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Physiological and transcriptomic response of Medicago truncatula to colonization by high- or low-benefit arbuscular mycorrhizal fungi

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Abstract

Arbuscular mycorrhizal (AM) fungi form a root endosymbiosis with many agronomically important crop species. They enhance the ability of their host to obtain nutrients from the soil and increase the tolerance to biotic and abiotic stressors. However, AM fungal species can differ in the benefits they provide to their host plants. Here, we examined the putative molecular mechanisms involved in the regulation of the physiological response of Medicago truncatula to colonization by Rhizophagus irregularis or Glomus aggregatum, which have previously been characterized as high- and low-benefit AM fungal species, respectively. Colonization with R. irregularis led to greater growth and nutrient uptake than colonization with G. aggregatum. These benefits were linked to an elevated expression in the roots of strigolactone biosynthesis genes (NSP1, NSP2, CCD7, and MAX1a), mycorrhiza-induced phosphate (PT8), ammonium (AMT2;3), and nitrate (NPF4.12) transporters and the putative ammonium transporter NIP1;5. R. irregularis also stimulated the expression of photosynthesis-related genes in the shoot and the upregulation of the sugar transporters SWEET1.2, SWEET3.3, and SWEET 12 and the lipid biosynthesis gene RAM2 in the roots. In contrast, G. aggregatum induced the expression of biotic stress defense response genes in the shoots, and several genes associated with abiotic stress in the roots. This suggests that either the host perceives colonization by G. aggregatum as pathogen attack or that G. aggregatum can prime host defense responses. Our findings highlight molecular mechanisms that host plants may use to regulate their association with high- and low-benefit arbuscular mycorrhizal symbionts.

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Data and material availability

The RNA-seq datasets generated for and analyzed in the current study are available on NCBI as BioProject ID PRJNA832760 and can be accessed at http://www.ncbi.nlm.nih.gov/bioproject/832760.

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Acknowledgements

We would like to thank Lindsay McKeever for performing the Kjeldahl degradations for the 15N/14N analyses.

Funding

This work was funded by the USDA (2017–67014-26530), the SD Soybean Research and Promotion Council, and the Agricultural Experiment Station at SDSU to HB and SS. KG acknowledges the financial support of the North Carolina Agriculture Research Service (NCARS), the North Carolina Soybean Producers Association (2019–1656), and the USDA (2020–67013-31800).

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Contributions

HB and SS conceived the original research plans; HB and AK designed the experiments; AK and JY performed the experiments, KRC and KG conducted the transcriptome analysis, and PP and GS completed the stable isotope analysis; KRC, AK, KG, JY, and PP analyzed the data; KRC wrote the article with input from all the authors; HB and SS supervised and completed the writing. HB agrees to serve as the author responsible for contact and ensures communication.

Corresponding author

Correspondence to Heike Bücking.

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The authors declare no competing interests.

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Cope, K.R., Kafle, A., Yakha, J.K. et al. Physiological and transcriptomic response of Medicago truncatula to colonization by high- or low-benefit arbuscular mycorrhizal fungi. Mycorrhiza 32, 281–303 (2022). https://doi.org/10.1007/s00572-022-01077-2

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  • DOI: https://doi.org/10.1007/s00572-022-01077-2

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