Organization of genetic variation in individuals of arbuscular mycorrhizal fungi

Abstract

Arbuscular mycorrhizal (AM) fungi (Glomeromycota) are thought to be the oldest group of asexual multicellular organisms. They colonize the roots of most land plants, where they facilitate mineral uptake from the soil in exchange for plant-assimilated carbon1. Cells of AM fungi contain hundreds of nuclei. Unusual polymorphism of ribosomal DNA observed in individual spores of AM fungi inspired a hypothesis that heterokaryosis—that is, the coexistence of many dissimilar nuclei in cells—occurs throughout the AM fungal life history2,3. Here we report a genetic approach to test the hypothesis of heterokaryosis in AM fungi. Our study of the transmission of polymorphic genetic markers in natural isolates of Glomus etunicatum, coupled with direct amplification of rDNA from microdissected nuclei by polymerase chain reaction, supports the alternative hypothesis of homokaryosis, in which nuclei populating AM fungal individuals are genetically uniform. Intrasporal rDNA polymorphism contained in each nucleus signals a relaxation of concerted evolution4, a recombination-driven process that is responsible for homogenizing rDNA repeats5. Polyploid organization of glomeromycotan genomes could accommodate intranuclear rDNA polymorphism and buffer these apparently asexual organisms against the effects of accumulating mutations.

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Figure 1: Sorting of variants of a polymorphic marker in single-spore cultures of Glomus.
Figure 2: PLS1 variation in G. etunicatum field isolates.
Figure 3: rDNA variation in G. etunicatum field isolates.
Figure 4: Distribution of rDNA variation among individual nuclei in two Glomus species.

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Acknowledgements

We thank W. Pawlowski for help with the spore nuclei count; P. Bethke for advice on nuclei microdissection; D. Baker, T. Galagher, B. King, T. Lee and T. Szaro for technical assistance; J. A. Fortin for G. intraradices; D. Douds for the DC1 isolate of Ri T-DNA-transformed carrot roots developed by G. Bécard; and D. J. Read, T. Bruns, A. Burt and the members of the Taylor laboratory for comments on the manuscript. This work was supported by the Torrey Mesa Research Institute-Syngenta Biotechnology and the National Research Initiative Competitive Grants Program (NRICGP) of the US Department of Agriculture.

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Correspondence to Teresa E. Pawlowska.

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Pawlowska, T., Taylor, J. Organization of genetic variation in individuals of arbuscular mycorrhizal fungi. Nature 427, 733–737 (2004). https://doi.org/10.1038/nature02290

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