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No evidence of regulation in root-mediated iron reduction in two Strategy I cluster-rooted Banksia species (Proteaceae)

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Abstract

Aims

Non-mycorrhizal species such as Banksia (Proteaceae) that depend on root exudates to acquire phosphorus (P) are prominent in south-western Australia, a biodiversity hotspot on severely P-impoverished soils. We investigated the consequences of an exudate-releasing P-mobilising strategy related to control of iron (Fe) acquisition in two Banksia species, B. attenuata R.Br. and B. laricina C. Gardner, that differ greatly in their geographical distribution and rarity.

Methods

We undertook solution culture experiments to measure root-mediated Fe reduction (FeR) in non-cluster and cluster roots at four stages of cluster-root development, and whole root systems for plants grown at 2 to 300 μM Fe (as Fe-EDTA). As a positive control, we used Pisum sativum (cv. Dunn) to validate the FeR assay.

Results

Unlike typical Strategy I species, both Banksia species showed no significant variation in FeR, for either cluster or non-cluster roots, when grown at a wide range of Fe supply. For roots of different developmental stages, we measured a range for B. attenuata cluster roots of 0.13 ± 0.03 to 1.29 ± 0.14 μmol Fe3+ reduced g−1 FW h−1 and 0.56 ± 0.11 to 1.10 ± 0.24 μmol Fe3+ reduced g−1 FW h−1 in non-cluster roots. Similarly, for B. laricina cluster-roots, FeR ranged from 0.22 ± 0.07 to 1.21 ± 0.37 μmol Fe3+ reduced g−1 FW h−1, and in non-cluster roots from 0.56 ± 0.11 to 0.71 ± 0.08 μmol Fe3+ reduced g−1 FW h−1. We also observed only minor differences for whole-root system FeR, and even though B. attenuata showed signs of leaf Fe deficiency in the 2 μM Fe treatment, its FeR was the lowest of both species across all treatments at 0.079 ± 0.009 μmol Fe3+ reduced g−1 FW h−1, compared with the fastest rate of 0.20 ± 0.014 μmol Fe3+ reduced g−1 FW h−1 for B. laricina in the 28 μM Fe treatment. Taking plants through a pulse from low to high Fe, then back to low Fe supply did not elucidate any significant response in FeR.

Conclusions

Although Fe acquisition is tightly controlled in the investigated Banksia species, such control is not based on regulation of FeR, which challenges the model that is commonly accepted for Strategy I species.

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Acknowledgements

Contents of this publication do not necessarily reflect the views or policies of the US Department of Agriculture, nor does mention of trade names, commercial products, or organizations imply endorsement by the US Government. We thank the Western Australia Parks and Wildlife Service for their permission to collect seeds under permit. The authors would like to thank Blake Wood, Bill Piasini and Robert Creasy for assistance with plant maintenance; Blake Wood and Calum Irvine for assistance with FeR assays; Sonja Jakob, Etienne Laliberté, Caio Guilherme Pereira and Gerald Page for statistical advice and assistance with data analysis and interpretation and Cheeming Li for his efforts to isolate ferric reductase proteins. HL and EJV were supported by the Australian Research Council (ARC, DP0209245). Finally, the authors would like to express their gratitude to the anonymous reviewers for their constructive comments.

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Authors and Affiliations

  1. School of Biological Sciences, The University of Western Australia, 35 Stirling Highway, Crawley (Perth), Western Australia, 6009, Australia

    Gregory R. Cawthray, Michael W. Shane, Erik J. Veneklaas & Hans Lambers

  2. School of Agriculture, Food and Wine, The University of Adelaide, Glen Osmond, SA, 5064, Australia

    Matthew D. Denton

  3. USDA-ARS Edward T. Schafer Agricultural Research Center, 1616 Albrecht Boulevard N, Fargo, ND, 58102-2765, USA

    Michael A. Grusak

  4. School of Agriculture and Environment, The University of Western Australia, 35 Stirling Highway, Crawley (Perth), Western Australia, 6009, Australia

    Erik J. Veneklaas

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  1. Gregory R. Cawthray
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Correspondence to Gregory R. Cawthray.

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Cawthray, G.R., Denton, M.D., Grusak, M.A. et al. No evidence of regulation in root-mediated iron reduction in two Strategy I cluster-rooted Banksia species (Proteaceae). Plant Soil 461, 203–218 (2021). https://doi.org/10.1007/s11104-021-04849-5

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