New insights into HcPTR2A and HcPTR2B, two high-affinity peptide transporters from the ectomycorrhizal model fungus Hebe

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ORIGINAL ARTICLE

New insights into HcPTR2A and HcPTR2B, two high-affinity peptide transporters from the ectomycorrhizal model fungus Hebeloma cylindrosporum Tobias Müller 1 & Benjamin Neuhäuser 2 & Uwe Ludewig 2 & Gabriella Houdinet 3 & Sabine D. Zimmermann 3 & Pierre Emmanuel Courty 4 & Daniel Wipf 1,4 Received: 16 March 2020 / Accepted: 15 August 2020 # Springer-Verlag GmbH Germany, part of Springer Nature 2020

Abstract While plants mainly rely on the use of inorganic nitrogen sources like ammonium and nitrate, soil-borne microorganisms like the ectomycorrhizal fungus Hebeloma cylindrosporum can also take up soil organic N in the form of amino acids and peptides that they use as nitrogen and carbon sources. Following the previous identification and functional expression in yeast of two PTR-like peptide transporters, the present study details the functions and substrates of HcPTR2A and HcPTR2B by analysing their transport kinetics in Xenopus laevis oocytes. While both transporters mediated high-affinity di- and tripeptide transport, HcPTR2A also showed low-affinity transport of several amino acids—mostly hydrophobic ones with large side chains. Keywords Ectomycorrhiza . Peptide transporter . Gene expression . Heterologous expression

Introduction Nitrogen (N) is one of the most limiting factors for plant growth even though it is among the most abundant elements on Earth (Vance 2001). The efficiency and ability to use such limiting nutrients is an important component of plant productivity (McKane et al. 2002). Soil-available N forms are largely dependent on different environmental factors like the climate, soil type, acidification and nitrification processes, but also on vegetation and management—e.g. fertilisation. When the soil Electronic supplementary material The online version of this article (https://doi.org/10.1007/s00572-020-00983-7) contains supplementary material, which is available to authorized users. * Daniel Wipf [email protected] 1

IZMB, Transport in Ectomycorrhiza, University Bonn, 53115 Bonn, Germany

2

Institute of Crop Science, Nutritional Crop Physiology, University of Hohenheim, Fruwirthstr. 20, D-70593 Stuttgart, Germany

3

BPMP, Univ Montpellier, CNRS, INRAE, Institut Agro, Montpellier, France

4

Agroécologie, AgroSup Dijon, CNRS, Université de Bourgogne, INRAE, Université de Bourgogne Franche-Comté, 17 Rue Sully, 21000 Dijon, France

is relatively acidic, cold or poorly aerated, ammonium (NH4+) will remain the predominant N form available to plants; in contrast, when soil conditions are favourable to nitrification, ammonification will be followed by conversion to nitrate (Marschner 2012). In forest soils, N is present either in its main inorganic forms NH4+ and NO3− or in organic compounds like amino acids, peptides and proteins (Marschner 2012; Chalot and Brun 1998). Plants generally acquire N in its inorganic forms, followed by intracellular reduction into NH4+, assimilation into glutamine and subsequently other amino acids and organic compounds. Reduction of NO3− to NH4+ is assoc