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Colletotrichum orbiculare Secretes Virulence Effectors to a Biotrophic Interface at the Primary Hyphal Neck via Exocytosis Coupled with SEC22-Mediated Traffic

Hiroki Irieda, Hitomi Maeda, Kaoru Akiyama, Asuka Hagiwara, Hiromasa Saitoh, Aiko Uemura, Ryohei Terauchi, Yoshitaka Takano
Hiroki Irieda
aGraduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan
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Hitomi Maeda
aGraduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan
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Kaoru Akiyama
bHanaichi Ultrastructure Research Institute, Okazaki 444-0076, Japan
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Asuka Hagiwara
aGraduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan
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Hiromasa Saitoh
cIwate Biotechnology Research Center, Iwate 024-0003, Japan
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Aiko Uemura
cIwate Biotechnology Research Center, Iwate 024-0003, Japan
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Ryohei Terauchi
cIwate Biotechnology Research Center, Iwate 024-0003, Japan
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Yoshitaka Takano
aGraduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan
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  • For correspondence: ytakano@kais.kyoto-u.ac.jp

Published May 2014. DOI: https://doi.org/10.1105/tpc.113.120600

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  • © 2014 American Society of Plant Biologists. All rights reserved.

Abstract

The hemibiotrophic pathogen Colletotrichum orbiculare develops biotrophic hyphae inside cucumber (Cucumis sativus) cells via appressorial penetration; later, the pathogen switches to necrotrophy. C. orbiculare also expresses specific effectors at different stages. Here, we found that virulence-related effectors of C. orbiculare accumulate in a pathogen–host biotrophic interface. Fluorescence-tagged effectors accumulated in a ring-like region around the neck of the biotrophic primary hyphae. Fluorescence imaging of cellular components and transmission electron microscopy showed that the ring-like signals of the effectors localized at the pathogen–plant interface. Effector accumulation at the interface required induction of its expression during the early biotrophic phase, suggesting that transcriptional regulation may link to effector localization. We also investigated the route of effector secretion to the interface. An exocytosis-related component, the Rab GTPase SEC4, localized to the necks of biotrophic primary hyphae adjacent to the interface, thereby suggesting focal effector secretion. Disruption of SEC4 in C. orbiculare reduced virulence and impaired effector delivery to the ring signal interface. Disruption of the v-SNARE SEC22 also reduced effector delivery. These findings suggest that biotrophy-expressed effectors are secreted, via the endoplasmic reticulum-to-Golgi route and subsequent exocytosis, toward the interface generated between C. orbiculare and the host cell.

  • Glossary

    TEM
    transmission electron microscopy
    BIC
    biotrophic interfacial complex
    ER
    endoplasmic reticulum
    dpi
    days postinoculation
    FRAP
    fluorescence recovery after photobleaching
    • Received November 10, 2013.
    • Revised April 20, 2014.
    • Accepted May 2, 2014.
    • Published May 21, 2014.
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    Colletotrichum orbiculare Secretes Virulence Effectors to a Biotrophic Interface at the Primary Hyphal Neck via Exocytosis Coupled with SEC22-Mediated Traffic
    Hiroki Irieda, Hitomi Maeda, Kaoru Akiyama, Asuka Hagiwara, Hiromasa Saitoh, Aiko Uemura, Ryohei Terauchi, Yoshitaka Takano
    The Plant Cell May 2014, 26 (5) 2265-2281; DOI: 10.1105/tpc.113.120600

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    Colletotrichum orbiculare Secretes Virulence Effectors to a Biotrophic Interface at the Primary Hyphal Neck via Exocytosis Coupled with SEC22-Mediated Traffic
    Hiroki Irieda, Hitomi Maeda, Kaoru Akiyama, Asuka Hagiwara, Hiromasa Saitoh, Aiko Uemura, Ryohei Terauchi, Yoshitaka Takano
    The Plant Cell May 2014, 26 (5) 2265-2281; DOI: 10.1105/tpc.113.120600
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