Significant genetic and phenotypic changes arising from clonal growth of a single spore of an arbuscular mycorrhizal fungus over multiple generations

Abstract

Summary Arbuscular mycorrhizal fungi (AMF) are highly successful plant symbionts. They reproduce clonally producing multinucleate spores. It has been suggested that some AMF harbor genetically different nuclei. However, recent advances in sequencing the Glomus irregulare genome have indicated very low within‐fungus polymorphism. We tested the null hypothesis that, with no genetic differences among nuclei, no significant genetic or phenotypic variation would occur among clonal single spore lines generated from one initial AMF spore. Furthermore, no additional variation would be expected in the following generations of single spore lines. Genetic diversity contained in one initial spore repeatedly gave rise to genetically different variants of the fungus with novel phenotypes. The genetic changes represented quantitative changes in allele frequencies, most probably as a result of changes in the frequency of genetic variation partitioned on different nuclei. The genetic and phenotypic variation is remarkable, given that it arose repeatedly from one clonal individual. Our results highlight the dynamic nature of AMF genetics. Even though within‐fungus genetic variation is low, some is probably partitioned among nuclei and potentially causes changes in the phenotype. Our results are important for understanding AMF genetics, as well as for researchers and biotechnologists hoping to use AMF genetic diversity for the improvement of AMF inoculum.

Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis

“…Another study failed to find evidence for heterokaryosis, however, and the authors suggested that the genetic variation that they observed potentially could be due to polyploidy, although no studies of ploidy were conducted (14). A recent study of Rhizophagus irregularis (but not isolate DAOM-197198) provided further evidence in favor of heterokaryosis (15), so this remains an open question. Another hypothesis, specific for multicopy ribosomal DNA, is that variation among copies could exist within nuclei of a homokaryotic AM fungus and this is supported by some studies (14,16).…”

Rapid genotypic change and plasticity in arbuscular mycorrhizal fungi is caused by a host shift and enhanced by segregation

“…Rapid genotypic and phenotypic change in mycorrhizal fungi C Angelard et al frequency (Angelard et al, 2010;Ehinger et al, 2012).…”

“…We carried out quantitative analyses on the frequency of alleles at the Bg112 locus in the AMF lines on different hosts as they signify potential changes in relative nucleotype frequency (Angelard et al, 2010;Ehinger et al, 2012). Four alleles of the Bg112 locus co-occur in each AMF line and can be distinguished by length and sequence polymorphism (Angelard et al, 2010).…”

“…It could also allow the fungus to be genotypically different in different parts of the same network. AMF also exhibit partial segregation, producing new vegetative spores with different nucleotype frequencies (Angelard et al, 2010;Ehinger et al, 2012). Thus, an AMF also has a way to produce genotypically different offspring even though they grow vegetatively.…”

Inclusive fitness in agriculture

“…While the level of genetic difference among nuclei is still a topic of heated debate [81,82], it is well established that a single AM fungal spore can contain hundreds of nuclei [83 -85]. From this individual spore, an array of genetically different progeny-displaying different phenotypes-can potentially arise [86]. While the exact mechanism is not well understood, the fungal phenotype is thought to be a reflection of the frequency of different nucleotypes within the individual fungus [87,88].…”