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Evolution of the EKA family of powdery mildew avirulence-effector genes from the ORF 1 of a LINE retrotransposon.

Amselem J, Vigouroux M, Oberhaensli S, Brown JK, Bindschedler LV, Skamnioti P, Wicker T, Spanu PD, Quesneville H, Sacristán S - BMC Genomics (2015)

Bottom Line: The Avrk1 and Avra10 avirulence (AVR) genes encode effectors that increase the pathogenicity of the fungus Blumeria graminis f.sp. hordei (Bgh), the powdery mildew pathogen, in susceptible barley plants.The Class I LINE retrotransposon copies homologous to Avrk1 and Avra10 represent 6.5 % of the Bgh annotated genome and, among them, we identified 293 AVR/effector candidate genes.The co-option of Avra10 and Avrk1 as effectors from truncated copies of retrotransposons explains the huge number of homologues in Bgh genome that could act as dynamic reservoirs from which new effector genes may evolve.

View Article: PubMed Central - PubMed

Affiliation: INRA, UR1164 URGI Unité de Recherche Génomique-Info, Institut National de la Recherche Agronomique de Versailles-Grignon, Versailles, 78026, France. joelle.amselem@versailles.inra.fr.

ABSTRACT

Background: The Avrk1 and Avra10 avirulence (AVR) genes encode effectors that increase the pathogenicity of the fungus Blumeria graminis f.sp. hordei (Bgh), the powdery mildew pathogen, in susceptible barley plants. In resistant barley, MLK1 and MLA10 resistance proteins recognize the presence of AVRK1 and AVRA10, eliciting the hypersensitive response typical of gene for gene interactions. Avrk1 and Avra10 have more than 1350 homologues in Bgh genome, forming the EKA (Effectors homologous to Avr k 1 and Avr a 10) gene family.

Results: We tested the hypothesis that the EKA family originated from degenerate copies of Class I LINE retrotransposons by analysing the EKA family in the genome of Bgh isolate DH14 with bioinformatic tools specially developed for the analysis of Transposable Elements (TE) in genomes. The Class I LINE retrotransposon copies homologous to Avrk1 and Avra10 represent 6.5 % of the Bgh annotated genome and, among them, we identified 293 AVR/effector candidate genes. We also experimentally identified peptides that indicated the translation of several predicted proteins from EKA family members, which had higher relative abundance in haustoria than in hyphae.

Conclusions: Our analyses indicate that Avrk1 and Avra10 have evolved from part of the ORF1 gene of Class I LINE retrotransposons. The co-option of Avra10 and Avrk1 as effectors from truncated copies of retrotransposons explains the huge number of homologues in Bgh genome that could act as dynamic reservoirs from which new effector genes may evolve. These data provide further evidence for recruitment of retrotransposons in the evolution of new biological functions.

No MeSH data available.


Kryze potential genome copy containing an ORF1 homologous to AVRk1 containing a cysteine-rich NB domain (PF00098.16_zf-CCHC_GAG) and a putative ORF2p with RT (PFAM: PF00078.20) and RH (PFAM: PF00075.17) domains. a Blgr_v3_contig_001018.fa:18231..24230 bp corresponding to Bgh_RIX_G4472 full-length copy with 3000 bp downstream region. AVRK1 alignment (in red) and domains annotated by PASTEC classifier (green) are represented. b Blue lines represent the two TE genomic copies mapped in the context of all the copies (brown lines) plotted to the reference TE consensus sequences Bgh_RIX_G4472 and Bgh_RIX_G5646
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Fig3: Kryze potential genome copy containing an ORF1 homologous to AVRk1 containing a cysteine-rich NB domain (PF00098.16_zf-CCHC_GAG) and a putative ORF2p with RT (PFAM: PF00078.20) and RH (PFAM: PF00075.17) domains. a Blgr_v3_contig_001018.fa:18231..24230 bp corresponding to Bgh_RIX_G4472 full-length copy with 3000 bp downstream region. AVRK1 alignment (in red) and domains annotated by PASTEC classifier (green) are represented. b Blue lines represent the two TE genomic copies mapped in the context of all the copies (brown lines) plotted to the reference TE consensus sequences Bgh_RIX_G4472 and Bgh_RIX_G5646

Mentions: Any of the nine TE consensus sequences similar to Avrk1 could be considered full-length LINE retrotransposons containing both ORF 1 and ORF 2. Seven out these nine TE consensus sequences matched 34 full-length fragments spanning the whole TE consensus sequence. In order to look for putative ORF2 that had been overlooked during TE search and annotation, we extracted the genome sequences of these 34 fragments and searched for LINE-ORF2 domains within the 3000 bp downstream of the ORF1. PASTEC TEclassifier [20] identified the characteristic RT-RH domain at the expected location in one of those sequences (Fig. 3A). Thus, we found a potential genome copy of a full-length LINE retrotransposon with 2 ORFs (that we hereafter name Kryze) in a full-length genome copy annotated by TE consensus Bgh_RIX_G4472 (81.5 % of nucleotide identity), extended to 3000 bp downstream. The ORF 1 of Kryze is similar to Avrk1 (67 % amino-acid identity), and the extended 3000 bp containing the ORF2 of Kryze are similar (71.5 % nucleotide identity) to the TE consensus Bgh_RIX_G5646 (Fig. 3B).Fig. 3


Evolution of the EKA family of powdery mildew avirulence-effector genes from the ORF 1 of a LINE retrotransposon.

Amselem J, Vigouroux M, Oberhaensli S, Brown JK, Bindschedler LV, Skamnioti P, Wicker T, Spanu PD, Quesneville H, Sacristán S - BMC Genomics (2015)

Kryze potential genome copy containing an ORF1 homologous to AVRk1 containing a cysteine-rich NB domain (PF00098.16_zf-CCHC_GAG) and a putative ORF2p with RT (PFAM: PF00078.20) and RH (PFAM: PF00075.17) domains. a Blgr_v3_contig_001018.fa:18231..24230 bp corresponding to Bgh_RIX_G4472 full-length copy with 3000 bp downstream region. AVRK1 alignment (in red) and domains annotated by PASTEC classifier (green) are represented. b Blue lines represent the two TE genomic copies mapped in the context of all the copies (brown lines) plotted to the reference TE consensus sequences Bgh_RIX_G4472 and Bgh_RIX_G5646
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4641428&req=5

Fig3: Kryze potential genome copy containing an ORF1 homologous to AVRk1 containing a cysteine-rich NB domain (PF00098.16_zf-CCHC_GAG) and a putative ORF2p with RT (PFAM: PF00078.20) and RH (PFAM: PF00075.17) domains. a Blgr_v3_contig_001018.fa:18231..24230 bp corresponding to Bgh_RIX_G4472 full-length copy with 3000 bp downstream region. AVRK1 alignment (in red) and domains annotated by PASTEC classifier (green) are represented. b Blue lines represent the two TE genomic copies mapped in the context of all the copies (brown lines) plotted to the reference TE consensus sequences Bgh_RIX_G4472 and Bgh_RIX_G5646
Mentions: Any of the nine TE consensus sequences similar to Avrk1 could be considered full-length LINE retrotransposons containing both ORF 1 and ORF 2. Seven out these nine TE consensus sequences matched 34 full-length fragments spanning the whole TE consensus sequence. In order to look for putative ORF2 that had been overlooked during TE search and annotation, we extracted the genome sequences of these 34 fragments and searched for LINE-ORF2 domains within the 3000 bp downstream of the ORF1. PASTEC TEclassifier [20] identified the characteristic RT-RH domain at the expected location in one of those sequences (Fig. 3A). Thus, we found a potential genome copy of a full-length LINE retrotransposon with 2 ORFs (that we hereafter name Kryze) in a full-length genome copy annotated by TE consensus Bgh_RIX_G4472 (81.5 % of nucleotide identity), extended to 3000 bp downstream. The ORF 1 of Kryze is similar to Avrk1 (67 % amino-acid identity), and the extended 3000 bp containing the ORF2 of Kryze are similar (71.5 % nucleotide identity) to the TE consensus Bgh_RIX_G5646 (Fig. 3B).Fig. 3

Bottom Line: The Avrk1 and Avra10 avirulence (AVR) genes encode effectors that increase the pathogenicity of the fungus Blumeria graminis f.sp. hordei (Bgh), the powdery mildew pathogen, in susceptible barley plants.The Class I LINE retrotransposon copies homologous to Avrk1 and Avra10 represent 6.5 % of the Bgh annotated genome and, among them, we identified 293 AVR/effector candidate genes.The co-option of Avra10 and Avrk1 as effectors from truncated copies of retrotransposons explains the huge number of homologues in Bgh genome that could act as dynamic reservoirs from which new effector genes may evolve.

View Article: PubMed Central - PubMed

Affiliation: INRA, UR1164 URGI Unité de Recherche Génomique-Info, Institut National de la Recherche Agronomique de Versailles-Grignon, Versailles, 78026, France. joelle.amselem@versailles.inra.fr.

ABSTRACT

Background: The Avrk1 and Avra10 avirulence (AVR) genes encode effectors that increase the pathogenicity of the fungus Blumeria graminis f.sp. hordei (Bgh), the powdery mildew pathogen, in susceptible barley plants. In resistant barley, MLK1 and MLA10 resistance proteins recognize the presence of AVRK1 and AVRA10, eliciting the hypersensitive response typical of gene for gene interactions. Avrk1 and Avra10 have more than 1350 homologues in Bgh genome, forming the EKA (Effectors homologous to Avr k 1 and Avr a 10) gene family.

Results: We tested the hypothesis that the EKA family originated from degenerate copies of Class I LINE retrotransposons by analysing the EKA family in the genome of Bgh isolate DH14 with bioinformatic tools specially developed for the analysis of Transposable Elements (TE) in genomes. The Class I LINE retrotransposon copies homologous to Avrk1 and Avra10 represent 6.5 % of the Bgh annotated genome and, among them, we identified 293 AVR/effector candidate genes. We also experimentally identified peptides that indicated the translation of several predicted proteins from EKA family members, which had higher relative abundance in haustoria than in hyphae.

Conclusions: Our analyses indicate that Avrk1 and Avra10 have evolved from part of the ORF1 gene of Class I LINE retrotransposons. The co-option of Avra10 and Avrk1 as effectors from truncated copies of retrotransposons explains the huge number of homologues in Bgh genome that could act as dynamic reservoirs from which new effector genes may evolve. These data provide further evidence for recruitment of retrotransposons in the evolution of new biological functions.

No MeSH data available.