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Transcriptome analysis of the white pine blister rust pathogen Cronartium ribicola: de novo assembly, expression profiling, and identification of candidate effectors.

Liu JJ, Sturrock RN, Sniezko RA, Williams H, Benton R, Zamany A - BMC Genomics (2015)

Bottom Line: This study further identified a repertoire of candidate effectors and other pathogenicity determinants.This comprehensive transcriptome profiling substantially improves our current understanding of molecular WP-BR interactions.The repertoire of candidate effectors and other putative pathogenicity determinants identified here are valuable for future functional analysis of Cri virulence and pathogenicity.

View Article: PubMed Central - PubMed

Affiliation: Pacific Forestry Centre, Canadian Forest Service, Natural Resources Canada, 506 West Burnside Road, Victoria, BC, V8Z 1M5, Canada. Jun-Jun.Liu@NRCan-RNCan.gc.ca.

ABSTRACT

Background: The fungus Cronartium ribicola (Cri) is an economically and ecologically important forest pathogen that causes white pine blister rust (WPBR) disease on five-needle pines. To cause stem cankers and kill white pine trees the fungus elaborates a life cycle with five stages of spore development on five-needle pines and the alternate host Ribes plants. To increase our understanding of molecular WP-BR interactions, here we report genome-wide transcriptional profile analysis of C. ribicola using RNA-seq.

Results: cDNA libraries were constructed from aeciospore, urediniospore, and western white pine (Pinus monticola) tissues post Cri infection. Over 200 million RNA-seq 100-bp paired-end (PE) reads from rust fungal spores were de novo assembled and a reference transcriptome was generated with 17,880 transcripts that were expressed from 13,629 unigenes. A total of 734 unique proteins were predicted as a part of the Cri secretome from complete open reading frames (ORFs), and 41 % of them were Cronartium-specific. This study further identified a repertoire of candidate effectors and other pathogenicity determinants. Differentially expressed genes (DEGs) were identified to gain an understanding of molecular events important during the WPBR fungus life cycle by comparing Cri transcriptomes at different infection stages. Large-scale changes of in planta gene expression profiles were observed, revealing that multiple fungal biosynthetic pathways were enhanced during mycelium growth inside infected pine stem tissues. Conversely, many fungal genes that were up-regulated at the urediniospore stage appeared to be signalling components and transporters. The secreted fungal protein genes that were up-regulated in pine needle tissues during early infection were primarily associated with cell wall modifications, possibly to mask the rust pathogen from plant defenses.

Conclusion: This comprehensive transcriptome profiling substantially improves our current understanding of molecular WP-BR interactions. The repertoire of candidate effectors and other putative pathogenicity determinants identified here are valuable for future functional analysis of Cri virulence and pathogenicity.

No MeSH data available.


Related in: MedlinePlus

Cronartium ribicola life cycle with five stages of spore development. a Blisters on the infected white pine stem; b Aeciospore; c Aeciospore germination; d Rust fungus growth on an infected Ribes leaf; e Urediniospores; f Telia on Ribes leaf; g One-year-old susceptible seedling ~6 months (March) post needle infection by basidiospores; h A typical canker on western white pine stem ~20 months post infection on needles. The four rust development stages sampled for comparative analysis of rust fungal transcriptomes are indicated by red letters
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Fig1: Cronartium ribicola life cycle with five stages of spore development. a Blisters on the infected white pine stem; b Aeciospore; c Aeciospore germination; d Rust fungus growth on an infected Ribes leaf; e Urediniospores; f Telia on Ribes leaf; g One-year-old susceptible seedling ~6 months (March) post needle infection by basidiospores; h A typical canker on western white pine stem ~20 months post infection on needles. The four rust development stages sampled for comparative analysis of rust fungal transcriptomes are indicated by red letters

Mentions: C. ribicola is an obligate biotrophic fungus and requires an alternate host plant (mainly Ribes species) for completion of its life cycle (Fig. 1) [5]. In spring (or summer for high elevation species like whitebark pine) aeciospores are released from stem cankers of susceptible five-needle pines and dispersed by air onto Ribes plants. Aeciospores germinate on Ribes leaves to initiate the asexual stage of infection, which involves mycelium growth in Ribes leaf tissue, sporulation to produce urediniospores, and repeated infection of nearby Ribes by urediniospores throughout the summer season. In late summer or early fall, telia begin to grow and produce rows of teliospores. As the weather becomes wet and cooler, teliospores germinate in place and produce basidia, where basidiospores are developed, dispersed via air movement and subsequently to infect pine host. The germinated basidiospore enters pine needles through stomata, and hyphae then grow along vascular tissues into the branch and stem. The mycelium continues to spread in the bark tissues of susceptible five-needle pines, resulting in a swollen canker in the next spring or summer.Fig. 1


Transcriptome analysis of the white pine blister rust pathogen Cronartium ribicola: de novo assembly, expression profiling, and identification of candidate effectors.

Liu JJ, Sturrock RN, Sniezko RA, Williams H, Benton R, Zamany A - BMC Genomics (2015)

Cronartium ribicola life cycle with five stages of spore development. a Blisters on the infected white pine stem; b Aeciospore; c Aeciospore germination; d Rust fungus growth on an infected Ribes leaf; e Urediniospores; f Telia on Ribes leaf; g One-year-old susceptible seedling ~6 months (March) post needle infection by basidiospores; h A typical canker on western white pine stem ~20 months post infection on needles. The four rust development stages sampled for comparative analysis of rust fungal transcriptomes are indicated by red letters
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4559923&req=5

Fig1: Cronartium ribicola life cycle with five stages of spore development. a Blisters on the infected white pine stem; b Aeciospore; c Aeciospore germination; d Rust fungus growth on an infected Ribes leaf; e Urediniospores; f Telia on Ribes leaf; g One-year-old susceptible seedling ~6 months (March) post needle infection by basidiospores; h A typical canker on western white pine stem ~20 months post infection on needles. The four rust development stages sampled for comparative analysis of rust fungal transcriptomes are indicated by red letters
Mentions: C. ribicola is an obligate biotrophic fungus and requires an alternate host plant (mainly Ribes species) for completion of its life cycle (Fig. 1) [5]. In spring (or summer for high elevation species like whitebark pine) aeciospores are released from stem cankers of susceptible five-needle pines and dispersed by air onto Ribes plants. Aeciospores germinate on Ribes leaves to initiate the asexual stage of infection, which involves mycelium growth in Ribes leaf tissue, sporulation to produce urediniospores, and repeated infection of nearby Ribes by urediniospores throughout the summer season. In late summer or early fall, telia begin to grow and produce rows of teliospores. As the weather becomes wet and cooler, teliospores germinate in place and produce basidia, where basidiospores are developed, dispersed via air movement and subsequently to infect pine host. The germinated basidiospore enters pine needles through stomata, and hyphae then grow along vascular tissues into the branch and stem. The mycelium continues to spread in the bark tissues of susceptible five-needle pines, resulting in a swollen canker in the next spring or summer.Fig. 1

Bottom Line: This study further identified a repertoire of candidate effectors and other pathogenicity determinants.This comprehensive transcriptome profiling substantially improves our current understanding of molecular WP-BR interactions.The repertoire of candidate effectors and other putative pathogenicity determinants identified here are valuable for future functional analysis of Cri virulence and pathogenicity.

View Article: PubMed Central - PubMed

Affiliation: Pacific Forestry Centre, Canadian Forest Service, Natural Resources Canada, 506 West Burnside Road, Victoria, BC, V8Z 1M5, Canada. Jun-Jun.Liu@NRCan-RNCan.gc.ca.

ABSTRACT

Background: The fungus Cronartium ribicola (Cri) is an economically and ecologically important forest pathogen that causes white pine blister rust (WPBR) disease on five-needle pines. To cause stem cankers and kill white pine trees the fungus elaborates a life cycle with five stages of spore development on five-needle pines and the alternate host Ribes plants. To increase our understanding of molecular WP-BR interactions, here we report genome-wide transcriptional profile analysis of C. ribicola using RNA-seq.

Results: cDNA libraries were constructed from aeciospore, urediniospore, and western white pine (Pinus monticola) tissues post Cri infection. Over 200 million RNA-seq 100-bp paired-end (PE) reads from rust fungal spores were de novo assembled and a reference transcriptome was generated with 17,880 transcripts that were expressed from 13,629 unigenes. A total of 734 unique proteins were predicted as a part of the Cri secretome from complete open reading frames (ORFs), and 41 % of them were Cronartium-specific. This study further identified a repertoire of candidate effectors and other pathogenicity determinants. Differentially expressed genes (DEGs) were identified to gain an understanding of molecular events important during the WPBR fungus life cycle by comparing Cri transcriptomes at different infection stages. Large-scale changes of in planta gene expression profiles were observed, revealing that multiple fungal biosynthetic pathways were enhanced during mycelium growth inside infected pine stem tissues. Conversely, many fungal genes that were up-regulated at the urediniospore stage appeared to be signalling components and transporters. The secreted fungal protein genes that were up-regulated in pine needle tissues during early infection were primarily associated with cell wall modifications, possibly to mask the rust pathogen from plant defenses.

Conclusion: This comprehensive transcriptome profiling substantially improves our current understanding of molecular WP-BR interactions. The repertoire of candidate effectors and other putative pathogenicity determinants identified here are valuable for future functional analysis of Cri virulence and pathogenicity.

No MeSH data available.


Related in: MedlinePlus