The genome and lifestage-specific transcriptomes of a plant-parasitic nematode and its host reveal susceptibility genes involved in trans-kingdom synthesis of vitamin B5

Shahid Siddique; Zoran S. Radakovic; Clarissa Hiltl; Clement Pellegrin; Thomas J. Baum; Helen Beasley; Andrew F. Bent; Oliver Chitambo; Divykriti Chopra; Etienne G. J. Danchin; Eric Grenier; Samer S. Habash; M. Shamim Hasan; Johannes Helder; Tarek Hewezi; Julia Holbein; Martijn Holterman; Sławomir Janakowski; Georgios D. Koutsovoulos; Olaf P. Kranse; Jose L. Lozano-Torres; Tom R. Maier; Rick E. Masonbrink; Badou Mendy; Esther Riemer; Mirosław Sobczak; Unnati Sonawala; Mark G. Sterken; Peter Thorpe; Joris J. M. van Steenbrugge; Nageena Zahid; Florian Grundler; Sebastian Eves-van den Akker

doi:10.1038/s41467-022-33769-w

The genome and lifestage-specific transcriptomes of a plant-parasitic nematode and its host reveal susceptibility genes involved in trans-kingdom synthesis of vitamin B5

Shahid Siddique, Zoran S. Radakovic, Clarissa Hiltl, Clement Pellegrin, Thomas J. Baum, Helen Beasley, Andrew F. Bent, Oliver Chitambo, Divykriti Chopra, Etienne G. J. Danchin, Eric Grenier, Samer S. Habash, M. Shamim Hasan, Johannes Helder, Tarek Hewezi, Julia Holbein, Martijn Holterman, Sławomir Janakowski, Georgios D. Koutsovoulos, Olaf P. KranseJose L. Lozano-Torres, Tom R. Maier, Rick E. Masonbrink, Badou Mendy, Esther Riemer, Mirosław Sobczak, Unnati Sonawala, Mark G. Sterken, Peter Thorpe, Joris J. M. van Steenbrugge, Nageena Zahid, Florian Grundler^*, Sebastian Eves-van den Akker^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

27 Citations (Scopus)

6 Downloads (Pure)

Abstract

Plant-parasitic nematodes are a major threat to crop production in all agricultural systems. The scarcity of classical resistance genes highlights a pressing need to find new ways to develop nematode-resistant germplasm. Here, we sequence and assemble a high-quality phased genome of the model cyst nematode Heterodera schachtii to provide a platform for the first system-wide dual analysis of host and parasite gene expression over time, covering all major parasitism stages. Analysis of the hologenome of the plant-nematode infection site identified metabolic pathways that were incomplete in the parasite but complemented by the host. Using a combination of bioinformatic, genetic, and biochemical approaches, we show that a highly atypical completion of vitamin B5 biosynthesis by the parasitic animal, putatively enabled by a horizontal gene transfer from a bacterium, is required for full pathogenicity. Knockout of either plant-encoded or now nematode-encoded steps in the pathway significantly reduces parasitic success. Our experiments establish a reference for cyst nematodes, further our understanding of the evolution of plant-parasitism by nematodes, and show that congruent differential expression of metabolic pathways in the infection hologenome represents a new way to find nematode susceptibility genes. The approach identifies genome-editing-amenable targets for future development of nematode-resistant crops.

Original language	English
Article number	6190
Number of pages	19
Journal	Nature Communications
Volume	13
DOIs	https://doi.org/10.1038/s41467-022-33769-w
Publication status	Published - 19 Oct 2022

Access to Document

10.1038/s41467-022-33769-wLicence: CC BY

Siddique_2022_NC_Genome-lifestyle_CC
Copyright © The Author(s) 2022. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
Final published version, 3.83 MBLicence: CC BY

ISSF Funding Mar2021 - P Thorpe: ISSF Funding March 2021
Thorpe, P. J. (PI)
The Wellcome Trust
1/04/21 → 31/03/22
Project: Standard
Institutional Strategic Support Fund 2: ISSF 2
Naismith, J. (PI)
The Wellcome Trust
1/11/14 → 31/10/16
Project: Standard

The genome and lifestage-specific transcriptomes of a plant-parasitic nematode and its host reveal susceptibility genes involved in trans-kingdom synthesis of vitamin B5 (dataset)
Thorpe, P. J. (Creator), NCBI GenBank, 2022
https://www.ncbi.nlm.nih.gov/nuccore/JAHGVF000000000.1 and one more link, https://www.ncbi.nlm.nih.gov/bioproject/PRJNA722882 (show fewer)
Dataset
The genome and lifestage-specific transcriptomes of a plant-parasitic nematode and its host reveal susceptibility genes involved in trans-kingdom synthesis of vitamin B5 (code)
Thorpe, P. J. (Creator), GitHub, 2022
https://github.com/sebastianevda/H.schachtii_genome and 2 more links, https://github.com/OlafKranse/ALT_caller_for_pilon, https://github.com/peterthorpe5/Heterodera_schachtii_genome_assembly (show fewer)
Dataset: Software

Cite this

Siddique, S., Radakovic, Z. S., Hiltl, C., Pellegrin, C., Baum, T. J., Beasley, H., Bent, A. F., Chitambo, O., Chopra, D., Danchin, E. G. J., Grenier, E., Habash, S. S., Hasan, M. S., Helder, J., Hewezi, T., Holbein, J., Holterman, M., Janakowski, S., Koutsovoulos, G. D., ... Eves-van den Akker, S. (2022). The genome and lifestage-specific transcriptomes of a plant-parasitic nematode and its host reveal susceptibility genes involved in trans-kingdom synthesis of vitamin B5. Nature Communications, 13, Article 6190. https://doi.org/10.1038/s41467-022-33769-w

@article{477743ff40b3474096aae6d01851498c,

title = "The genome and lifestage-specific transcriptomes of a plant-parasitic nematode and its host reveal susceptibility genes involved in trans-kingdom synthesis of vitamin B5",

abstract = "Plant-parasitic nematodes are a major threat to crop production in all agricultural systems. The scarcity of classical resistance genes highlights a pressing need to find new ways to develop nematode-resistant germplasm. Here, we sequence and assemble a high-quality phased genome of the model cyst nematode Heterodera schachtii to provide a platform for the first system-wide dual analysis of host and parasite gene expression over time, covering all major parasitism stages. Analysis of the hologenome of the plant-nematode infection site identified metabolic pathways that were incomplete in the parasite but complemented by the host. Using a combination of bioinformatic, genetic, and biochemical approaches, we show that a highly atypical completion of vitamin B5 biosynthesis by the parasitic animal, putatively enabled by a horizontal gene transfer from a bacterium, is required for full pathogenicity. Knockout of either plant-encoded or now nematode-encoded steps in the pathway significantly reduces parasitic success. Our experiments establish a reference for cyst nematodes, further our understanding of the evolution of plant-parasitism by nematodes, and show that congruent differential expression of metabolic pathways in the infection hologenome represents a new way to find nematode susceptibility genes. The approach identifies genome-editing-amenable targets for future development of nematode-resistant crops.",

author = "Shahid Siddique and Radakovic, {Zoran S.} and Clarissa Hiltl and Clement Pellegrin and Baum, {Thomas J.} and Helen Beasley and Bent, {Andrew F.} and Oliver Chitambo and Divykriti Chopra and Danchin, {Etienne G. J.} and Eric Grenier and Habash, {Samer S.} and Hasan, {M. Shamim} and Johannes Helder and Tarek Hewezi and Julia Holbein and Martijn Holterman and S{\l}awomir Janakowski and Koutsovoulos, {Georgios D.} and Kranse, {Olaf P.} and Lozano-Torres, {Jose L.} and Maier, {Tom R.} and Masonbrink, {Rick E.} and Badou Mendy and Esther Riemer and Miros{\l}aw Sobczak and Unnati Sonawala and Sterken, {Mark G.} and Peter Thorpe and {van Steenbrugge}, {Joris J. M.} and Nageena Zahid and Florian Grundler and {Eves-van den Akker}, Sebastian",

note = "Funding: The work at University of Bonn was supported by the Federal Ministry of Education and Research, Germany (BMBF) (Grant 031A326B to FMWG) and by the German Research Foundation (DFG) (Grant SI1739/3–1 and SI1739/5-1 to S.S.). M.S.H. was supported by a fellowship from German Academic Exchange Service (DAAD; Grant 91525252)). The work at University of California Davis was supported by the National Science Foundation (NSF) (Grant IOS-1954929) and National Institute of Food and Agriculture (NIFA) (Grant 20-3994). Work on plant-parasitic nematodes at the University of Cambridge is supported by DEFRA license 125034/359149/3, and funded by BBSRC grants BB/R011311/1, BB/N021908/1, and BB/S006397/1. C.P. received funding from the European Union{\textquoteright}s Horizon 2020 research and innovation programme under grant agreement no. 882941. P.T. was supported by the University of St Andrews Bioinformatics Unit, funded by Wellcome Trust ISSF awards 105621/Z/14/Z and 204821/Z/16/Z. Work at Iowa State University was supported by Hatch and State of Iowa funds and a grant from the North Central Soybean Research Program. J.L.L.-T. was supported by an NWO domain Applied and Engineering Sciences VENI grant (14250) and a Wageningen University & Research Experimental Plant Sciences strategic funds grant. M.G.S. was supported by NWO domain Applied and Engineering Sciences VENI grant (17282).",

year = "2022",

month = oct,

day = "19",

doi = "10.1038/s41467-022-33769-w",

language = "English",

volume = "13",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Nature publishing group",

}

Siddique, S, Radakovic, ZS, Hiltl, C, Pellegrin, C, Baum, TJ, Beasley, H, Bent, AF, Chitambo, O, Chopra, D, Danchin, EGJ, Grenier, E, Habash, SS, Hasan, MS, Helder, J, Hewezi, T, Holbein, J, Holterman, M, Janakowski, S, Koutsovoulos, GD, Kranse, OP, Lozano-Torres, JL, Maier, TR, Masonbrink, RE, Mendy, B, Riemer, E, Sobczak, M, Sonawala, U, Sterken, MG, Thorpe, P, van Steenbrugge, JJM, Zahid, N, Grundler, F & Eves-van den Akker, S 2022, 'The genome and lifestage-specific transcriptomes of a plant-parasitic nematode and its host reveal susceptibility genes involved in trans-kingdom synthesis of vitamin B5', Nature Communications, vol. 13, 6190. https://doi.org/10.1038/s41467-022-33769-w

TY - JOUR

T1 - The genome and lifestage-specific transcriptomes of a plant-parasitic nematode and its host reveal susceptibility genes involved in trans-kingdom synthesis of vitamin B5

AU - Siddique, Shahid

AU - Radakovic, Zoran S.

AU - Hiltl, Clarissa

AU - Pellegrin, Clement

AU - Baum, Thomas J.

AU - Beasley, Helen

AU - Bent, Andrew F.

AU - Chitambo, Oliver

AU - Chopra, Divykriti

AU - Danchin, Etienne G. J.

AU - Grenier, Eric

AU - Habash, Samer S.

AU - Hasan, M. Shamim

AU - Helder, Johannes

AU - Hewezi, Tarek

AU - Holbein, Julia

AU - Holterman, Martijn

AU - Janakowski, Sławomir

AU - Koutsovoulos, Georgios D.

AU - Kranse, Olaf P.

AU - Lozano-Torres, Jose L.

AU - Maier, Tom R.

AU - Masonbrink, Rick E.

AU - Mendy, Badou

AU - Riemer, Esther

AU - Sobczak, Mirosław

AU - Sonawala, Unnati

AU - Sterken, Mark G.

AU - Thorpe, Peter

AU - van Steenbrugge, Joris J. M.

AU - Zahid, Nageena

AU - Grundler, Florian

AU - Eves-van den Akker, Sebastian

N1 - Funding: The work at University of Bonn was supported by the Federal Ministry of Education and Research, Germany (BMBF) (Grant 031A326B to FMWG) and by the German Research Foundation (DFG) (Grant SI1739/3–1 and SI1739/5-1 to S.S.). M.S.H. was supported by a fellowship from German Academic Exchange Service (DAAD; Grant 91525252)). The work at University of California Davis was supported by the National Science Foundation (NSF) (Grant IOS-1954929) and National Institute of Food and Agriculture (NIFA) (Grant 20-3994). Work on plant-parasitic nematodes at the University of Cambridge is supported by DEFRA license 125034/359149/3, and funded by BBSRC grants BB/R011311/1, BB/N021908/1, and BB/S006397/1. C.P. received funding from the European Union’s Horizon 2020 research and innovation programme under grant agreement no. 882941. P.T. was supported by the University of St Andrews Bioinformatics Unit, funded by Wellcome Trust ISSF awards 105621/Z/14/Z and 204821/Z/16/Z. Work at Iowa State University was supported by Hatch and State of Iowa funds and a grant from the North Central Soybean Research Program. J.L.L.-T. was supported by an NWO domain Applied and Engineering Sciences VENI grant (14250) and a Wageningen University & Research Experimental Plant Sciences strategic funds grant. M.G.S. was supported by NWO domain Applied and Engineering Sciences VENI grant (17282).

PY - 2022/10/19

Y1 - 2022/10/19

N2 - Plant-parasitic nematodes are a major threat to crop production in all agricultural systems. The scarcity of classical resistance genes highlights a pressing need to find new ways to develop nematode-resistant germplasm. Here, we sequence and assemble a high-quality phased genome of the model cyst nematode Heterodera schachtii to provide a platform for the first system-wide dual analysis of host and parasite gene expression over time, covering all major parasitism stages. Analysis of the hologenome of the plant-nematode infection site identified metabolic pathways that were incomplete in the parasite but complemented by the host. Using a combination of bioinformatic, genetic, and biochemical approaches, we show that a highly atypical completion of vitamin B5 biosynthesis by the parasitic animal, putatively enabled by a horizontal gene transfer from a bacterium, is required for full pathogenicity. Knockout of either plant-encoded or now nematode-encoded steps in the pathway significantly reduces parasitic success. Our experiments establish a reference for cyst nematodes, further our understanding of the evolution of plant-parasitism by nematodes, and show that congruent differential expression of metabolic pathways in the infection hologenome represents a new way to find nematode susceptibility genes. The approach identifies genome-editing-amenable targets for future development of nematode-resistant crops.

AB - Plant-parasitic nematodes are a major threat to crop production in all agricultural systems. The scarcity of classical resistance genes highlights a pressing need to find new ways to develop nematode-resistant germplasm. Here, we sequence and assemble a high-quality phased genome of the model cyst nematode Heterodera schachtii to provide a platform for the first system-wide dual analysis of host and parasite gene expression over time, covering all major parasitism stages. Analysis of the hologenome of the plant-nematode infection site identified metabolic pathways that were incomplete in the parasite but complemented by the host. Using a combination of bioinformatic, genetic, and biochemical approaches, we show that a highly atypical completion of vitamin B5 biosynthesis by the parasitic animal, putatively enabled by a horizontal gene transfer from a bacterium, is required for full pathogenicity. Knockout of either plant-encoded or now nematode-encoded steps in the pathway significantly reduces parasitic success. Our experiments establish a reference for cyst nematodes, further our understanding of the evolution of plant-parasitism by nematodes, and show that congruent differential expression of metabolic pathways in the infection hologenome represents a new way to find nematode susceptibility genes. The approach identifies genome-editing-amenable targets for future development of nematode-resistant crops.

U2 - 10.1038/s41467-022-33769-w

DO - 10.1038/s41467-022-33769-w

M3 - Article

SN - 2041-1723

VL - 13

JO - Nature Communications

JF - Nature Communications

M1 - 6190

ER -

The genome and lifestage-specific transcriptomes of a plant-parasitic nematode and its host reveal susceptibility genes involved in trans-kingdom synthesis of vitamin B5

Abstract

Access to Document

Fingerprint

Projects

ISSF Funding Mar2021 - P Thorpe: ISSF Funding March 2021

Institutional Strategic Support Fund 2: ISSF 2

Datasets

The genome and lifestage-specific transcriptomes of a plant-parasitic nematode and its host reveal susceptibility genes involved in trans-kingdom synthesis of vitamin B5 (dataset)

The genome and lifestage-specific transcriptomes of a plant-parasitic nematode and its host reveal susceptibility genes involved in trans-kingdom synthesis of vitamin B5 (code)

Cite this