Paper · 2014 · Purdue e-Pubs (Purdue University System)

Characterization of adult plant resistance in the maize-Cochliobolus carbonum race 1 pathosystem revealed a close connection between plant immunity and metabolism

Sandeep Marla

16
claims
31
verbatim quotes
0
citations
4
research areas
—
Not open access

Abstract

The role if any that host metabolism plays in plant immunity remains an open question. Our research on adult plant resistance (APR) in maize to Cochliobolus carbonum race1 (CCR1), a pathogen that causes a lethal leaf blight disease, seems to provide an interesting glimpse into this question. CCR1 causes disease by using a cyclic tetrapeptide that has been named HC-toxin. This virulence action is countered by the disease resistance gene Hm1 that inactivates HC-toxin by encoding an NADPH-dependent reductase (HCTR). Resistance conferred by Hm1 is absolute and operates in every part of the plant. In contrast, an allele of Hm1 (Hm1A) confers protection only at maturity and not at the seedling stage. The HCTR encoded by Hm1A differs from the wild-type HCTR by five amino acid substitutions, which we predicted only weaken the activity of HCTR and not inactivate it completely. We used targeted mutagenesis with EMS to test this hypothesis. This procedure led to the generation of two new alleles of Hm1 that, like Hm1A , conferred effective resistance to CCR1 only at maturity. These APR alleles of Hm1 were the result of single amino acid substitutions. In one allele the substitution was from Threonine to Methionine at residue 90 (T90M) and the other had a Valine to Methionine conversion at residue 210 (V210M). Five fully susceptible alleles were also found in this study, and they all had undergone drastic mutations such as the formation of premature stop codons. These results demonstrate that the APR alleles of Hm1 are the result of partial loss-of-function mutations of the gene. The question, of course, is why weak alleles behave of Hm1 fail to confer resistance in corn seedlings? One possibility is that it may have something to do with the fluctuating levels of NADPH (a cofactor for HCTR) in corn seedlings. Given that Hm1A seedlings become resistant to CCR1 when grown under extended photoperiod or in the presence of 3% sucrose, are consistent with our hypothesis. During our quest for the mechanistic basis of APR, we identified maize seedlings incubated in continuous dark for 48 hours turned susceptible to CCR1 Tox-, the non-toxin producing isolate. This loss of resistance is described as "DILI", dark-induced loss of immunity. Genetic studies revealed DILI is independent of Hm1 and CCR1 toxin producing ability. In addition to CCR1, Cochliobolus heterostrophus, Magnaporthe grisea and Colletotrichum graminicola were able to infect dark-incubated plants, showing that DILI is not pathogen specific. But what happens in dark that is making maize seedlings susceptible to different pathogens. One possibility could be loss of photosynthesis in the dark. Our results from DCMU herbicide which inhibits photosynthesis showed that loss of photosynthesis is responsible for DILI. Interestingly, by supplementing sugars DILI was suppressed, showing that starvation induced by loss of sugars is indeed responsible for DILI. Supporting these results, transcriptome analysis showed complete shut-down of metabolism. Fascinatingly, this is the first time we are showing a direct correlation between metabolism and immunity in the plant kingdom.

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The text the model read, with the source record’s inline markup (italics, sub- and superscripts) rendered and its character entities decoded; quote offsets refer to the raw text.

Claims 16

Observationobservedoriginal resultmixedmeasured

Claim · model-written summary

The Hm1A allele protects maize from CCR1 only at maturity, not as seedlings.

Taxon
maizeZea mayse1
Organ / stage
maturity and not at the seedling stagee0
Interactor
Cochliobolus carbonum race1Bipolaris zeicolae1pathogen
Gene
Hm1Ae0
Outcome
protectione0

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 ↗
Bipolaris zeicola
Bipolaris zeicola · InteractorEric McKenzie · CC BY 3.0 · Wikimedia Commons ↗

Verbatim

e0

“an allele of Hm1 (Hm1A) confers protection only at maturity and not at the seedling stage”

✓ located verbatim in the source · abstract, characters 613–702 · show in text ↑
e1

“in maize to Cochliobolus carbonum race1 (CCR1)”

✓ located verbatim in the source · abstract, characters 132–178 · show in text ↑
Method / resourceobservedoriginal resultpositivemeasured

Claim · model-written summary

EMS mutagenesis produced two Hm1 alleles giving maize effective CCR1 resistance only at maturity.

Taxon
maizeZea mayse1
Interactor
Cochliobolus carbonum race1Bipolaris zeicolae1pathogen
Gene
Hm1e0
Outcome
effective resistance to CCR1e0
Value
two new allelese0

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 ↗
Bipolaris zeicola
Bipolaris zeicola · InteractorEric McKenzie · CC BY 3.0 · Wikimedia Commons ↗

Verbatim

e0

“This procedure led to the generation of two new alleles of Hm1 that, like Hm1A , conferred effective resistance to CCR1 only at maturity”

✓ located verbatim in the source · abstract, characters 944–1080 · show in text ↑
e1

“in maize to Cochliobolus carbonum race1 (CCR1)”

✓ located verbatim in the source · abstract, characters 132–178 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

One adult-resistance Hm1 allele had a threonine-to-methionine substitution at residue 90.

Taxon
maizeZea mayse1
Material
one allelee0
Outcome
Threonine to Methionine at residue 90 (T90M)e0

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

e0

“In one allele the substitution was from Threonine to Methionine at residue 90 (T90M)”

✓ located verbatim in the source · abstract, characters 1159–1243 · show in text ↑
e1

“Our research on adult plant resistance (APR) in maize to Cochliobolus carbonum race1 (CCR1)”

✓ located verbatim in the source · abstract, characters 87–178 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

The other adult-resistance Hm1 allele had a valine-to-methionine substitution at residue 210.

Taxon
maizeZea mayse1
Material
the othere0
Outcome
Valine to Methionine conversion at residue 210 (V210M)e0

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

e0

“the other had a Valine to Methionine conversion at residue 210 (V210M)”

✓ located verbatim in the source · abstract, characters 1248–1318 · show in text ↑
e1

“Our research on adult plant resistance (APR) in maize to Cochliobolus carbonum race1 (CCR1)”

✓ located verbatim in the source · abstract, characters 87–178 · show in text ↑
Observationobservedoriginal resultnegativemeasured

Claim · model-written summary

Five fully susceptible Hm1 alleles had drastic mutations including premature stop codons.

Taxon
maizeZea mayse1
Gene
allelese0
Outcome
fully susceptible allelese0
Value
Fivee0
Qualifier
premature stop codonse0

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

e0

“Five fully susceptible alleles were also found in this study, and they all had undergone drastic mutations such as the formation of premature stop codons”

✓ located verbatim in the source · abstract, characters 1320–1473 · show in text ↑
e1

“Our research on adult plant resistance (APR) in maize to Cochliobolus carbonum race1 (CCR1)”

✓ located verbatim in the source · abstract, characters 87–178 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

Adult plant resistance alleles of Hm1 were partial loss-of-function mutations.

Taxon
maizeZea mayse1
Gene
Hm1e0
Outcome
APR alleles of Hm1e0
Qualifier
partial loss-of-function mutationse0

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

e0

“These results demonstrate that the APR alleles of Hm1 are the result of partial loss-of-function mutations of the gene”

✓ located verbatim in the source · abstract, characters 1475–1593 · show in text ↑
e1

“Our research on adult plant resistance (APR) in maize to Cochliobolus carbonum race1 (CCR1)”

✓ located verbatim in the source · abstract, characters 87–178 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

An extended photoperiod made Hm1A maize seedlings resistant to CCR1.

Taxon
maizeZea mayse1
Material
Hm1A seedlingse0
Treatment
extended photoperiode0
Outcome
resistant to CCR1e0
Direction
resistante0

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

e0

“Hm1A seedlings become resistant to CCR1 when grown under extended photoperiod”

✓ located verbatim in the source · abstract, characters 1840–1917 · show in text ↑
e1

“Our research on adult plant resistance (APR) in maize to Cochliobolus carbonum race1 (CCR1)”

✓ located verbatim in the source · abstract, characters 87–178 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Three percent sucrose made Hm1A maize seedlings resistant to CCR1.

Taxon
maizeZea mayse1
Material
Hm1A seedlingse0
Treatment
3% sucrosee0
Outcome
resistant to CCR1e0
Direction
resistante0

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

e0

“Hm1A seedlings become resistant to CCR1 when grown under extended photoperiod or in the presence of 3% sucrose”

✓ located verbatim in the source · abstract, characters 1840–1950 · show in text ↑
e1

“Our research on adult plant resistance (APR) in maize to Cochliobolus carbonum race1 (CCR1)”

✓ located verbatim in the source · abstract, characters 87–178 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Continuous darkness for 48 hours made maize seedlings susceptible to a nontoxin-producing CCR1 isolate.

Taxon
maizeZea mayse0
Treatment
continuous dark for 48 hourse0
Interactor
CCR1 Tox-e0pathogen
Outcome
susceptible to CCR1 Tox-e0
Direction
susceptiblee0

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

e0

“maize seedlings incubated in continuous dark for 48 hours turned susceptible to CCR1 Tox-, the non-toxin producing isolate”

✓ located verbatim in the source · abstract, characters 2053–2175 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Dark-induced loss of immunity was independent of Hm1 and CCR1 toxin production.

Taxon
maizeZea mayse1
Gene
Hm1e0
Outcome
DILIe0
Qualifier
independent of Hm1 and CCR1 toxin producing abilitye0

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

e0

“Genetic studies revealed DILI is independent of Hm1 and CCR1 toxin producing ability”

✓ located verbatim in the source · abstract, characters 2256–2340 · show in text ↑
e1

“Our research on adult plant resistance (APR) in maize to Cochliobolus carbonum race1 (CCR1)”

✓ located verbatim in the source · abstract, characters 87–178 · show in text ↑
Observationobservedoriginal resultnegativemeasured

Claim · model-written summary

Cochliobolus heterostrophus infected dark-incubated maize plants.

Taxon
maizeZea mayse1
Interactor
Cochliobolus heterostrophusBipolaris maydise0pathogen
Outcome
infect dark-incubated plantse0

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 ↗
Bipolaris maydis
Bipolaris maydis · InteractorDavid B. Langston · CC BY 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“Cochliobolus heterostrophus, Magnaporthe grisea and Colletotrichum graminicola were able to infect dark-incubated plants”

✓ located verbatim in the source · abstract, characters 2363–2483 · show in text ↑
e1

“Our research on adult plant resistance (APR) in maize to Cochliobolus carbonum race1 (CCR1)”

✓ located verbatim in the source · abstract, characters 87–178 · show in text ↑
Observationobservedoriginal resultnegativemeasured

Claim · model-written summary

Magnaporthe grisea infected dark-incubated maize plants.

Taxon
maizeZea mayse1
Interactor
Magnaporthe griseaPyricularia griseae0pathogen
Outcome
infect dark-incubated plantse0

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 ↗
Pyricularia grisea
Pyricularia grisea · InteractorPublic domain · Wikimedia Commons ↗

Verbatim

e0

“Cochliobolus heterostrophus, Magnaporthe grisea and Colletotrichum graminicola were able to infect dark-incubated plants”

✓ located verbatim in the source · abstract, characters 2363–2483 · show in text ↑
e1

“Our research on adult plant resistance (APR) in maize to Cochliobolus carbonum race1 (CCR1)”

✓ located verbatim in the source · abstract, characters 87–178 · show in text ↑
Observationobservedoriginal resultnegativemeasured

Claim · model-written summary

Colletotrichum graminicola infected dark-incubated maize plants.

Taxon
maizeZea mayse1
Interactor
Colletotrichum graminicolaColletotrichum graminicolae0pathogen
Outcome
infect dark-incubated plantse0

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 ↗
Colletotrichum graminicola
Colletotrichum graminicola · Interactor · picture from its Wikimedia Commons categoryClemson University - USDA Cooperative Extension Slide Series, Bugwood.org · CC BY 3.0 · Wikimedia Commons ↗

Verbatim

e0

“Cochliobolus heterostrophus, Magnaporthe grisea and Colletotrichum graminicola were able to infect dark-incubated plants”

✓ located verbatim in the source · abstract, characters 2363–2483 · show in text ↑
e1

“Our research on adult plant resistance (APR) in maize to Cochliobolus carbonum race1 (CCR1)”

✓ located verbatim in the source · abstract, characters 87–178 · show in text ↑
Mechanismauthor interpretationoriginal resultnegativemeasured

Claim · model-written summary

DCMU inhibition of photosynthesis indicated that loss of photosynthesis causes dark-induced loss of immunity.

Taxon
maizeZea mayse1
Treatment
DCMU herbicidee0
Outcome
DILIe0
Qualifier
loss of photosynthesise0

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

e0

“Our results from DCMU herbicide which inhibits photosynthesis showed that loss of photosynthesis is responsible for DILI”

✓ located verbatim in the source · abstract, characters 2682–2802 · show in text ↑
e1

“Our research on adult plant resistance (APR) in maize to Cochliobolus carbonum race1 (CCR1)”

✓ located verbatim in the source · abstract, characters 87–178 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Sugar supplementation suppressed dark-induced loss of immunity.

Taxon
maizeZea mayse1
Treatment
supplementing sugarse0
Outcome
DILIe0
Direction
suppressede0

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

e0

“by supplementing sugars DILI was suppressed”

✓ located verbatim in the source · abstract, characters 2819–2862 · show in text ↑
e1

“Our research on adult plant resistance (APR) in maize to Cochliobolus carbonum race1 (CCR1)”

✓ located verbatim in the source · abstract, characters 87–178 · show in text ↑
Observationobservedoriginal resultnegativemeasured

Claim · model-written summary

Transcriptome analysis showed a complete shutdown of metabolism during dark-induced loss of immunity.

Taxon
maizeZea mayse1
Outcome
metabolisme0
Direction
complete shut-downe0

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

e0

“transcriptome analysis showed complete shut-down of metabolism”

✓ located verbatim in the source · abstract, characters 2972–3034 · show in text ↑
e1

“Our research on adult plant resistance (APR) in maize to Cochliobolus carbonum race1 (CCR1)”

✓ located verbatim in the source · abstract, characters 87–178 · show in text ↑

sucrose · disease · Zea mays (maize)Positive and negative results

4 papers: 2 positive, 2 negative or no effect

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

  1. no effect
  2. negative
  3. positive
See all 4 papers →

light · disease · Zea mays (maize)Positive and negative results

7 papers: 3 positive, 4 negative or no effect

2 papers in the same direction as this paper · 4 in the opposite direction

  1. negative
  2. negative
  3. negative

3 papers more in this group

See all 7 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.