Clade 5 aspartic proteases of Phytophthora infestans are virulence factors implied in RXLR effector cleavage

Charikleia Schoina, Natalie Verbeek-de Kruif, Francine Govers, Klaas Bouwmeester

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Late blight caused by the oomycete pathogen Phytophthora infestans is one of the most destructive diseases in potato cultivation. To successfully colonize its host, P. infestans secretes a suite of effector proteins that undermine plant immunity, many of which contain a conserved N-terminal RXLR motif that strongly resembles the host targeting motif in effectors of the malaria parasite Plasmodium falciparum. In this study, we focus on three P. infestans clade 5 aspartic proteases (PiAPs) that are homologous to Plasmepsin V (PMV), a Pl. falciparum AP responsible for cleaving effectors prior to translocation into red blood cells. Malaria parasites expressing mutated PMV are impaired in effector translocation and are less virulent. To determine whether clade 5 PiAPs play similar roles in virulence, we characterized P. infestans transformants with either reduced or enhanced PiAP expression levels. Phytophthora infestans transformants with altered PiAP10 or PiAP12 expression were found to be impaired in mycelial growth and sporangia production, and are hampered in their virulence on potato leaves. This was not observed in PiAP11 transformants. Activity assays showed that PiAP10 and PiAP12 possess moderate protease activity, and can potentially cleave the RXLR effector PiAVR4, but not a PiAVR4 version with a mutated RXLR motif. These findings imply that P. infestans APs function in the proteolytic cleavage of RXLR effectors, and warrant further investigation to verify and confirm the role of clade 5 PiAPs in effector processing.

Original languageEnglish
Pages (from-to)17-29
JournalEuropean Journal of Plant Pathology
Volume154
Issue number1
Early online date23 Mar 2019
DOIs
Publication statusPublished - May 2019

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aspartic proteinases
Phytophthora infestans
virulence
plasmepsin
Plasmodium falciparum
malaria
potatoes
parasites
Oomycetes
sporangia
plant proteins
erythrocytes
proteinases
immunity

Keywords

  • Enzymatic activity
  • Late blight disease
  • Pathogenicity
  • Plant-pathogen interactions
  • Proteolysis

Cite this

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title = "Clade 5 aspartic proteases of Phytophthora infestans are virulence factors implied in RXLR effector cleavage",
abstract = "Late blight caused by the oomycete pathogen Phytophthora infestans is one of the most destructive diseases in potato cultivation. To successfully colonize its host, P. infestans secretes a suite of effector proteins that undermine plant immunity, many of which contain a conserved N-terminal RXLR motif that strongly resembles the host targeting motif in effectors of the malaria parasite Plasmodium falciparum. In this study, we focus on three P. infestans clade 5 aspartic proteases (PiAPs) that are homologous to Plasmepsin V (PMV), a Pl. falciparum AP responsible for cleaving effectors prior to translocation into red blood cells. Malaria parasites expressing mutated PMV are impaired in effector translocation and are less virulent. To determine whether clade 5 PiAPs play similar roles in virulence, we characterized P. infestans transformants with either reduced or enhanced PiAP expression levels. Phytophthora infestans transformants with altered PiAP10 or PiAP12 expression were found to be impaired in mycelial growth and sporangia production, and are hampered in their virulence on potato leaves. This was not observed in PiAP11 transformants. Activity assays showed that PiAP10 and PiAP12 possess moderate protease activity, and can potentially cleave the RXLR effector PiAVR4, but not a PiAVR4 version with a mutated RXLR motif. These findings imply that P. infestans APs function in the proteolytic cleavage of RXLR effectors, and warrant further investigation to verify and confirm the role of clade 5 PiAPs in effector processing.",
keywords = "Enzymatic activity, Late blight disease, Pathogenicity, Plant-pathogen interactions, Proteolysis",
author = "Charikleia Schoina and {Verbeek-de Kruif}, Natalie and Francine Govers and Klaas Bouwmeester",
year = "2019",
month = "5",
doi = "10.1007/s10658-019-01713-2",
language = "English",
volume = "154",
pages = "17--29",
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Clade 5 aspartic proteases of Phytophthora infestans are virulence factors implied in RXLR effector cleavage. / Schoina, Charikleia; Verbeek-de Kruif, Natalie; Govers, Francine; Bouwmeester, Klaas.

In: European Journal of Plant Pathology, Vol. 154, No. 1, 05.2019, p. 17-29.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Clade 5 aspartic proteases of Phytophthora infestans are virulence factors implied in RXLR effector cleavage

AU - Schoina, Charikleia

AU - Verbeek-de Kruif, Natalie

AU - Govers, Francine

AU - Bouwmeester, Klaas

PY - 2019/5

Y1 - 2019/5

N2 - Late blight caused by the oomycete pathogen Phytophthora infestans is one of the most destructive diseases in potato cultivation. To successfully colonize its host, P. infestans secretes a suite of effector proteins that undermine plant immunity, many of which contain a conserved N-terminal RXLR motif that strongly resembles the host targeting motif in effectors of the malaria parasite Plasmodium falciparum. In this study, we focus on three P. infestans clade 5 aspartic proteases (PiAPs) that are homologous to Plasmepsin V (PMV), a Pl. falciparum AP responsible for cleaving effectors prior to translocation into red blood cells. Malaria parasites expressing mutated PMV are impaired in effector translocation and are less virulent. To determine whether clade 5 PiAPs play similar roles in virulence, we characterized P. infestans transformants with either reduced or enhanced PiAP expression levels. Phytophthora infestans transformants with altered PiAP10 or PiAP12 expression were found to be impaired in mycelial growth and sporangia production, and are hampered in their virulence on potato leaves. This was not observed in PiAP11 transformants. Activity assays showed that PiAP10 and PiAP12 possess moderate protease activity, and can potentially cleave the RXLR effector PiAVR4, but not a PiAVR4 version with a mutated RXLR motif. These findings imply that P. infestans APs function in the proteolytic cleavage of RXLR effectors, and warrant further investigation to verify and confirm the role of clade 5 PiAPs in effector processing.

AB - Late blight caused by the oomycete pathogen Phytophthora infestans is one of the most destructive diseases in potato cultivation. To successfully colonize its host, P. infestans secretes a suite of effector proteins that undermine plant immunity, many of which contain a conserved N-terminal RXLR motif that strongly resembles the host targeting motif in effectors of the malaria parasite Plasmodium falciparum. In this study, we focus on three P. infestans clade 5 aspartic proteases (PiAPs) that are homologous to Plasmepsin V (PMV), a Pl. falciparum AP responsible for cleaving effectors prior to translocation into red blood cells. Malaria parasites expressing mutated PMV are impaired in effector translocation and are less virulent. To determine whether clade 5 PiAPs play similar roles in virulence, we characterized P. infestans transformants with either reduced or enhanced PiAP expression levels. Phytophthora infestans transformants with altered PiAP10 or PiAP12 expression were found to be impaired in mycelial growth and sporangia production, and are hampered in their virulence on potato leaves. This was not observed in PiAP11 transformants. Activity assays showed that PiAP10 and PiAP12 possess moderate protease activity, and can potentially cleave the RXLR effector PiAVR4, but not a PiAVR4 version with a mutated RXLR motif. These findings imply that P. infestans APs function in the proteolytic cleavage of RXLR effectors, and warrant further investigation to verify and confirm the role of clade 5 PiAPs in effector processing.

KW - Enzymatic activity

KW - Late blight disease

KW - Pathogenicity

KW - Plant-pathogen interactions

KW - Proteolysis

U2 - 10.1007/s10658-019-01713-2

DO - 10.1007/s10658-019-01713-2

M3 - Article

VL - 154

SP - 17

EP - 29

JO - European Journal of Plant Pathology

JF - European Journal of Plant Pathology

SN - 0929-1873

IS - 1

ER -