superiore1
Comparator
fungal and bacterial PGPM strainse1

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

Zea mays
Zea mays · TaxonAkwugo · CC BY-SA 4.0 · Wikimedia Commons ↗
Trichoderma harzianum
Trichoderma harzianum · InteractorUS Department of Agriculture, Agricultural Research Service, Systematic Botany and Mycology Laboratory, [1] · Public domain · Wikimedia Commons ↗

Verbatim

t0

“Hormonal Cold Stress Adaptations in Maize”

✓ located verbatim in the source · title, characters 104–145 · show in text ↑
e1

“A pre-selection trial with fungal and bacterial PGPM strains revealed superior cold-protective performance for a microbial consortium of Trichoderma harzianum OMG16 and Bacillus spp. with Zn/Mn supplementation (CombiA+)”

✓ located verbatim in the source · abstract, characters 497–716 · show in text ↑
Recommendationauthor interpretationoriginal resultpositivebasis n/a

Claim · model-written summary

Mitigation of cold stress in maize relies on a strategic combination of stress-protective nutrients with selected microbial inoculants.

Taxon
MaizeZea mayst0
Outcome
mitigation of cold stresse1

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

Zea mays
Zea mays · TaxonAkwugo · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

t0

“Hormonal Cold Stress Adaptations in Maize”

✓ located verbatim in the source · title, characters 104–145 · show in text ↑
e1

“Our results suggest the mitigation of cold stress and reduction of stress priming effects on maize plants due to improved ROS detoxification and induction of hormonal stress adaptations rely on the strategic combination of stress-protective nutrients with selected microbial inoculants”

✓ located verbatim in the source · abstract, characters 2119–2404 · show in text ↑

zinc atom · growth · Zea mays (maize)Results differ

224 papers: 183 positive, 41 negative or no effect

182 papers in the same direction as this paper · 41 in the opposite direction

  1. positive
    Zinc supplementation recovered growth in zinc-deficient maize.

    Gibberellin Relationships in Zinc-Deficient Plants · 1986 · compared with zinc-deficient maize plants

    Same directionCited by this paper

  2. no effect
  3. no effect

220 papers more in this group

See all 224 papers →

zinc atom · yield · Zea mays (maize)Results differ

441 papers: 391 positive, 50 negative or no effect

390 papers in the same direction as this paper · 47 in the opposite direction · 3 reporting no difference from an alternative

  1. positive
  2. negative
  3. negative

437 papers more in this group

See all 441 papers →

zinc atom · pest · Zea mays (maize)Positive and negative results

9 papers: 7 positive, 2 negative or no effect

6 papers in the same direction as this paper · 2 in the opposite direction

  1. no effect
  2. negative
  3. positive

5 papers more in this group

See all 9 papers →

manganese atom · growth · Zea mays (maize)Positive and negative results

18 papers: 16 positive, 2 negative or no effect

15 papers in the same direction as this paper · 2 in the opposite direction

  1. negative
  2. negative
  3. positive

14 papers more in this group

See all 18 papers →

manganese atom · yield · Zea mays (maize)Positive and negative results

28 papers: 22 positive, 6 negative or no effect

21 papers in the same direction as this paper · 5 in the opposite direction · 1 reporting no difference from an alternative

  1. positive
  2. negative
  3. no effect

24 papers more in this group

See all 28 papers →

manganese atom · pest · Zea mays (maize)Results agree

3 papers: 3 positive, 0 negative or no effect

2 papers in the same direction as this paper

  1. positive
  2. positive
See all 3 papers →

cold · growth · Zea mays (maize)Results differ

73 papers: 16 positive, 57 negative or no effect

56 papers in the same direction as this paper · 16 in the opposite direction

  1. negative
  2. positive
  3. positive

69 papers more in this group

See all 73 papers →

cold · pest · Zea mays (maize)Positive and negative results

9 papers: 2 positive, 7 negative or no effect

6 papers in the same direction as this paper · 2 in the opposite direction

  1. positive
  2. positive
  3. no effect

5 papers more in this group

See all 9 papers →

8 of 10 groups shown: named compounds and organisms first, then groups whose results differ (checked claim by claim), then those with positive and negative results, then the smaller groups.

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.