Delivery of cytoplasmic and apoplastic effectors from Phytophthora infestans haustoria by distinct secretion pathways

Shumei Wang, Petra C. Boevink, Lydia Welsh, Ruofang Zhang, Stephen C. Whisson, Paul J. R. Birch (Lead / Corresponding author)

Research output: Contribution to journalArticle

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Abstract

• The potato blight pathogen Phytophthora infestans secretes effector proteins that are delivered inside (cytoplasmic) or can act outside (apoplastic) plant cells to neutralise host immunity. Little is known about how and where effectors are secreted during infection, yet such knowledge is essential to understand and combat crop disease.• We used transient Agrobacterium-mediated in planta expression, transformation of P. infestans with fluorescent protein-fusions and confocal microscopy to investigate delivery of effectors to plant cells during infection.
• The cytoplasmic effector Pi04314, expressed as an mRFP-fusion protein with a signal peptide to secrete it from plant cells, does not passively re-enter the cells upon secretion. However, Pi04314-mRFP expressed in P. infestans is translocated from haustoria, which form intimate interactions with plant cells, to accumulate at its sites-of-action in the host nucleus. The well-characterised apoplastic effector EPIC1 was also secreted from haustoria. EPIC1 secretion was inhibited by brefeldin A (BFA), demonstrating that it is delivered by conventional Golgi-mediated secretion. In contrast, Pi04314 secretion was insensitive to BFA treatment, indicating that the cytoplasmic effector follows an alternative route for delivery into plant cells.
• P. infestans haustoria are thus sites for delivery of both apoplastic and cytoplasmic effectors during infection, following distinct secretion pathways.
Original languageEnglish
Pages (from-to)205-215
Number of pages11
JournalNew Phytologist
Volume29
Issue number8
Early online date31 Jul 2017
DOIs
Publication statusPublished - 29 Aug 2017

Fingerprint

Phytophthora infestans
Secretory Pathway
Plant Cells
secretion
Brefeldin A
brefeldin A
cells
Infection
Agrobacterium
Proteins
infection
Solanum tuberosum
Protein Sorting Signals
Confocal Microscopy
Plantae
Immunity
signal peptide
blight
proteins
immunity

Keywords

  • effector translocation
  • plant disease
  • plant immunity
  • effector-triggered susceptibility
  • secretion
  • apoplastic effector
  • virulence

Cite this

Wang, Shumei ; Boevink, Petra C. ; Welsh, Lydia ; Zhang, Ruofang ; Whisson, Stephen C. ; Birch, Paul J. R. / Delivery of cytoplasmic and apoplastic effectors from Phytophthora infestans haustoria by distinct secretion pathways. In: New Phytologist. 2017 ; Vol. 29, No. 8. pp. 205-215.
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abstract = "• The potato blight pathogen Phytophthora infestans secretes effector proteins that are delivered inside (cytoplasmic) or can act outside (apoplastic) plant cells to neutralise host immunity. Little is known about how and where effectors are secreted during infection, yet such knowledge is essential to understand and combat crop disease.• We used transient Agrobacterium-mediated in planta expression, transformation of P. infestans with fluorescent protein-fusions and confocal microscopy to investigate delivery of effectors to plant cells during infection.• The cytoplasmic effector Pi04314, expressed as an mRFP-fusion protein with a signal peptide to secrete it from plant cells, does not passively re-enter the cells upon secretion. However, Pi04314-mRFP expressed in P. infestans is translocated from haustoria, which form intimate interactions with plant cells, to accumulate at its sites-of-action in the host nucleus. The well-characterised apoplastic effector EPIC1 was also secreted from haustoria. EPIC1 secretion was inhibited by brefeldin A (BFA), demonstrating that it is delivered by conventional Golgi-mediated secretion. In contrast, Pi04314 secretion was insensitive to BFA treatment, indicating that the cytoplasmic effector follows an alternative route for delivery into plant cells.• P. infestans haustoria are thus sites for delivery of both apoplastic and cytoplasmic effectors during infection, following distinct secretion pathways.",
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Delivery of cytoplasmic and apoplastic effectors from Phytophthora infestans haustoria by distinct secretion pathways. / Wang, Shumei; Boevink, Petra C.; Welsh, Lydia; Zhang, Ruofang; Whisson, Stephen C.; Birch, Paul J. R. (Lead / Corresponding author).

In: New Phytologist, Vol. 29, No. 8, 29.08.2017, p. 205-215.

Research output: Contribution to journalArticle

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AB - • The potato blight pathogen Phytophthora infestans secretes effector proteins that are delivered inside (cytoplasmic) or can act outside (apoplastic) plant cells to neutralise host immunity. Little is known about how and where effectors are secreted during infection, yet such knowledge is essential to understand and combat crop disease.• We used transient Agrobacterium-mediated in planta expression, transformation of P. infestans with fluorescent protein-fusions and confocal microscopy to investigate delivery of effectors to plant cells during infection.• The cytoplasmic effector Pi04314, expressed as an mRFP-fusion protein with a signal peptide to secrete it from plant cells, does not passively re-enter the cells upon secretion. However, Pi04314-mRFP expressed in P. infestans is translocated from haustoria, which form intimate interactions with plant cells, to accumulate at its sites-of-action in the host nucleus. The well-characterised apoplastic effector EPIC1 was also secreted from haustoria. EPIC1 secretion was inhibited by brefeldin A (BFA), demonstrating that it is delivered by conventional Golgi-mediated secretion. In contrast, Pi04314 secretion was insensitive to BFA treatment, indicating that the cytoplasmic effector follows an alternative route for delivery into plant cells.• P. infestans haustoria are thus sites for delivery of both apoplastic and cytoplasmic effectors during infection, following distinct secretion pathways.

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