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Genetic control of arbuscular mycorrhizal colonization by Rhizophagus intraradices in Helianthus annuus (L.)

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Abstract

Plant symbiosis with arbuscular mycorrhizal (AM) fungi provides many benefits, including increased nutrient uptake, drought tolerance, and belowground pathogen resistance. To develop a better understanding of the genetic architecture of mycorrhizal symbiosis, we conducted a genome-wide association study (GWAS) of this plant-fungal interaction in cultivated sunflower. A diversity panel of cultivated sunflower (Helianthus annuus L.) was phenotyped for root colonization under inoculation with the AM fungus Rhizophagus intraradices. Using a mixed linear model approach with a high-density genetic map, we identified genomic regions that are likely associated with R. intraradices colonization in sunflower. Additionally, we used a set of twelve diverse lines to assess the effect that inoculation with R. intraradices has on dried shoot biomass and macronutrient uptake. Colonization among lines in the mapping panel ranged from 0–70% and was not correlated with mycorrhizal growth response, shoot phosphorus response, or shoot potassium response among the Core 12 lines. Association mapping yielded three single-nucleotide polymorphisms (SNPs) that were significantly associated with R. intraradices colonization. This is the first study to use GWAS to identify genomic regions associated with AM colonization in an Asterid eudicot species. Three genes of interest identified from the regions containing these SNPs are likely related to plant defense.

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Data availability

Data are provided in the supporting information and the Dryad Digital Repository at [https://doi.org/10.5061/dryad.18931zcz5].

Code availability

Code for the GWAS pipeline was reviewed and published in Temme et al. (2020). It is available online (at https://github.com/aatemme/Sunflower-GWAS-v2).

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Acknowledgements

The authors wish to thank Abigail Tripka for assistance sterilizing soil, filling pots, and imaging roots, as well as Gillian Gomer for assistance with imaging roots, and other members of the Mason Lab for assistance with planting and harvesting. The authors also thank the Louisiana State University Extension Soil Testing and Plant Analysis Laboratory for assistance with plant nutrient analysis and the International Culture Collection of (Vesicular) Arbuscular Mycorrhizal Fungi for providing the AM fungal culture used in this study.

Funding

This work was funded by a UCF Vice President for Research Advancement of Early Career Researchers award to CMM, as well as a UCF Office of Undergraduate Research grant to KNS. KNS was supported by a Summer Undergraduate Research Fellowship during the pilot stages of this work and a version of this work constituted the UCF Honors Undergraduate Thesis of KNS.

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Contributions

K.N.S. and C.M.M. designed and carried out the study. K.N.S. led assessment of colonization for plant lines and conducted phenotypic data analysis. J.A.D., A.A.T., J.M.B., E.W.G., and K.N.S. conducted GWAS and candidate gene analyses. K.N.S. wrote the first draft of the manuscript. All authors contributed to the discussion and editing of the final manuscript.

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Correspondence to Chase M. Mason.

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Supplementary Information

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572_2021_1050_MOESM1_ESM.csv

Supplementary file1 (CSV 7 KB). Data S1 Root colonization data usedfor association mapping.

572_2021_1050_MOESM2_ESM.csv

Supplementary file2 (CSV 11 KB). Data S2 Phenotypic data for Core 12 lines.

572_2021_1050_MOESM3_ESM.csv

Supplementary file3 (CSV 157 KB). Data S3 Significant and suggestive genes formycorrhizal colonization traits of interest.

572_2021_1050_MOESM4_ESM.pdf

Supplementary file4 (PDF 590 KB). Figure S1 Mycorrhizal colonization and biomass of wild and cultivated sunflower invarying soil phosphorus conditions. Figure S2 Microscopic images of Helianthusannuus roots stained with trypan blue after inoculation with Rhizophagus intraradices. Figure S3 Validation of methodused to score AM colonization in roots against the McGonigle method. Figure S4 Mean colonization, mycorrhizal growth response(MGR), and shoot nutrient response of phosphorus and potassium as measured inthe Core 12 lines. FigureS5 Mean aboveground dry biomass forthe Core 12 lines under control and inoculated conditions. FigureS6 Correlation matrix between mycorrhizal colonization traits used in thisstudy and root traits measured in Masalia et al. (2018). Methods S1 Methods for examination ofcolonization and mycorrhizal response in wild and cultivated sunflower.

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Stahlhut, K.N., Dowell, J.A., Temme, A.A. et al. Genetic control of arbuscular mycorrhizal colonization by Rhizophagus intraradices in Helianthus annuus (L.). Mycorrhiza 31, 723–734 (2021). https://doi.org/10.1007/s00572-021-01050-5

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