Whole-genome re-sequencing reveals the impact of the interaction of copy number variants of the rhg1 and Rhg4 genes on broad-based resistance to soybean cyst nematode

Gunvant Patil, Naoufal Lakhssassi, Jinrong Wan, Li Song, Zhou Zhou, Mariola Klepadlo, Tri D. Vuong, Adrian O. Stec, Sondus S. Kahil, Vincent Colantonio, Babu Valliyodan, J. Hollis Rice, Sarbottam Piya, Tarek Hewezi, Robert M Stupar, Khalid Meksem, Henry T. Nguyen

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

Soybean cyst nematode (SCN) is the most devastating plant-parasitic nematode. Most commercial soybean varieties with SCN resistance are derived from PI88788. Resistance derived from PI88788 is breaking down due to narrow genetic background and SCN population shift. PI88788 requires mainly the rhg1-b locus, while ‘Peking’ requires rhg1-a and Rhg4 for SCN resistance. In the present study, whole genome re-sequencing of 106 soybean lines was used to define the Rhg haplotypes and investigate their responses to the SCN HG-Types. The analysis showed a comprehensive profile of SNPs and copy number variations (CNV) at these loci. CNV of rhg1 (GmSNAP18) only contributed towards resistance in lines derived from PI88788 and ‘Cloud’. At least 5.6 copies of the PI88788-type rhg1 were required to confer SCN resistance, regardless of the Rhg4 (GmSHMT08) haplotype. However, when the GmSNAP18 copies dropped below 5.6, a ‘Peking’-type GmSHMT08 haplotype was required to ensure SCN resistance. This points to a novel mechanism of epistasis between GmSNAP18 and GmSHMT08 involving minimum requirements for copy number. The presence of more Rhg4 copies confers resistance to multiple SCN races. Moreover, transcript abundance of the GmSHMT08 in root tissue correlates with more copies of the Rhg4 locus, reinforcing SCN resistance. Finally, haplotype analysis of the GmSHMT08 and GmSNAP18 promoters inferred additional levels of the resistance mechanism. This is the first report revealing the genetic basis of broad-based resistance to SCN and providing new insight into epistasis, haplotype-compatibility, CNV, promoter variation and its impact on broad-based disease resistance in plants.

Original languageEnglish (US)
Pages (from-to)1595-1611
Number of pages17
JournalPlant Biotechnology Journal
Volume17
Issue number8
DOIs
StatePublished - Aug 1 2019

Fingerprint

Heterodera glycines
Soybeans
Cysts
Genome
genome
Genes
haplotypes
genes
Haplotypes
epistasis
loci
promoter regions
soybeans
plant parasitic nematodes
resistance mechanisms
Disease Resistance
genetic background
disease resistance
Single Nucleotide Polymorphism

Keywords

  • SCN
  • broad-based resistance
  • copy number variation
  • haplotype analysis
  • rhg1
  • soybean

Cite this

Whole-genome re-sequencing reveals the impact of the interaction of copy number variants of the rhg1 and Rhg4 genes on broad-based resistance to soybean cyst nematode. / Patil, Gunvant; Lakhssassi, Naoufal; Wan, Jinrong; Song, Li; Zhou, Zhou; Klepadlo, Mariola; Vuong, Tri D.; Stec, Adrian O.; Kahil, Sondus S.; Colantonio, Vincent; Valliyodan, Babu; Rice, J. Hollis; Piya, Sarbottam; Hewezi, Tarek; Stupar, Robert M; Meksem, Khalid; Nguyen, Henry T.

In: Plant Biotechnology Journal, Vol. 17, No. 8, 01.08.2019, p. 1595-1611.

Research output: Contribution to journalArticle

Patil, G, Lakhssassi, N, Wan, J, Song, L, Zhou, Z, Klepadlo, M, Vuong, TD, Stec, AO, Kahil, SS, Colantonio, V, Valliyodan, B, Rice, JH, Piya, S, Hewezi, T, Stupar, RM, Meksem, K & Nguyen, HT 2019, 'Whole-genome re-sequencing reveals the impact of the interaction of copy number variants of the rhg1 and Rhg4 genes on broad-based resistance to soybean cyst nematode', Plant Biotechnology Journal, vol. 17, no. 8, pp. 1595-1611. https://doi.org/10.1111/pbi.13086
Patil, Gunvant ; Lakhssassi, Naoufal ; Wan, Jinrong ; Song, Li ; Zhou, Zhou ; Klepadlo, Mariola ; Vuong, Tri D. ; Stec, Adrian O. ; Kahil, Sondus S. ; Colantonio, Vincent ; Valliyodan, Babu ; Rice, J. Hollis ; Piya, Sarbottam ; Hewezi, Tarek ; Stupar, Robert M ; Meksem, Khalid ; Nguyen, Henry T. / Whole-genome re-sequencing reveals the impact of the interaction of copy number variants of the rhg1 and Rhg4 genes on broad-based resistance to soybean cyst nematode. In: Plant Biotechnology Journal. 2019 ; Vol. 17, No. 8. pp. 1595-1611.
@article{6f801d763877485f83812ca5f36590fb,
title = "Whole-genome re-sequencing reveals the impact of the interaction of copy number variants of the rhg1 and Rhg4 genes on broad-based resistance to soybean cyst nematode",
abstract = "Soybean cyst nematode (SCN) is the most devastating plant-parasitic nematode. Most commercial soybean varieties with SCN resistance are derived from PI88788. Resistance derived from PI88788 is breaking down due to narrow genetic background and SCN population shift. PI88788 requires mainly the rhg1-b locus, while ‘Peking’ requires rhg1-a and Rhg4 for SCN resistance. In the present study, whole genome re-sequencing of 106 soybean lines was used to define the Rhg haplotypes and investigate their responses to the SCN HG-Types. The analysis showed a comprehensive profile of SNPs and copy number variations (CNV) at these loci. CNV of rhg1 (GmSNAP18) only contributed towards resistance in lines derived from PI88788 and ‘Cloud’. At least 5.6 copies of the PI88788-type rhg1 were required to confer SCN resistance, regardless of the Rhg4 (GmSHMT08) haplotype. However, when the GmSNAP18 copies dropped below 5.6, a ‘Peking’-type GmSHMT08 haplotype was required to ensure SCN resistance. This points to a novel mechanism of epistasis between GmSNAP18 and GmSHMT08 involving minimum requirements for copy number. The presence of more Rhg4 copies confers resistance to multiple SCN races. Moreover, transcript abundance of the GmSHMT08 in root tissue correlates with more copies of the Rhg4 locus, reinforcing SCN resistance. Finally, haplotype analysis of the GmSHMT08 and GmSNAP18 promoters inferred additional levels of the resistance mechanism. This is the first report revealing the genetic basis of broad-based resistance to SCN and providing new insight into epistasis, haplotype-compatibility, CNV, promoter variation and its impact on broad-based disease resistance in plants.",
keywords = "SCN, broad-based resistance, copy number variation, haplotype analysis, rhg1, soybean",
author = "Gunvant Patil and Naoufal Lakhssassi and Jinrong Wan and Li Song and Zhou Zhou and Mariola Klepadlo and Vuong, {Tri D.} and Stec, {Adrian O.} and Kahil, {Sondus S.} and Vincent Colantonio and Babu Valliyodan and Rice, {J. Hollis} and Sarbottam Piya and Tarek Hewezi and Stupar, {Robert M} and Khalid Meksem and Nguyen, {Henry T.}",
year = "2019",
month = "8",
day = "1",
doi = "10.1111/pbi.13086",
language = "English (US)",
volume = "17",
pages = "1595--1611",
journal = "Plant Biotechnology Journal",
issn = "1467-7644",
publisher = "Wiley-Blackwell",
number = "8",

}

TY - JOUR

T1 - Whole-genome re-sequencing reveals the impact of the interaction of copy number variants of the rhg1 and Rhg4 genes on broad-based resistance to soybean cyst nematode

AU - Patil, Gunvant

AU - Lakhssassi, Naoufal

AU - Wan, Jinrong

AU - Song, Li

AU - Zhou, Zhou

AU - Klepadlo, Mariola

AU - Vuong, Tri D.

AU - Stec, Adrian O.

AU - Kahil, Sondus S.

AU - Colantonio, Vincent

AU - Valliyodan, Babu

AU - Rice, J. Hollis

AU - Piya, Sarbottam

AU - Hewezi, Tarek

AU - Stupar, Robert M

AU - Meksem, Khalid

AU - Nguyen, Henry T.

PY - 2019/8/1

Y1 - 2019/8/1

N2 - Soybean cyst nematode (SCN) is the most devastating plant-parasitic nematode. Most commercial soybean varieties with SCN resistance are derived from PI88788. Resistance derived from PI88788 is breaking down due to narrow genetic background and SCN population shift. PI88788 requires mainly the rhg1-b locus, while ‘Peking’ requires rhg1-a and Rhg4 for SCN resistance. In the present study, whole genome re-sequencing of 106 soybean lines was used to define the Rhg haplotypes and investigate their responses to the SCN HG-Types. The analysis showed a comprehensive profile of SNPs and copy number variations (CNV) at these loci. CNV of rhg1 (GmSNAP18) only contributed towards resistance in lines derived from PI88788 and ‘Cloud’. At least 5.6 copies of the PI88788-type rhg1 were required to confer SCN resistance, regardless of the Rhg4 (GmSHMT08) haplotype. However, when the GmSNAP18 copies dropped below 5.6, a ‘Peking’-type GmSHMT08 haplotype was required to ensure SCN resistance. This points to a novel mechanism of epistasis between GmSNAP18 and GmSHMT08 involving minimum requirements for copy number. The presence of more Rhg4 copies confers resistance to multiple SCN races. Moreover, transcript abundance of the GmSHMT08 in root tissue correlates with more copies of the Rhg4 locus, reinforcing SCN resistance. Finally, haplotype analysis of the GmSHMT08 and GmSNAP18 promoters inferred additional levels of the resistance mechanism. This is the first report revealing the genetic basis of broad-based resistance to SCN and providing new insight into epistasis, haplotype-compatibility, CNV, promoter variation and its impact on broad-based disease resistance in plants.

AB - Soybean cyst nematode (SCN) is the most devastating plant-parasitic nematode. Most commercial soybean varieties with SCN resistance are derived from PI88788. Resistance derived from PI88788 is breaking down due to narrow genetic background and SCN population shift. PI88788 requires mainly the rhg1-b locus, while ‘Peking’ requires rhg1-a and Rhg4 for SCN resistance. In the present study, whole genome re-sequencing of 106 soybean lines was used to define the Rhg haplotypes and investigate their responses to the SCN HG-Types. The analysis showed a comprehensive profile of SNPs and copy number variations (CNV) at these loci. CNV of rhg1 (GmSNAP18) only contributed towards resistance in lines derived from PI88788 and ‘Cloud’. At least 5.6 copies of the PI88788-type rhg1 were required to confer SCN resistance, regardless of the Rhg4 (GmSHMT08) haplotype. However, when the GmSNAP18 copies dropped below 5.6, a ‘Peking’-type GmSHMT08 haplotype was required to ensure SCN resistance. This points to a novel mechanism of epistasis between GmSNAP18 and GmSHMT08 involving minimum requirements for copy number. The presence of more Rhg4 copies confers resistance to multiple SCN races. Moreover, transcript abundance of the GmSHMT08 in root tissue correlates with more copies of the Rhg4 locus, reinforcing SCN resistance. Finally, haplotype analysis of the GmSHMT08 and GmSNAP18 promoters inferred additional levels of the resistance mechanism. This is the first report revealing the genetic basis of broad-based resistance to SCN and providing new insight into epistasis, haplotype-compatibility, CNV, promoter variation and its impact on broad-based disease resistance in plants.

KW - SCN

KW - broad-based resistance

KW - copy number variation

KW - haplotype analysis

KW - rhg1

KW - soybean

UR - http://www.scopus.com/inward/record.url?scp=85068126972&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85068126972&partnerID=8YFLogxK

U2 - 10.1111/pbi.13086

DO - 10.1111/pbi.13086

M3 - Article

C2 - 30688400

AN - SCOPUS:85068126972

VL - 17

SP - 1595

EP - 1611

JO - Plant Biotechnology Journal

JF - Plant Biotechnology Journal

SN - 1467-7644

IS - 8

ER -