UV radiation boosts ribosome production in Fusarium mangiferae filaments

When ultraviolet light strikes a growing fungal filament, the expected response is shutdown: DNA damage halts growth, and ribosome biogenesis, one of the most energy-demanding processes in any cell, is dialed down. A new study of the mango malformation pathogen Fusarium mangiferae reports the opposite. Researchers at the Hebrew University of Jerusalem found that when filaments of this fungus were irradiated with ultraviolet C radiation, ribosome levels rose and translation capacity increased significantly. The induction appeared after the fungus had formed multicellular filaments, not during spore germination, and blocking it modestly but measurably reduced both ultraviolet survival and the repair of ultraviolet-induced DNA lesions. The authors propose that this response represents a previously unrecognized strategy for coping with DNA damage, one aimed primarily at protecting gene expression itself from the disruptive effects of ultraviolet radiation on transcription.

Ultraviolet light is a central determinant in the ecology and physiology of microbes, and DNA is among its most vulnerable targets. The most common ultraviolet lesions are cyclobutane pyrimidine dimers and 6-4 photoproducts, both of which severely distort the DNA helix. These distortions interrupt DNA replication, stalling replication forks and ultimately causing cell death. Ultraviolet exposure is also mutagenic, producing point mutations, most commonly C-to-T transitions, and it inhibits transcription by stalling RNA polymerases on damaged templates. Because mutants in DNA repair are extremely sensitive to ultraviolet light, cells across the tree of life have evolved layered mechanisms to remove these lesions, from photolyases that directly reverse damage to nucleotide excision repair pathways that scan the genome for helix distortions using proteins such as Ddb1 and Xpc.

The bacterial SOS response has long served as the model of the cellular reaction to ultraviolet damage. During SOS activation, DNA repair, recombination, and damage tolerance genes are induced at the mRNA level, some of them up to 100-fold. A comparable, comprehensive induction of DNA repair genes has never been demonstrated in fungi, although individual repair genes are ultraviolet-induced in yeasts and Neurospora crassa. The new work began from an unexpected observation in a prior transcriptomic analysis: when Fusarium mangiferae and Fusarium oxysporum were irradiated at 14 hours post-inoculation, a stage at which filaments are established with ten or more nuclei, genes related to translation were strongly induced rather than repressed. At 8 hours post-inoculation, when germination involves only one or two nuclei, the same genes were downregulated, as expected for DNA damage.

The surprise is contextual. In fast-growing yeast cells, up to 60 percent of genes participate in ribosome biogenesis, a resource-intensive enterprise that is reliably curtailed during growth arrest. Translation is reduced in response to ultraviolet and oxidative stress, and DNA damage triggers dissociation of RNA polymerase I from yeast ribosomal genes. In humans, DNA repair proteins such as the Ape1 endonuclease and the Werner syndrome helicase normally localize to the nucleolus, where they are thought to support ribosome biogenesis, and they dissociate once the DNA damage response is triggered. Against this backdrop, ultraviolet-induced ribosome buildup in a filamentous fungus inverts a pattern documented in bacteria, yeast, and human cells alike.

To investigate, the team cultured microconidia of F. mangiferae strain MRC7560 and irradiated germlings and filaments at 8 and 14 hours post-inoculation with ultraviolet C doses ranging from 30 to 200 joules per square meter at 254 nanometers, with fluence verified by radiometry. Reanalysis of RNA sequencing data from filaments irradiated at 14 hours post-inoculation, grouped across recovery times of zero, 30, and 60 minutes, confirmed that translation and ribosome biogenesis ranked among the most significantly induced biological modules. Pyrimidine biosynthesis and mitochondrion-related processes were upregulated at the highest dose, while protein degradation modules were downregulated. The authors note that this combination suggests ribonucleoside triphosphates are being consumed for substantial ribosome assembly. Growth delay was verified: irradiated filaments showed no significant change in nuclear number during the first four hours after exposure, confirming that the induction was not simply a byproduct of unchecked proliferation.

The team then measured ribosomes directly. Filaments were irradiated and harvested two hours later, and ribosomal fractions were enriched by ultracentrifugation through a 35 percent sucrose cushion. Although equal amounts of RNA were loaded, the pellet concentration after recovery from 200 joules per square meter was 1.3-fold higher than in unirradiated controls, with a stable ratio across experiments. When dissolved pellets were separated on 10 to 50 percent sucrose gradients, the absorbance peak of irradiated samples was higher, wider, and shifted toward the denser bottom fractions. The area under the curve for irradiated versus unirradiated samples was 1.28 plus or minus 0.19 across four independent experiments. Agarose gel analysis of gradient fractions confirmed increased ribosomal RNA band intensity after irradiation, even at a low dose of 50 joules per square meter, with stronger signals in the bottom fractions indicating more polysomes, although the authors caution that their setup could not determine whether the polysomal fraction specifically increased.

To test translation capacity directly, the researchers used PUNCH-P, a protocol in which isolated ribosomes are incubated with biotinylated puromycin so that nascent polypeptide chains can be detected with streptavidin-linked peroxidase. The puromycin-peptide signal rose after irradiation in F. mangiferae, and the same procedures applied to F. oxysporum revealed higher RNA concentrations across gradients, stronger ribosomal band intensities, and greater translation capacity, albeit attenuated relative to F. mangiferae. Ultraviolet induction of rRNA transcription was probed with actinomycin D, an inhibitor of RNA polymerase I. Pretreatment with 500 nanomolar actinomycin D completely suppressed ultraviolet-induced ribosome biosynthesis, and ultraviolet-induced translation was significantly delayed, though it eventually occurred to a much lesser extent. By contrast, Rbin2, an inhibitor of ribosome maturation, suppressed ultraviolet-induced translation capacity with no recovery. The comparison between the two inhibitors suggests that ultraviolet also induces ribosome maturation, which explains why minimal induced translation persists even when new rRNA synthesis is blocked.

Functional relevance followed from perturbation experiments. In liquid holding assays, in which irradiated cells are suspended in water for 24 hours before plating, actinomycin D increased fungal sensitivity to 50 joules per square meter across all developmental stages, most strongly at the filament stage. Cycloheximide, a protein synthesis inhibitor, similarly reduced viability when combined with irradiation, with the strongest decrease, about 30 percent, in irradiated 14-hour filaments. Repair was also impaired: an immunodot blot assay using anti-CPD antibodies showed that without actinomycin D only 10 percent of the ultraviolet lesion signal remained after 24 hours, whereas 40 percent remained with the inhibitor. The authors emphasize that the effect, while significant, is modest compared with the severe shutdown seen when the bacterial SOS response is abolished, and they acknowledge that actinomycin D may also inhibit mRNA transcription at some level. Ribosome profiling by RNA sequencing of total RNA and heavy and light gradient fractions showed that ultraviolet-irradiated fungi had more than triple the number of distinct mRNA species associated with ribosomes from the bottom of the gradient, 430 versus 130. The largest group of these mRNAs encodes gene expression machinery, including transcription, splicing, polyadenylation, ribosome biogenesis, and protein folding, with modules for metabolism, secretion, and DNA repair also represented. Among repair-associated transcripts were Ddb1, homologous recombination genes such as rad55 and mus81, DNA synthesis genes including polymerase delta components and mcm3, translesion polymerases zeta and kappa, and cell cycle genes such as cdc6 and aurora kinase. Notably, 165 of the 430 ribosome-associated genes had been induced by ultraviolet within the first hour, indicating that early transcripts were undergoing translation two hours later.

Mechanistically, the target of rapamycin pathway proved necessary for the immediate induction. Pretreatment with rapamycin completely changed the ultraviolet effect on gene expression, with very little overlap between genes induced with and without the drug, and the ultraviolet induction of ribosome biogenesis genes was abolished under rapamycin exposure. Yet ultraviolet still induced roughly 1,000 genes under rapamycin, dominated by carbon and amino acid metabolic modules, and, intriguingly, when gene expression was compared directly under rapamycin with or without ultraviolet, ribosome biogenesis and translation genes were induced even with TOR repressed. Ultraviolet exposure also rescued rapamycin toxicity across all developmental stages, especially at the germling stage, while rapamycin did not reduce ultraviolet survival at the filament stage. The authors interpret this as evidence that ultraviolet induces mechanisms operating upstream of, or in parallel with, TOR, possibly involving PKA signaling whose balance with TOR shifts during fungal development. They hypothesize that ultraviolet-induced translation capacity compensates for the negative effect of ultraviolet on transcription, and that transcription-coupled repair may be less efficient in Fusarium species than in other organisms, making transcription machinery induction a compensatory response. Because commitment to ribosome biogenesis is energetically costly and may increase fungal vulnerability to stress, the authors suggest that exploiting this response could open new avenues for fighting Fusarium pathogens, though whether other stresses or other filamentous fungi share the response remains to be determined.

Subject of Research: UV-induced ribosome biogenesis and translation in Fusarium mangiferae

Article Title: UV-induced translation capacity in Fusarium mangiferae

Article References: Hoang, Q., Milo, S., Mukherjee, D., & Covo, S. (2026). UV-induced translation capacity in Fusarium mangiferae. Frontiers in Fungal Biology, 7, Article 1965588. https://doi.org/10.3389/ffunb.2026.1965588

Image Credits: AI Generated

DOI: 10.3389/ffunb.2026.1965588

Keywords: Fusarium mangiferae, UV radiation, DNA damage response, ribosome biogenesis, translation, TOR signaling, DNA repair, filamentous fungi, PUNCH-P, transcription-coupled repair, plant pathogen, rapamycin