The half-size ABC transporters STR1 and STR2 are indispensable for mycorrhizal arbuscule formation in rice

Authors

  • Caroline Gutjahr,

    1. Department of Plant Molecular Biology, University of Lausanne, Biophore Building, 1015 Lausanne, Switzerland
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  • Dragica Radovanovic,

    1. Department of Plant Molecular Biology, University of Lausanne, Biophore Building, 1015 Lausanne, Switzerland
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  • Jessika Geoffroy,

    1. Department of Plant Molecular Biology, University of Lausanne, Biophore Building, 1015 Lausanne, Switzerland
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  • Quan Zhang,

    1. Boyce Thompson Institute for Plant Research, Cornell University, Ithaca, NY 14853, USA
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    • Present address: LC; UMR INRA 1088/CNRS 5184/U. Bourgogne, Plant-Microbe-Environment, INRA-CMSE, BP 86510, 21065 Dijon cedex, France. SKC; Bayer Crop Science, Breeding and Trait Development, 108 Pasir Panjang Rd, # 05-14, Singapore 118535. QZ; Department of Biology, Campus Box 1137, Washington University in St Louis, St Louis, MO 63130, USA.

  • Heike Siegler,

    1. Department of Plant Molecular Biology, University of Lausanne, Biophore Building, 1015 Lausanne, Switzerland
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  • Marco Chiapello,

    1. Department of Plant Molecular Biology, University of Lausanne, Biophore Building, 1015 Lausanne, Switzerland
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  • Leonardo Casieri,

    1. Department of Plant Molecular Biology, University of Lausanne, Biophore Building, 1015 Lausanne, Switzerland
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    • Present address: LC; UMR INRA 1088/CNRS 5184/U. Bourgogne, Plant-Microbe-Environment, INRA-CMSE, BP 86510, 21065 Dijon cedex, France. SKC; Bayer Crop Science, Breeding and Trait Development, 108 Pasir Panjang Rd, # 05-14, Singapore 118535. QZ; Department of Biology, Campus Box 1137, Washington University in St Louis, St Louis, MO 63130, USA.

  • Kyungsook An,

    1. Crop Biotech Institute and Department of Plant Molecular Systems Biotechnology, Kyung Hee University, Yongin 446-701, Korea
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  • Gynheung An,

    1. Crop Biotech Institute and Department of Plant Molecular Systems Biotechnology, Kyung Hee University, Yongin 446-701, Korea
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  • Emmanuel Guiderdoni,

    1. CIRAD, UMR AGAP 1096, TA 108/03 Avenue Agropolis, 34398 Montpellier Cedex 5, France
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  • Chellian Santhosh Kumar,

    1. Department of Plant Biology, University of California Davis, Davis, CA 95616, USA
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    • Present address: LC; UMR INRA 1088/CNRS 5184/U. Bourgogne, Plant-Microbe-Environment, INRA-CMSE, BP 86510, 21065 Dijon cedex, France. SKC; Bayer Crop Science, Breeding and Trait Development, 108 Pasir Panjang Rd, # 05-14, Singapore 118535. QZ; Department of Biology, Campus Box 1137, Washington University in St Louis, St Louis, MO 63130, USA.

  • Venkatesan Sundaresan,

    1. Department of Plant Biology, University of California Davis, Davis, CA 95616, USA
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  • Maria J. Harrison,

    1. Boyce Thompson Institute for Plant Research, Cornell University, Ithaca, NY 14853, USA
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  • Uta Paszkowski

    Corresponding author
    1. Department of Plant Molecular Biology, University of Lausanne, Biophore Building, 1015 Lausanne, Switzerland
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(fax +41 21 692 4195; e-mail uta.paszkowski@unil.ch).

Summary

The central structure of the symbiotic association between plants and arbuscular mycorrhizal (AM) fungi is the fungal arbuscule that delivers minerals to the plant. Our earlier transcriptome analyses identified two half-size ABCG transporters that displayed enhanced mRNA levels in mycorrhizal roots. We now show specific transcript accumulation in arbusculated cells of both genes during symbiosis. Presently, arbuscule-relevant factors from monocotyledons have not been reported. Mutation of either of the Oryza sativa (rice) ABCG transporters blocked arbuscule growth of different AM fungi at a small and stunted stage, recapitulating the phenotype of Medicago truncatula stunted arbuscule 1 and 2 (str1 and str2) mutants that are deficient in homologous ABCG genes. This phenotypic resemblance and phylogenetic analysis suggest functional conservation of STR1 and STR2 across the angiosperms. Malnutrition of the fungus underlying limited arbuscular growth was excluded by the absence of complementation of the str1 phenotype by wild-type nurse plants. Furthermore, plant AM signaling was found to be intact, as arbuscule-induced marker transcript accumulation was not affected in str1 mutants. Strigolactones have previously been hypothesized to operate as intracellular hyphal branching signals and possible substrates of STR1 and STR2. However, full arbuscule development in the strigolactone biosynthesis mutants d10 and d17 suggested strigolactones to be unlikely substrates of STR1/STR2. Interestingly, rice STR1 is associated with a cis-natural antisense transcript (antiSTR1). Analogous to STR1 and STR2, at the root cortex level, the antiSTR1 transcript is specifically detected in arbusculated cells, suggesting unexpected modes of STR1 regulation in rice.

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