High-Level Molecular Diversity of Copper-Zinc Superoxide Dismutase Genes among and within Species of Arbuscular Mycorrhizal Fungi

Abstract

In the ecologically important arbuscular mycorrhizal fungi (AMF), Sod1 encodes a functional polypeptide that confers increased tolerance to oxidative stress and that is upregulated inside the roots during early steps of the symbiosis with host plants. It is still unclear whether its expression is directed at scavenging reactive oxygen species (ROS) produced by the host, if it plays a role in the fungus-host dialogue, or if it is a consequence of oxidative stress from the surrounding environment. All these possibilities are equally likely, and molecular variation at the Sod1 locus can possibly have adaptive implications for one or all of the three mentioned functions. In this paper, we analyzed the diversity of the Sod1 gene in six AMF species, as well as 14 Glomus intraradices isolates from a single natural population. By sequencing this locus, we identified a large amount of nucleotide and amino acid molecular diversity both among AMF species and individuals, suggesting a rapid divergence of its codons. The Sod1 gene was monomorphic within each isolate we analyzed, and quantitative PCR strongly suggest this locus is present as a single copy in G. intraradices. Maximum-likelihood analyses performed using a variety of models for codon evolution indicated that a number of amino acid sites most likely evolved under the regime of positive selection among AMF species. In addition, we found that some isolates of G. intraradices from a natural population harbor very divergent orthologous Sod1 sequences, and our analysis suggested that diversifying selection, rather than recombination, was responsible for the persistence of this molecular diversity within the AMF population.Positive Darwinian selection is a potential signature of genetic conflicts. This has been demonstrated in host-pathogen interactions using molecular evidence (3, 37) and is also supported by theoretical predictions (7,29,34,35). In sharp contrast, how genes evolve in a mutualistic environment remains largely unexplored. Strong selective constraints on genes that are specifically expressed during symbiotic stages are expected, and, indeed, slow rates of evolution have been predicted in conceptual models of mutualism because only weak selection pressures are expected in the host environment (8). Conversely, mutualism has been considered as a less harmonious interaction because the organisms involved have been predicted to evolve mechanisms to avoid overexploitation by their partners (20,24). Evolution of such mechanisms in the host could create selective pressures for change in the symbiont. In

Characterization of a CuZn superoxide dismutase gene in the arbuscular mycorrhizal fungus Glomus intraradices

“…Interestingly, some isolates of G. intraradices from a natural population were shown to harbor very divergent orthologous SOD1 sequences (Corradi et al 2009). It has been hypothesized that this high rates of protein evolution might be driven by evolutionary forces to facilitate interactions with the host plants at an organismic (colonization of root tissues) and/or ecosystem (widening the host range) level.…”

“…The predicted protein has 157 amino acid residues with a molecular mass of 16.3 kDa. The deduced amino acid sequence is closely related to fungal CuZnSOD homologs, showing the highest similarity to partial CuZnSOD gene sequences from different Glomus species (98-80% identity; Corradi et al 2009), 73% similarity to the G. margarita homolog (Lanfranco et al 2005) and approximately 70% similarity to sequences from ascomycotan CuZnSODs. An alignment of the GintSOD1 protein sequence with those from the AM fungus G. margarita, the ericoid mycorrhizal fungus Oidiodendrom maius and the ascomycetes Paecilomyces tenuipes, Claviceps purpurea, S. cerevisiae and Aspergillus niger revealed that it contains features characteristic of CuZnSOD proteins, such as the conserved histidine and aspartate residues essential for dismutation and metal binding (Fig.…”

Arbuscular mycorrhizal association enhances drought tolerance potential of promising bioenergy grass (Saccharum arundinaceum retz.)

“…In addition, most AMF species contained Sod1 genes that are upregulated inside roots and imparts drought tolerance to host plants (Corradi et al 2009). Higher activity of SOD suggests that AMF plants possessed more efficient superoxide dismutation in line with decreasing soil water content so that more effective detoxification of superoxide radicals into H 2 O 2 takes place (Zou et al 2015).…”

Arbuscular Mycorrhiza: The Challenge to Understand the Genetics of the Fungal Partner

“…However, one gene, the superoxide dismutase, Sod1, that is up-regulated in the fungus during the development of the symbiosis has been identified in AMF (56). Interestingly, this gene shows extremely high variability in AMF, even among isolates of G. intraradices from one field (17). What is even more striking about the variation is that it appears to be subject to diversifying selection where variants have high levels of substitutions leading to changes in the amino acid sequence of the protein.…”