Sequence exchange between R genes converts virus resistance into nematode resistance, and vice versa

Erik J. Slootweg, K.B. Koropacka, Jan Roosien, Robert Dees, Hein Overmars, Rene Klein Lankhorst, Casper van Schaik, Rikus Pomp, Liesbeth Bouwman-Smits, Hans Helder, Arjen Schots, Jaap Bakker, Geert Smant, Aska Goverse

Research output: Contribution to journalArticleAcademicpeer-review

6 Citations (Scopus)

Abstract

Plants have evolved a limited repertoire of NB-LRR disease resistance (R) genes to protect themselves against a myriad of pathogens. This limitation is thought to be counterbalanced by the rapid evolution of NB-LRR proteins, as only few sequence changes have been shown to be sufficient to alter resistance specificities towards novel strains of a pathogen. However, little is known about the flexibility of NB-LRR genes to switch resistance specificities between phylogenetically unrelated pathogens. To investigate this, we created domain swaps between the close homologs Gpa2 and Rx1, which confer resistance in potato to the cyst nematode Globodera pallida and Potato virus X (PVX), respectively. The genetic fusion of the CC-NB-ARC of Gpa2 with the LRR of Rx1 (Gpa2CN/Rx1L) resulted in autoactivity, but lowering the protein levels restored its specific activation response including extreme resistance to PVX in potato shoots. The reciprocal construct (Rx1CN/Gpa2L) showed a loss-of-function phenotype, but exchange of the first 3 LRR repeats of Rx1 was sufficient to regain a wild type resistance response to G. pallida in the roots. These data demonstrate that exchanging the recognition moiety in the LRR is sufficient to convert extreme virus resistance in the leaves into mild nematode resistance in the roots, and vice versa. In addition, we show that the CC-NB-ARC can operate independently of the recognition specificities defined by the LRR domain, either above or belowground. These data show the versatility of NB-LRR genes to generate resistances to unrelated pathogens with completely different lifestyles and routes of invasion.
Original languageEnglish
Pages (from-to)498-510
JournalPlant Physiology
Volume175
DOIs
Publication statusPublished - 2017

Fingerprint

Potexvirus
vpr Genes
AIDS-Related Complex
Solanum tuberosum
Switch Genes
Nematoda
Viruses
Globodera pallida
Potato virus X
viruses
Disease Resistance
pathogens
Life Style
Cysts
Proteins
genes
potatoes
Phenotype
cyst nematodes
Genes

Cite this

@article{8649b61fba0f4330855e044394454025,
title = "Sequence exchange between R genes converts virus resistance into nematode resistance, and vice versa",
abstract = "Plants have evolved a limited repertoire of NB-LRR disease resistance (R) genes to protect themselves against a myriad of pathogens. This limitation is thought to be counterbalanced by the rapid evolution of NB-LRR proteins, as only few sequence changes have been shown to be sufficient to alter resistance specificities towards novel strains of a pathogen. However, little is known about the flexibility of NB-LRR genes to switch resistance specificities between phylogenetically unrelated pathogens. To investigate this, we created domain swaps between the close homologs Gpa2 and Rx1, which confer resistance in potato to the cyst nematode Globodera pallida and Potato virus X (PVX), respectively. The genetic fusion of the CC-NB-ARC of Gpa2 with the LRR of Rx1 (Gpa2CN/Rx1L) resulted in autoactivity, but lowering the protein levels restored its specific activation response including extreme resistance to PVX in potato shoots. The reciprocal construct (Rx1CN/Gpa2L) showed a loss-of-function phenotype, but exchange of the first 3 LRR repeats of Rx1 was sufficient to regain a wild type resistance response to G. pallida in the roots. These data demonstrate that exchanging the recognition moiety in the LRR is sufficient to convert extreme virus resistance in the leaves into mild nematode resistance in the roots, and vice versa. In addition, we show that the CC-NB-ARC can operate independently of the recognition specificities defined by the LRR domain, either above or belowground. These data show the versatility of NB-LRR genes to generate resistances to unrelated pathogens with completely different lifestyles and routes of invasion.",
author = "Slootweg, {Erik J.} and K.B. Koropacka and Jan Roosien and Robert Dees and Hein Overmars and {Klein Lankhorst}, Rene and {van Schaik}, Casper and Rikus Pomp and Liesbeth Bouwman-Smits and Hans Helder and Arjen Schots and Jaap Bakker and Geert Smant and Aska Goverse",
year = "2017",
doi = "10.1104/pp.17.00485",
language = "English",
volume = "175",
pages = "498--510",
journal = "Plant Physiology",
issn = "0032-0889",
publisher = "American Society of Plant Biologists",

}

Sequence exchange between R genes converts virus resistance into nematode resistance, and vice versa. / Slootweg, Erik J.; Koropacka, K.B.; Roosien, Jan; Dees, Robert; Overmars, Hein; Klein Lankhorst, Rene; van Schaik, Casper; Pomp, Rikus; Bouwman-Smits, Liesbeth; Helder, Hans; Schots, Arjen; Bakker, Jaap; Smant, Geert; Goverse, Aska.

In: Plant Physiology, Vol. 175, 2017, p. 498-510.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Sequence exchange between R genes converts virus resistance into nematode resistance, and vice versa

AU - Slootweg, Erik J.

AU - Koropacka, K.B.

AU - Roosien, Jan

AU - Dees, Robert

AU - Overmars, Hein

AU - Klein Lankhorst, Rene

AU - van Schaik, Casper

AU - Pomp, Rikus

AU - Bouwman-Smits, Liesbeth

AU - Helder, Hans

AU - Schots, Arjen

AU - Bakker, Jaap

AU - Smant, Geert

AU - Goverse, Aska

PY - 2017

Y1 - 2017

N2 - Plants have evolved a limited repertoire of NB-LRR disease resistance (R) genes to protect themselves against a myriad of pathogens. This limitation is thought to be counterbalanced by the rapid evolution of NB-LRR proteins, as only few sequence changes have been shown to be sufficient to alter resistance specificities towards novel strains of a pathogen. However, little is known about the flexibility of NB-LRR genes to switch resistance specificities between phylogenetically unrelated pathogens. To investigate this, we created domain swaps between the close homologs Gpa2 and Rx1, which confer resistance in potato to the cyst nematode Globodera pallida and Potato virus X (PVX), respectively. The genetic fusion of the CC-NB-ARC of Gpa2 with the LRR of Rx1 (Gpa2CN/Rx1L) resulted in autoactivity, but lowering the protein levels restored its specific activation response including extreme resistance to PVX in potato shoots. The reciprocal construct (Rx1CN/Gpa2L) showed a loss-of-function phenotype, but exchange of the first 3 LRR repeats of Rx1 was sufficient to regain a wild type resistance response to G. pallida in the roots. These data demonstrate that exchanging the recognition moiety in the LRR is sufficient to convert extreme virus resistance in the leaves into mild nematode resistance in the roots, and vice versa. In addition, we show that the CC-NB-ARC can operate independently of the recognition specificities defined by the LRR domain, either above or belowground. These data show the versatility of NB-LRR genes to generate resistances to unrelated pathogens with completely different lifestyles and routes of invasion.

AB - Plants have evolved a limited repertoire of NB-LRR disease resistance (R) genes to protect themselves against a myriad of pathogens. This limitation is thought to be counterbalanced by the rapid evolution of NB-LRR proteins, as only few sequence changes have been shown to be sufficient to alter resistance specificities towards novel strains of a pathogen. However, little is known about the flexibility of NB-LRR genes to switch resistance specificities between phylogenetically unrelated pathogens. To investigate this, we created domain swaps between the close homologs Gpa2 and Rx1, which confer resistance in potato to the cyst nematode Globodera pallida and Potato virus X (PVX), respectively. The genetic fusion of the CC-NB-ARC of Gpa2 with the LRR of Rx1 (Gpa2CN/Rx1L) resulted in autoactivity, but lowering the protein levels restored its specific activation response including extreme resistance to PVX in potato shoots. The reciprocal construct (Rx1CN/Gpa2L) showed a loss-of-function phenotype, but exchange of the first 3 LRR repeats of Rx1 was sufficient to regain a wild type resistance response to G. pallida in the roots. These data demonstrate that exchanging the recognition moiety in the LRR is sufficient to convert extreme virus resistance in the leaves into mild nematode resistance in the roots, and vice versa. In addition, we show that the CC-NB-ARC can operate independently of the recognition specificities defined by the LRR domain, either above or belowground. These data show the versatility of NB-LRR genes to generate resistances to unrelated pathogens with completely different lifestyles and routes of invasion.

U2 - 10.1104/pp.17.00485

DO - 10.1104/pp.17.00485

M3 - Article

VL - 175

SP - 498

EP - 510

JO - Plant Physiology

JF - Plant Physiology

SN - 0032-0889

ER -