Transposable elements contribute to fungal genes and impact fungal lifestyle

Abstract

The last decade brought a still growing experimental evidence of mobilome impact on host’s gene expression. We systematically analysed genomic location of transposable elements (TEs) in 625 publicly available fungal genomes from the NCBI database in order to explore their potential roles in genome evolution and correlation with species’ lifestyle. We found that non-autonomous TEs and remnant copies are evenly distributed across genomes. In consequence, they also massively overlap with regions annotated as genes, which suggests a great contribution of TE-derived sequences to host’s coding genome. Younger and potentially active TEs cluster with one another away from genic regions. This non-randomness is a sign of either selection against insertion of TEs in gene proximity or target site preference among some types of TEs. Proteins encoded by genes with old transposable elements insertions have significantly less repeat and protein-protein interaction motifs but are richer in enzymatic domains. However, genes only proximal to TEs do not display any functional enrichment. Our findings show that adaptive cases of TE insertion remain a marginal phenomenon, and the overwhelming majority of TEs are evolving neutrally. Eventually, animal-related and pathogenic fungi have more TEs inserted into genes than fungi with other lifestyles. This is the first systematic, kingdom-wide study concerning mobile elements and their genomic neighbourhood. The obtained results should inspire further research concerning the roles TEs played in evolution and how they shape the life we know today.

Tracking of Diversity and Evolution in the Brown Rot Fungi Monilinia fructicola, Monilinia fructigena, and Monilinia laxa

“…TEs with structural features of functional domains that are necessary for autonomous transposition ( Havecker et al, 2004 ; Casacuberta and González, 2013 ; Castanera et al, 2016 ) were detected only in M. fructigena. A similar result was observed in S. sclerotiorum , and to a much lesser extent, in B. cinerea , which suggests the presence of active TEs also in these genomes, in agreement with previous reports ( Santana et al, 2014 ; Muszewska et al, 2019 ).…”

Tracking of Diversity and Evolution in the Brown Rot Fungi Monilinia fructicola, Monilinia fructigena, and Monilinia laxa

“…TEs with structural features of functional domains that are necessary for autonomous transposition ( Havecker et al, 2004 ; Casacuberta and González, 2013 ; Castanera et al, 2016 ) were detected only in M. fructigena. A similar result was observed in S. sclerotiorum , and to a much lesser extent, in B. cinerea , which suggests the presence of active TEs also in these genomes, in agreement with previous reports ( Santana et al, 2014 ; Muszewska et al, 2019 ).…”

Analyses of transposable elements in arbuscular mycorrhizal fungi support evolutionary parallels with filamentous plant pathogens

“…In most species, effectors exhibit a right-skewed TE frequency distribution, supporting genome compartmentalization where dynamic, TE-dense regions harbor SPs and effector genes. This pattern aligns with the “two-speed genome” model observed in plant pathogens [35,37,38,40], and the A/B genome compartments reported in the model AMF R. irregularis [12,23,26].…”

Cryptic genetic structure and copy-number variation in the ubiquitous forest symbiotic fungus Cenococcum geophilum

“…With about 75% of its genome comprising TEs, C. geophilum exhibits the highest proportion of transposons and retrotransposons found in ECM fungi (18–75%; Miyauchi et al ., 2020) and other Dothideomycetes (1–75%; Peter et al ., 2016). Our findings corroborate the recent proliferation of species-specific TEs and its evolutionary significance in affecting functional rearrangements of the genome (Daboussi and Capy, 2003; Muszewska et al ., 2019). However, other mechanisms such as aneuploidy, chromosomal duplication, unequal crossing over may also be responsible for these gene duplications (Bourne et al ., 2014).…”

Tracking of Diversity and Evolution in the Brown Rot Fungi Monilinia fructicola, Monilinia fructigena, and Monilinia laxa

“…TEs with structural features of functional domains that are necessary for autonomous transposition ( Havecker et al, 2004 ; Casacuberta and González, 2013 ; Castanera et al, 2016 ) were detected only in M. fructigena. A similar result was observed in S. sclerotiorum , and to a much lesser extent, in B. cinerea , which suggests the presence of active TEs also in these genomes, in agreement with previous reports ( Santana et al, 2014 ; Muszewska et al, 2019 ).…”

Analyses of transposable elements in arbuscular mycorrhizal fungi support evolutionary parallels with filamentous plant pathogens

“…In most species, effectors exhibit a right-skewed TE frequency distribution, supporting genome compartmentalization where dynamic, TE-dense regions harbor SPs and effector genes. This pattern aligns with the “two-speed genome” model observed in plant pathogens [35,37,38,40], and the A/B genome compartments reported in the model AMF R. irregularis [12,23,26].…”

Cryptic genetic structure and copy-number variation in the ubiquitous forest symbiotic fungus Cenococcum geophilum

“…With about 75% of its genome comprising TEs, C. geophilum exhibits the highest proportion of transposons and retrotransposons found in ECM fungi (18–75%; Miyauchi et al ., 2020) and other Dothideomycetes (1–75%; Peter et al ., 2016). Our findings corroborate the recent proliferation of species-specific TEs and its evolutionary significance in affecting functional rearrangements of the genome (Daboussi and Capy, 2003; Muszewska et al ., 2019). However, other mechanisms such as aneuploidy, chromosomal duplication, unequal crossing over may also be responsible for these gene duplications (Bourne et al ., 2014).…”

Tracking of Diversity and Evolution in the Brown Rot Fungi Monilinia fructicola, Monilinia fructigena, and Monilinia laxa

“…TEs with structural features of functional domains that are necessary for autonomous transposition ( Havecker et al, 2004 ; Casacuberta and González, 2013 ; Castanera et al, 2016 ) were detected only in M. fructigena. A similar result was observed in S. sclerotiorum , and to a much lesser extent, in B. cinerea , which suggests the presence of active TEs also in these genomes, in agreement with previous reports ( Santana et al, 2014 ; Muszewska et al, 2019 ).…”

Analyses of transposable elements in arbuscular mycorrhizal fungi support evolutionary parallels with filamentous plant pathogens

“…In most species, effectors exhibit a right-skewed TE frequency distribution, supporting genome compartmentalization where dynamic, TE-dense regions harbor SPs and effector genes. This pattern aligns with the “two-speed genome” model observed in plant pathogens [35,37,38,40], and the A/B genome compartments reported in the model AMF R. irregularis [12,23,26].…”

Cryptic genetic structure and copy-number variation in the ubiquitous forest symbiotic fungus Cenococcum geophilum

“…With about 75% of its genome comprising TEs, C. geophilum exhibits the highest proportion of transposons and retrotransposons found in ECM fungi (18–75%; Miyauchi et al ., 2020) and other Dothideomycetes (1–75%; Peter et al ., 2016). Our findings corroborate the recent proliferation of species-specific TEs and its evolutionary significance in affecting functional rearrangements of the genome (Daboussi and Capy, 2003; Muszewska et al ., 2019). However, other mechanisms such as aneuploidy, chromosomal duplication, unequal crossing over may also be responsible for these gene duplications (Bourne et al ., 2014).…”