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Mycorrhizal symbiosis alleviates Mn toxicity and downregulates Mn transporter genes in Eucalyptus tereticornis under contrasting soil phosphorus

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Abstract

Background and aims

Tropical soils often present two issues that can hinder plant growth: low phosphorus (P) and high manganese (Mn) availability. Eucalyptus tereticornis is frequently cultivated in such soils. We investigated the effects of Mn in E. tereticornis under contrasting soil P availability and hypothesized that arbuscular mycorrhizal (AM) symbiosis could alleviate Mn toxicity by improving P nutrition and altering the expression of Mn transporter genes.

Methods

Inoculated (AM) and non-inoculated (NM) seedlings grew for seven months in a soil with low or sufficient P availability, under three Mn doses: control, 75 and 150 mg kg−1 Mn. We assessed growth, AM colonization, nutrient concentrations, and the expression of eight genes related to Mn transport and homeostasis in roots. Mn distribution at one-leaf level was determined by μ-XRF.

Results

Low P exacerbated Mn toxicity and hindered plant growth. Mycorrhizal symbiosis did not influence Mn accumulation, but improved growth and Mn tolerance at low P, partly by improving P nutrition. At sufficient P, foliar Mn reached 3500 mg kg−1, and μ-XRF patterns suggest preferential accumulation in the leaf lamina compared to margins or midribs. In NM plants, the vacuolar transporters EtVIT1 and EtMTP8 and the Mn-nicotianamine influx transporter EtYSL6 were the most responsive genes to Mn, while in AM roots most were downregulated.

Conclusion

Vacuolar sequestration and transport of complexed Mn are important mechanisms behind Mn tolerance in E. tereticornis. We propose that Mn is transported via the mycorrhizal pathway, explaining why it does not elicit the same molecular response observed in NM roots.

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Data availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

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Acknowledgments

We would like to thank Dr. Luana F. Torres for assisting with the optimization of a good quality RNA extraction protocol and Dr. Franklin M. O. Silva for helping with the IRGA measurements and harvest. We also thank the research fellowship to Prof Paulo Mazzafera (CNPq - Conselho Nacional de Desenvolvimento Científico e Tecnológico—Brazil, Grant number 306002/2020-5).

Funding

This study was supported by the São Paulo Research Foundation (FAPESP - Grant Number 2016/25498-0). We would also like to thank FAPESP for the post-doc fellowship and funding for V.H. De Oliveira (Grant Number 2019/10243-4).

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Authors

Contributions

Conceptualization by V.H. De Oliveira, S.A.L. de Andrade and P. Mazzafera. Investigation and data collection by V.H. De Oliveira. Data analysis by V.H. De Oliveira, S.A.L. de Andrade and G.S. Montanha. Methodology by V.H. De Oliveira, G.S. Montanha and H.W.P. Carvalho. Supervision by S.A.L. de Andrade. Original draft by V.H. De Oliveira. All authors reviewed and edited the manuscript. All authors have read and agreed to the published version of the manuscript.

Corresponding authors

Correspondence to Vinicius H. De Oliveira or Sara Adrián L. de Andrade.

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Competing interests

The authors have no relevant financial or non-financial interests to disclose.

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Responsible Editor: Antony Van der Ent.

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De Oliveira, V.H., Montanha, G.S., Carvalho, H.W.P. et al. Mycorrhizal symbiosis alleviates Mn toxicity and downregulates Mn transporter genes in Eucalyptus tereticornis under contrasting soil phosphorus. Plant Soil 489, 361–383 (2023). https://doi.org/10.1007/s11104-023-06024-4

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  • DOI: https://doi.org/10.1007/s11104-023-06024-4

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