Combining Transcriptomics and Proteomics Reveals Potential Post-transcriptional Control of Gene Expression After Light Exposure in Metarhizium acridum

Abstract

Light is an important stimulus for fungi as it regulates many diverse and important biological processes. Metarhizium acridum is an entomopathogenic fungus currently used for the biological control of insect pests. The success of this approach is heavily dependent on tolerance to environmental stresses. It was previously reported that light exposure increases tolerance to ultraviolet radiation in M. acridum . There is no information in the literature about how light globally influences gene expression in this fungus. We employed a combination of mRNA-Sequencing and high-throughput proteomics to study how light regulates gene expression both transcriptionally and post-transcriptionally. Mycelium was exposed to light for 5 min and changes at the mRNA and protein levels were followed in time-course experiments for two and four hours, respectively. After light exposure, changes in mRNA abundance were observed for as much as 1128 genes or 11.3% of the genome. However, only 57 proteins changed in abundance and at least 347 significant changes at the mRNA level were not translated to the protein level. We observed that light downregulated subunits of the eukaryotic translation initiation factor 3, the eIF5A-activating enzyme deoxyhypusine hydroxylase, and ribosomal proteins. We hypothesize that light is perceived as a stress by the cell that responds to it by reducing translational activity. Overall, our results indicate that light acts both as a signal and a stressor to M. acridum and highlight the importance of measuring protein levels in order to fully understand light responses in fungi.

Molecular basis and regulatory mechanisms underlying fungal insecticides' resistance to solar ultraviolet irradiation

“…In these studies, conidia produced on scant media or under stressful conditions generally were more resistant to a UV irradiation than those produced on rich media or under normal culture conditions. In addition, fast‐growing M. acirdum hyphae became more tolerant to UVB after a short period of exposure to white or blue/UVA light because the light exposure induced the upregulation of a photolyase gene and transcriptional changes of many light‐responsive genes 62–64 . The UVB resistance of M. acridum and M. robertsii was enhanced in the conidia produced on a riboflavin‐inclusive medium relative to those produced on a riboflavin‐free medium 65 .…”

Human cellular homeostasis buffers trans-acting translational effects of heterologous gene expression with very different codon usage bias

“…Despite this technical gap, our results contribute to the growing evidence obtained by combining transcriptomics and proteomics (or Ribo-Seq) approaches, showing that proteomes tend to be more stable, and/or to display a larger inertia to change, than transcriptomes. Such a trend has been communicated for yeasts species ( McManus et al, 2014 ), for the molecular responses of other fungi either to stressors or environmental cues ( Blevins et al, 2019; Brancini et al, 2019 ), as well as across primates ( Khan et al, 2013 ). In this regard, it has been shown that human tissues involved in similar broad functions display similar proteomes, even if their transcriptomes are divergent ( Wang D et al, 2019 ) and that this trend is conserved across evolutionary timescales for mammals ( Wang ZY et al, 2020) .…”

Long-lasting effects of red and blue light exposure on the growth of soil fungi

“…The modulation of the UV stress response by a preliminary light exposure is a well known phenomenon, e.g. observed in Metarhizium acridum, and the respective molecular machinery of the signaling cascade leading to the upregulation of certain genes involved in the UV protection has been already described (Rangel et al 2015;Brancini et al 2016Brancini et al , 2018aBrancini et al , 2019Dias et al 2020). Experiments with testing different fungal species to UV stress may clarify this hypothesis.…”

“…Also, in a number of studies, photoinduced responses were measured after constant or protracted exposure of fungi to the light of various wavelengths. By contrast, much less data are available on the long lasting or delayed responses occurring after brief exposure, while such 'memory'-based effects in fungi has been known from classic studies (Zalokar 1955;Betina and Zajacova 1978;Schrott 1980) and confirmed in more recent experiments (Schmoll et al 2010;Brancini et al 2016Brancini et al , 2018aBrancini et al , 2019. And again, there is a gap in current knowledge regarding the species-related peculiarities of gross photoinduced reactions in such experimental conditions.…”