Comparative Genomics Including the Early-Diverging Smut Fungus<i>Ceraceosorus bombacis</i>Reveals Signatures of Parallel Evolution within Plant and Animal Pathogens of Fungi and Oomycetes

Sharma, Rahul; Xia, Xiaojuan; Riess, Kai; Bauer, Robert; Thines, Marco

doi:10.1093/gbe/evv162

Cited by 20 publications

(27 citation statements)

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“…thlaspeos has a typical smut genome with unique effectors that suggest adaptation to dicot hosts With a size of c. 20 Mb, a low repeat content, and 6239 predicted gene models, the genome of T. thlaspeos has the typical characteristics of most sequenced smut fungi. Despite the adaptation to a dicot host, its absolute gene content and predicted functional categories largely overlap with grass-infecting smut fungi (Sharma et al, 2015;Dutheil et al, 2016). However, two unique features stand out from the genome assembly and annotation.…”

Section: Discussionmentioning

confidence: 99%

Smut infection of perennial hosts: the genome and the transcriptome of the Brassicaceae smut fungus Thecaphora thlaspeos reveal functionally conserved and novel effectors

et al. 2019

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Summary Biotrophic fungal plant pathogens can balance their virulence and form intricate relationships with their hosts. Sometimes, this leads to systemic host colonization over long time scales without macroscopic symptoms. However, how plant‐pathogenic endophytes manage to establish their sustained systemic infection remains largely unknown. Here, we present a genomic and transcriptomic analysis of Thecaphora thlaspeos. This relative of the well studied grass smut Ustilago maydis is the only smut fungus adapted to Brassicaceae hosts. Its ability to overwinter with perennial hosts and its systemic plant infection including roots are unique characteristics among smut fungi. The T. thlaspeos genome was assembled to the chromosome level. It is a typical smut genome in terms of size and genome characteristics. In silico prediction of candidate effector genes revealed common smut effector proteins and unique members. For three candidates, we have functionally demonstrated effector activity. One of these, TtTue1, suggests a potential link to cold acclimation. On the plant side, we found evidence for a typical immune response as it is present in other infection systems, despite the absence of any macroscopic symptoms during infection. Our findings suggest that T. thlaspeos distinctly balances its virulence during biotrophic growth ultimately allowing for long‐lived infection of its perennial hosts.

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Section: Discussionmentioning

confidence: 99%

Smut infection of perennial hosts: the genome and the transcriptome of the Brassicaceae smut fungus Thecaphora thlaspeos reveal functionally conserved and novel effectors

et al. 2019

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“…To avoid recognition by R-proteins, many secreted effectors adapt quickly and show limited conservation (Schirawski et al , 2010; Laurie et al , 2012). However, conservation of putative secreted effector protein (PSEP)-encoding genes among related pathogens has been reported (Hemetsberger et al , 2015; Sharma et al, 2015). These effectors have been termed “core” effectors (Sharma et al 2014).…”

Section: Discussionmentioning

confidence: 99%

“…Also in P. antarctica isolated from sediments in Antarctica, these effectors remained conserved, with secretion signal peptides intact. If these effectors were not needed anymore, it can be expected that they would either get lost quickly, as in U. pennsylvanica after a host jump from monocots to dicots (Sharma et al , 2014), or acquire new functions (Sharma et al , 2015). For Pep1 , the finding that orthologs from all yeast-only species were able to fully restore pathogenicity in U. maydis , demonstrates that its virulence function remained conserved amongst species.…”

Section: Discussionmentioning

confidence: 99%

“…For successful colonization of hosts, pathogens secrete hundreds of effector proteins (Latijnhouwers et al , 2003). Effectors often have limited sequence conservation (Schirawski et al , 2010; Kemen et al , 2011; Sharma et al , 2014), but some are conserved in genomes of related pathogens (Sharma et al 2014, 2015; Quinn et al 2013; Hemetsberger et al 2015; Lanver et al (2017). Previous definitions of putative effector proteins were often associated with several restrictions, such as size cutoff (e.g.…”

Section: Introductionmentioning

confidence: 99%

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Pseudozyma saprotrophic yeasts have retained a large effector arsenal, including functional Pep1 orthologs

Sharma

Ökmen

Doehlemann

et al. 2018

Preprint

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SummaryThe basidiomycete smut fungi are predominantly plant parasitic, causing severe losses in some crops. Most species feature a saprotrophic haploid yeast stage, and several smut fungi are only known from this stage, with some isolated from habitats without suitable hosts, e.g. from Antarctica. Thus, these species are generally believed to be apathogenic, but recent findings that some of these might have a plant pathogenic sexual counterpart, casts doubts on the validity of this hypothesis. Here, four Pseudozyma genomes were re-annotated and compared to published smut pathogens and the well-characterised effector gene Pep1 from these species was checked for its ability to complement a Pep1 deletion strain of Ustilago maydis. It was found that 113 high-confidence putative effector proteins were conserved among smut and Pseudozyma genomes. Among these were several validated effector proteins, including Pep1. By genetic complementation we show that Pep1 homologs from the supposedly apathogenic yeasts restore virulence in Pep1-deficient mutants Ustilago maydis. Thus, it is concluded that Pseudozyma species have retained a suite of effectors. This hints at the possibility that Pseudozyma species have kept an unknown plant pathogenic stage for sexual recombination or that these effectors have positive effects when colonising plant surfaces.

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“…Furthermore, pit1 and pit2 are divergently 692 2 8 transcribed, which makes it likely that the expression of pit1 and pit2 is co-regulated. In 693 addition, this gene arrangement of pit1 and pit2 is conserved in U. hordei, U. maydis, S. 694 scitamineum and S. reilianum (Sharma et al 2015). This finding has led to the speculation 695 that Pit1 and Pit2 somehow act together to govern virulence of U. maydis and related smut 696 fungi.…”

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confidence: 99%

Positively selected effector genes and their contribution to virulence in the smut fungusSporisorium reilianum

Schweizer

Münch

Mannhaupt

et al. 2017

Preprint

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47Plants and fungi display a broad range of interactions in natural and agricultural ecosystems 48 ranging from symbiosis to parasitism. These ecological interactions result in coevolution 49 between genes belonging to different partners. A well-understood example are secreted fungal 50 effector proteins and their host targets, which play an important role in pathogenic 51 interactions. Biotrophic smut fungi (Basidiomycota) are well-suited to investigate the 52 evolution of plant pathogens, because several reference genomes and genetic tools are 53 available for these species. Here, we used the genomes of Sporisorium reilianum f. sp. zeae 54 and S. reilianum f. sp. reilianum, two closely related formae speciales infecting maize and 55 sorghum, respectively, together with the genomes of Ustilago hordei, Ustilago maydis and 56Sporisorium scitamineum to identify and characterize genes displaying signatures of positive 57 selection. We identified 154 gene families having undergone positive selection during species 58 divergence in at least one lineage, among which 77% were identified in the two investigated 59 formae speciales of S. reilianum. Remarkably, only 29% of positively selected genes encode 60 predicted secreted proteins. We assessed the contribution to virulence of nine of these 61 candidate effector genes in S. reilianum f. sp. zeae by deleting individual genes, including a 62 homologue of the effector gene pit2 previously characterized in U. maydis. Only the pit2 63 deletion mutant was found to be strongly reduced in virulence. Additional experiments are 64 required to understand the molecular mechanisms underlying the selection forces acting on 65 the other candidate effector genes, as well as the large fraction of positively selected genes 66 encoding predicted cytoplasmic proteins. 67 68

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Comparative Genomics Including the Early-Diverging Smut FungusCeraceosorus bombacisReveals Signatures of Parallel Evolution within Plant and Animal Pathogens of Fungi and Oomycetes

Cited by 20 publications

References 106 publications

Smut infection of perennial hosts: the genome and the transcriptome of the Brassicaceae smut fungus Thecaphora thlaspeos reveal functionally conserved and novel effectors

Smut infection of perennial hosts: the genome and the transcriptome of the Brassicaceae smut fungus Thecaphora thlaspeos reveal functionally conserved and novel effectors

Pseudozyma saprotrophic yeasts have retained a large effector arsenal, including functional Pep1 orthologs

Positively selected effector genes and their contribution to virulence in the smut fungusSporisorium reilianum

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