A Plasmodium-like virulence effector of the soybean cyst nematode suppresses plant innate immunity

Jason B. Noon, Mingsheng Qi, Danielle N. Sill, Usha Muppirala, Sebastian Eves-van den Akker, Thomas R. Maier, Drena Dobbs, Melissa G. Mitchum, Tarek Hewezi, Thomas J. Baum (Lead / Corresponding author)

Research output: Contribution to journalArticle

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Abstract

Heterodera glycines, the soybean cyst nematode, delivers effector proteins into soybean roots to initiate and maintain an obligate parasitic relationship. HgGLAND18 encodes a candidate H. glycines effector and is expressed throughout the infection process. We used a combination of molecular, genetic, bioinformatic and phylogenetic analyses to determine the role of HgGLAND18 during H. glycines infection. HgGLAND18 is necessary for pathogenicity in compatible interactions with soybean. The encoded effector strongly suppresses both basal and hypersensitive cell death innate immune responses, and immunosuppression requires the presence and coordination between multiple protein domains. The N-terminal domain in HgGLAND18 contains unique sequence similarity to domains of an immunosuppressive effector of Plasmodium spp., the malaria parasites. The Plasmodium effector domains functionally complement the loss of the N-terminal domain from HgGLAND18. In-depth sequence searches and phylogenetic analyses demonstrate convergent evolution between effectors from divergent parasites of plants and animals as the cause of sequence and functional similarity.

Original languageEnglish
Pages (from-to)444-460
Number of pages17
JournalNew Phytologist
Volume212
Issue number2
Early online date6 Jun 2016
DOIs
Publication statusPublished - Oct 2016

Fingerprint

Plant Immunity
Heterodera glycines
Plasmodium
Soybeans
Innate Immunity
Glycine
Virulence
Cysts
virulence
Parasites
Plasmodium malariae
Soybean Proteins
Immunosuppressive Agents
Infection
Computational Biology
parasites
immunosuppressive agents
Immunosuppression
convergent evolution
Molecular Biology

Keywords

  • Plasmodium
  • Circumsporozoite protein (CSP)
  • Convergent evolution
  • GLAND18
  • Immunity
  • Malaria
  • Pathogenicity
  • Soybean cyst nematode

Cite this

Noon, J. B., Qi, M., Sill, D. N., Muppirala, U., Eves-van den Akker, S., Maier, T. R., ... Baum, T. J. (2016). A Plasmodium-like virulence effector of the soybean cyst nematode suppresses plant innate immunity. New Phytologist, 212(2), 444-460. https://doi.org/10.1111/nph.14047
Noon, Jason B. ; Qi, Mingsheng ; Sill, Danielle N. ; Muppirala, Usha ; Eves-van den Akker, Sebastian ; Maier, Thomas R. ; Dobbs, Drena ; Mitchum, Melissa G. ; Hewezi, Tarek ; Baum, Thomas J. / A Plasmodium-like virulence effector of the soybean cyst nematode suppresses plant innate immunity. In: New Phytologist. 2016 ; Vol. 212, No. 2. pp. 444-460.
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abstract = "Heterodera glycines, the soybean cyst nematode, delivers effector proteins into soybean roots to initiate and maintain an obligate parasitic relationship. HgGLAND18 encodes a candidate H. glycines effector and is expressed throughout the infection process. We used a combination of molecular, genetic, bioinformatic and phylogenetic analyses to determine the role of HgGLAND18 during H. glycines infection. HgGLAND18 is necessary for pathogenicity in compatible interactions with soybean. The encoded effector strongly suppresses both basal and hypersensitive cell death innate immune responses, and immunosuppression requires the presence and coordination between multiple protein domains. The N-terminal domain in HgGLAND18 contains unique sequence similarity to domains of an immunosuppressive effector of Plasmodium spp., the malaria parasites. The Plasmodium effector domains functionally complement the loss of the N-terminal domain from HgGLAND18. In-depth sequence searches and phylogenetic analyses demonstrate convergent evolution between effectors from divergent parasites of plants and animals as the cause of sequence and functional similarity.",
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Noon, JB, Qi, M, Sill, DN, Muppirala, U, Eves-van den Akker, S, Maier, TR, Dobbs, D, Mitchum, MG, Hewezi, T & Baum, TJ 2016, 'A Plasmodium-like virulence effector of the soybean cyst nematode suppresses plant innate immunity', New Phytologist, vol. 212, no. 2, pp. 444-460. https://doi.org/10.1111/nph.14047

A Plasmodium-like virulence effector of the soybean cyst nematode suppresses plant innate immunity. / Noon, Jason B.; Qi, Mingsheng; Sill, Danielle N.; Muppirala, Usha; Eves-van den Akker, Sebastian; Maier, Thomas R.; Dobbs, Drena; Mitchum, Melissa G.; Hewezi, Tarek; Baum, Thomas J. (Lead / Corresponding author).

In: New Phytologist, Vol. 212, No. 2, 10.2016, p. 444-460.

Research output: Contribution to journalArticle

TY - JOUR

T1 - A Plasmodium-like virulence effector of the soybean cyst nematode suppresses plant innate immunity

AU - Noon, Jason B.

AU - Qi, Mingsheng

AU - Sill, Danielle N.

AU - Muppirala, Usha

AU - Eves-van den Akker, Sebastian

AU - Maier, Thomas R.

AU - Dobbs, Drena

AU - Mitchum, Melissa G.

AU - Hewezi, Tarek

AU - Baum, Thomas J.

N1 - Funding: Hatch Act and State of Iowa; Iowa Soybean Association; USDA-NIFA-AFRI. Grant Number: 2015-67013-23511.

PY - 2016/10

Y1 - 2016/10

N2 - Heterodera glycines, the soybean cyst nematode, delivers effector proteins into soybean roots to initiate and maintain an obligate parasitic relationship. HgGLAND18 encodes a candidate H. glycines effector and is expressed throughout the infection process. We used a combination of molecular, genetic, bioinformatic and phylogenetic analyses to determine the role of HgGLAND18 during H. glycines infection. HgGLAND18 is necessary for pathogenicity in compatible interactions with soybean. The encoded effector strongly suppresses both basal and hypersensitive cell death innate immune responses, and immunosuppression requires the presence and coordination between multiple protein domains. The N-terminal domain in HgGLAND18 contains unique sequence similarity to domains of an immunosuppressive effector of Plasmodium spp., the malaria parasites. The Plasmodium effector domains functionally complement the loss of the N-terminal domain from HgGLAND18. In-depth sequence searches and phylogenetic analyses demonstrate convergent evolution between effectors from divergent parasites of plants and animals as the cause of sequence and functional similarity.

AB - Heterodera glycines, the soybean cyst nematode, delivers effector proteins into soybean roots to initiate and maintain an obligate parasitic relationship. HgGLAND18 encodes a candidate H. glycines effector and is expressed throughout the infection process. We used a combination of molecular, genetic, bioinformatic and phylogenetic analyses to determine the role of HgGLAND18 during H. glycines infection. HgGLAND18 is necessary for pathogenicity in compatible interactions with soybean. The encoded effector strongly suppresses both basal and hypersensitive cell death innate immune responses, and immunosuppression requires the presence and coordination between multiple protein domains. The N-terminal domain in HgGLAND18 contains unique sequence similarity to domains of an immunosuppressive effector of Plasmodium spp., the malaria parasites. The Plasmodium effector domains functionally complement the loss of the N-terminal domain from HgGLAND18. In-depth sequence searches and phylogenetic analyses demonstrate convergent evolution between effectors from divergent parasites of plants and animals as the cause of sequence and functional similarity.

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KW - Circumsporozoite protein (CSP)

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KW - GLAND18

KW - Immunity

KW - Malaria

KW - Pathogenicity

KW - Soybean cyst nematode

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DO - 10.1111/nph.14047

M3 - Article

VL - 212

SP - 444

EP - 460

JO - New Phytologist

JF - New Phytologist

SN - 0028-646X

IS - 2

ER -

Noon JB, Qi M, Sill DN, Muppirala U, Eves-van den Akker S, Maier TR et al. A Plasmodium-like virulence effector of the soybean cyst nematode suppresses plant innate immunity. New Phytologist. 2016 Oct;212(2):444-460. https://doi.org/10.1111/nph.14047