Resistance breaking Root-knot nematodes carry a fitness cost associated with defective feeding site development
- 1Department of Plant Pathology, University of California, Davis, Davis, California, United States of America
- 2Department of Entomology and Nematology, University of California, Davis, Davis, California, United States of America
- 3Department of Botany and Plant Physiology, Institute of Biology, Warsaw University of Life Sciences, Warsaw, Poland
Abstract
Root-knot nematodes (RKNs) cause an estimated 157 billion dollars in annual yield losses worldwide. In tomato, resistance to RKNs is conferred by the single dominant resistance gene Mi-1, which has been widely integrated into commercial cultivars. Prolonged and widespread use of Mi-1 has led to the emergence of resistance-breaking populations in tomato fields worldwide; however, the consequences of resistance breaking for nematode performance on susceptible hosts remain poorly understood. Here, we compared infection outcomes of two closely related strains of Meloidogyne javanica, VW4 (Mi-1–avirulent; wild-type) and VW5 (Mi-1–virulent; resistance-breaking), on three susceptible hosts: tomato, cucumber, and rice. Across all hosts, VW5 produced significantly fewer eggs than VW4, revealing a fitness cost associated with Mi-1 virulence. Light and transmission electron microscopy of tomato and cucumber galls revealed impaired feeding site establishment by VW5. Consistent with these observations, transcriptomic profiling of nematode-infected roots showed that VW5 infection induced weaker host transcriptional reprogramming than VW4 and lacked host gene expression signatures associated with effective suppression of plant defense responses. Together, these findings demonstrate that adaptation to Mi-1-mediated resistance is accompanied by a fitness cost on susceptible plants and impaired feeding site formation and altered host reprogramming. Furthermore, these results establish VW4 and VW5 as a powerful resource for understanding host genes and pathways required for successful parasitism and feeding site development. Author summary: Root-knot nematodes are microscopic plant parasites that cause major yield losses in many crops, including tomato, cucumber, and rice. Tomato cultivars that carry the resistance gene Mi-1 can prevent successful parasitism by several root-knot nematode species. However, some nematode populations have evolved the ability to overcome this resistance, compromising the durability of resistant cultivars. In this study, we compared two closely related strains of Meloidogyne javanica: VW4, which cannot reproduce on tomato with the Mi-1 resistance gene, and VW5, which successfully reproduced in resistant tomato. However, VW5 produced substantially fewer eggs than VW4 on susceptible tomato, cucumber, and rice, indicating a reproductive fitness cost associated with breaking resistance. Microscopy revealed that VW5 induced abnormal and structurally compromised feeding sites in susceptible plants. Comparison of cucumber gene expression in infected roots showed that VW5 caused weaker early reprogramming of host gene expression than did VW4, particularly in pathways associated with feeding-site development and host-cell remodeling. Together, these findings indicate that the ability to overcome Mi-1 resistance is associated with reduced performance on susceptible hosts due to impaired ability to manipulate host tissues.
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BibTeX
@article{blundell2026resistance,
title = {{Resistance breaking Root-knot nematodes carry a fitness cost associated with defective feeding site development}},
author = {Alison C. Blundell and Emma Shigekane-Kraft and Sławomir Janakowski and Mirosław Sobczak and Dadong Dai and Yali Zhang and Pallavi Shakya and Ching-Jung Lin and Valerie M. Williamson and Shahid Siddique},
journal = {PLOS Pathogens},
year = {2026},
month = sep,
doi = {10.1371/journal.ppat.1014581},
url = {https://journals.plos.org/plospathogens/article?id=10.1371/journal.ppat.1014581},
note = {CC BY 4.0},
}
RIS
TY - JOUR
TI - Resistance breaking Root-knot nematodes carry a fitness cost associated with defective feeding site development
AU - Alison C. Blundell
AU - Emma Shigekane-Kraft
AU - Sławomir Janakowski
AU - Mirosław Sobczak
AU - Dadong Dai
AU - Yali Zhang
AU - Pallavi Shakya
AU - Ching-Jung Lin
AU - Valerie M. Williamson
AU - Shahid Siddique
PY - 2026
DA - 2026/09/11
JO - PLOS Pathogens
DO - 10.1371/journal.ppat.1014581
UR - https://journals.plos.org/plospathogens/article?id=10.1371/journal.ppat.1014581
AB - Root-knot nematodes (RKNs) cause an estimated 157 billion dollars in annual yield losses worldwide. In tomato, resistance to RKNs is conferred by the single dominant resistance gene Mi-1, which has been widely integrated into commercial cultivars. Prolonged and widespread use of Mi-1 has led to the emergence of resistance-breaking populations in tomato fields worldwide; however, the consequences of resistance breaking for nematode performance on susceptible hosts remain poorly understood. Here, we compared infection outcomes of two closely related strains of Meloidogyne javanica, VW4 (Mi-1–avirulent; wild-type) and VW5 (Mi-1–virulent; resistance-breaking), on three susceptible hosts: tomato, cucumber, and rice. Across all hosts, VW5 produced significantly fewer eggs than VW4, revealing a fitness cost associated with Mi-1 virulence. Light and transmission electron microscopy of tomato and cucumber galls revealed impaired feeding site establishment by VW5. Consistent with these observations, transcriptomic profiling of nematode-infected roots showed that VW5 infection induced weaker host transcriptional reprogramming than VW4 and lacked host gene expression signatures associated with effective suppression of plant defense responses. Together, these findings demonstrate that adaptation to Mi-1-mediated resistance is accompanied by a fitness cost on susceptible plants and impaired feeding site formation and altered host reprogramming. Furthermore, these results establish VW4 and VW5 as a powerful resource for understanding host genes and pathways required for successful parasitism and feeding site development. Author summary: Root-knot nematodes are microscopic plant parasites that cause major yield losses in many crops, including tomato, cucumber, and rice. Tomato cultivars that carry the resistance gene Mi-1 can prevent successful parasitism by several root-knot nematode species. However, some nematode populations have evolved the ability to overcome this resistance, compromising the durability of resistant cultivars. In this study, we compared two closely related strains of Meloidogyne javanica: VW4, which cannot reproduce on tomato with the Mi-1 resistance gene, and VW5, which successfully reproduced in resistant tomato. However, VW5 produced substantially fewer eggs than VW4 on susceptible tomato, cucumber, and rice, indicating a reproductive fitness cost associated with breaking resistance. Microscopy revealed that VW5 induced abnormal and structurally compromised feeding sites in susceptible plants. Comparison of cucumber gene expression in infected roots showed that VW5 caused weaker early reprogramming of host gene expression than did VW4, particularly in pathways associated with feeding-site development and host-cell remodeling. Together, these findings indicate that the ability to overcome Mi-1 resistance is associated with reduced performance on susceptible hosts due to impaired ability to manipulate host tissues.
SN - 1553-7374
ER -