Paper · 2014 · BMC Genomics

Resistance to Botrytis cinerea in Solanum lycopersicoides involves widespread transcriptional reprogramming

Jonathon E Smith; Bemnet Mengesha; Hua Tang; et al.

9
claims
18
verbatim quotes
87
citations
3
research areas
✓
Open access · cc-by

Abstract

BACKGROUND: Tomato (Solanum lycopersicum), one of the world's most important vegetable crops, is highly susceptible to necrotrophic fungal pathogens such as Botrytis cinerea and Alternaria solani. Improving resistance through conventional breeding has been hampered by a shortage of resistant germplasm and difficulties in introgressing resistance into elite germplasm without linkage drag. The goal of this study was to explore natural variation among wild Solanum species to identify new sources of resistance to necrotrophic fungi and dissect mechanisms underlying resistance against B. cinerea. RESULTS: Among eight wild species evaluated for resistance against B. cinerea and A. solani, S. lycopersicoides expressed the highest levels of resistance against both pathogens. Resistance against B. cinerea manifested as containment of pathogen growth. Through next-generation RNA sequencing and de novo assembly of the S. lycopersicoides transcriptome, changes in gene expression were analyzed during pathogen infection. In response to B. cinerea, differentially expressed transcripts grouped into four categories: genes whose expression rapidly increased then rapidly decreased, genes whose expression rapidly increased and plateaued, genes whose expression continually increased, and genes with decreased expression. Homology-based searches also identified a limited number of highly expressed B. cinerea genes. Almost immediately after infection by B. cinerea, S. lycopersicoides suppressed photosynthesis and metabolic processes involved in growth, energy generation, and response to stimuli, and simultaneously induced various defense-related genes, including pathogenesis-related protein 1 (PR1), a beta-1,3-glucanase (glucanase), and a subtilisin-like protease, indicating a shift in priority towards defense. Moreover, cluster analysis revealed novel, uncharacterized genes that may play roles in defense against necrotrophic fungal pathogens in S. lycopersicoides. The expression of orthologous defense-related genes in S. lycopersicum after infection with B. cinerea revealed differences in the onset and intensity of induction, thus illuminating a potential mechanism explaining the increased susceptibility. Additionally, metabolic pathway analyses identified putative defense-related categories of secondary metabolites. CONCLUSIONS: In sum, this study provided insight into resistance against necrotrophic fungal pathogens in the Solanaceae, as well as novel sequence resources for S. lycopersicoides.

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Claims 9

Observationobservedoriginal resultpositivemeasured

Claim · model-written summary

Solanum lycopersicoides expressed the highest levels of resistance to Botrytis cinerea and Alternaria solani among eight wild species.

Taxon
S. lycopersicoidesSolanum lycopersicoidese0
Interactor
B. cinereaBotrytis cinereae0pathogen
Second interactor
A. solaniAlternaria solanie0pathogen
Outcome
resistancee0
Direction
highest levelse0
Comparator
eight wild speciese0

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

Botrytis cinerea
Botrytis cinerea · InteractorRasbak · CC BY-SA 3.0 · Wikimedia Commons ↗
Alternaria solani
Alternaria solani · Second interactorClemson University - USDA Cooperative Extension Slide Series · CC BY 3.0 us · Wikimedia Commons ↗

Verbatim

e0

“Among eight wild species evaluated for resistance against B. cinerea and A. solani, S. lycopersicoides expressed the highest levels of resistance against both pathogens”

✓ located verbatim in the source · abstract, characters 608–776 · show in text ↑
Observationobservedoriginal resultpositivemeasured

Claim · model-written summary

Resistance of S. lycopersicoides to B. cinerea manifested as containment of pathogen growth.

Taxon
S. lycopersicoidesSolanum lycopersicoidese0
Interactor
B. cinereaBotrytis cinereae1pathogen
Outcome
containment of pathogen growthe1

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

Botrytis cinerea
Botrytis cinerea · InteractorRasbak · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“Among eight wild species evaluated for resistance against B. cinerea and A. solani, S. lycopersicoides expressed the highest levels of resistance against both pathogens”

✓ located verbatim in the source · abstract, characters 608–776 · show in text ↑
e1

“Resistance against B. cinerea manifested as containment of pathogen growth”

✓ located verbatim in the source · abstract, characters 778–852 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

In response to B. cinerea, differentially expressed transcripts of S. lycopersicoides grouped into four categories.

Taxon
S. lycopersicoidesSolanum lycopersicoidese0
Interactor
B. cinereaBotrytis cinereae2pathogen
Outcome
differentially expressed transcriptse2
Value
four categoriese2

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

Botrytis cinerea
Botrytis cinerea · InteractorRasbak · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“Among eight wild species evaluated for resistance against B. cinerea and A. solani, S. lycopersicoides expressed the highest levels of resistance against both pathogens”

✓ located verbatim in the source · abstract, characters 608–776 · show in text ↑
e2

“In response to B. cinerea, differentially expressed transcripts grouped into four categories”

✓ located verbatim in the source · abstract, characters 1023–1115 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Almost immediately after B. cinerea infection, S. lycopersicoides suppressed photosynthesis and metabolic processes.

Taxon
S. lycopersicoidesSolanum lycopersicoidese4
Treatment
infection by B. cinereae3
Interactor
B. cinereaBotrytis cinereae3pathogen
Outcome
photosynthesis and metabolic processese4
Direction
suppressede4
Qualifier
Almost immediatelye3

Not reportedComparator

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

Botrytis cinerea
Botrytis cinerea · InteractorRasbak · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“Among eight wild species evaluated for resistance against B. cinerea and A. solani, S. lycopersicoides expressed the highest levels of resistance against both pathogens”

✓ located verbatim in the source · abstract, characters 608–776 · show in text ↑
e3

“Almost immediately after infection by B. cinerea”

✓ located verbatim in the source · abstract, characters 1416–1464 · show in text ↑
e4

“S. lycopersicoides suppressed photosynthesis and metabolic processes involved in growth, energy generation, and response to stimuli”

✓ located verbatim in the source · abstract, characters 1466–1597 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

B. cinerea infection induced defense-related genes in S. lycopersicoides, including PR1 and a glucanase.

Taxon
S. lycopersicoidesSolanum lycopersicoidese0
Treatment
infection by B. cinereae3
Interactor
B. cinereaBotrytis cinereae3pathogen
Gene
pathogenesis-related protein 1 (PR1)e5
Outcome
defense-related genese5
Direction
inducede5
Qualifier
a beta-1,3-glucanase (glucanase), and a subtilisin-like proteasee5

Not reportedComparator

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

Botrytis cinerea
Botrytis cinerea · InteractorRasbak · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“Among eight wild species evaluated for resistance against B. cinerea and A. solani, S. lycopersicoides expressed the highest levels of resistance against both pathogens”

✓ located verbatim in the source · abstract, characters 608–776 · show in text ↑
e3

“Almost immediately after infection by B. cinerea”

✓ located verbatim in the source · abstract, characters 1416–1464 · show in text ↑
e5

“simultaneously induced various defense-related genes, including pathogenesis-related protein 1 (PR1), a beta-1,3-glucanase (glucanase), and a subtilisin-like protease”

✓ located verbatim in the source · abstract, characters 1603–1769 · show in text ↑
Observationauthor interpretationoriginal resultmeasured

Claim · model-written summary

Cluster analysis suggested novel uncharacterized genes may play roles in defense against necrotrophic fungi in S. lycopersicoides.

Taxon
S. lycopersicoidesSolanum lycopersicoidese0
Outcome
novel, uncharacterized genese6
Qualifier
may play roles in defense against necrotrophic fungal pathogense6

Verbatim

e0

“Among eight wild species evaluated for resistance against B. cinerea and A. solani, S. lycopersicoides expressed the highest levels of resistance against both pathogens”

✓ located verbatim in the source · abstract, characters 608–776 · show in text ↑
e6

“cluster analysis revealed novel, uncharacterized genes that may play roles in defense against necrotrophic fungal pathogens”

✓ located verbatim in the source · abstract, characters 1829–1952 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Orthologous defense-related genes in S. lycopersicum showed differences in onset and intensity of induction after B. cinerea infection.

Taxon
S. lycopersicumSolanum lycopersicume7
Interactor
B. cinereaBotrytis cinereae7pathogen
Gene
orthologous defense-related genese7
Outcome
onset and intensity of inductione7

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 ↗
Botrytis cinerea
Botrytis cinerea · InteractorRasbak · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e7

“The expression of orthologous defense-related genes in S. lycopersicum after infection with B. cinerea revealed differences in the onset and intensity of induction”

✓ located verbatim in the source · abstract, characters 1976–2139 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Metabolic pathway analyses identified putative defense-related categories of secondary metabolites in S. lycopersicoides.

Taxon
S. lycopersicoidesSolanum lycopersicoidese0
Outcome
putative defense-related categories of secondary metabolitese1

Verbatim

e0

“Among eight wild species evaluated for resistance against B. cinerea and A. solani, S. lycopersicoides expressed the highest levels of resistance against both pathogens”

✓ located verbatim in the source · abstract, characters 608–776 · show in text ↑
e1

“metabolic pathway analyses identified putative defense-related categories of secondary metabolites”

✓ located verbatim in the source · abstract, characters 2236–2334 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Homology-based searches identified a limited number of highly expressed B. cinerea genes during infection.

Taxon
S. lycopersicoidesSolanum lycopersicoidese0
Interactor
B. cinereaBotrytis cinereae1pathogen
Outcome
highly expressed B. cinerea genese1

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

Botrytis cinerea
Botrytis cinerea · InteractorRasbak · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“Among eight wild species evaluated for resistance against B. cinerea and A. solani, S. lycopersicoides expressed the highest levels of resistance against both pathogens”

✓ located verbatim in the source · abstract, characters 608–776 · show in text ↑
e1

“Homology-based searches also identified a limited number of highly expressed B. cinerea genes”

✓ located verbatim in the source · abstract, characters 1321–1414 · show in text ↑