Phytophthora infestans small phospholipase D-like proteins elicit plant cell death and promote virulence

Harold J.G. Meijer, Charikleia Schoina, Shutong Wang, Klaas Bouwmeester, Chenlei Hua, Francine Govers

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

The successful invasion of host tissue by (hemi-)biotrophic plant pathogens is dependent on modifications of the host plasma membrane to facilitate the two-way transfer of proteins and other compounds. Haustorium formation and the establishment of extrahaustorial membranes are probably dependent on a variety of enzymes that modify membranes in a coordinated fashion. Phospholipases, enzymes that hydrolyse phospholipids, have been implicated as virulence factors in several pathogens. The oomycete Phytophthora infestans is a hemibiotrophic pathogen that causes potato late blight. It possesses different classes of phospholipase D (PLD) proteins, including small PLD-like proteins with and without signal peptide (sPLD-likes and PLD-likes, respectively). Here, we studied the role of sPLD-like-1, sPLD-like-12 and PLD-like-1 in the infection process. They are expressed in expanding lesions on potato leaves and during in vitro growth, with the highest transcript levels in germinating cysts. When expressed in planta in the presence of the silencing suppressor P19, all three elicited a local cell death response that was visible at the microscopic level as autofluorescence and strongly boosted in the presence of calcium. Moreover, inoculation of leaves expressing the small PLD-like genes resulted in increased lesion growth and greater numbers of sporangia, but this was abolished when mutated PLD-like genes were expressed with non-functional PLD catalytic motifs. These results show that the three small PLD-likes are catalytically active and suggest that their enzymatic activity is required for the promotion of virulence, possibly by executing membrane modifications to support the growth of P. infestans in the host.

LanguageEnglish
Pages180-193
JournalMolecular Plant Pathology
Volume20
Issue number2
Early online date1 Sep 2018
DOIs
Publication statusPublished - Feb 2019

Fingerprint

Phytophthora infestans
Phospholipase D
phospholipase D
Plant Cells
plant proteins
virulence
Virulence
cell death
Cell Death
membrane
protein
pathogen
lesion
potato
Proteins
enzyme
lesions (plant)
gene
Solanum tuberosum
cyst

Keywords

  • calcium
  • late blight disease
  • oomycete
  • phospholipases
  • phospholipids
  • signal peptide

Cite this

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title = "Phytophthora infestans small phospholipase D-like proteins elicit plant cell death and promote virulence",
abstract = "The successful invasion of host tissue by (hemi-)biotrophic plant pathogens is dependent on modifications of the host plasma membrane to facilitate the two-way transfer of proteins and other compounds. Haustorium formation and the establishment of extrahaustorial membranes are probably dependent on a variety of enzymes that modify membranes in a coordinated fashion. Phospholipases, enzymes that hydrolyse phospholipids, have been implicated as virulence factors in several pathogens. The oomycete Phytophthora infestans is a hemibiotrophic pathogen that causes potato late blight. It possesses different classes of phospholipase D (PLD) proteins, including small PLD-like proteins with and without signal peptide (sPLD-likes and PLD-likes, respectively). Here, we studied the role of sPLD-like-1, sPLD-like-12 and PLD-like-1 in the infection process. They are expressed in expanding lesions on potato leaves and during in vitro growth, with the highest transcript levels in germinating cysts. When expressed in planta in the presence of the silencing suppressor P19, all three elicited a local cell death response that was visible at the microscopic level as autofluorescence and strongly boosted in the presence of calcium. Moreover, inoculation of leaves expressing the small PLD-like genes resulted in increased lesion growth and greater numbers of sporangia, but this was abolished when mutated PLD-like genes were expressed with non-functional PLD catalytic motifs. These results show that the three small PLD-likes are catalytically active and suggest that their enzymatic activity is required for the promotion of virulence, possibly by executing membrane modifications to support the growth of P. infestans in the host.",
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Phytophthora infestans small phospholipase D-like proteins elicit plant cell death and promote virulence. / Meijer, Harold J.G.; Schoina, Charikleia; Wang, Shutong; Bouwmeester, Klaas; Hua, Chenlei; Govers, Francine.

In: Molecular Plant Pathology, Vol. 20, No. 2, 02.2019, p. 180-193.

Research output: Contribution to journalArticleAcademicpeer-review

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T1 - Phytophthora infestans small phospholipase D-like proteins elicit plant cell death and promote virulence

AU - Meijer, Harold J.G.

AU - Schoina, Charikleia

AU - Wang, Shutong

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AU - Hua, Chenlei

AU - Govers, Francine

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N2 - The successful invasion of host tissue by (hemi-)biotrophic plant pathogens is dependent on modifications of the host plasma membrane to facilitate the two-way transfer of proteins and other compounds. Haustorium formation and the establishment of extrahaustorial membranes are probably dependent on a variety of enzymes that modify membranes in a coordinated fashion. Phospholipases, enzymes that hydrolyse phospholipids, have been implicated as virulence factors in several pathogens. The oomycete Phytophthora infestans is a hemibiotrophic pathogen that causes potato late blight. It possesses different classes of phospholipase D (PLD) proteins, including small PLD-like proteins with and without signal peptide (sPLD-likes and PLD-likes, respectively). Here, we studied the role of sPLD-like-1, sPLD-like-12 and PLD-like-1 in the infection process. They are expressed in expanding lesions on potato leaves and during in vitro growth, with the highest transcript levels in germinating cysts. When expressed in planta in the presence of the silencing suppressor P19, all three elicited a local cell death response that was visible at the microscopic level as autofluorescence and strongly boosted in the presence of calcium. Moreover, inoculation of leaves expressing the small PLD-like genes resulted in increased lesion growth and greater numbers of sporangia, but this was abolished when mutated PLD-like genes were expressed with non-functional PLD catalytic motifs. These results show that the three small PLD-likes are catalytically active and suggest that their enzymatic activity is required for the promotion of virulence, possibly by executing membrane modifications to support the growth of P. infestans in the host.

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KW - calcium

KW - late blight disease

KW - oomycete

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KW - phospholipids

KW - signal peptide

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M3 - Article

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T2 - Molecular Plant Pathology

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