Paper · 2022 · Phytopathology Research

Multiomic approaches reveal novel lineage-specific effectors in the potato and tomato early blight pathogen Alternaria solani

Jinhui Wang; Siyu Xiao; Lijia Zheng; et al.

13
claims
24
verbatim quotes
14
citations
3
research areas
✓
Open access · cc-by

Abstract

Abstract The effectome of the necrotrophic fungal pathogen, Alternaria solani , was determined using multiomics. In total, 238 effector candidates were predicted from the A. solani genome, and apoplastic effectors constitute most of the total candidate effector proteins (AsCEPs). Comparative genomics revealed two main groups of AsCEPs: lineage-specific and conserved effectors. RNA-Seq analysis revealed that the most highly expressed genes encoding AsCEPs were enriched with lineage-specific forms. Two lineage-specific effector genes, AsCEP19 and AsCEP20 , were found to form a ‘head-to-head’ gene pair located near an AT-rich region on the chromosome. To date, AsCEP19 and AsCEP20 have been found only in a few fungal species. Phylogenetic inference revealed that AsCEP19 and AsCEP20 were likely acquired by the common ancestor of A. solani and A. tomatophila via horizontal gene transfer, probably mediated by long terminal repeat retrotransposon. RT-qPCR analysis showed that AsCEP19 and AsCEP20 are tightly coexpressed in a host-specific manner and that they are upregulated at advanced stages of A. solani infection only in solanaceous hosts. Transient expression of AsCEP19 and AsCEP20 in Nicotiana benthamiana plants showed that these effectors could promote Phytophthora infestans infection. AsCEP19 and AsCEP20 were required for the full virulence of A. solani on host potato, because deletion of this gene pair significantly reduced the size of necrotic lesions on potato leaves. Transient expression of AsCEP20 could elicit plant cell death depending on the presence of its signal peptide, indicating that AsCEP20 is a necrosis-inducing apoplastic effector with the mature form localized specifically in chloroplasts. Our work provides a better understanding of the function and evolution of necrotrophic fungal effectors, and helps explain the high aggressiveness of A. solani against solanaceous crops.

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

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Claims 13

Observationobservedoriginal resultmeasured

Claim · model-written summary

Alternaria solani genome yields 238 effector candidates.

Interactor
A. solaniAlternaria solanie1pathogen
Outcome
effector candidatese1
Value
238e1

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

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗
Solanum tuberosum
Solanum tuberosum · TaxonScott Bauer, USDA ARS · Public domain · Wikimedia Commons ↗
Alternaria solani
Alternaria solani · InteractorClemson University - USDA Cooperative Extension Slide Series · CC BY 3.0 us · Wikimedia Commons ↗

Verbatim

t0

“potato and tomato early blight pathogen”

✓ located verbatim in the source · title, characters 68–107 · show in text ↑
e1

“In total, 238 effector candidates were predicted from the A. solani genome”

✓ located verbatim in the source · abstract, characters 113–187 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Apoplastic effectors make up most of the candidate effector proteins of Alternaria solani.

Outcome
apoplastic effectorse2
Qualifier
most of the total candidate effector proteinse2

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

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗
Solanum tuberosum
Solanum tuberosum · TaxonScott Bauer, USDA ARS · Public domain · Wikimedia Commons ↗

Verbatim

t0

“potato and tomato early blight pathogen”

✓ located verbatim in the source · title, characters 68–107 · show in text ↑
e2

“apoplastic effectors constitute most of the total candidate effector proteins (AsCEPs)”

✓ located verbatim in the source · abstract, characters 193–279 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Comparative genomics of Alternaria solani revealed two groups of candidate effectors.

Outcome
groups of AsCEPse3
Value
twoe3

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

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗
Solanum tuberosum
Solanum tuberosum · TaxonScott Bauer, USDA ARS · Public domain · Wikimedia Commons ↗

Verbatim

t0

“potato and tomato early blight pathogen”

✓ located verbatim in the source · title, characters 68–107 · show in text ↑
e3

“Comparative genomics revealed two main groups of AsCEPs: lineage-specific and conserved effectors”

✓ located verbatim in the source · abstract, characters 281–378 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

The most highly expressed Alternaria solani effector genes are enriched with lineage-specific forms.

Outcome
most highly expressed genes encoding AsCEPs were enriched with lineage-specific formse4

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

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗
Solanum tuberosum
Solanum tuberosum · TaxonScott Bauer, USDA ARS · Public domain · Wikimedia Commons ↗

Verbatim

t0

“potato and tomato early blight pathogen”

✓ located verbatim in the source · title, characters 68–107 · show in text ↑
e4

“RNA-Seq analysis revealed that the most highly expressed genes encoding AsCEPs were enriched with lineage-specific forms”

✓ located verbatim in the source · abstract, characters 380–500 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

AsCEP19 and AsCEP20 form a head-to-head gene pair located near an AT-rich region of the chromosome.

Gene
AsCEP19 and AsCEP20e5
Outcome
located near an AT-rich region on the chromosomee5
Qualifier
head-to-heade5

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

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗
Solanum tuberosum
Solanum tuberosum · TaxonScott Bauer, USDA ARS · Public domain · Wikimedia Commons ↗

Verbatim

t0

“potato and tomato early blight pathogen”

✓ located verbatim in the source · title, characters 68–107 · show in text ↑
e5

“Two lineage-specific effector genes, AsCEP19 and AsCEP20, were found to form a ‘head-to-head’ gene pair located near an AT-rich region on the chromosome”

✓ located after whitespace/quote normalisation · abstract, characters 502–655 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

AsCEP19 and AsCEP20 were likely acquired by the common ancestor of A. solani and A. tomatophila through horizontal gene transfer.

Gene
AsCEP19 and AsCEP20e6
Outcome
acquired by the common ancestor of A. solani and A. tomatophilae6
Qualifier
via horizontal gene transfere6

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

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗
Solanum tuberosum
Solanum tuberosum · TaxonScott Bauer, USDA ARS · Public domain · Wikimedia Commons ↗

Verbatim

t0

“potato and tomato early blight pathogen”

✓ located verbatim in the source · title, characters 68–107 · show in text ↑
e6

“AsCEP19 and AsCEP20 were likely acquired by the common ancestor of A. solani and A. tomatophila via horizontal gene transfer”

✓ located verbatim in the source · abstract, characters 769–893 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

AsCEP19 and AsCEP20 are tightly coexpressed in a host-specific manner.

Gene
AsCEP19 and AsCEP20e7
Outcome
tightly coexpressede7
Qualifier
in a host-specific mannere7

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

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗
Solanum tuberosum
Solanum tuberosum · TaxonScott Bauer, USDA ARS · Public domain · Wikimedia Commons ↗

Verbatim

t0

“potato and tomato early blight pathogen”

✓ located verbatim in the source · title, characters 68–107 · show in text ↑
e7

“AsCEP19 and AsCEP20 are tightly coexpressed in a host-specific manner”

✓ located verbatim in the source · abstract, characters 983–1052 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

The AsCEP19 and AsCEP20 pair is upregulated at advanced infection stages only in solanaceous hosts.

Taxon
solanaceous hostse1
Interactor
A. solaniAlternaria solanie1pathogen
Outcome
upregulated at advanced stages of A. solani infectione1
Qualifier
only in solanaceous hostse1

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

Alternaria solani
Alternaria solani · InteractorClemson University - USDA Cooperative Extension Slide Series · CC BY 3.0 us · Wikimedia Commons ↗

Verbatim

e1

“they are upregulated at advanced stages of A. solani infection only in solanaceous hosts”

✓ located verbatim in the source · abstract, characters 1062–1150 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Transient expression of AsCEP19 and AsCEP20 in Nicotiana benthamiana promoted Phytophthora infestans infection.

Taxon
Nicotiana benthamianaNicotiana benthamianae1
Treatment
Transient expressione1
Interactor
Phytophthora infestansPhytophthora infestanse1pathogen
Gene
AsCEP19 and AsCEP20e1
Outcome
Phytophthora infestans infectione1
Direction
promotee1

Not reportedComparator

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

Nicotiana benthamiana
Nicotiana benthamiana · TaxonCharles Andres · CC BY-SA 3.0 · Wikimedia Commons ↗
Phytophthora infestans
Phytophthora infestans · InteractorHoward F. Schwartz, Colorado State University, United States · CC BY 3.0 us · Wikimedia Commons ↗

Verbatim

e1

“Transient expression of AsCEP19 and AsCEP20 in Nicotiana benthamiana plants showed that these effectors could promote Phytophthora infestans infection”

✓ located verbatim in the source · abstract, characters 1152–1302 · show in text ↑
Intervention effectobservedoriginal resultpositivesignificant (as stated)measured

Claim · model-written summary

Deleting the AsCEP19 and AsCEP20 gene pair significantly reduced necrotic lesion size on potato leaves, showing full virulence of Alternaria solani on host potato.

Treatment
deletion of this gene paire1
Interactor
A. solaniAlternaria solanie2pathogen
Outcome
size of necrotic lesions on potato leavese1
Direction
reducede1
Qualifier
full virulencee2

Not reportedComparator

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

Solanum tuberosum
Solanum tuberosum · TaxonScott Bauer, USDA ARS · Public domain · Wikimedia Commons ↗
Alternaria solani
Alternaria solani · InteractorClemson University - USDA Cooperative Extension Slide Series · CC BY 3.0 us · Wikimedia Commons ↗

Verbatim

e1

“deletion of this gene pair significantly reduced the size of necrotic lesions on potato leaves”

✓ located verbatim in the source · abstract, characters 1398–1492 · show in text ↑
e2

“AsCEP19 and AsCEP20 were required for the full virulence of A. solani on host potato”

✓ located verbatim in the source · abstract, characters 1304–1388 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Transient expression of AsCEP20 could elicit plant cell death.

Treatment
Transient expression of AsCEP20e1
Gene
AsCEP20e1
Outcome
plant cell deathe1
Direction
elicite1

Not reportedComparator

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

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗
Solanum tuberosum
Solanum tuberosum · TaxonScott Bauer, USDA ARS · Public domain · Wikimedia Commons ↗

Verbatim

t0

“potato and tomato early blight pathogen”

✓ located verbatim in the source · title, characters 68–107 · show in text ↑
e1

“Transient expression of AsCEP20 could elicit plant cell death depending on the presence of its signal peptide”

✓ located verbatim in the source · abstract, characters 1494–1603 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Mature AsCEP20 is localized specifically in chloroplasts.

Gene
AsCEP20e1
Outcome
mature form localized specifically in chloroplastse1

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

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗
Solanum tuberosum
Solanum tuberosum · TaxonScott Bauer, USDA ARS · Public domain · Wikimedia Commons ↗

Verbatim

t0

“potato and tomato early blight pathogen”

✓ located verbatim in the source · title, characters 68–107 · show in text ↑
e1

“AsCEP20 is a necrosis-inducing apoplastic effector with the mature form localized specifically in chloroplasts”

✓ located verbatim in the source · abstract, characters 1621–1731 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

AsCEP20 is a necrosis-inducing apoplastic effector.

Gene
AsCEP20e1
Outcome
necrosis-inducing apoplastic effectore1

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

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗
Solanum tuberosum
Solanum tuberosum · TaxonScott Bauer, USDA ARS · Public domain · Wikimedia Commons ↗

Verbatim

t0

“potato and tomato early blight pathogen”

✓ located verbatim in the source · title, characters 68–107 · show in text ↑
e1

“AsCEP20 is a necrosis-inducing apoplastic effector with the mature form localized specifically in chloroplasts”

✓ located verbatim in the source · abstract, characters 1621–1731 · show in text ↑

loss of function · Alternaria solani · Solanum tuberosum (potato)Positive and negative results

6 papers: 5 positive, 1 negative or no effect

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

  1. positive
  2. negative
  3. positive

2 papers more in this group

See all 6 papers →

transgenic · cytology · Solanum tuberosum (potato)Results agree

2 papers: 0 positive, 2 negative or no effect

1 paper in the same direction as this paper

  1. negative
See all 2 papers →

transgenic · cytology · Solanum lycopersicum (tomato)Results agree

5 papers: 0 positive, 5 negative or no effect

4 papers in the same direction as this paper

  1. negative
  2. no effect
  3. no effect

1 paper more in this group

See all 5 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.