Paper · 2022 · Plant Biotechnology Journal

A rust fungus effector directly binds plant pre‐mRNA splice site to reprogram alternative splicing and suppress host immunity

Chunlei Tang; Qiang Xu; Jinren Zhao; et al.

8
claims
17
verbatim quotes
57
citations
2
research areas
✓
Open access

Abstract

Alternative splicing (AS) is a crucial post-transcriptional regulatory mechanism in plant resistance. However, whether and how plant pathogens target splicing in their host remains mostly unknown. For example, although infection by Puccinia striiformis f. sp. tritici (Pst), a pathogenic fungus that severely affects the yield of wheat worldwide, has been shown to significantly influence the levels of alternatively spliced transcripts in the host, the mechanisms that govern this process, and its functional consequence have not been examined. Here, we identified Pst_A23 as a new Pst arginine-rich effector that localizes to host nuclear speckles, nuclear regions enriched in splicing factors. We demonstrated that transient expression of Pst_A23 suppresses plant basal defence dependent on the Pst_A23 nuclear speckle localization and that this protein plays an important role in virulence, stable silencing of which improves wheat stripe rust resistance. Remarkably, RNA-Seq data revealed that AS patterns of 588 wheat genes are altered in Pst_A23-overexpressing lines compared to control plants. To further examine the direct relationship between Pst_A23 and AS, we confirmed direct binding between two RNA motifs predicted from these altered splicing sites and Pst_A23 in vitro. The two RNA motifs we chose occur in the cis-element of TaXa21-H and TaWRKY53, and we validated that Pst_A23 overexpression results in decreased functional transcripts of TaXa21-H and TaWRKY53 while silencing of TaXa21-H and TaWRKY53 impairs wheat resistance to Pst. Overall, this represents formal evidence that plant pathogens produce 'splicing' effectors, which regulate host pre-mRNA splicing by direct engagement of the splicing sites, thereby interfering with host immunity.

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Claims 8

Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Transient expression of Pst_A23 suppresses plant basal defence, dependent on its nuclear speckle localization.

Treatment
transient expression of Pst_A23e1
Interactor
Puccinia striiformis f. sp. triticiPuccinia striiformis f. sp. triticie0pathogen
Gene
Pst_A23e1
Outcome
plant basal defencee1
Direction
suppressese1

Not reportedComparator

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

Triticum aestivum
Triticum aestivum · TaxonRasbak · CC BY-SA 3.0 · Wikimedia Commons ↗
Puccinia striiformis f. sp. tritici
Puccinia striiformis f. sp. tritici · InteractorBrauna55 · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“infection by Puccinia striiformis f. sp. tritici (Pst), a pathogenic fungus that severely affects the yield of wheat worldwide”

✓ located verbatim in the source · abstract, characters 219–345 · show in text ↑
e1

“transient expression of Pst_A23 suppresses plant basal defence dependent on the Pst_A23 nuclear speckle localization”

✓ located verbatim in the source · abstract, characters 718–834 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Pst_A23 is a Puccinia striiformis arginine-rich effector that localizes to host nuclear speckles in wheat.

Interactor
Pste2pathogen
Gene
Pst_A23e2
Outcome
localizes to host nuclear specklese2

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

Triticum aestivum
Triticum aestivum · TaxonRasbak · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“infection by Puccinia striiformis f. sp. tritici (Pst), a pathogenic fungus that severely affects the yield of wheat worldwide”

✓ located verbatim in the source · abstract, characters 219–345 · show in text ↑
e2

“identified Pst_A23 as a new Pst arginine-rich effector that localizes to host nuclear speckles”

✓ located verbatim in the source · abstract, characters 555–649 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

Stable silencing of Pst_A23 improves wheat stripe rust resistance.

Treatment
stable silencinge3
Interactor
Puccinia striiformis f. sp. triticiPuccinia striiformis f. sp. triticie0pathogen
Outcome
wheat stripe rust resistancee3
Direction
improvese3

Not reportedComparator

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

Triticum aestivum
Triticum aestivum · TaxonRasbak · CC BY-SA 3.0 · Wikimedia Commons ↗
Puccinia striiformis f. sp. tritici
Puccinia striiformis f. sp. tritici · InteractorBrauna55 · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“infection by Puccinia striiformis f. sp. tritici (Pst), a pathogenic fungus that severely affects the yield of wheat worldwide”

✓ located verbatim in the source · abstract, characters 219–345 · show in text ↑
e3

“stable silencing of which improves wheat stripe rust resistance”

✓ located verbatim in the source · abstract, characters 895–958 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Pst_A23 overexpression altered the alternative splicing patterns of 588 wheat genes compared with control plants.

Treatment
Pst_A23-overexpressing linese4
Outcome
AS patterns of 588 wheat genese4
Direction
alterede4
Value
588e4
Comparator
control plantse4

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

Triticum aestivum
Triticum aestivum · TaxonRasbak · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e4

“RNA-Seq data revealed that AS patterns of 588 wheat genes are altered in Pst_A23-overexpressing lines compared to control plants”

✓ located verbatim in the source · abstract, characters 972–1100 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Pst_A23 directly binds two RNA motifs predicted from the altered splicing sites in vitro.

Gene
Pst_A23e5
Outcome
direct binding between two RNA motifse5

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

Triticum aestivum
Triticum aestivum · TaxonRasbak · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“infection by Puccinia striiformis f. sp. tritici (Pst), a pathogenic fungus that severely affects the yield of wheat worldwide”

✓ located verbatim in the source · abstract, characters 219–345 · show in text ↑
e5

“we confirmed direct binding between two RNA motifs predicted from these altered splicing sites and Pst_A23 in vitro”

✓ located verbatim in the source · abstract, characters 1169–1284 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Pst_A23 overexpression decreased the functional transcripts of TaXa21-H and TaWRKY53 in wheat.

Treatment
Pst_A23 overexpressione6
Gene
TaXa21-H and TaWRKY53e6
Outcome
functional transcripts of TaXa21-H and TaWRKY53e6
Direction
decreasede6

Not reportedComparator

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

Triticum aestivum
Triticum aestivum · TaxonRasbak · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“infection by Puccinia striiformis f. sp. tritici (Pst), a pathogenic fungus that severely affects the yield of wheat worldwide”

✓ located verbatim in the source · abstract, characters 219–345 · show in text ↑
e6

“Pst_A23 overexpression results in decreased functional transcripts of TaXa21-H and TaWRKY53”

✓ located verbatim in the source · abstract, characters 1387–1478 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Silencing of TaXa21-H and TaWRKY53 impairs wheat resistance to Pst.

Treatment
silencing of TaXa21-H and TaWRKY53e7
Interactor
Pste7pathogen
Gene
TaXa21-H and TaWRKY53e7
Outcome
wheat resistance to Pste7
Direction
impairse7

Not reportedComparator

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

Triticum aestivum
Triticum aestivum · TaxonRasbak · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“infection by Puccinia striiformis f. sp. tritici (Pst), a pathogenic fungus that severely affects the yield of wheat worldwide”

✓ located verbatim in the source · abstract, characters 219–345 · show in text ↑
e7

“silencing of TaXa21-H and TaWRKY53 impairs wheat resistance to Pst”

✓ located verbatim in the source · abstract, characters 1485–1551 · show in text ↑
Mechanismauthor interpretationoriginal resultnegativemeasured

Claim · model-written summary

Plant pathogens produce splicing effectors that regulate host pre-mRNA splicing by direct engagement of the splicing sites, thereby interfering with host immunity.

Interactor
plant pathogense1pathogen
Outcome
host immunitye2
Qualifier
by direct engagement of the splicing sitese3

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

Triticum aestivum
Triticum aestivum · TaxonRasbak · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“infection by Puccinia striiformis f. sp. tritici (Pst), a pathogenic fungus that severely affects the yield of wheat worldwide”

✓ located verbatim in the source · abstract, characters 219–345 · show in text ↑
e1

“this represents formal evidence that plant pathogens produce”

✓ located verbatim in the source · abstract, characters 1562–1622 · show in text ↑
e2

“thereby interfering with host immunity”

✓ located verbatim in the source · abstract, characters 1727–1765 · show in text ↑
e3

“by direct engagement of the splicing sites”

✓ located verbatim in the source · abstract, characters 1683–1725 · show in text ↑

transgenic · Puccinia striiformis f. sp. tritici · Triticum aestivum (wheat)Positive and negative results

3 papers: 2 positive, 1 negative or no effect

2 in the opposite direction

  1. positive
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loss of function · Puccinia striiformis f. sp. tritici · Triticum aestivum (wheat)Positive and negative results

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loss of function · disease · Triticum aestivum (wheat)Positive and negative results

177 papers: 81 positive, 96 negative or no effect

95 papers in the same direction as this paper · 81 in the opposite direction

  1. 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.