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Signatures of adaptation to a monocot host in the plant-parasitic cyst nematode Heterodera sacchari

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Signatures of adaptation to a monocot host in the plant-parasitic cyst nematode Heterodera sacchari. / Pokhare, Somnath S.; Thorpe, Peter ; Hedley, Pete; Morris, Jennifer; Habash, Samer S.; Elashry, Abdelnaser; Eves-van den Akker, Sebastian; Grundler, Florian M. W.; Jones, John.

In: The Plant Journal, Vol. 103, No. 4, 17.08.2020, p. 1263-1274.

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Pokhare, SS, Thorpe, P, Hedley, P, Morris, J, Habash, SS, Elashry, A, Eves-van den Akker, S, Grundler, FMW & Jones, J 2020, 'Signatures of adaptation to a monocot host in the plant-parasitic cyst nematode Heterodera sacchari', The Plant Journal, vol. 103, no. 4, pp. 1263-1274. https://doi.org/10.1111/tpj.14910

APA

Pokhare, S. S., Thorpe, P., Hedley, P., Morris, J., Habash, S. S., Elashry, A., Eves-van den Akker, S., Grundler, F. M. W., & Jones, J. (2020). Signatures of adaptation to a monocot host in the plant-parasitic cyst nematode Heterodera sacchari. The Plant Journal, 103(4), 1263-1274. https://doi.org/10.1111/tpj.14910

Vancouver

Pokhare SS, Thorpe P, Hedley P, Morris J, Habash SS, Elashry A et al. Signatures of adaptation to a monocot host in the plant-parasitic cyst nematode Heterodera sacchari. The Plant Journal. 2020 Aug 17;103(4):1263-1274. https://doi.org/10.1111/tpj.14910

Author

Pokhare, Somnath S. ; Thorpe, Peter ; Hedley, Pete ; Morris, Jennifer ; Habash, Samer S. ; Elashry, Abdelnaser ; Eves-van den Akker, Sebastian ; Grundler, Florian M. W. ; Jones, John. / Signatures of adaptation to a monocot host in the plant-parasitic cyst nematode Heterodera sacchari. In: The Plant Journal. 2020 ; Vol. 103, No. 4. pp. 1263-1274.

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@article{3d49e0fc02a44307bbc7a15e1527312b,
title = "Signatures of adaptation to a monocot host in the plant-parasitic cyst nematode Heterodera sacchari",
abstract = "Interactions between plant‐parasitic nematodes and their hosts are mediated by effectors, i.e. secreted proteins that manipulate the plant to the benefit of the pathogen. To understand the role of effectors in host adaptation in nematodes, we analysed the transcriptome of Heterodera sacchari , a cyst nematode parasite of rice (Oryza sativa ) and sugarcane (Saccharum officinarum ). A multi‐gene phylogenetic analysis showed that H. sacchari and the cereal cyst nematode Heterodera avenae share a common evolutionary origin and that they evolved to parasitise monocot plants from a common dicot‐parasitic ancestor. We compared the effector repertoires of H. sacchari with those of the dicot parasites Heterodera glycines and Globodera rostochiensis to understand the consequences of this transition. While, in general, effector repertoires are similar between the species, comparing effectors and non‐effectors of H. sacchari and G. rostochiensis shows that effectors have accumulated more mutations than non‐effectors. Although most effectors show conserved spatiotemporal expression profiles and likely function, some H. sacchari effectors are adapted to monocots. This is exemplified by the plant‐peptide hormone mimics, the CLAVATA3/EMBRYO SURROUNDING REGION‐like (CLE) effectors. Peptide hormones encoded by H. sacchari CLE effectors are more similar to those from rice than those from other plants, or those from other plant‐parasitic nematodes. We experimentally validated the functional significance of these observations by demonstrating that CLE peptides encoded by H. sacchari induce a short root phenotype in rice, whereas those from a related dicot parasite do not. These data provide a functional example of effector evolution that co‐occurred with the transition from a dicot‐parasitic to a monocot‐parasitic lifestyle.",
keywords = "Peptide hormone mimics, Effectors, Heterodera sacchari, Transcriptomics",
author = "Pokhare, {Somnath S.} and Peter Thorpe and Pete Hedley and Jennifer Morris and Habash, {Samer S.} and Abdelnaser Elashry and {Eves-van den Akker}, Sebastian and Grundler, {Florian M. W.} and John Jones",
note = "Somnath Pokhare was supported by a fellowship provided by the Indian Council of Agricultural Research (ICAR), Government of India. This work was also supported by Royal Society International Exchanges award number IE150670 and by the Rural and Environmental Science and Analytical Services Division of the Scottish Government. SEvdA is supported by Biotechnology and Biological Sciences Research Council grants BB/R011311/1 and BB/S006397/1. This work benefited from interactions funded through COST Action FA1208. The authors thank Dr Danny Coyne (IITA) for providing the starter culture of the H. sacchari population used for this work. Bioinformatics and Computational Biology analyses were supported by the University of St Andrews Bioinformatics Unit which is funded by a Wellcome Trust ISSF award [grant 105621/Z/14/Z].",
year = "2020",
month = aug,
day = "17",
doi = "10.1111/tpj.14910",
language = "English",
volume = "103",
pages = "1263--1274",
journal = "The Plant Journal",
issn = "0960-7412",
publisher = "Wiley-Blackwell",
number = "4",

}

RIS (suitable for import to EndNote) - Download

TY - JOUR

T1 - Signatures of adaptation to a monocot host in the plant-parasitic cyst nematode Heterodera sacchari

AU - Pokhare, Somnath S.

AU - Thorpe, Peter

AU - Hedley, Pete

AU - Morris, Jennifer

AU - Habash, Samer S.

AU - Elashry, Abdelnaser

AU - Eves-van den Akker, Sebastian

AU - Grundler, Florian M. W.

AU - Jones, John

N1 - Somnath Pokhare was supported by a fellowship provided by the Indian Council of Agricultural Research (ICAR), Government of India. This work was also supported by Royal Society International Exchanges award number IE150670 and by the Rural and Environmental Science and Analytical Services Division of the Scottish Government. SEvdA is supported by Biotechnology and Biological Sciences Research Council grants BB/R011311/1 and BB/S006397/1. This work benefited from interactions funded through COST Action FA1208. The authors thank Dr Danny Coyne (IITA) for providing the starter culture of the H. sacchari population used for this work. Bioinformatics and Computational Biology analyses were supported by the University of St Andrews Bioinformatics Unit which is funded by a Wellcome Trust ISSF award [grant 105621/Z/14/Z].

PY - 2020/8/17

Y1 - 2020/8/17

N2 - Interactions between plant‐parasitic nematodes and their hosts are mediated by effectors, i.e. secreted proteins that manipulate the plant to the benefit of the pathogen. To understand the role of effectors in host adaptation in nematodes, we analysed the transcriptome of Heterodera sacchari , a cyst nematode parasite of rice (Oryza sativa ) and sugarcane (Saccharum officinarum ). A multi‐gene phylogenetic analysis showed that H. sacchari and the cereal cyst nematode Heterodera avenae share a common evolutionary origin and that they evolved to parasitise monocot plants from a common dicot‐parasitic ancestor. We compared the effector repertoires of H. sacchari with those of the dicot parasites Heterodera glycines and Globodera rostochiensis to understand the consequences of this transition. While, in general, effector repertoires are similar between the species, comparing effectors and non‐effectors of H. sacchari and G. rostochiensis shows that effectors have accumulated more mutations than non‐effectors. Although most effectors show conserved spatiotemporal expression profiles and likely function, some H. sacchari effectors are adapted to monocots. This is exemplified by the plant‐peptide hormone mimics, the CLAVATA3/EMBRYO SURROUNDING REGION‐like (CLE) effectors. Peptide hormones encoded by H. sacchari CLE effectors are more similar to those from rice than those from other plants, or those from other plant‐parasitic nematodes. We experimentally validated the functional significance of these observations by demonstrating that CLE peptides encoded by H. sacchari induce a short root phenotype in rice, whereas those from a related dicot parasite do not. These data provide a functional example of effector evolution that co‐occurred with the transition from a dicot‐parasitic to a monocot‐parasitic lifestyle.

AB - Interactions between plant‐parasitic nematodes and their hosts are mediated by effectors, i.e. secreted proteins that manipulate the plant to the benefit of the pathogen. To understand the role of effectors in host adaptation in nematodes, we analysed the transcriptome of Heterodera sacchari , a cyst nematode parasite of rice (Oryza sativa ) and sugarcane (Saccharum officinarum ). A multi‐gene phylogenetic analysis showed that H. sacchari and the cereal cyst nematode Heterodera avenae share a common evolutionary origin and that they evolved to parasitise monocot plants from a common dicot‐parasitic ancestor. We compared the effector repertoires of H. sacchari with those of the dicot parasites Heterodera glycines and Globodera rostochiensis to understand the consequences of this transition. While, in general, effector repertoires are similar between the species, comparing effectors and non‐effectors of H. sacchari and G. rostochiensis shows that effectors have accumulated more mutations than non‐effectors. Although most effectors show conserved spatiotemporal expression profiles and likely function, some H. sacchari effectors are adapted to monocots. This is exemplified by the plant‐peptide hormone mimics, the CLAVATA3/EMBRYO SURROUNDING REGION‐like (CLE) effectors. Peptide hormones encoded by H. sacchari CLE effectors are more similar to those from rice than those from other plants, or those from other plant‐parasitic nematodes. We experimentally validated the functional significance of these observations by demonstrating that CLE peptides encoded by H. sacchari induce a short root phenotype in rice, whereas those from a related dicot parasite do not. These data provide a functional example of effector evolution that co‐occurred with the transition from a dicot‐parasitic to a monocot‐parasitic lifestyle.

KW - Peptide hormone mimics

KW - Effectors

KW - Heterodera sacchari

KW - Transcriptomics

U2 - 10.1111/tpj.14910

DO - 10.1111/tpj.14910

M3 - Article

VL - 103

SP - 1263

EP - 1274

JO - The Plant Journal

JF - The Plant Journal

SN - 0960-7412

IS - 4

ER -

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