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

Abstract

Arbuscular mycorrhizal fungi (AMF) are among the most abundant symbionts of plants, improving plant productivity and diversity. They are thought to mostly grow vegetatively, a trait assumed to limit adaptability. However, AMF can also harbor genetically different nuclei (nucleotypes). It has been shown that one AMF can produce genotypically novel offspring with proportions of different nucleotypes. We hypothesized that (1) AMF respond rapidly to a change of environment (plant host) through changes in the frequency of nucleotypes; (2) genotypically novel offspring exhibit different genetic responses to environmental change than the parent; and (3) genotypically novel offspring exhibit a wide range of phenotypic plasticity to a change of environment. We subjected AMF parents and offspring to a host shift. We observed rapid and large genotypic changes in all AMF lines that were not random. Genotypic and phenotypic responses were different among offspring and their parents. Even though growing vegetatively, AMF offspring display a broad range of genotypic and phenotypic changes in response to host shift. We conclude that AMF have the ability to rapidly produce variable progeny, increasing their probability to produce offspring with different fitness than their parents and, consequently, their potential adaptability to new environmental conditions. Such genotypic and phenotypic flexibility could be a fast alternative to sexual reproduction and is likely to be a key to the ecological success of AMF.

Figure 1

Conceptual design of the experiment. Segregated lines were started from the isolation and culture of single spores from a given initial line. Each initial and segregated line was then replicated and cultivated under identical conditions with roots of D. carota for 13 months, including three subculturing events (see Materials and Methods). Initial and segregated lines were further maintained on D. carota and also transferred to a new plant host (S. tuberosum). The AMF lines were then cultured for 19 months (including three more subculturing events) on one or the other plant host and the AMF phenotypes and genotypes were measured.

Figure 2

Relative frequency of four Bg112 alleles was altered by a host shift. Change in the relative frequency of Bg112 alleles following a host shift. Positive values represent an increase in frequency of an allele due to a shift from D. carota to S. tuberosum and negative values represent a decrease in the frequency of a given allele due to a shift from D. carota to S. tuberosum. (a) Change in frequency of alleles measured on three initial lines and their segregated lines. (b) Change in frequency of alleles for line S4 and its segregated lines as measured by 454 pyrosequencing. See Table 4 for associated multivariate analysis of variance (MANOVA) statistics.

Figure 3

Host shift altered phenotypes of the AMF lines. Spore of initial and segregated lines growing on two hosts D. carota and S. tuberosum. (a) Line S3 and its segregated lines. (b) Line S4 and its segregated lines. (c) Line Sc1 and its segregated lines. (d) Line Sc2 and its segregated lines. Black bars: initial lines. White bars: segregated lines. See Table 5 for statistical analyses.