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Common protein sequence signatures associate with Sclerotinia borealis lifestyle and secretion in fungal pathogens of the Sclerotiniaceae.

Badet T, Peyraud R, Raffaele S - Front Plant Sci (2015)

Bottom Line: To spread successfully, S. borealis must synthesize proteins adapted to function in its specific environment.We found that enrichment in Thr, depletion in Glu and Lys, and low disorder frequency in hot loops are significantly associated with S. borealis proteins.High index proteins were also enriched in function associated with plant colonization in S. borealis, and in in planta-induced genes in S. sclerotiorum.

View Article: PubMed Central - PubMed

Affiliation: Laboratoire des Interactions Plantes-Microorganismes, Institut National de la Recherche Agronomique, UMR441 Castanet-Tolosan, France ; Laboratoire des Interactions Plantes-Microorganismes, Centre National de la Recherche Scientifique, UMR2594 Castanet-Tolosan, France.

ABSTRACT
Fungal plant pathogens produce secreted proteins adapted to function outside fungal cells to facilitate colonization of their hosts. In many cases such as for fungi from the Sclerotiniaceae family the repertoire and function of secreted proteins remains elusive. In the Sclerotiniaceae, whereas Sclerotinia sclerotiorum and Botrytis cinerea are cosmopolitan broad host-range plant pathogens, Sclerotinia borealis has a psychrophilic lifestyle with a low optimal growth temperature, a narrow host range and geographic distribution. To spread successfully, S. borealis must synthesize proteins adapted to function in its specific environment. The search for signatures of adaptation to S. borealis lifestyle may therefore help revealing proteins critical for colonization of the environment by Sclerotiniaceae fungi. Here, we analyzed amino acids usage and intrinsic protein disorder in alignments of groups of orthologous proteins from the three Sclerotiniaceae species. We found that enrichment in Thr, depletion in Glu and Lys, and low disorder frequency in hot loops are significantly associated with S. borealis proteins. We designed an index to report bias in these properties and found that high index proteins were enriched among secreted proteins in the three Sclerotiniaceae fungi. High index proteins were also enriched in function associated with plant colonization in S. borealis, and in in planta-induced genes in S. sclerotiorum. We highlight a novel putative antifreeze protein and a novel putative lytic polysaccharide monooxygenase identified through our pipeline as candidate proteins involved in colonization of the environment. Our findings suggest that similar protein signatures associate with S. borealis lifestyle and with secretion in the Sclerotiniaceae. These signatures may be useful for identifying proteins of interest as targets for the management of plant diseases.

No MeSH data available.


Related in: MedlinePlus

Proportion of S. sclerotiorum proteins encoded by genes differentially expressed in planta according to sTEKhot cutoff values. In S. sclerotiorum complete genome (sTEKhot ≥ 0), the proportion of genes induced ≥2-fold in planta is ~4.31%, whereas it reaches ~27.1%.among proteins with sTEKhot ≥ 2 (dotted line).
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Figure 7: Proportion of S. sclerotiorum proteins encoded by genes differentially expressed in planta according to sTEKhot cutoff values. In S. sclerotiorum complete genome (sTEKhot ≥ 0), the proportion of genes induced ≥2-fold in planta is ~4.31%, whereas it reaches ~27.1%.among proteins with sTEKhot ≥ 2 (dotted line).

Mentions: To further support the association between high sTEKhot index and colonization of the environment, and particularly host plants, we analyzed the distribution of sTEKhot values in S. sclerotiorum genes differentially regulated in planta. For this, we took advantage of S. sclerotiorum microarray gene expression data generated by Amselem et al. from infected sunflower cotyledons (Amselem et al., 2011). In this dataset, out of 14 503 predicted protein coding genes, 615 were induced at least two-fold during infection of sunflower (4.31%) and 458 genes down-regulated at least two-fold (3.21%). The proportion of genes induced in planta reached 27.1% of S. sclerotiorum genes encoding proteins with sTEKhot ≥ 2, representing ~6.3-fold enrichment (Figure 7). The proportion of genes down-regulated in planta reached 12.1% of S. sclerotiorum genes encoding proteins with sTEKhot ≥ 2, representing ~3.8-fold enrichment. S. sclerotiorum proteins with sTEKhot > 1 include six proteins with CFEM domain, a Cys-rich domain with proposed role in fungal pathogenesis, two proteins with a cerato-platanin domain, one of which being the ortholog of B. cinerea pathogen associated molecular pattern BcSpl1 (Frías et al., 2011), 27 proteins with a pectin lyase fold found in Aspergillus virulence factors (Mayans et al., 1997), and 29 out of 78 effector candidates proposed by Guyon et al. (2014). These findings are consistent with important role in the colonization of the host plant for some proteins with high sTEKhot values.


Common protein sequence signatures associate with Sclerotinia borealis lifestyle and secretion in fungal pathogens of the Sclerotiniaceae.

Badet T, Peyraud R, Raffaele S - Front Plant Sci (2015)

Proportion of S. sclerotiorum proteins encoded by genes differentially expressed in planta according to sTEKhot cutoff values. In S. sclerotiorum complete genome (sTEKhot ≥ 0), the proportion of genes induced ≥2-fold in planta is ~4.31%, whereas it reaches ~27.1%.among proteins with sTEKhot ≥ 2 (dotted line).
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Figure 7: Proportion of S. sclerotiorum proteins encoded by genes differentially expressed in planta according to sTEKhot cutoff values. In S. sclerotiorum complete genome (sTEKhot ≥ 0), the proportion of genes induced ≥2-fold in planta is ~4.31%, whereas it reaches ~27.1%.among proteins with sTEKhot ≥ 2 (dotted line).
Mentions: To further support the association between high sTEKhot index and colonization of the environment, and particularly host plants, we analyzed the distribution of sTEKhot values in S. sclerotiorum genes differentially regulated in planta. For this, we took advantage of S. sclerotiorum microarray gene expression data generated by Amselem et al. from infected sunflower cotyledons (Amselem et al., 2011). In this dataset, out of 14 503 predicted protein coding genes, 615 were induced at least two-fold during infection of sunflower (4.31%) and 458 genes down-regulated at least two-fold (3.21%). The proportion of genes induced in planta reached 27.1% of S. sclerotiorum genes encoding proteins with sTEKhot ≥ 2, representing ~6.3-fold enrichment (Figure 7). The proportion of genes down-regulated in planta reached 12.1% of S. sclerotiorum genes encoding proteins with sTEKhot ≥ 2, representing ~3.8-fold enrichment. S. sclerotiorum proteins with sTEKhot > 1 include six proteins with CFEM domain, a Cys-rich domain with proposed role in fungal pathogenesis, two proteins with a cerato-platanin domain, one of which being the ortholog of B. cinerea pathogen associated molecular pattern BcSpl1 (Frías et al., 2011), 27 proteins with a pectin lyase fold found in Aspergillus virulence factors (Mayans et al., 1997), and 29 out of 78 effector candidates proposed by Guyon et al. (2014). These findings are consistent with important role in the colonization of the host plant for some proteins with high sTEKhot values.

Bottom Line: To spread successfully, S. borealis must synthesize proteins adapted to function in its specific environment.We found that enrichment in Thr, depletion in Glu and Lys, and low disorder frequency in hot loops are significantly associated with S. borealis proteins.High index proteins were also enriched in function associated with plant colonization in S. borealis, and in in planta-induced genes in S. sclerotiorum.

View Article: PubMed Central - PubMed

Affiliation: Laboratoire des Interactions Plantes-Microorganismes, Institut National de la Recherche Agronomique, UMR441 Castanet-Tolosan, France ; Laboratoire des Interactions Plantes-Microorganismes, Centre National de la Recherche Scientifique, UMR2594 Castanet-Tolosan, France.

ABSTRACT
Fungal plant pathogens produce secreted proteins adapted to function outside fungal cells to facilitate colonization of their hosts. In many cases such as for fungi from the Sclerotiniaceae family the repertoire and function of secreted proteins remains elusive. In the Sclerotiniaceae, whereas Sclerotinia sclerotiorum and Botrytis cinerea are cosmopolitan broad host-range plant pathogens, Sclerotinia borealis has a psychrophilic lifestyle with a low optimal growth temperature, a narrow host range and geographic distribution. To spread successfully, S. borealis must synthesize proteins adapted to function in its specific environment. The search for signatures of adaptation to S. borealis lifestyle may therefore help revealing proteins critical for colonization of the environment by Sclerotiniaceae fungi. Here, we analyzed amino acids usage and intrinsic protein disorder in alignments of groups of orthologous proteins from the three Sclerotiniaceae species. We found that enrichment in Thr, depletion in Glu and Lys, and low disorder frequency in hot loops are significantly associated with S. borealis proteins. We designed an index to report bias in these properties and found that high index proteins were enriched among secreted proteins in the three Sclerotiniaceae fungi. High index proteins were also enriched in function associated with plant colonization in S. borealis, and in in planta-induced genes in S. sclerotiorum. We highlight a novel putative antifreeze protein and a novel putative lytic polysaccharide monooxygenase identified through our pipeline as candidate proteins involved in colonization of the environment. Our findings suggest that similar protein signatures associate with S. borealis lifestyle and with secretion in the Sclerotiniaceae. These signatures may be useful for identifying proteins of interest as targets for the management of plant diseases.

No MeSH data available.


Related in: MedlinePlus