Paper · 2024 · Frontiers in Plant Science

Phosphate accumulation in rice leaves promotes fungal pathogenicity and represses host immune responses during pathogen infection

Héctor Martín-Cardoso; Mireia Bundó; Beatriz Val-Torregrosa; et al.

10
claims
13
verbatim quotes
12
citations
4
research areas
✓
Open access · cc-by

Abstract

Rice is one of the most important crops in the world and a staple food for more than half of the world’s population. At present, the blast disease caused by the fungus Magnaporthe oryzae poses a severe threat to food security through reduction of rice yields worldwide. High phosphate fertilization has previously been shown to increase blast susceptibility. At present, however, our knowledge on the mechanisms underpinning phosphate-induced susceptibility to M. oryzae infection in rice is limited. In this work, we conducted live cell imaging on rice sheaths inoculated with a M. oryzae strain expressing two fluorescently-tagged M. oryzae effectors. We show that growing rice under high phosphate fertilization, and subsequent accumulation of phosphate in leaf sheaths, promotes invasive growth of M. oryzae . Consistent with this, stronger expression of M. oryzae effectors and Pathogenicity Mitogen-activated Protein Kinase ( PMK1 ) occurs in leaf sheaths of rice plants grown under high a phosphate regime. Down-regulation of fungal genes encoding suppressors of plant cell death and up-regulation of plant cell death-inducing effectors also occurs in sheaths of phosphate over-accumulating rice plants. Treatment with high Pi causes alterations in the expression of fungal phosphate transporter genes potentially contributing to pathogen virulence. From the perspective of the plant, Pi accumulation in leaf sheaths prevents H 2 O 2 accumulation early during M. oryzae infection which was associated to a weaker activation of Respiratory Burst Oxidase Homologs ( RBOHs ) genes involved in reactive oxygen species (ROS) production. Further, a weaker activation of defense-related genes occurs during infection in rice plants over-accumulating phosphate. From these results, it can be concluded that phosphate fertilization has an effect on the two interacting partners, pathogen and host. Phosphate-mediated stimulation of fungal effector genes (e.g., potentiation of fungal pathogenicity) in combination with repression of pathogen-inducible immune responses (e.g., ROS accumulation, defense gene expression) explains higher colonization by M. oryzae in rice tissues accumulating phosphate. Phosphate content can therefore be considered as an important factor in determining the outcome of the rice/ M. oryzae interaction. As fertilizers and pesticides are commonly used in rice cultivation to maintain optimal yield and to prevent losses caused by pathogens, a better understanding of how phosphate impacts blast susceptibility is crucial for developing strategies to rationally optimize fertilizer and pesticide use in rice production.

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Claims 10

Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

High phosphate fertilization promoted invasive growth of M. oryzae in rice sheaths.

Organ / stage
leaf sheathse0
Treatment
high phosphate fertilizatione0
Interactor
M. oryzaePyricularia oryzaee0pathogen
Outcome
invasive growth of M. oryzaee0
Direction
promotese0

Not reportedComparator

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

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗
Pyricularia oryzae
Pyricularia oryzae · InteractorJie-Hao Ou · CC BY 4.0 · iNaturalist ↗

Verbatim

e0

“growing rice under high phosphate fertilization, and subsequent accumulation of phosphate in leaf sheaths, promotes invasive growth of M. oryzae”

✓ located verbatim in the source · abstract, characters 667–811 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

High phosphate increased M. oryzae effector expression in rice leaf sheaths.

Organ / stage
leaf sheathse0
Treatment
high a phosphate regimee0
Interactor
M. oryzaePyricularia oryzaee0pathogen
Outcome
expression of M. oryzae effectorse0
Direction
strongere0

Not reportedComparator

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

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗
Pyricularia oryzae
Pyricularia oryzae · InteractorJie-Hao Ou · CC BY 4.0 · iNaturalist ↗

Verbatim

e0

“stronger expression of M. oryzae effectors and Pathogenicity Mitogen-activated Protein Kinase ( PMK1 ) occurs in leaf sheaths of rice plants grown under high a phosphate regime”

✓ located verbatim in the source · abstract, characters 836–1012 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

High phosphate increased fungal PMK1 expression in rice leaf sheaths.

Organ / stage
leaf sheathse0
Treatment
high a phosphate regimee0
Interactor
M. oryzaePyricularia oryzaee0pathogen
Gene
PMK1e0
Outcome
Pathogenicity Mitogen-activated Protein Kinase ( PMK1 )e0
Direction
strongere0

Not reportedComparator

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

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗
Pyricularia oryzae
Pyricularia oryzae · InteractorJie-Hao Ou · CC BY 4.0 · iNaturalist ↗

Verbatim

e0

“stronger expression of M. oryzae effectors and Pathogenicity Mitogen-activated Protein Kinase ( PMK1 ) occurs in leaf sheaths of rice plants grown under high a phosphate regime”

✓ located verbatim in the source · abstract, characters 836–1012 · show in text ↑
Observationobservedoriginal resultnegativemeasured

Claim · model-written summary

Fungal genes encoding suppressors of plant cell death were downregulated in phosphate accumulating rice sheaths.

Organ / stage
sheathse0
Outcome
fungal genes encoding suppressors of plant cell deathe0
Direction
Down-regulatione0
Qualifier
phosphate over-accumulating rice plantse0

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

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“Down-regulation of fungal genes encoding suppressors of plant cell death and up-regulation of plant cell death-inducing effectors also occurs in sheaths of phosphate over-accumulating rice plants”

✓ located verbatim in the source · abstract, characters 1014–1209 · show in text ↑
Observationobservedoriginal resultnegativemeasured

Claim · model-written summary

Fungal plant cell death inducing effectors were upregulated in phosphate accumulating rice sheaths.

Organ / stage
sheathse0
Outcome
plant cell death-inducing effectorse0
Direction
up-regulatione0
Qualifier
phosphate over-accumulating rice plantse0

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

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“Down-regulation of fungal genes encoding suppressors of plant cell death and up-regulation of plant cell death-inducing effectors also occurs in sheaths of phosphate over-accumulating rice plants”

✓ located verbatim in the source · abstract, characters 1014–1209 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

High Pi altered fungal phosphate transporter gene expression.

Treatment
high Pie0
Outcome
expression of fungal phosphate transporter genese0

Not reportedComparatorDirection

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

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“Treatment with high Pi causes alterations in the expression of fungal phosphate transporter genes potentially contributing to pathogen virulence”

✓ located verbatim in the source · abstract, characters 1211–1355 · show in text ↑
t0

“rice”

✓ located verbatim in the source · title, characters 26–30 · show in text ↑
Associationobservedoriginal resultnegativemeasured

Claim · model-written summary

Pi accumulation prevented early hydrogen peroxide accumulation in infected rice leaf sheaths.

Organ / stage
leaf sheathse0
Interactor
M. oryzaePyricularia oryzaee0pathogen
Outcome
H 2 O 2 accumulatione0
Direction
preventse0

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

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗
Pyricularia oryzae
Pyricularia oryzae · InteractorJie-Hao Ou · CC BY 4.0 · iNaturalist ↗

Verbatim

e0

“Pi accumulation in leaf sheaths prevents H 2 O 2 accumulation early during M. oryzae infection”

✓ located verbatim in the source · abstract, characters 1392–1486 · show in text ↑
t0

“rice”

✓ located verbatim in the source · title, characters 26–30 · show in text ↑
Observationobservedoriginal resultnegativemeasured

Claim · model-written summary

RBOH activation was weaker during infection of phosphate accumulating rice.

Gene
RBOHse0
Outcome
activation of Respiratory Burst Oxidase Homologs ( RBOHs ) genese0
Direction
weakere0

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

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“weaker activation of Respiratory Burst Oxidase Homologs ( RBOHs ) genes involved in reactive oxygen species (ROS) production”

✓ located verbatim in the source · abstract, characters 1513–1637 · show in text ↑
t0

“rice”

✓ located verbatim in the source · title, characters 26–30 · show in text ↑
Observationobservedoriginal resultnegativemeasured

Claim · model-written summary

Defense gene activation was weaker during infection of phosphate accumulating rice.

Outcome
activation of defense-related genese0
Direction
weakere0
Qualifier
over-accumulating phosphatee0

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

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“a weaker activation of defense-related genes occurs during infection in rice plants over-accumulating phosphate”

✓ located verbatim in the source · abstract, characters 1648–1759 · show in text ↑
Mechanismauthor interpretationoriginal resultnegativemeasured

Claim · model-written summary

The authors attribute higher fungal colonization in phosphate accumulating rice to induced effectors and repressed host immunity.

Interactor
M. oryzaePyricularia oryzaee0pathogen
Outcome
higher colonization by M. oryzaee0
Qualifier
Phosphate-mediated stimulation of fungal effector genese0

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

Oryza sativa
Oryza sativa · Taxon · picture from its Wikimedia Commons categoryDesmanthus4food · CC BY-SA 3.0 us · Wikimedia Commons ↗
Pyricularia oryzae
Pyricularia oryzae · InteractorJie-Hao Ou · CC BY 4.0 · iNaturalist ↗

Verbatim

e0

“Phosphate-mediated stimulation of fungal effector genes (e.g., potentiation of fungal pathogenicity) in combination with repression of pathogen-inducible immune responses (e.g., ROS accumulation, defense gene expression) explains higher colonization by M. oryzae in rice tissues accumulating phosphate”

✓ located verbatim in the source · abstract, characters 1896–2197 · show in text ↑

fertilization · Pyricularia oryzae · Oryza sativa (rice)Positive and negative results

5 papers: 2 positive, 3 negative or no effect

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

  1. negative
  2. positive
  3. 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.