Paper · 2022 · PLoS Pathogens

A new family of structurally conserved fungal effectors displays epistatic interactions with plant resistance proteins

Noureddine Lazar; Carl H. Mesarich; Yohann Petit-Houdenot; et al.

9
claims
23
verbatim quotes
73
citations
3
research areas
✓
Open access · cc-by

Abstract

Recognition of a pathogen avirulence (AVR) effector protein by a cognate plant resistance (R) protein triggers a set of immune responses that render the plant resistant. Pathogens can escape this so-called Effector-Triggered Immunity (ETI) by different mechanisms including the deletion or loss-of-function mutation of the AVR gene, the incorporation of point mutations that allow recognition to be evaded while maintaining virulence function, and the acquisition of new effectors that suppress AVR recognition. The Dothideomycete Leptosphaeria maculans, causal agent of oilseed rape stem canker, is one of the few fungal pathogens where suppression of ETI by an AVR effector has been demonstrated. Indeed, AvrLm4-7 suppresses Rlm3- and Rlm9-mediated resistance triggered by AvrLm3 and AvrLm5-9, respectively. The presence of AvrLm4-7 does not impede AvrLm3 and AvrLm5-9 expression, and the three AVR proteins do not appear to physically interact. To decipher the epistatic interaction between these L. maculans AVR effectors, we determined the crystal structure of AvrLm5-9 and obtained a 3D model of AvrLm3, based on the crystal structure of Ecp11-1, a homologous AVR effector candidate from Fulvia fulva. Despite a lack of sequence similarity, AvrLm5-9 and AvrLm3 are structural analogues of AvrLm4-7 (structure previously characterized). Structure-informed sequence database searches identified a larger number of putative structural analogues among L. maculans effector candidates, including the AVR effector AvrLmS-Lep2, all produced during the early stages of oilseed rape infection, as well as among effector candidates from other phytopathogenic fungi. These structural analogues are named LARS (for Leptosphaeria AviRulence and Suppressing) effectors. Remarkably, transformants of L. maculans expressing one of these structural analogues, Ecp11-1, triggered oilseed rape immunity in several genotypes carrying Rlm3. Furthermore, this resistance could be suppressed by AvrLm4-7. These results suggest that Ecp11-1 shares a common activity with AvrLm3 within the host plant which is detected by Rlm3, or that the Ecp11-1 structure is sufficiently close to that of AvrLm3 to be recognized by Rlm3.

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

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 9

Mechanismobservedoriginal resultmeasured

Claim · model-written summary

AvrLm4-7 suppresses Rlm3 mediated resistance triggered by AvrLm3.

Taxon
oilseed rapeBrassica napust0
Interactor
Leptosphaeria maculansPlenodomus lingame1pathogene0
Gene
AvrLm4-7e0
Outcome
Rlm3- and Rlm9-mediated resistancee0

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

Brassica napus
Brassica napus · TaxonDidier Descouens · CC BY-SA 4.0 · Wikimedia Commons ↗
Plenodomus lingam
Plenodomus lingam · InteractorJie-Hao Ou · CC BY 4.0 · Wikimedia Commons ↗

Verbatim

e0

“AvrLm4-7 suppresses Rlm3- and Rlm9-mediated resistance triggered by AvrLm3 and AvrLm5-9, respectively.”

✓ located verbatim in the source · abstract, characters 707–809 · show in text ↑
t0

“oilseed rape stem canker”

✓ located verbatim in the source · abstract, characters 571–595 · show in text ↑
e1

“Leptosphaeria maculans”

✓ located verbatim in the source · abstract, characters 531–553 · show in text ↑
Mechanismobservedoriginal resultmeasured

Claim · model-written summary

AvrLm4-7 suppresses Rlm9 mediated resistance triggered by AvrLm5-9.

Taxon
oilseed rapeBrassica napust0
Interactor
Leptosphaeria maculansPlenodomus lingame1pathogene0
Gene
AvrLm5-9e0
Outcome
Rlm3- and Rlm9-mediated resistancee0

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

Brassica napus
Brassica napus · TaxonDidier Descouens · CC BY-SA 4.0 · Wikimedia Commons ↗
Plenodomus lingam
Plenodomus lingam · InteractorJie-Hao Ou · CC BY 4.0 · Wikimedia Commons ↗

Verbatim

e0

“AvrLm4-7 suppresses Rlm3- and Rlm9-mediated resistance triggered by AvrLm3 and AvrLm5-9, respectively.”

✓ located verbatim in the source · abstract, characters 707–809 · show in text ↑
t0

“oilseed rape stem canker”

✓ located verbatim in the source · abstract, characters 571–595 · show in text ↑
e1

“Leptosphaeria maculans”

✓ located verbatim in the source · abstract, characters 531–553 · show in text ↑
Observationobservedoriginal resultno effectmeasured

Claim · model-written summary

AvrLm4-7 did not impede AvrLm3 or AvrLm5-9 expression.

Taxon
oilseed rapeBrassica napust0
Interactor
Leptosphaeria maculansPlenodomus lingame1pathogene0
Gene
AvrLm4-7e0
Outcome
AvrLm3 and AvrLm5-9 expressione0
Direction
does not impedee0

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

Brassica napus
Brassica napus · TaxonDidier Descouens · CC BY-SA 4.0 · Wikimedia Commons ↗
Plenodomus lingam
Plenodomus lingam · InteractorJie-Hao Ou · CC BY 4.0 · Wikimedia Commons ↗

Verbatim

e0

“The presence of AvrLm4-7 does not impede AvrLm3 and AvrLm5-9 expression”

✓ located verbatim in the source · abstract, characters 810–881 · show in text ↑
t0

“oilseed rape stem canker”

✓ located verbatim in the source · abstract, characters 571–595 · show in text ↑
e1

“Leptosphaeria maculans”

✓ located verbatim in the source · abstract, characters 531–553 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

The three AVR proteins did not appear to physically interact.

Taxon
oilseed rapeBrassica napust0
Interactor
Leptosphaeria maculansPlenodomus lingame1pathogene0
Outcome
the three AVR proteins do not appear to physically interacte0

Not reportedDirection

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

Brassica napus
Brassica napus · TaxonDidier Descouens · CC BY-SA 4.0 · Wikimedia Commons ↗
Plenodomus lingam
Plenodomus lingam · InteractorJie-Hao Ou · CC BY 4.0 · Wikimedia Commons ↗

Verbatim

e0

“the three AVR proteins do not appear to physically interact”

✓ located verbatim in the source · abstract, characters 887–946 · show in text ↑
t0

“oilseed rape stem canker”

✓ located verbatim in the source · abstract, characters 571–595 · show in text ↑
e1

“Leptosphaeria maculans”

✓ located verbatim in the source · abstract, characters 531–553 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

AvrLm5-9 and AvrLm3 were structural analogues of AvrLm4-7 despite sequence dissimilarity.

Taxon
oilseed rapeBrassica napust0
Interactor
Leptosphaeria maculansPlenodomus lingame1pathogene0
Gene
AvrLm5-9 and AvrLm3e0
Outcome
structural analogues of AvrLm4-7e0

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

Brassica napus
Brassica napus · TaxonDidier Descouens · CC BY-SA 4.0 · Wikimedia Commons ↗
Plenodomus lingam
Plenodomus lingam · InteractorJie-Hao Ou · CC BY 4.0 · Wikimedia Commons ↗

Verbatim

e0

“Despite a lack of sequence similarity, AvrLm5-9 and AvrLm3 are structural analogues of AvrLm4-7”

✓ located verbatim in the source · abstract, characters 1208–1303 · show in text ↑
t0

“oilseed rape stem canker”

✓ located verbatim in the source · abstract, characters 571–595 · show in text ↑
e1

“Leptosphaeria maculans”

✓ located verbatim in the source · abstract, characters 531–553 · show in text ↑
Method / resourceobservedoriginal resultmeasured

Claim · model-written summary

Sequence searches identified further structural analogues among L. maculans effectors including AvrLmS-Lep2.

Taxon
oilseed rapeBrassica napust0
Interactor
L. maculansPlenodomus lingame0pathogen
Gene
AvrLmS-Lep2e0
Outcome
putative structural analogues among L. maculans effector candidatese0
Value
a larger numbere0

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

Brassica napus
Brassica napus · TaxonDidier Descouens · CC BY-SA 4.0 · Wikimedia Commons ↗
Plenodomus lingam
Plenodomus lingam · InteractorJie-Hao Ou · CC BY 4.0 · Wikimedia Commons ↗

Verbatim

e0

“Structure-informed sequence database searches identified a larger number of putative structural analogues among L. maculans effector candidates, including the AVR effector AvrLmS-Lep2”

✓ located verbatim in the source · abstract, characters 1342–1525 · show in text ↑
t0

“oilseed rape stem canker”

✓ located verbatim in the source · abstract, characters 571–595 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

The searches also identified analogous effectors in other phytopathogenic fungi.

Taxon
oilseed rapeBrassica napust0
Interactor
other phytopathogenic fungie0pathogen
Outcome
effector candidates from other phytopathogenic fungie0

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

Brassica napus
Brassica napus · TaxonDidier Descouens · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“as well as among effector candidates from other phytopathogenic fungi”

✓ located verbatim in the source · abstract, characters 1591–1660 · show in text ↑
t0

“oilseed rape stem canker”

✓ located verbatim in the source · abstract, characters 571–595 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Ecp11-1 expressing L. maculans transformants triggered immunity in oilseed rape genotypes carrying Rlm3.

Taxon
oilseed rapeBrassica napuse0
Treatment
transformants of L. maculans expressing one of these structural analogues, Ecp11-1e0
Interactor
L. maculansPlenodomus lingame0pathogen
Gene
Rlm3e0
Outcome
oilseed rape immunitye0

Not reportedComparatorDirection

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

Brassica napus
Brassica napus · TaxonDidier Descouens · CC BY-SA 4.0 · Wikimedia Commons ↗
Plenodomus lingam
Plenodomus lingam · InteractorJie-Hao Ou · CC BY 4.0 · Wikimedia Commons ↗

Verbatim

e0

“transformants of L. maculans expressing one of these structural analogues, Ecp11-1, triggered oilseed rape immunity in several genotypes carrying Rlm3”

✓ located verbatim in the source · abstract, characters 1774–1924 · show in text ↑
Mechanismobservedoriginal resultmeasured

Claim · model-written summary

AvrLm4-7 suppressed the resistance triggered by Ecp11-1.

Taxon
oilseed rapeBrassica napust0
Interactor
Leptosphaeria maculansPlenodomus lingame1pathogene0
Gene
AvrLm4-7e0
Outcome
this resistancee0

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

Brassica napus
Brassica napus · TaxonDidier Descouens · CC BY-SA 4.0 · Wikimedia Commons ↗
Plenodomus lingam
Plenodomus lingam · InteractorJie-Hao Ou · CC BY 4.0 · Wikimedia Commons ↗

Verbatim

e0

“this resistance could be suppressed by AvrLm4-7”

✓ located verbatim in the source · abstract, characters 1939–1986 · show in text ↑
t0

“oilseed rape stem canker”

✓ located verbatim in the source · abstract, characters 571–595 · show in text ↑
e1

“Leptosphaeria maculans”

✓ located verbatim in the source · abstract, characters 531–553 · show in text ↑

Plenodomus lingam · disease · Brassica napus (oilseed rape)Positive and negative results

2 papers: 1 positive, 1 negative or no effect

1 in the opposite direction

  1. no effect
See all 2 papers →

transgenic · disease · Brassica napus (oilseed rape)Results agree

7 papers: 7 positive, 0 negative or no effect

6 papers in the same direction as this paper

  1. positive
  2. positive
  3. positive

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.