Genome‐wide alternative splicing profiling in the fungal plant pathogen <i>Sclerotinia sclerotiorum</i> during the colonization of diverse host families

Ibrahim, Heba M. M.; Kusch, Stefan; Didelon, Marie; Raffaele, Sylvain

doi:10.1111/mpp.13006

Cited by 24 publications

(18 citation statements)

References 80 publications

(126 reference statements)

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“…In muscle, brain, and gut, we also found several ASGs whose function may be involved in the cellular response to stresses (e.g., oxidative stress and DNA damage). Thus, our study supports that AS can act as an efficient mechanism in responding to environmental or cellular stresses, which has been extensively implicated in both animals and plants (Grantham & Brisson, 2018 ; Ibrahim et al., 2021 ; Kijewska et al., 2018 ). More importantly, our current study further indicates that AS may play a more important role than gene expression regulation in coping with the severe cellular stress in nature (see also Singh et al., 2017 ; Jacobs & Elmer, 2021 ; Martín et al., 2021 ).…”

Section: Discussionsupporting

confidence: 85%

“…Mitochondrial dysfunction usually results in a decreased rate of ATP production and thus an increased rate of ROS generation, which will cause severe cellular stress (Ballard & Towarnicki, 2020 ; Ellison & Burton, 2006 ). Gene expression changes and alternative splicing (AS), acting as important transcriptional regulations, have been shown to play essential roles for cells and organisms in responding to environmental or cellular stresses efficiently (Ibrahim et al., 2021 ; Lee et al., 2021 ).…”

Section: Discussionmentioning

confidence: 99%

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Extensive alternative splicing triggered by mitonuclear mismatch in naturally introgressed Rhinolophus bats

Chen

Mao

2021

Ecology and Evolution

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Mitochondrial function needs strong interactions of mitochondrial and nuclear (mitonuclear) genomes, which can be disrupted by mitonuclear mismatch due to mitochondrial DNA (mtDNA) introgression between two formerly isolated populations or taxa. This mitonuclear disruption may cause severe cellular stress in mismatched individuals. Gene expression changes and alternative splicing (AS) are two important transcriptional regulations to respond to environmental or cellular stresses. We previously identified a naturally introgressed population in the intermediate horseshoe bat (Rhinolophus affinis). Individuals from this population belong to R. a. himalayanus and share almost identical nuclear genetic background; however, some of them had mtDNA from another subspecies (R. a. macrurus). With this unique natural system, we examined gene expression changes in six tissues between five mitonuclear mismatched and five matched individuals. A small number of differentially expressed genes (DEGs) were identified, and functional enrichment analysis revealed that most DEGs were related to immune response although some may be involved in response to oxidative stress. In contrast, we identified extensive AS events and alternatively spliced genes (ASGs) between mismatched and matched individuals. Functional enrichment analysis revealed that multiple ASGs were directly or indirectly associated with energy production in mitochondria which is vital for survival of organism. To our knowledge, this is the first study to examine the role of AS in responding to cellular stress caused by mitonuclear mismatch in natural populations. Our results suggest that AS may play a more important role than gene expression regulation in responding to severe environmental or cellular stresses.

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Section: Discussionsupporting

confidence: 85%

Section: Discussionmentioning

confidence: 99%

Extensive alternative splicing triggered by mitonuclear mismatch in naturally introgressed Rhinolophus bats

Chen

Mao

2021

Ecology and Evolution

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“…Isoforms merely expressed in planta by host-specific AS were identified in this phytopathogen. Thereby, colonization of diverse host families led to the accumulation of different transcripts and, consequently, altered protein domain structures, suggesting alternative functions of the isoforms during plant infection [ 29 ].…”

Section: Discussionmentioning

confidence: 99%

Evidence of a New MoYpd1p Phosphotransferase Isoform in the Multistep Phosphorelay System of Magnaporthe oryzae

Bühring

Yemelin

Michna

et al. 2021

JoF

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Different external stimuli are perceived by multiple sensor histidine kinases and transmitted by phosphorylation via the phosphotransfer protein Ypd1p in the multistep phosphorelay system of the high osmolarity glycerol signaling pathway of filamentous fungi. How the signal propagation takes place is still not known in detail since multiple sensor histidine kinase genes in most filamentous fungi are coded in the genome, whereas only one gene for Ypd1p exists. That raises the hypothesis that various Ypd1p isoforms are produced from a single gene sequence, perhaps by alternative splicing, facilitating a higher variability in signal transduction. We found that the mRNA of MoYPD1 in the rice blast fungus Magnaporthe oryzae is subjected to an increased structural variation and amplified putative isoforms on a cDNA level. We then generated mutant strains overexpressing these isoforms, purified the products, and present here one previously unknown MoYpd1p isoform on a proteome level. Alternative splicing was found to be a valid molecular mechanism to increase the signal diversity in eukaryotic multistep phosphorelay systems.

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“…By contrast, a study of a few effector candidate genes suggested the existence of plant host-specific expression patterns (Guyon et al, 2014) and various small RNAs are differentially expressed on A. thaliana and common bean (Phaseolus vulgaris) (Derbyshire et al, 2019b). Furthermore, various isoforms originating from host-specific alternative splicing add additional plasticity to the transcriptomic profile of S. sclerotiorum (Ibrahim et al, 2020) and suggest polyspecialist adaptations in this species. Nevertheless, the extent to which the S. sclerotiorum genome harbors signatures of adaptation to a polyspecialist lifestyle has not been fully elucidated.…”

Section: Introductionmentioning

confidence: 99%

“…To test whether S. sclerotiorum activates distinct gene sets for the infection of diverse host species, we took advantage of transcriptomic expression data obtained from in vitro cultures of S. sclerotiorum and during infection of plants covering major botanical families in the Pentapetalae (Ibrahim et al, 2020; Peyraud et al, 2019; Sucher et al, 2020). We reveal a flexible, host-specific transcriptional program driven by core and host-response co-expression (SPREx) clusters.…”

Section: Introductionmentioning

confidence: 99%

Transcriptional response to host chemical cues underpins expansion of host range in a fungal plant pathogen lineage

Kusch

Larrouy

Ibrahim

et al. 2020

Preprint

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The host range of parasites is an important factor in assessing the dynamics of disease epidemics. The evolution of pathogens to accommodate new hosts may lead to host range expansion, a process the molecular bases of which are largely enigmatic. The fungus Sclerotinia sclerotiorum parasitizes more than 400 plant species from diverse eudicot families while its close relative, S. trifoliorum, is restricted to plants from the Fabaceae family. We analyzed S. sclerotiorum global transcriptome reprogramming on hosts from six botanical families and reveal a flexible, host-specific transcriptional program driven by core and host-response co-expression (SPREx) gene clusters. We generated a chromosome-level genome assembly for S. trifoliorum and found near-complete gene space conservation in broad and narrow host range Sclerotinia species. However, S. trifoliorum showed increased sensitivity to the Brassicaceae defense compound camalexin. Inter-specific transcriptome analyses revealed a lack of transcriptional response to camalexin in S. trifoliorum and provide evidence that cis-regulatory variation associates with the genetic accommodation of Brassicaceae in the Sclerotinia host range. Our work demonstrates adaptive plasticity of a broad host range pathogen with specific responses to different host plants and demonstrates the co-existence of signatures for generalist and polyspecialist life styles in the genome of a plant pathogen. We reason that this mechanism enables the emergence of new disease with no or limited gene flow between strains and species, and could underlie the emergence of new epidemics originating from wild plants in agricultural settings.

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Genome‐wide alternative splicing profiling in the fungal plant pathogen Sclerotinia sclerotiorum during the colonization of diverse host families

Cited by 24 publications

References 80 publications

Extensive alternative splicing triggered by mitonuclear mismatch in naturally introgressed Rhinolophus bats

Extensive alternative splicing triggered by mitonuclear mismatch in naturally introgressed Rhinolophus bats

Evidence of a New MoYpd1p Phosphotransferase Isoform in the Multistep Phosphorelay System of Magnaporthe oryzae

Transcriptional response to host chemical cues underpins expansion of host range in a fungal plant pathogen lineage

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