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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

The sTEKhot index discriminates S. borealis proteins in core ortholog groups and whole predicted proteomes. (A) Overall distribution of sTEKhot values from the three fungal species within COGs. Each bubble represents a COG positioned according to the contribution of each ortholog (sTEKhot%) to the total sTEKhot of the COG. Therefore, orthologs that have similar sTEKhot values in all three species appear at the center of the plot, while COGs appear near the corner of the species harboring the ortholog with the highest sTEKhot otherwise. The size of bubbles is proportional to the sTEKhot value of S. borealis orthologs. Data points are frequent above the 40% line for S. borealis sTEKhot, and less so for S. sclerotiorum and B. cinerea sTEKhot indicating frequent higher sTEKhot values in S. borealis orthologs. (B) Species distribution of orthologs having the highest sTEKhot value in COGs. (C) Distribution of the sTEKhot index in the whole predicted proteome of the three fungi.
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Figure 4: The sTEKhot index discriminates S. borealis proteins in core ortholog groups and whole predicted proteomes. (A) Overall distribution of sTEKhot values from the three fungal species within COGs. Each bubble represents a COG positioned according to the contribution of each ortholog (sTEKhot%) to the total sTEKhot of the COG. Therefore, orthologs that have similar sTEKhot values in all three species appear at the center of the plot, while COGs appear near the corner of the species harboring the ortholog with the highest sTEKhot otherwise. The size of bubbles is proportional to the sTEKhot value of S. borealis orthologs. Data points are frequent above the 40% line for S. borealis sTEKhot, and less so for S. sclerotiorum and B. cinerea sTEKhot indicating frequent higher sTEKhot values in S. borealis orthologs. (B) Species distribution of orthologs having the highest sTEKhot value in COGs. (C) Distribution of the sTEKhot index in the whole predicted proteome of the three fungi.

Mentions: Several studies reported biases in amino acid usage in the proteome of extremophiles and proposed indices able to discriminate proteins from extremophilic and related mesophilic organisms (Suhre and Claverie, 2003; Zeldovich et al., 2007; Wang and Lercher, 2010). To analyze the degree to which intrinsic protein disorder and amino acid usage of individual proteins matches with specific patterns identified in S. borealis predicted proteome, we designed the S. borealis T (Thr), E (Glu), K (Lys), hot (hot loops) index as follows:(1)sTEKhot=TE+K+hotwhere “T,” “E,” and “K” are the normalized frequencies of Thr, Glu and Lys respectively in a given protein sequence, and “hot” is the normalized frequency of hot loops in this sequence. We computed the sTEKhot index for each protein in the predicted proteomes of S. borealis, S. sclerotiorum, and B. cinerea. First, we compared the distribution of sTEKhot values in COGs by plotting all values in a ternary plot (Figure 4A). This revealed that sTEKhot values are distributed along an axis pointing toward S. borealis angle, clearly showing that sTEKhot values of S. borealis orthologs are major contributors to the structure of the dataset. There was 692 COGs in which S. borealis sTEKhot value accounted for >40% of the total sTEKhot for the COG, but only 388 and 345 in which S. sclerotiorum and B. cinerea sTEKhot values respectively accounted for >40% of the total sKTEHhot for the COG (Figure 4A). Consistently, S. borealis has the highest sTEKhot value in 42.7% of COGS (2761), whereas S. sclerotiorum and B. cinerea have the highest sTEKhot value in 28.3% (1845) and 28.8% (1865) of the COGs respectively (Figure 4B).


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)

The sTEKhot index discriminates S. borealis proteins in core ortholog groups and whole predicted proteomes. (A) Overall distribution of sTEKhot values from the three fungal species within COGs. Each bubble represents a COG positioned according to the contribution of each ortholog (sTEKhot%) to the total sTEKhot of the COG. Therefore, orthologs that have similar sTEKhot values in all three species appear at the center of the plot, while COGs appear near the corner of the species harboring the ortholog with the highest sTEKhot otherwise. The size of bubbles is proportional to the sTEKhot value of S. borealis orthologs. Data points are frequent above the 40% line for S. borealis sTEKhot, and less so for S. sclerotiorum and B. cinerea sTEKhot indicating frequent higher sTEKhot values in S. borealis orthologs. (B) Species distribution of orthologs having the highest sTEKhot value in COGs. (C) Distribution of the sTEKhot index in the whole predicted proteome of the three fungi.
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Related In: Results  -  Collection

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Show All Figures
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Figure 4: The sTEKhot index discriminates S. borealis proteins in core ortholog groups and whole predicted proteomes. (A) Overall distribution of sTEKhot values from the three fungal species within COGs. Each bubble represents a COG positioned according to the contribution of each ortholog (sTEKhot%) to the total sTEKhot of the COG. Therefore, orthologs that have similar sTEKhot values in all three species appear at the center of the plot, while COGs appear near the corner of the species harboring the ortholog with the highest sTEKhot otherwise. The size of bubbles is proportional to the sTEKhot value of S. borealis orthologs. Data points are frequent above the 40% line for S. borealis sTEKhot, and less so for S. sclerotiorum and B. cinerea sTEKhot indicating frequent higher sTEKhot values in S. borealis orthologs. (B) Species distribution of orthologs having the highest sTEKhot value in COGs. (C) Distribution of the sTEKhot index in the whole predicted proteome of the three fungi.
Mentions: Several studies reported biases in amino acid usage in the proteome of extremophiles and proposed indices able to discriminate proteins from extremophilic and related mesophilic organisms (Suhre and Claverie, 2003; Zeldovich et al., 2007; Wang and Lercher, 2010). To analyze the degree to which intrinsic protein disorder and amino acid usage of individual proteins matches with specific patterns identified in S. borealis predicted proteome, we designed the S. borealis T (Thr), E (Glu), K (Lys), hot (hot loops) index as follows:(1)sTEKhot=TE+K+hotwhere “T,” “E,” and “K” are the normalized frequencies of Thr, Glu and Lys respectively in a given protein sequence, and “hot” is the normalized frequency of hot loops in this sequence. We computed the sTEKhot index for each protein in the predicted proteomes of S. borealis, S. sclerotiorum, and B. cinerea. First, we compared the distribution of sTEKhot values in COGs by plotting all values in a ternary plot (Figure 4A). This revealed that sTEKhot values are distributed along an axis pointing toward S. borealis angle, clearly showing that sTEKhot values of S. borealis orthologs are major contributors to the structure of the dataset. There was 692 COGs in which S. borealis sTEKhot value accounted for >40% of the total sTEKhot for the COG, but only 388 and 345 in which S. sclerotiorum and B. cinerea sTEKhot values respectively accounted for >40% of the total sKTEHhot for the COG (Figure 4A). Consistently, S. borealis has the highest sTEKhot value in 42.7% of COGS (2761), whereas S. sclerotiorum and B. cinerea have the highest sTEKhot value in 28.3% (1845) and 28.8% (1865) of the COGs respectively (Figure 4B).

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