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Journal of Integrative Agriculture  2014, Vol. 13 Issue (2): 244-254    DOI: 10.1016/S2095-3119(13)60648-6
Special Focus:Cereal Rusts and Powdery Advanced Online Publication | Current Issue | Archive | Adv Search |
How Specific is Non-Hypersensitive Host and Nonhost Resistance of Barley to Rust and Mildew Fungi?
 Niks R E
Laboratory of Plant Breeding, Wageningen University, P.O. Box 386, 6700 AJ Wageningen, The Netherlands
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摘要  Full nonhost resistance can be defined as immunity, displayed by an entire plant species against all genotypes of a plant pathogen. Interesting biological questions are, whether the genes responsible for the nonhost status of a plant species have a general or a specific effectiveness to heterologous (“nonhost”) pathogens? Is the nonhost resistance to pathogens of plant species that are related to the nonhost based on R-genes or on other types of genes? We study this question in barley (Hordeum vulgare L.), which is a near-nonhost to several rusts (Puccinia) of cereals and grasses. By crosses and selection we accumulated susceptibility and developed an experimental line, SusPtrit, with high susceptibility to at least nine different heterologous rust taxa such as the wheat and Agropyron leaf rusts (P. triticina and P. persistens, respectively). At the microscopic level there is also some variation among barley accessions in the degree that the heterologous wheat powdery mildew (Blumeria graminis f.sp. tritici) is able to form haustoria in epidermal cells. So, also the genetics of the variation in level of nonhost resistance to heterologous mildew fungi can be studied in barley. Our data obtained on mapping populations involving three regular nonhost-immune accessions (Vada, Cebada Capa and Golden Promise) suggest that nonhost resistance is the joined effect of multiple, quantitative genes (QTLs) and very occasionally a major gene (R-gene?) is involved. Most QTLs have effect to only one or two heterologous rusts, but some have a wider spectrum. This was confirmed in a set of QTL-NILs. Those QTL-NILs are used to fine-map the effective genes. In some cases, a QTL region with effectiveness to several heterologous rusts might be a cluster of genes with a more narrow spectrum of effectiveness. Our evidence suggests that nonhost resistance in barley to rust and powdery mildew fungi of related Gramineae is not due to R-genes, but to pathogen species-specific quantitative resistance genes.

Abstract  Full nonhost resistance can be defined as immunity, displayed by an entire plant species against all genotypes of a plant pathogen. Interesting biological questions are, whether the genes responsible for the nonhost status of a plant species have a general or a specific effectiveness to heterologous (“nonhost”) pathogens? Is the nonhost resistance to pathogens of plant species that are related to the nonhost based on R-genes or on other types of genes? We study this question in barley (Hordeum vulgare L.), which is a near-nonhost to several rusts (Puccinia) of cereals and grasses. By crosses and selection we accumulated susceptibility and developed an experimental line, SusPtrit, with high susceptibility to at least nine different heterologous rust taxa such as the wheat and Agropyron leaf rusts (P. triticina and P. persistens, respectively). At the microscopic level there is also some variation among barley accessions in the degree that the heterologous wheat powdery mildew (Blumeria graminis f.sp. tritici) is able to form haustoria in epidermal cells. So, also the genetics of the variation in level of nonhost resistance to heterologous mildew fungi can be studied in barley. Our data obtained on mapping populations involving three regular nonhost-immune accessions (Vada, Cebada Capa and Golden Promise) suggest that nonhost resistance is the joined effect of multiple, quantitative genes (QTLs) and very occasionally a major gene (R-gene?) is involved. Most QTLs have effect to only one or two heterologous rusts, but some have a wider spectrum. This was confirmed in a set of QTL-NILs. Those QTL-NILs are used to fine-map the effective genes. In some cases, a QTL region with effectiveness to several heterologous rusts might be a cluster of genes with a more narrow spectrum of effectiveness. Our evidence suggests that nonhost resistance in barley to rust and powdery mildew fungi of related Gramineae is not due to R-genes, but to pathogen species-specific quantitative resistance genes.
Keywords:  genetics       specificity       basal resistance  
Received: 09 July 2013   Accepted:
Fund: 

I gratefully acknowledge the funding of parts of the research reported here by BioExploit, TritNONHOST (ERA-PG), Xunta de Galicia through the program of Angeles Alvariño, Technology Universiti Malaysia, and the Agricultural Research and Education Organization (AREO) and the Ministry of Science Research and Technology of I.R. of Iran.

Corresponding Authors:  Niks R E, Tel: +31-317-482508, E-mail: rients.niks@wur.nl     E-mail:  rients.niks@wur.nl
About author:  Niks R E, Tel: +31-317-482508, E-mail: rients.niks@wur.nl

Cite this article: 

Niks R E. 2014. How Specific is Non-Hypersensitive Host and Nonhost Resistance of Barley to Rust and Mildew Fungi?. Journal of Integrative Agriculture, 13(2): 244-254.

Aghnoum R, Marcel T C, Johrde A, Pecchioni N, Schweizer P, Niks R E. 2010. Basal resistance of barley to barley powdery mildew: Connecting QTLs and candidate genes. Molecular Plant-Microbe Interactions, 23, 91- 102.

Aghnoum R, Niks R E. 2010. Specificity and levels of non-host resistance of barley to non-adapted Blumeria graminis forms. New Phytologist, 185, 275-284

 Atienza S G, Jafary H, Niks R E. 2004. Accumulation of genes for susceptibility to rust fungi for which barley is nearly a nonhost results in two barley lines with extreme multiple susceptibility. Planta, 220, 71-79

 Ayliffe M, Devilla R, Mago R, White R, Talbot M, Pryor A, Leung H. 2011. Nonhost resistance of rice to rust pathogens. Molecular Plant-Microbe Interactions, 24, 1143-1155

 van Berloo R, Aalbers H, Werkman A, Niks R E. 2001. Resistance QTL confirmed through development of QTL-NILs for barley leaf rust resistance. Molecular Breeding, 8, 187-195

 Caldo R A, Nettleton D, Peng J, Wise R P. 2006. Stage- specific suppression of basal defense discriminates barley plants containing fast- and delayed-acting Mla powdery mildew resistance alleles. Molecular Plant- Microbe Interactions, 19, 939-947

 Chisholm ST, Coaker G, Day B, Staskawicz B J. 2006. Host-microbe interactions: Shaping the evolution of the plant immune response. Cell, 124, 803-814

 Christopher-Kozjan R, Heath M C. 2003. Cytological and pharmacological evidence that biotrophic fungi trigger different cell death execution processes in host and nonhost cells during the hypersensitive response. Physiological and Molecular Plant Pathology, 62, 265- 275.

Coaker G, Falick A, Staskawicz B. 2005. Activation of a phytopathogenic bacterial effector protein by a eukaryotic cyclophilin. Science, 308, 548-550

 Costa J M, Corey A, Hayes P M, Jobet C, Kleinhofs A, Kopisch-Obusch A, Kramer S F, Kudrna D, Li M, Riera-Lizarazu O, et al. 2001. Molecular mapping of the Oregon Wolfe barleys: A phenotypically polymorphic doubled-haploid population. Theoretical and Applied Genetics, 103, 415-424.

da Cunha L, McFall A J, Mackey D. 2006. Innate immunity in plants: a continuum of layered defenses. Microbes and Infection, 8, 1372-1381

 Elmhirst J F, Heath M C. 1987. Interactions of the bean rust and cowpea rust fungi with species of the Phaseolus- Vigna plant complex. I. Fungal growth and development. Canadian Journal of Botany, 65, 1096-1107

 González A M, Marcel T C, Kohutova Z, Stam P, van der Linden C G, Niks R E. 2010. Peroxidase profiling reveals genetic linkage between peroxidase gene clusters and basal host and non-host resistance to rusts and mildew in barley. PLoS-ONE, 5, e10495.

Heath M C. 1974. Light and electron microscope studies of the interactions of host and nonhost plants with cowpea rust Uromyces phaseoli var. vignae. Physiological Plant Pathology, 4, 403-414

 Heath M C. 1981. Resistance of plants to rust infection. Phytopathology, 71, 971-974

 Heath M C. 1991. Tansley review No.33. Evolution of resistance to fungal parasitism in natural ecosystems. New Phytologist, 119, 331-343

 Heath M C. 2001. Non-host resistance to plant pathogens: nonspecific defence or the result of specific recognition events? Physiological and Molecular Plant Pathology, 58, 53-54

 Heath M C. 2002. Cellular interactions between biotrophic fungal pathogens and host or nonhost plants. Canadian Journal of Plant Pathology, 24, 259-264

 Heath M C. 2003. Nonhost resistance in plants to microbial pathogens. In: Ezekowitz R A B, Hoffmann J A, eds., Innate Immunity. Humana Press, Totowa, NJ, USA. pp. 47-57

 van der Hoorn R A L, Kamoun S. 2008. From guard to decoy: A new model for perception of plant pathogen effectors. The Plant Cell, 20, 2009-2017

 Ingle R A, Carstens M, Denby K J. 2006. PAMP recognition and the plant-pathogen arms race. BioEssays, 28, 880- 889.

 Jafary H, Albertazzi G, Marcel T C, Niks R E. 2008. High diversity of genes for nonhost resistance of barley to heterologous rust fungi. Genetics, 178, 2327-2339

 Jafary H, Szabo L J, Niks R E. 2006. Innate nonhost immunity in barley to different heterologous rust fungi is controlled by sets of resistance genes with different and overlapping specificities. Molecular Plant-Microbe Interactions, 19, 1270-1279

 Johnson R, Lovell N K. 1994. Genetics of resistance of wheat to barley attacking races of Puccinia striiformis. Cereal Rusts and Powdery Mildews Bulletin, 22, 32-40

 Jones J D, Dangl J L. 2006. The plant immune system. Nature, 444, 323-329

 Kamoun S. 2006. A catalogue of the effector secretome of plant pathogenic Oomycetes. Annual Review of Phytopathology, 44, 41-60

 Krattinger S G, Lagudah E S, Spielmeyer W, Singh R P, Huerta-Espino J, McFadden H, Bossolini E, Selter L L, Keller B. 2009. A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science, 323, 1360-1363

Lahaye T, Bonas U 2001. Molecular secrets of bacterial type III effector proteins. Trends in Plant Science, 6, 479-485

 Li X, Lin H, Zhang W, Zou Y, Zhang J, Tang X, Zhou J M. 2005. Flagellin induces innate immunity in nonhost interactions that is suppressed by Pseudomonas syringae effectors. Proceedings of the National Academy of Sciences of the United States of America, 102, 12990- 12995.

 Lillemo M, Asalf B, Singh R P, Huerta-Espino J, Chen X M, He Z H, Bjornstad A. 2008. The adult plant rust resistance loci Lr34/Yr18 and Lr46/Yr29 are important determinants of partial resistance to powdery mildew in bread wheat line Saar. Theoretical and Applied Genetics, 116, 1155-1166

 Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M, Stein M, Landtag J, Brandt W, Rosahl S, Scheel D, et al. 2005. Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science, 310, 1180- 1183.

Lu M, Tang X, Zhou J M. 2001. Arabidopsis NHO1 is required for general resistance against Pseudomonas bacteria. The Plant Cell, 13, 437-447

 Mackey D, McFall A J. 2006. MAMPs and MIMPs: proposed classifications for inducers of innate immunity. Molecular Microbiology, 61, 1365-1371

 Mains E B. 1933. Host specialization in the leaf rust of grasses, Puccinia rubigo-vera. Papers of the Michigan Academy of Science, Arts and Letters, XVII, 289-394

 Marcel T C, Aghnoum R, Durand J, Varshney R K, Niks R E. 2007b. Dissection of the barley 2L1.0 region carrying the ‘Laevigatum’ quantitative resistance gene to leaf rust using near isogenic lines (NIL) and sub-NIL. Molecular Plant-Microbe Interactions, 20, 1604-1615

 Marcel T C, Gorguet, M B. Truong T, Kohutova Z, Vels A, Niks R E. 2008. Isolate-specificity of quantitative trait loci for partial resistance of barley to Puccinia hordei confirmed in mapping populations and near-isogenic lines. New Phytologist, 177, 743-755

 Marcel T C, Varshney R K, Barbieri M, Jafary H, de Kock M J D, Graner A, Niks R E. 2007a. A high-density consensus map of barley to compare the distribution of QTLs for partial resistance to Puccinia hordei and of defence gene homologues. Theoretical and applied Genetics, 114, 487-500

 Martens J W, Green G J, Buchannon K W. 1983. Inheritance of resistance to Puccinia graminis f.sp. avenae in a Hordeum vulgare selection. Canadian Journal of Plant Pathology, 5, 266-268

 Niks R E. 1987. Nonhost plant species as donors for resis- tan ce to pathogens with narrow host range. I. Deter mina- tion of nonhost status. Euphytica, 36, 841-852

 Niks R E, 1988. Nonhost plant species as donors for resis- tance to pathogens with narrow host range. II. Con cepts and evidence on the genetic basis of nonhost resis tance. Euphytica, 37, 89-99

 Niks R E, Marcel T C. 2009. Nonhost resistance and basal resistance: how to explain specificity? New Phytologist, 182, 817-828

 Nomura K, Melotto M, He S Y. 2005. Suppression of host defence in compatible plant - Pseudomonas syringae interactions. Current Opinion in Plant Biology, 8, 361- 368.

O’Connell R J, Panstruga R. 2006. Tête à tête inside a plant cell: establishing compatibility between plants and biotrophic fungi and oomycetes. New Phytologist, 171, 699-718

 Pahalawatta V, Chen X M. 2005. Inheritance and molecular mapping of barley genes conferring resistance to wheat stripe rust. Phytopathology, 95, 884-889

 Panstruga R. 2003. Establishing compatibility between plants and obligate pathogens. Current Opinion in Plant Biology, 6, 320-326

 Rodrigues P, Garrood J M, Shen Q H, Smith P H, Boyd L A. 2004. The genetics of non-host disease resistance in wheat to barley yellow rust. Theoretical and Applied Genetics, 109, 425-432

 Schulze-Lefert P, Panstruga R. 2011. A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends in Plant Science, 16, 117-125

 Schweizer P. 2007. Nonhost resistance of plants to powdery mildew - New opportunities to unravel the mystery. Physiological and Molecular Plant Pathology, 70, 3-7

 Shao F, Golstein C, Ade J, Stoutemyer M, Dixon J E, Innes R W. 2003. Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science, 301, 1230-1233

 Shafiei R, Hang C, Kang J G, Loake G J. 2007. Identification of loci controlling non-host disease resistance in Arabidopsis against the leaf rust pathogen Puccinia triticina. Molecular Plant Pathology, 8, 773-784

 Truman W, de Zabala M T, Grant M. 2006. Type III effectors orchestrate a complex interplay between transcriptional networks to modify basal defence responses during pathogenesis and resistance. The Plant Journal, 46, 14-33

 Yeo F K S, Hensel G, Vozábová T, Martin-Sanz A, Marcel T C, Kumlehn J J, Niks R E. 2014. Golden SusPtrit - a genetically well transformable barley line for studies on the resistance to rust fungi. Theoretical and Applied Genetics, doi: 10.1007/s00122-013-2221-7
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