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Genetic Architecture of Basal Resistance of Barley to Puccinia Hordei

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Genetic Architecture of Basal Resistance of Barley to Puccinia Hordei Genetic architecture of basal resistance of barley to Puccinia hordei Thierry C. Marcel Promotor: Prof. Dr. Richard G. F. Visser Hoogleraar in de Plantenveredeling, Wageningen Universiteit Co-promotor: Dr. Rients E. Niks Universitair docent, Laboratorium voor Plantenveredeling, Wageningen Universiteit Promotiecommissie: Prof. Dr. Ir. Pierre J. G. M. de Wit Wageningen Universiteit Prof. Dr. Rob W. Goldbach Wageningen Universiteit Dr. Ir. Chris A. Maliepaard Wageningen Universiteit Prof. Dr. Andreas Graner Leibniz-Institute of Plant Genetics & Crop Plant Research, IPK, Gatersleben, Germany Dit onderzoek is uitgevoerd binnen de onderzoekschool ‘Experimental Plant Sciences’ Thierry C. Marcel Genetic architecture of basal resistance of barley to Puccinia hordei Proefschrift ter verkrijging van de graad van doctor op gezag van de rector magnificus van Wageningen Universiteit Prof. Dr. M. J. Kropff in het openbaar te verdedigen op vrijdag 11 mei 2007 des namiddags te 13:30 in de Aula Thierry C. Marcel (2007) Genetic architecture of basal resistance of barley to Puccinia hordei PhD thesis, Wageningen University, The Netherlands With summaries in English, Dutch and French ISBN 978-90-8504-645-5 Abstract Marcel TC, 2007. Genetic architecture of basal resistance of barley to Puccinia hordei . PhD thesis, Wageningen University, The Netherlands. With summaries in English, Dutch and French. Partial resistance to leaf rust ( Puccinia hordei Otth) in barley is a quantitative resistance that is not based on hypersensitivity. This resistance hampers haustorium formation and results in a long latency period in greenhouse tests. The resistance is due to genes with relatively small, quantitative effects, located on so called quantitative trait loci (QTL). A detailed chromosome map of barley, containing 3,258 molecular markers, was constructed and used as a platform to compare the genetic positions of QTLs across different mapping populations. This confirmed that partial resistance in barley to P. hordei is controlled by a high diversity of genes, each mapping population segregating for a different set of QTLs. Another consensus map was constructed that gathered together 775 barley microsatellite markers. The introgression of single QTL-allele or combination of QTL-alleles in near isogenic lines (NILs) allowed us to confirm the effect of three target QTLs ( Rphq2 , Rphq3 and Rphq4 ) in seedling disease tests performed in greenhouse compartments and in field disease tests. The use of several leaf rust isolates revealed the clear isolate-specific effect of Rphq4 . Gene Rphq2 was easy to detect in seedlings of the corresponding NILs and was located in a physical region of high recombination. The position of Rphq2 was refined to a 0.1 cM genetic interval that corresponds probably with only a relatively short stretch of DNA. This makes it feasible to pick the gene up from a bacterial DNA (BAC) library in not too distant future. Contents Chapter 1 9 General introduction Chapter 2 19 A high-density consensus map of barley to compare the distribution of QTLs for partial resistance to Puccinia hordei and of defence gene homologues Chapter3 41 A high-density barley microsatellite consensus map with 775 SSR loci Chapter 4 63 Dissection of the barley 2L1.0 region carrying the ‘ Laevigatum ’ quantitative resistance gene to leaf rust using near isogenic lines (NILs) and sub-NILs Chapter 5 89 The verification of QTLs for partial resistance to Puccinia hordei in NILs of barley confirms an isolate-specific effect Chapter 6 111 General discussion Appendixes 129 References Summary Samenvatting Résumé Acknowledgements Curriculum Vitae and Publications Colour Figures CHAPTER 1 General Introduction . Barley leaf infected with leaf rust GENERAL I NTRODUCTION General introduction Rusts and barley leaf rust Rust fungi (Basidiomycota, Uredinales) consist of more than 5,000 species of obligate plant pathogens that possess some of the most complex life cycles in the Eumycota (Hiratsuka and Sato 1982 ). Rust diseases cause serious economic damage worldwide on agricultural, forest and ornamental plants. These fungi are of great interest not only for the economic problems that they cause, but also for their highly specialised relationship with host plants. One of the unique features of rust fungi is that they have up to five functionally and morphologically different spore states in their life cycles. The typical progression of spore states is basidiospore ( N), pycniospores or spermatium ( N), aeciospore ( N+N), urediospore ( N+N), teliospore ( N+N → 2 N → N). This is further complicated because, in addition to the different numbers of spore states, they often need two unrelated groups of host plant species to complete their life cycles (heteroecious). Some can complete their life cycles on only one kind of host plant (autoecious). For many rust species, like Puccinia hordei , completion of the sexual stages is not required for perpetuation of the rust in nature, since the asexual stage (uredia) may continue infinitely. Leaf rust is an important disease of barley ( Hordeum vulgare L.) in many regions of the world. Yield losses up to 32% have been reported in susceptible cultivars. The causal agent, Puccinia hordei Otth, is a heteroecious fungus with the dikaryotic stage limited in nature to H. vulgare and the sexual stage to Ornithogalum species. Parasitically the fungus is confined to the source host species, except that reciprocal inoculations with leaf rust of H. spontaneum and H. vulgare L. were successful (Anikster and Wahl 1979 ). Telia on the main host are profusely formed where Ornithogalum plants are present. D’Oliveira ( 1960 ) demonstrated that 32 species of Ornithogalum are compatible with P. hordei . The center of origin and diversification of these species coincides at least partly with that of H. spontaneum - the putative progenitor of cultivated barley - but includes the regions where barley has been cultivated since remote antiquity. To initiate the dikaryotic stage, the urediospore forms a germ tube that responds to topographical features of the leaf surface so that it grows towards a stoma and recognises its presence by responding to the ridges around the stomatal lips (Heath et al. 1997 ; Vaz Patto and Niks 2001). In response to the stomatal lips, the fungus sequentially forms an appressorium over the stomatal opening, an infection peg that grows between the guard cells, a torpedo shaped substomatal vesicle in the substomatal space, and an infection hypha that grows intercellularly between mesophyll cells (Fig. 1). Then, the fungus forms an intercellular mycelium from which intracellular haustoria are formed. These haustoria are generally 11 CHAPTER 1 considered to be feeding structures and they develop from haustorial mother cells that adhere to the plant cell surface (Mendgen et al. 2000 ). During the other, monokaryotic, parasitic stage, rust fungi usually penetrate directly into epidermal cells and the only pre-penetration structure is the appressorium produced by the basidiospore germ tube (Longo et al. 2006 ). Figure 2. A young rust fungal colony, about 60 hours old, in a cereal leaf. The sequence of development is germination of the urediospore (U), formation of an appressorium (A) from the germ tube (GT) over a stoma, penetration past the guard cells (GC) via a penetration peg (PP), formation of a substomatal vesicle (SV), growth of an infection hypha (IH), formation of the primary haustorium (PH), then branching and growth of intercellular hyphae (ICH), and formation of additional haustoria (H). The haustorium mother cells (HMC) are indicated in bold outline. (Drawn by Dr. J. Chong; Reprinted from Harder 1984 ). Boundaries of basal resistance Basal resistance is a term commonly used by scientific authors to refer to the early defence response of plants to a pathogen attack. Basal defence is the complement of the term of basic compatibility, and refers to a defence system that is not based on a hypersensitive response (Heath 1991 ). Basic compatibility is the state that results from the capacity of the microbe to deal effectively with the defence that plant species perform against unadapted microbial intruders. The definition of basal resistance is particularly vague in plant pathology and it would be necessary to delimit its physiological boundaries to obtain a uniform discussion within the scientific community. A clear definition of basal resistance is difficult to give 12 GENERAL I NTRODUCTION because of our limited knowledge in the actual biological events that happen in the early steps of plant defence. Also, as our understanding advances, the idea that plant defence systems rely on a continuum of layered defences seems to defy man-made boundaries and definitions (Heath 2001 ; da Cunha et al. 2006 ). A non-host or host resistance? Non-host resistance is the resistance shown by an entire plant species to a specific parasite or pathogen (Heath 2000 ). Non-host resistance to maladapted pathogens can be the result of effective non-specific defences such as physical and constitutive chemical features. For rust fungi, the topography of the leaf surface is an example of physical feature to which the fungus should be adapted for successful colonisation (Vaz Patto and Niks 2001). As for chemical factors, preformed peptides and secondary metabolites are potential deterrents against microbial infection. Such physical and chemical responses are often referred to as the preformed barriers of a non-host plant to its potential pathogens. Additionally,
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