Genetic exchange in an arbuscular mycorrhizal fungus results in increased rice growth and altered mycorrhiza-specific gene transcription

Abstract

Arbuscular mycorrhizal fungi (AMF) are obligate symbionts with most terrestrial plants. They improve plant nutrition, particularly phosphate acquisition, and thus are able to improve plant growth. In exchange, the fungi obtain photosynthetically fixed carbon. AMF are coenocytic, meaning that many nuclei coexist in a common cytoplasm. Genetic exchange recently has been demonstrated in the AMF Glomus intraradices, allowing nuclei of different Glomus intraradices strains to mix. Such genetic exchange was shown previously to have negative effects on plant growth and to alter fungal colonization. However, no attempt was made to detect whether genetic exchange in AMF can alter plant gene expression and if this effect was time dependent. Here, we show that genetic exchange in AMF also can be beneficial for rice growth, and that symbiosis-specific gene transcription is altered by genetic exchange. Moreover, our results show that genetic exchange can change the dynamics of the colonization of the fungus in the plant. Our results demonstrate that the simple manipulation of the genetics of AMF can have important consequences for their symbiotic effects on plants such as rice, which is considered the most important crop in the world. Exploiting natural AMF genetic variation by generating novel AMF genotypes through genetic exchange is a potentially useful tool in the development of AMF inocula that are more beneficial for crop growth.

Fig. 1.

Plant shoot dry weight (g) of Oryza sativa at 6, 9, and 12 weeks following inoculation. Black bars represent the growth of plants inoculated with parental lines of AMF Glomus intraradices, white bars represent the growth of plants inoculated with crossed lines resulting from a cross between C3 and D1 lines, and hatched bars represent the growth of the uninoculated treatment. Errors bars indicate ± 1 SE. The following numbers of samples of each strain were taken at 6 weeks: NM, 12; C3, 8; D1, 11; Sb, 6; Sc2, 8; and Sd, 5. The following numbers of samples were taken at 9 weeks: NM, 12; C3: 11; D1, 12; Sb, 12; Sc2, 12; and Sd, 10. The following numbers of samples were taken at 12 weeks: NM, 12; C3, 7; D1, 9; Sb, 10; Sc2, 8; and Sd, 8.

Fig. 2.

Mycorrhizal fungal colonization (percent root length colonized) in the roots of O. sativa at 6, 9, and 12 weeks after inoculation. Black bars represent colonization by parental lines and white bars by crossed lines, originating from crosses between C3 and D1. Error bars indicate ± 1 standard error (SE). Bars topped by different letters within each harvest are significantly different at P ≤ 0.05. The following numbers of samples were taken at 6 weeks: NM, 12; C3, 8; D1, 11; Sb, 6; Sc2, 8; and Sd, 5. The following numbers of samples were taken at 9 weeks: NM, 12, C3, 11; D1, 12; Sb, 12; Sc2, 12; and Sd, 10. The following numbers of samples were taken at 12 weeks: NM, 12, C3, 7; D1, 9; Sb, 10; Sc2, 8; and Sd, 8.

Fig. 3.

Effect of genetic exchange in AMF on transcription of AM1 (a), AM3 (b), AM10 (c), and AM14 (d) genes in the roots of O. sativa. The relative transcription is measured as the relative fluorescence, where the fluorescence values have been standardized relative to the transcription of the housekeeping genes ubiquitin and cyclophilin. Black bars represent the relative transcription of genes when plants were inoculated with parental lines C3 and D1. White bars represent the relative transcription of genes when plants were inoculated with crossed lines Sb, Sc2, and Sd, originating from crosses between C3 and D1 lines. Error bars indicate ± 1 SE. Bars topped by different letters are significantly different at P ≤ 0.05. Plant root samples were pooled to obtain three replicates for each treatment (n = 3).