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GeSUT4 mediates sucrose import at the symbiotic interface for carbon allocation of heterotrophic Gastrodia elata (orchidaceae)
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  • Li-Hsuan Ho,
  • Yung-I Lee,
  • Shu-Ying Hsieh,
  • I-Shiuan Lin,
  • Yun-Chien Wu,
  • Han-Yu Ko,
  • Patrick Klemens,
  • Ekkehard Neuhaus,
  • Yi-Min Chen,
  • Tzu-Pi Huang,
  • Chih-Hsin Yeh,
  • WOEI-JIUN GUO
Li-Hsuan Ho
National Cheng Kung University
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Yung-I Lee
National Museum of Natural Science
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Shu-Ying Hsieh
National Cheng Kung University
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I-Shiuan Lin
National Cheng Kung University
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Yun-Chien Wu
National Cheng Kung University
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Han-Yu Ko
National Cheng Kung University
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Patrick Klemens
University of Kaiserslautern
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Ekkehard Neuhaus
University of Kaiserslautern
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Yi-Min Chen
National Cheng Kung University
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Tzu-Pi Huang
National Chung Hsing University
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Chih-Hsin Yeh
Council of Agriculture
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WOEI-JIUN GUO
National Cheng Kung University
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Abstract

Gastrodia elata, a fully mycoheterotrophic orchid without photosynthetic ability, only grows symbiotically with the fungus Armillaria. The mechanism of carbon distribution in this mycoheterotrophy is unknown. We detected high sucrose concentrations in all stages of Gastrodia tubers, suggesting sucrose may be the major sugar transported between fungus and orchid. Thick symplasm-isolated wall interfaces in colonized and adjacent large cells implied involvement of sucrose importers. Two sucrose transporter (SUT)-like genes, GeSUT4 and GeSUT3, were identified that are highly expressed in young Armillaria-colonized tubers. Yeast complementation and radio tracer experiments confirmed that GeSUT4 functioned as a high-affinity sucrose-specific proton-dependent importer. Plasma-membrane/tonoplast localization of GeSUT4-GFP fusions, and high RNA expression of GeSUT4 in symbiotic and large cells indicated that GeSUT4 likely functions in active sucrose transport for intercellular allocation and intracellular homeostasis. Transgenic Arabidopsis overexpressing GeSUT4 had larger leaves but sensitive to excess sucrose and roots were colonized with fewer mutualistic Bacillus, supporting the role of GeSUT4 in regulating sugar allocation. This is not only the first documented carbon import system in a mycoheterotrophic interaction, but also highlights the evolutionary importance of sucrose transporters for regulation of carbon flow in all types of plant-microbe interactions.

Peer review status:UNDER REVIEW

17 Apr 2020Submitted to Plant, Cell & Environment
20 Apr 2020Submission Checks Completed
20 Apr 2020Assigned to Editor
04 May 2020Reviewer(s) Assigned
26 May 2020Review(s) Completed, Editorial Evaluation Pending
17 Jun 20201st Revision Received
17 Jun 2020Submission Checks Completed
17 Jun 2020Assigned to Editor
19 Jun 2020Review(s) Completed, Editorial Evaluation Pending