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Modeling in yeast how rDNA introns slow growth and increase desiccation tolerance in lichens.

Authors
  • Armaleo, Daniele1
  • Chiou, Lilly1, 2
  • 1 Department of Biology, Duke University, Durham, NC 27708, USA.
  • 2 Curriculum in Genetics and Molecular Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.
Type
Published Article
Journal
G3 Genes|Genome|Genetics
Publisher
The Genetics Society of America
Publication Date
Oct 19, 2021
Volume
11
Issue
11
Identifiers
DOI: 10.1093/g3journal/jkab279
PMID: 34849787
Source
Medline
Keywords
Language
English
License
Unknown

Abstract

We connect ribosome biogenesis to desiccation tolerance in lichens, widespread symbioses between specialized fungi (mycobionts) and unicellular phototrophs. We test whether the introns present in the nuclear ribosomal DNA of lichen mycobionts contribute to their anhydrobiosis. Self-splicing introns are found in the rDNA of several eukaryotic microorganisms, but most introns populating lichen rDNA are unable to self-splice, being either catalytically impaired group I introns, or spliceosomal introns ectopically present in rDNA. Although the mycobiont's splicing machinery removes all introns from rRNA, Northern analysis indicates delayed post-transcriptional removal during rRNA processing, suggesting interference with ribosome assembly. To study the effects of lichen introns in a model system, we used CRISPR to introduce a spliceosomal rDNA intron from the lichen fungus Cladonia grayi into all nuclear rDNA copies of Saccharomyces cerevisiae, which lacks rDNA introns. Three intron-bearing yeast mutants were constructed with the intron inserted either in the 18S rRNA genes, the 25S rRNA genes, or in both. The mutants removed the introns correctly but had half the rDNA genes of the wildtype, grew 4.4-6 times slower, and were 40-1700 times more desiccation tolerant depending on intron position and number. Intracellular trehalose, a disaccharide implicated in desiccation tolerance, was detected at low concentration. Our data suggest that the interference of the splicing machinery with ribosome assembly leads to fewer ribosomes and proteins and to slow growth and increased desiccation tolerance in the yeast mutants. The relevance of these findings for slow growth and desiccation tolerance in lichens is discussed. © The Author(s) 2021. Published by Oxford University Press on behalf of Genetics Society of America.

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