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      Genetics of resistance to Zymoseptoria tritici and applications to wheat breeding

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          Highlights

          • We review the genetics of wheat resistance to Septoria tritici blotch, with a map of known genes.

          • Qualitative resistance is usually monogenic, genotype-specific and non-durable.

          • Quantitative resistance is generally polygenic with low specificity and greater durability.

          • Major requirements for resistance breeding are diverse germplasm and field sites with severe Septoria.

          Abstract

          This paper reviews current knowledge about genes for resistance to Septoria tritici blotch (STB) of wheat, caused by Zymoseptoria tritici (formerly Mycosphaerella graminicola). These genes can be placed into two classes, although a few may have characteristics of both classes. Qualitative resistance is controlled by genes which control large fractions of genetic variation, 21 of which have been discovered and mapped so far. Most of them have been shown to be genotype-specific, being effective against the minority of Z. tritici isolates which are avirulent, and Stb6 has been shown to control a gene-for-gene relationship. Most qualitative resistances are unlikely to be durable and some formerly effective genes have been overcome by the evolution of pathogen virulence. Quantitative resistance is generally controlled by genes with small-to-moderate effects on STB. They have generally weaker specificity than qualitative genes and have provided more durable resistance. 89 genome regions carrying quantitative trait loci (QTL) or meta-QTL have been identified to date. Some QTL have been mapped at or near loci of qualitative genes, especially Stb6, which is present in several sources of resistance. Another gene of particular interest is Stb16q, which has been effective against all Z. tritici isolates tested so far. In addition to resistance, the susceptibility of wheat cultivars to STB can also be reduced by disease escape traits, some of which may be undesirable in breeding. The fundamental requirements for breeding for STB-resistance are genetic diversity for resistance in wheat germplasm and a field trial site at which STB epidemics occur regularly and effective selection can be conducted for resistance combined with other desirable traits. If these are in place, knowledge of resistance genes can be applied to improving control of STB.

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          Most cited references130

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          A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat.

          Agricultural crops benefit from resistance to pathogens that endures over years and generations of both pest and crop. Durable disease resistance, which may be partial or complete, can be controlled by several genes. Some of the most devastating fungal pathogens in wheat are leaf rust, stripe rust, and powdery mildew. The wheat gene Lr34 has supported resistance to these pathogens for more than 50 years. Lr34 is now shared by wheat cultivars around the world. Here, we show that the LR34 protein resembles adenosine triphosphate-binding cassette transporters of the pleiotropic drug resistance subfamily. Alleles of Lr34 conferring resistance or susceptibility differ by three genetic polymorphisms. The Lr34 gene, which functions in the adult plant, stimulates senescence-like processes in the flag leaf tips and edges.
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            Plant-parasite coevolution: bridging the gap between genetics and ecology.

            We review current ideas about coevolution of plants and parasites, particularly processes that generate genetic diversity. Frequencies of host resistance and parasite virulence alleles that interact in gene-for-gene (GFG) relationships coevolve in the familiar boom-and-bust cycle, in which resistance is selected when virulence is rare, and virulence is selected when resistance is common. The cycle can result in stable polymorphism when diverse ecological and epidemiological factors cause negative direct frequency-dependent selection (ndFDS) on host resistance, parasite virulence, or both, such that the benefit of a trait to fitness declines as its frequency increases. Polymorphism can also be stabilized by overdominance, when heterozygous hosts have greater resistance than homozygotes to diverse pathogens. Genetic diversity can also persist in the form of statistical polymorphism, sustained by random processes acting on gene frequencies and population size. Stable polymorphism allows alleles to be long-lived and genetic variation to be detectable in natural populations. In agriculture, many of the factors promoting stability in host-parasite interactions have been lost, leading to arms races of host defenses and parasite effectors. Copyright © 2011 by Annual Reviews. All rights reserved.
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              Durability of plant major resistance genes to pathogens depends on the genetic background, experimental evidence and consequences for breeding strategies.

              * The breakdown of plant resistance by pathogen populations is a limit to the genetic control of crop disease. Polygenic resistance is postulated as a durable alternative to defeated major resistance genes. Here, we tested this postulate in the pepper-Potato virus Y interaction. * The virus was selected for virulence towards monogenic and polygenic host resistance, using serial inoculations in laboratory and in natural epidemic conditions. The frequency of resistance breakdown and the genetic changes in the virus avirulence gene were analysed. * The monogenic resistance provided by the pvr2(3) gene was defeated at high frequency when introgressed in a susceptible genetic background whereas it was not when combined to partial resistance quantitative trait loci. The suppression of emergence of virulent mutants because of the genetic background resulted both from a differential selection effect and the necessity for the virus to generate multiple mutations. The virus adaptation to the polygenic resistance required a step-by-step selection with a primary selection for virulence towards the major gene, followed by selection for adaptation to the genetic background. * Polygenic resistance proved more durable than monogenic resistance, but breeding strategies giving priority to major resistance factors may jeopardize the progress in durability expected from polygenic resistance.
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                Author and article information

                Contributors
                Journal
                Fungal Genet Biol
                Fungal Genet. Biol
                Fungal Genetics and Biology
                Academic Press
                1087-1845
                1096-0937
                1 June 2015
                June 2015
                : 79
                : 33-41
                Affiliations
                [a ]John Innes Centre, Norwich Research Park, Colney, Norwich NR4 7UH, England, United Kingdom
                [b ]INRA, UMR 1095, Genetics, Diversity and Ecophysiology of Cereals, F-63100 Clermont-Ferrand, France
                [c ]UBP, UMR 1095, Genetics, Diversity and Ecophysiology of Cereals, F-63100 Clermont-Ferrand, France
                Author notes
                [* ]Corresponding authors at: John Innes Centre, Norwich Research Park, Colney, Norwich NR4 7UH, England, United Kingdom (J.K.M. Brown), INRA, UMR 1095, Genetics, Diversity and Ecophysiology of Cereals, F-63100 Clermont-Ferrand, France (C. Saintenac). james.brown@ 123456jic.ac.uk cyrille.saintenac@ 123456clermont.inra.fr
                Article
                S1087-1845(15)00083-3
                10.1016/j.fgb.2015.04.017
                4510316
                26092788
                953f4633-24c9-4e16-88aa-b19f636c5303
                © 2015 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 25 January 2015
                : 15 April 2015
                : 18 April 2015
                Categories
                Article

                Plant science & Botany
                durable resistance,gene-for-gene relationship,genetic mapping,plant breeding,quantitative trait locus (qtl),septoria tritici blotch

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