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Biotrophic transportome in mutualistic plant–fungal interactions

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Abstract

Understanding the mechanisms that underlie nutrient use efficiency and carbon allocation along with mycorrhizal interactions is critical for managing croplands and forests soundly. Indeed, nutrient availability, uptake and exchange in biotrophic interactions drive plant growth and modulate biomass allocation. These parameters are crucial for plant yield, a major issue in the context of high biomass production. Transport processes across the polarized membrane interfaces are of major importance in the functioning of the established mycorrhizal association as the symbiotic relationship is based on a ‘fair trade’ between the fungus and the host plant. Nutrient and/or metabolite uptake and exchanges, at biotrophic interfaces, are controlled by membrane transporters whose regulation patterns are essential for determining the outcome of plant–fungus interactions and adapting to changes in soil nutrient quantity and/or quality. In the present review, we summarize the current state of the art regarding transport systems in the two major forms of mycorrhiza, namely ecto- and arbuscular mycorrhiza.

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Abbreviations

AAP:

Amino acid permeases

AAT:

Amino acid transporters

ABA:

Abscisic acid

AM:

Arbuscular mycorrhiza

AMT:

Ammonium transporter

APC:

Amino acid/polyamine/organocation

AQPs:

Aquaporins

AQR1:

Acids quinidine resistance 1

ATPase:

Adenosine triphosphate hydrolase

DP:

Direct pathway

ECM:

Ectomycorrhizal

ERM:

Extraradicular mycelium

EST:

Expressed sequence tag

GUS:

β-Glucuronidase gene

HAK:

H+ uptake permease

HIGS:

Host-induced gene silencing

IRM:

Intraradical mycelium

KUP:

K+ uptake permease

LPC:

Lyso-phosphatidylcholine

MIP:

Major intrinsic protein

MP:

Mycorrhizal pathway

MSTs:

Monosaccharide transporters

NCBI:

National Center for Biotechnology Information

NIP:

Nod 26-like intrinsic protein

NiR:

Nitrite reductase

NNP:

Nitrate/nitrite porter

NO3 - :

Nitrate

NR:

Nitrate reductase

NT:

Nitrate transporter

OPT:

Oligopeptide transporter

Pi :

Inorganic phosphate

PIPs:

Plasma membrane intrinsic proteins

POT:

Proton-coupled oligopeptide transporter

PTR:

Peptide transporter

RNAi:

RNA interference

SULTRs:

Sulphate transporters

SUTs/SUCs:

Sucrose transporters

TCA:

Trichloroacetic acid

TIPs:

Tonoplast intrinsic proteins

WT:

Wild type

YAT:

Yeast amino acid transporter

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Acknowledgments

All the authors of this work are thankful for the support of the ANR TRANSMUT (ANR-10-BLAN-1604-0). LC, NAL, JD, LB, MC and DW received financial support from the Burgundy Regional Council (PARI Agrale 8); NAL and DW received financial support from the Université Franco Italienne/Università Italo Francese. PEC received financial support from the Swiss National Science Foundation (grant no. PZ00P3_136651).

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  1. UMR Agroécologie INRA 1347/Agrosup/Université de Bourgogne, Pôle Interactions Plantes Microorganismes ERL 6300 CNRS, BP 86510, 21065, Dijon Cedex, France

    Leonardo Casieri, Nassima Ait Lahmidi, Joan Doidy, Laurent Bonneau, Maryse Charbonnier & Daniel Wipf

  2. UMR “Interaction Arbres Microorganismes”, Centre INRA Nancy, 54280, Champenoux, France

    Claire Veneault-Fourrey, Aude Migeon & Annick Brun

  3. UMR 5004 CNRS/INRA/SupAgro/UM2, Biochimie et Physiologie Moléculaire des Plantes, Campus INRA/SupAgro, 2 Place Viala, 34060, Montpellier Cedex 2, France

    Kevin Garcia, Amandine Delteil & Sabine Zimmermann

  4. Zurich-Basel Plant Science Center, Botanical Institute, University of Basel, Hebelstrasse 1, 4056, Basel, Switzerland

    Pierre-Emmanuel Courty

  5. UMR 1222 “Ecologie Fonctionnelle et Biogéochimie des Sols et Agrosystèmes” Eco&Sols, INRA 2 Montpellier, Place Viala, 34060, Montpellier Cedex 2, France

    Claude Plassard

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  1. Leonardo Casieri
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Correspondence to Leonardo Casieri.

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Leonardo Casieri and Nassima Ait Lahmidi contributed equally to the work.

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ESM 1

Gene IDs and accession numbers of plant Pi transporters used for Fig. 3 (DOC 213 kb)

ESM 2

Gene IDs and accession numbers of fungal Pi transporters used for Fig. 4 (DOC 185 kb)

ESM 3

Gene IDs and accession numbers of plant sulphate transporters used for Fig. 6 (DOC 147 kb)

ESM 4

Gene IDs and accession numbers of fungal sulphate transporters used for Fig. 7 (DOC 141 kb)

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Casieri, L., Ait Lahmidi, N., Doidy, J. et al. Biotrophic transportome in mutualistic plant–fungal interactions. Mycorrhiza 23, 597–625 (2013). https://doi.org/10.1007/s00572-013-0496-9

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