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Last update: May 2021

Menu Logo Principal Plant pathology unit - INRA AVIGNON

Pathologie vegetale

Zone de texte éditable et éditée et rééditée

Durability of plant resistance

Protecting a major resistance gene from breakdown with an appropriate genetic background – the concept of quantitative trait loci (QTLs) of resistance durability

 

Capsicum annuum

By itself, quantitative resistance is not necessarily durable. Experimental evolution of PVY in a pepper (Capsicum annuum) genotype carrying three resistance QTLs showed that the virus could adapt quickly to the resistance, which leads to an almost breakdown of that quantitative resistance. However, when combined with a major resistance gene, quantitative resistance can substantially improve the durability of the major gene. This was initially shown for the PVY-pepper pathosystem and further for plant resistance genes against fungi or nematodes.

The speed of evolution of PVY has allowed measuring the capacity of adaptation of the virus to a major resistance gene in a short period of time (~1 month) in a progeny of pepper lines that carried the same major resistance gene but differed for the genetic background. Importantly, this trait is highly heritable from the plant side and four « resistance durability » QTLs, i.e. QTLs that modified significantly the frequency of breakdown of the major resistance gene, were mapped.

Quantitative trait loci to preserve the durability of major resistance genes

The frequency of resistance breakdown is highly heritable and controlled by 4 “resistance durability” QTLs

The QTL with the strongest effect on linkage group P3 coincides with the eIFiso4E-coding gene, a gene of the same family as the major resistance gene studied (the pvr23 gene, encoding the eukaryotic initiation factor 4E, eIF4E). This suggests that the effect on resistance durability may be due to regulatory interactions between members of this small gene family. Moreover, the eIFiso4E-coding gene is involved in the resistance to two additional potyvirus species (Pepper veinal mottle virus and Chilli veinal mottle virus). Although the same eIFiso4E-coding gene is involved in the two traits, the allele of this gene that increases the spectrum of action of the resistance also decreases the resistance durability to PVY. This trade-off would have important consequences in breeding programs. Indeed, additional QTLs are required to obtain a cultivar that combines a large potyvirus resistance spectrum and a high durability potential.

Interestingly, two of the resistance durability QTLs map in the same regions as QTLs controlling within-plant virus accumulation, suggesting that the increase of resistance efficiency conferred by these two QTLs promoted resistance durability. This effect could be threefold.

The increase of resistance efficiency (i.e. decrease of virus accumulation) can (i) directly decrease the probability of appearance of resistance-breaking mutations in the PVY population and can indirectly (ii) alter the virus mutational pathways involved in resistance-breaking and (iii) slow down the selection of the resistance-breaking mutants once they have appeared. This latter effect may be the consequence of an increase of genetic drift in the virus population imposed by the resistance durability QTLs.

  • Montarry, J., Cartier, E., Jacquemond, M., Palloix, A., Moury, B. (2012). Virus adaptation to quantitative plant resistance: erosion or breakdown?. Journal of Evolutionary Biology, 25 (11), 2242-2252. DOI : 10.1111/j.1420-9101.2012.02600.x
  • Quenouille, J., Montarry, J., Palloix, A., Moury, B. (2013). Farther, slower, stronger: how the plant genetic background protects a major resistance gene from breakdown. Molecular Plant Pathology, 14 (2), 109-118. DOI : 10.1111/J.1364-3703.2012.00834.X
  • Quenouille, J., Paulhiac, E., Moury, B., Palloix, A. (2014). Quantitative trait loci from the host genetic background modulate the durability of a resistance gene: a rational basis for sustainable resistance breeding in plants. Heredity, 112 (6), 579-587. DOI : 10.1038/hdy.2013.138
  • Quenouille, J., Saint-Félix, L., Moury, B., Palloix, A. (2016). Diversity of genetic backgrounds modulating the durability of a major resistance gene. Analysis of a core collection of pepper landraces resistant to Potato virus Y. Molecular Plant Pathology, 17 (2), 296-302. DOI : 10.1111/mpp.12277
  • Tamisier, L., Rousseau, E., Barraille, S., Nemouchi, G., Szadkowski, M., Mailleret, L., Grognard, F., Fabre, F., Moury, B., Palloix, A. (2017). Quantitative trait loci in pepper control the effective population size of two RNA viruses at inoculation. Journal of General Virology, 98 (7), 1923-1931. , DOI : 10.1099/jgv.0.000835 http://prodinra.inra.fr/record/400552