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A comprehensive analysis of genes encoding small secreted proteins identifies candidate effectors in Melampsora larici-populina (poplar leaf rust)

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Abstract
The obligate biotrophic rust fungus Melampsora larici-populina is the most devastating and widespread pathogen of poplars. Studies over recent years have identified various small secreted proteins (SSP) from plant biotrophic filamentous pathogens and have highlighted their role as effectors in host-pathogen interactions. The recent analysis of the M. larici-populina genome sequence has revealed the presence of 1,184 SSP-encoding genes in this rust fungus. In the present study, the expression and evolutionary dynamics of these SSP were investigated to pinpoint the arsenal of putative effectors that could be involved in the interaction between the rust fungus and poplar. Similarity with effectors previously described in Melampsora spp., richness in cysteines, and organization in large families were extensively detailed and discussed. Positive selection analyses conducted over clusters of paralogous genes revealed fast-evolving candidate effectors. Transcript profiling of selected M. laricipopulina SSP showed a timely coordinated expression during leaf infection, and the accumulation of four candidate effectors in distinct rust infection structures was demonstrated by immunolocalization. This integrated and multifaceted approach helps to prioritize candidate effector genes for functional studies
Keywords
LACCARIA-BICOLOR, POSITIVE SELECTION, OBLIGATE BIOTROPHY, AVIRULENCE PROTEINS, CLADOSPORIUM-FULVUM, PATHOGEN INTERACTIONS, MULTIPLE SEQUENCE ALIGNMENT, PLANT-CELLS, FLAX RUST, RESISTANCE GENES

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MLA
Hacquard, Stéphane, et al. “A Comprehensive Analysis of Genes Encoding Small Secreted Proteins Identifies Candidate Effectors in Melampsora Larici-Populina (Poplar Leaf Rust).” MOLECULAR PLANT-MICROBE INTERACTIONS, vol. 25, no. 3, 2012, pp. 279–93, doi:10.1094/MPMI-09-11-0238.
APA
Hacquard, S., Joly, D. L., Lin, Y.-C., Tisserant, E., Feau, N., Delaruelle, C., … Duplessis, S. (2012). A comprehensive analysis of genes encoding small secreted proteins identifies candidate effectors in Melampsora larici-populina (poplar leaf rust). MOLECULAR PLANT-MICROBE INTERACTIONS, 25(3), 279–293. https://doi.org/10.1094/MPMI-09-11-0238
Chicago author-date
Hacquard, Stéphane, David L Joly, Yao-Cheng Lin, Emilie Tisserant, Nicolas Feau, Christine Delaruelle, Valérie Legué, et al. 2012. “A Comprehensive Analysis of Genes Encoding Small Secreted Proteins Identifies Candidate Effectors in Melampsora Larici-Populina (Poplar Leaf Rust).” MOLECULAR PLANT-MICROBE INTERACTIONS 25 (3): 279–93. https://doi.org/10.1094/MPMI-09-11-0238.
Chicago author-date (all authors)
Hacquard, Stéphane, David L Joly, Yao-Cheng Lin, Emilie Tisserant, Nicolas Feau, Christine Delaruelle, Valérie Legué, Annegret Kohler, Philippe Tanguay, Benjamin Petre, Pascal Frey, Yves Van de Peer, Pierre Rouzé, Francis Martin, Richard C Hamelin, and Sébastien Duplessis. 2012. “A Comprehensive Analysis of Genes Encoding Small Secreted Proteins Identifies Candidate Effectors in Melampsora Larici-Populina (Poplar Leaf Rust).” MOLECULAR PLANT-MICROBE INTERACTIONS 25 (3): 279–293. doi:10.1094/MPMI-09-11-0238.
Vancouver
1.
Hacquard S, Joly DL, Lin Y-C, Tisserant E, Feau N, Delaruelle C, et al. A comprehensive analysis of genes encoding small secreted proteins identifies candidate effectors in Melampsora larici-populina (poplar leaf rust). MOLECULAR PLANT-MICROBE INTERACTIONS. 2012;25(3):279–93.
IEEE
[1]
S. Hacquard et al., “A comprehensive analysis of genes encoding small secreted proteins identifies candidate effectors in Melampsora larici-populina (poplar leaf rust),” MOLECULAR PLANT-MICROBE INTERACTIONS, vol. 25, no. 3, pp. 279–293, 2012.
@article{2087559,
  abstract     = {{The obligate biotrophic rust fungus Melampsora larici-populina is the most devastating and widespread pathogen of poplars. Studies over recent years have identified various small secreted proteins (SSP) from plant biotrophic filamentous pathogens and have highlighted their role as effectors in host-pathogen interactions. The recent analysis of the M. larici-populina genome sequence has revealed the presence of 1,184 SSP-encoding genes in this rust fungus. In the present study, the expression and evolutionary dynamics of these SSP were investigated to pinpoint the arsenal of putative effectors that could be involved in the interaction between the rust fungus and poplar. Similarity with effectors previously described in Melampsora spp., richness in cysteines, and organization in large families were extensively detailed and discussed. Positive selection analyses conducted over clusters of paralogous genes revealed fast-evolving candidate effectors. Transcript profiling of selected M. laricipopulina SSP showed a timely coordinated expression during leaf infection, and the accumulation of four candidate effectors in distinct rust infection structures was demonstrated by immunolocalization. This integrated and multifaceted approach helps to prioritize candidate effector genes for functional studies}},
  author       = {{Hacquard, Stéphane and Joly, David L and Lin, Yao-Cheng and Tisserant, Emilie and Feau, Nicolas and Delaruelle, Christine and Legué, Valérie and Kohler, Annegret and Tanguay, Philippe and Petre, Benjamin and Frey, Pascal and Van de Peer, Yves and Rouzé, Pierre and Martin, Francis and Hamelin, Richard C and Duplessis, Sébastien}},
  issn         = {{0894-0282}},
  journal      = {{MOLECULAR PLANT-MICROBE INTERACTIONS}},
  keywords     = {{LACCARIA-BICOLOR,POSITIVE SELECTION,OBLIGATE BIOTROPHY,AVIRULENCE PROTEINS,CLADOSPORIUM-FULVUM,PATHOGEN INTERACTIONS,MULTIPLE SEQUENCE ALIGNMENT,PLANT-CELLS,FLAX RUST,RESISTANCE GENES}},
  language     = {{eng}},
  number       = {{3}},
  pages        = {{279--293}},
  title        = {{A comprehensive analysis of genes encoding small secreted proteins identifies candidate effectors in Melampsora larici-populina (poplar leaf rust)}},
  url          = {{http://dx.doi.org/10.1094/MPMI-09-11-0238}},
  volume       = {{25}},
  year         = {{2012}},
}

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