Comparative Genomics Identifies a Novel Conserved Protein, HpaT, in Proteobacterial Type III Secretion Systems that Do Not Possess the Putative Translocon Protein HrpF
Xanthomonas translucens is the causal agent of bacterial leaf streak, the most common bacterial disease of wheat and barley. To cause disease, most xanthomonads depend on a highly conserved type III secretion system, which translocates type III effectors into host plant cells. Mutagenesis of the con...
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| Format: | Article |
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Frontiers Media S.A.
2017-06-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | http://journal.frontiersin.org/article/10.3389/fmicb.2017.01177/full |
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| author | Céline Pesce Céline Pesce Jonathan M. Jacobs Jonathan M. Jacobs Edwige Berthelot Marion Perret Taca Vancheva Taca Vancheva Claude Bragard Ralf Koebnik |
| author_facet | Céline Pesce Céline Pesce Jonathan M. Jacobs Jonathan M. Jacobs Edwige Berthelot Marion Perret Taca Vancheva Taca Vancheva Claude Bragard Ralf Koebnik |
| author_sort | Céline Pesce |
| collection | DOAJ |
| description | Xanthomonas translucens is the causal agent of bacterial leaf streak, the most common bacterial disease of wheat and barley. To cause disease, most xanthomonads depend on a highly conserved type III secretion system, which translocates type III effectors into host plant cells. Mutagenesis of the conserved type III secretion gene hrcT confirmed that the X. translucens type III secretion system is required to cause disease on the host plant barley and to trigger a non-host hypersensitive response (HR) in pepper leaves. Type III effectors are delivered to the host cell by a surface appendage, the Hrp pilus, and a translocon protein complex that inserts into the plant cell plasma membrane. Homologs of the Xanthomonas HrpF protein, including PopF from Ralstonia solanacearum and NolX from rhizobia, are thought to act as a translocon protein. Comparative genomics revealed that X. translucens strains harbor a noncanonical hrp gene cluster, which rather shares features with type III secretion systems from Ralstonia solanacearum, Paraburkholderia andropogonis, Collimonas fungivorans, and Uliginosibacterium gangwonense than other Xanthomonas spp. Surprisingly, none of these bacteria, except R. solanacearum, encode a homolog of the HrpF translocon. Here, we aimed at identifying a candidate translocon from X. translucens. Notably, genomes from strains that lacked hrpF/popF/nolX instead encode another gene, called hpaT, adjacent to and co-regulated with the type III secretion system gene cluster. An insertional mutant in the X. translucens hpaT gene, which is the first gene of a two-gene operon, hpaT-hpaH, was non-pathogenic on barley and did not cause the HR or programmed cell death in non-host pepper similar to the hrcT mutant. The hpaT mutant phenotypes were partially complemented by either hpaT or the downstream gene, hpaH, which has been described as a facilitator of translocation in Xanthomonas oryzae. Interestingly, the hpaT mutant was also complemented by the hrpF gene from Xanthomonas euvesicatoria. These findings reveal that both HpaT and HpaH contribute to the injection of type III effectors into plant cells. |
| first_indexed | 2024-12-12T14:32:45Z |
| format | Article |
| id | doaj.art-476cca8cfb9c4daf86c0360d55ac4b7b |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-12T14:32:45Z |
| publishDate | 2017-06-01 |
| publisher | Frontiers Media S.A. |
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| spelling | doaj.art-476cca8cfb9c4daf86c0360d55ac4b7b2022-12-22T00:21:28ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2017-06-01810.3389/fmicb.2017.01177252902Comparative Genomics Identifies a Novel Conserved Protein, HpaT, in Proteobacterial Type III Secretion Systems that Do Not Possess the Putative Translocon Protein HrpFCéline Pesce0Céline Pesce1Jonathan M. Jacobs2Jonathan M. Jacobs3Edwige Berthelot4Marion Perret5Taca Vancheva6Taca Vancheva7Claude Bragard8Ralf Koebnik9UMR 186 IRD-Cirad-Université Montpellier IPMEMontpellier, FranceApplied Microbiology Phytopathology, Earth and Life Institute, Université catholique de LouvainLouvain-la-Neuve, BelgiumUMR 186 IRD-Cirad-Université Montpellier IPMEMontpellier, FranceApplied Microbiology Phytopathology, Earth and Life Institute, Université catholique de LouvainLouvain-la-Neuve, BelgiumUMR 186 IRD-Cirad-Université Montpellier IPMEMontpellier, FranceUMR 186 IRD-Cirad-Université Montpellier IPMEMontpellier, FranceUMR 186 IRD-Cirad-Université Montpellier IPMEMontpellier, FranceApplied Microbiology Phytopathology, Earth and Life Institute, Université catholique de LouvainLouvain-la-Neuve, BelgiumApplied Microbiology Phytopathology, Earth and Life Institute, Université catholique de LouvainLouvain-la-Neuve, BelgiumUMR 186 IRD-Cirad-Université Montpellier IPMEMontpellier, FranceXanthomonas translucens is the causal agent of bacterial leaf streak, the most common bacterial disease of wheat and barley. To cause disease, most xanthomonads depend on a highly conserved type III secretion system, which translocates type III effectors into host plant cells. Mutagenesis of the conserved type III secretion gene hrcT confirmed that the X. translucens type III secretion system is required to cause disease on the host plant barley and to trigger a non-host hypersensitive response (HR) in pepper leaves. Type III effectors are delivered to the host cell by a surface appendage, the Hrp pilus, and a translocon protein complex that inserts into the plant cell plasma membrane. Homologs of the Xanthomonas HrpF protein, including PopF from Ralstonia solanacearum and NolX from rhizobia, are thought to act as a translocon protein. Comparative genomics revealed that X. translucens strains harbor a noncanonical hrp gene cluster, which rather shares features with type III secretion systems from Ralstonia solanacearum, Paraburkholderia andropogonis, Collimonas fungivorans, and Uliginosibacterium gangwonense than other Xanthomonas spp. Surprisingly, none of these bacteria, except R. solanacearum, encode a homolog of the HrpF translocon. Here, we aimed at identifying a candidate translocon from X. translucens. Notably, genomes from strains that lacked hrpF/popF/nolX instead encode another gene, called hpaT, adjacent to and co-regulated with the type III secretion system gene cluster. An insertional mutant in the X. translucens hpaT gene, which is the first gene of a two-gene operon, hpaT-hpaH, was non-pathogenic on barley and did not cause the HR or programmed cell death in non-host pepper similar to the hrcT mutant. The hpaT mutant phenotypes were partially complemented by either hpaT or the downstream gene, hpaH, which has been described as a facilitator of translocation in Xanthomonas oryzae. Interestingly, the hpaT mutant was also complemented by the hrpF gene from Xanthomonas euvesicatoria. These findings reveal that both HpaT and HpaH contribute to the injection of type III effectors into plant cells.http://journal.frontiersin.org/article/10.3389/fmicb.2017.01177/fullXanthomonas translucensXanthomonas hyacinthiXanthomonas theicolaCollimonas fungivoranshrp genestranslocon |
| spellingShingle | Céline Pesce Céline Pesce Jonathan M. Jacobs Jonathan M. Jacobs Edwige Berthelot Marion Perret Taca Vancheva Taca Vancheva Claude Bragard Ralf Koebnik Comparative Genomics Identifies a Novel Conserved Protein, HpaT, in Proteobacterial Type III Secretion Systems that Do Not Possess the Putative Translocon Protein HrpF Frontiers in Microbiology Xanthomonas translucens Xanthomonas hyacinthi Xanthomonas theicola Collimonas fungivorans hrp genes translocon |
| title | Comparative Genomics Identifies a Novel Conserved Protein, HpaT, in Proteobacterial Type III Secretion Systems that Do Not Possess the Putative Translocon Protein HrpF |
| title_full | Comparative Genomics Identifies a Novel Conserved Protein, HpaT, in Proteobacterial Type III Secretion Systems that Do Not Possess the Putative Translocon Protein HrpF |
| title_fullStr | Comparative Genomics Identifies a Novel Conserved Protein, HpaT, in Proteobacterial Type III Secretion Systems that Do Not Possess the Putative Translocon Protein HrpF |
| title_full_unstemmed | Comparative Genomics Identifies a Novel Conserved Protein, HpaT, in Proteobacterial Type III Secretion Systems that Do Not Possess the Putative Translocon Protein HrpF |
| title_short | Comparative Genomics Identifies a Novel Conserved Protein, HpaT, in Proteobacterial Type III Secretion Systems that Do Not Possess the Putative Translocon Protein HrpF |
| title_sort | comparative genomics identifies a novel conserved protein hpat in proteobacterial type iii secretion systems that do not possess the putative translocon protein hrpf |
| topic | Xanthomonas translucens Xanthomonas hyacinthi Xanthomonas theicola Collimonas fungivorans hrp genes translocon |
| url | http://journal.frontiersin.org/article/10.3389/fmicb.2017.01177/full |
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