Understanding plant immunity as a surveillance system to detect invasion
Cook III, D.E. ; Mesarich, C.H. ; Thomma, B.P.H.J. - \ 2015
Annual Review of Phytopathology 53 (2015). - ISSN 0066-4286 - p. 541 - 563.
disease-resistance gene - bacterial elicitor flagellin - syringae effectors avrb - host-selective toxins - innate immunity - arabidopsis-thaliana - molecular-patterns - microbe interactions - durable resistance - necrotrophic pathogens
Various conceptual models to describe the plant immune system have been presented. The most recent paradigm to gain wide acceptance in the field is often referred to as the zigzag model, which reconciles the previously formulated gene-for-gene hypothesis with the recognition of general elicitors in a single model. This review focuses on the limitations of the current paradigm of molecular plant-microbe interactions and how it too narrowly defines the plant immune system. As such, we discuss an alternative view of plant innate immunity as a system that evolves to detect invasion. This view accommodates the range from mutualistic to parasitic symbioses that plants form with diverse organisms, as well as the spectrum of ligands that the plant immune system perceives. Finally, how this view can contribute to the current practice of resistance breeding is discussed.
An updated conventional- and a novel GM potato late blight R gene differential set for virulence monitoring of Phytophthora infestans
Suxian Zhu, Suxian ; Vossen, J.H. ; Bergervoet-van Deelen, J.E.M. ; Nijenhuis, M.A. ; Kodde, L.P. ; Kessel, G.J.T. ; Vleeshouwers, V.G.A.A. ; Visser, R.G.F. ; Jacobsen, E. - \ 2015
Euphytica 202 (2015)2. - ISSN 0014-2336 - p. 219 - 234.
resistance genes - solanum-bulbocastanum - disease resistance - durable resistance - rxlr effectors - united-states - pathogen - population - races - diversity
Late blight is an important disease in potato that is caused by the oomycete Phytophthora infestans. In the past, Solanum demissum late blight resistance (R) genes were introgressed into cultivated potato (Solanum tuberosum). Eleven of these resistant plants were selected to characterize the virulence spectrum of individual P. infestans isolates and to monitor the dynamics of virulence in P. infestans populations. These plants are referred to as the Mastenbroek and Black differential sets. It has long been assumed that each differential plant contained one single R gene. In the current study and previous studies, however, most Mastenbroek differential plants were shown to harbor multiple R gene(s), which blurs virulence typing of late blight isolates. In order to acquire more accurate virulence profiles, we extended the Mastenbroek differential set with Solanum spp. plants harboring reduced R gene complexity and with plants containing recently identified R genes from related but different Solanum species. In addition, a differential set of ten Genetically Modified (GM) plants harboring single late blight R genes in the same genetic background (Desiree). By analyzing the virulence spectra of recently collected isolates using both newly described differential sets, we found that the GM Desiree differential set was more accurate for isolate virulence typing than the conventional (extended) differential set. Besides, the GM Desiree differential set was shown to be useful as trap plants to isolate novel P. infestans strains and to monitor virulence towards particular R genes in P. infestans populations `on site´. Legislative restrictions are, however, limiting the use of the GM Desiree differential set.
Increased difficulties to control late blight in Tunisia are caused by a genetically diverse Phytophthora infestans population next to the clonal lineage NA-01
Harbaoui, K. ; Hamada, W. ; Li, Y. ; Vleeshouwers, V.G.A.A. ; Lee, T.A.J. van der - \ 2014
Plant Disease 98 (2014)7. - ISSN 0191-2917 - p. 898 - 908.
genotypic diversity - durable resistance - potato - tomato - plant - netherlands - virulence
In Tunisia, late blight caused by Phytophthora infestans is a serious threat to potato and tomato. The Mediterranean weather conditions can be conducive to infection in all seasons and the host crops, tomato and potato, are grown year round. Potato is planted and harvested in two to four overlapping intervals from August to June and tomato is grown both in open fields and in greenhouses. The consequences of these agricultural practices and the massive import of seed potato on the genetic variation of P. infestans are largely unknown. We conducted a survey in which 165 P. infestans isolates, collected from five subregions in Tunisia between 2006 and 2008, on which we studied genotypic diversity through nuclear (simple-sequence repeat [SSR]) markers and combined this with a previous study on their mitochondrial haplotypes (mtDNA). The phylogenetic analysis revealed the presence of a major clonal lineage (NA-01, A1 mating type, mitochondrial haplotype Ia). Isolates belonging to this clonal lineage were found in all regions and showed a relatively simple virulence pattern on a potato differential set carrying different Solanum demissum resistance genes. Apart from isolates belonging to this NA-01 clonal lineage, a group of isolates was found that showed a high genetic diversity, comprising both mating types and a more complex race structure that was found in the regions where late blight on potato was more difficult to control. The population on potato and tomato seems to be under different selection pressures. Isolates collected from tomato showed a low genetic diversity even though potato isolates collected simultaneously from the same location showed a high genetic diversity. Based on the SSR profile comparison, we could demonstrate that the four major clonal lineages found in the Netherlands and also in other European countries could not be found in Tunisia. Despite the massive import of potato seed from Europe, the P. infestans population in Tunisia was found to be clearly distinct
Functional analysis of potato genes involved in quantitative resistance to Phytophthora infestans
Du, J. ; Tian, Z.D. ; Liu, J. ; Vleeshouwers, V.G.A.A. ; Shi, X.L. ; Xie, C.H. - \ 2013
Molecular Biology Reports 40 (2013)2. - ISSN 0301-4851 - p. 957 - 967.
systemic acquired-resistance - beta-aminobutyric acid - late blight - disease resistance - nicotiana-benthamiana - anionic peroxidase - durable resistance - genome sequence - virus - plant
The most significant threat to potato production worldwide is the late blight disease, which is caused by the oomycete pathogen Phytophthora infestans. Based on previous cDNA microarrays and cDNA-amplified fragment length polymorphism analysis, 63 candidate genes that are expected to contribute to developing a durable resistance to late blight were selected for further functional analysis. We performed virus-induced gene silencing (VIGS) to these candidate genes on both Nicotiana benthamiana and potato, subsequently inoculated detached leaves and assessed the resistance level. Ten genes decreased the resistance to P. infestans after VIGS treatment. Among those, a lipoxygenase (LOX; EC 220.127.116.11) and a suberization-associated anionic peroxidase affected the resistance in both N. benthamiana and potato. Our results identify genes that may play a role in quantitative resistance mechanisms to late blight.
Fine mapping quantitative resistances to downy mildew in lettuce revealed multiple sub-QTLs with plant stage dependent effects reducing or even promoting the infection
Boer, E. den; Zhang, N. ; Pelgrom, K.T.B. ; Visser, R.G.F. ; Niks, R.E. ; Jeuken, M.J.W. - \ 2013
Theoretical and Applied Genetics 126 (2013)12. - ISSN 0040-5752 - p. 2995 - 3007.
backcross inbred lines - trait locus qtl - bremia-lactucae - leaf rust - durable resistance - stripe rust - genetic dissection - disease resistance - nonhost resistance - wild lettuce
Previous studies on the genetic dissection of the complete resistance of wild lettuce, Lactuca saligna, to downy mildew revealed 15 introgression regions that conferred plant stage dependent quantitative resistances (QTLs). Three backcross inbred lines (BILs), carrying an individual 30–50 cM long introgression segment from L. saligna in a cultivated lettuce, L. sativa, background, reduced infection by 60–70 % at young plant stage and by 30–50 % at adult plant stage in field situations. We studied these three quantitative resistances in order to narrow down their mapping interval and determine their number of loci, either single or multiple. We performed recombinant screenings and developed near isogenic lines (NILs) with smaller overlapping L. saligna introgressions (substitution mapping). In segregating introgression line populations, recombination was suppressed up to 17-fold compared to the original L. saligna × L. sativaF2 population. Recombination suppression depended on the chromosome region and was stronger suppressed at the smallest introgression lengths. Disease evaluation of the NILs revealed that the resistance of all three BILs was not explained by a single locus but by multiple sub-QTLs. The 17 L. saligna-derived sub-QTLs had a smaller and plant stage dependent resistance effect, some segments reducing; others even promoting downy mildew infection. Implications for lettuce breeding are outlined.
Evidence fr a Minor Gene-for-Minor Gene Interaction Explaining Nonhypersensitive Polygenic Partial Disease Resistance
González, A.M. ; Marcel, T.C. ; Niks, R.E. - \ 2012
Phytopathology 102 (2012)11. - ISSN 0031-949X - p. 1086 - 1093.
barley leaf rust - quantitative trait loci - isolate-specific qtls - near-isogenic lines - plant immune-system - puccinia-hordei - durable resistance - development stage - broad-spectrum - latent period
Partial resistance is a quantitative type of resistance that, by definition of Parlevliet, is not based on hypersensitivity. It is largely pathotype nonspecific, although some minor isolate-specific responses have been reported. In order to elucidate the isolate specificity of individual genes for partial resistance, three barley recombinant inbred line mapping populations were analyzed for resistance to the leaf rust fungus Puccinia hordei. The mapping populations were inoculated with one isolate avirulent and two isolates virulent to resistance gene Rph7g. Six significant quantitative trait loci (QTLs) were detected. Of these, two (Rphq3 and Rphq11) were detected with only the avirulent isolate (1.2.1.) and one (Rphq18) only with both virulent isolates (CO-04 and 28.1). The effectiveness of these QTLs was tested with 14 isolates, using a tester set of genotypes containing alleles for resistance or susceptibility for these QTLs. QTL Rphq18 was effective to only two isolates, CO-04 and 28.1, whereas Rphq3 and Rphq11 were ineffective to CO-04 and 28.1 but effective to all other isolates, except one. This resulted in a significant Person's differential interaction, which is a hallmark of a gene–for–gene interaction. The minor gene–for–minor gene interaction is not based on hypersensitivity and there is no evidence that the resistance is based on genes belonging to the nucleotide-binding leucine-rich repeat class.
New broad-spectrum resistance to septoria tritici blotch derived from synthetic hexaploid wheat
Tabib Ghaffary, M.S. ; Faris, J.D. ; Friesen, T.L. ; Visser, R.G.F. ; Lee, T.A.J. van der; Robert, O. ; Kema, G.H.J. - \ 2012
Theoretical and Applied Genetics 124 (2012)1. - ISSN 0040-5752 - p. 125 - 142.
mycosphaerella graminicola pathosystem - quantitative trait loci - aegilops-tauschii coss. - stagonospora nodorum blotch - multiple fungal pathogens - genetic-linkage map - bread wheat - durable resistance - rust resistance - common wheat
Septoria tritici blotch (STB), caused by the ascomycete Mycosphaerella graminicola, is one of the most devastating foliar diseases of wheat. We screened five synthetic hexaploid wheats (SHs), 13 wheat varieties that represent the differential set of cultivars and two susceptible checks with a global set of 20 isolates and discovered exceptionally broad STB resistance in SHs. Subsequent development and analyses of recombinant inbred lines (RILs) from a cross between the SH M3 and the highly susceptible bread wheat cv. Kulm revealed two novel resistance loci on chromosomes 3D and 5A. The 3D resistance was expressed in the seedling and adult plant stages, and it controlled necrosis (N) and pycnidia (P) development as well as the latency periods of these parameters. This locus, which is closely linked to the microsatellite marker Xgwm494, was tentatively designated Stb16q and explained from 41 to 71% of the phenotypic variation at seedling stage and 28-31% in mature plants. The resistance locus on chromosome 5A was specifically expressed in the adult plant stage, associated with SSR marker Xhbg247, explained 12-32% of the variation in disease, was designated Stb17, and is the first unambiguously identified and named QTL for adult plant resistance to M. graminicola. Our results confirm that common wheat progenitors might be a rich source of new Stb resistance genes/QTLs that can be deployed in commercial breeding programs
Genetic mapping of 14 avirulence genes in an EU-B04 x 1639 progeny of Venturia inaequalis
Broggini, G.A.L. ; Bus, V.G.M. ; Parravicini, G. ; Kumar, S. ; Groenwold, R. ; Gessler, C. - \ 2011
Fungal Genetics and Biology 48 (2011)2. - ISSN 1087-1845 - p. 166 - 176.
receptor-like genes - apple scab resistance - cke wint - disease-resistance - flax rust - magnaporthe-grisea - controlling pathogenicity - durable resistance - mutant characters - melampsora-lini
Durable resistance to apple scab (Venturia inaequalis (Cke) Wint; anamorph Spilocaea pomi Fries) is one of the major goals of apple (Malus) breeding programs. Since current scab resistance breeding is heavily reliant on genes with gene-for-gene relationships, a good understanding of the genetic basis of host–pathogen interactions needs to be developed for this strategy to be successful. While the genomic organization of apple scab resistance genes has been studied extensively, little is known about the avirulence genes in the pathogen. The progeny of a cross of European V. inaequalis race (1) isolate EU-B04 and race (1,2,8,9) isolate 1639 was used to generate a genetic map based on microsatellite and AFLP markers, and investigated for inheritance of avirulence traits on 20 Malus accessions representing 17 scab resistance genes. The accessions comprised scab differential hosts (0), (1), (2), (8), and (9), and hosts carrying known as well as not previously reported secondary resistance genes, including some identified in crosses that have resistant accessions ‘Geneva’, ‘Dolgo’, Malus baccata jackii, M. micromalus, or ‘Antonovka’ in their pedigree. The latter genes appear to be narrow spectrum genes that showed gene-for-gene relationships as a segregation ratio of Avr:avr = 1:1 was observed on 12 accessions, while a ratio of 3:1 was observed on five accessions and a ratio of 7:1 on one host. All progenies were shown to be pathogenic, as all of them were able to infect hosts (0) and (1). A genetic map consisting of 15 major linkage groups (LGs) and spanning 972 cM was generated with the aid of 156 markers. The map position of 12 avirulence traits was determined: eight avirulence genes mapped into two separate clusters (1: AvrVdg2, AvrVv1, AvrVu1, AvrVrjrd; and 2: AvrVu2, AvrVh3.2, AvrVs1, AvrVu4), while four avirulence genes (AvrRvi8, AvrVv2, AvrVt57 and AvrVsv) mapped to different LGs. AvrRvi2 and AvrRvi9 also are genetically linked, but showed an interaction with AvrRvi8, the nature of which is unclear. While AvrRvi8 segregated at 1:1 ratio, the other two Avrs segregated at 3:1 ratios. However, all progeny avirulent on hosts (2) and (9) were also avirulent on host (8) and further research is required to determine the avirulence gene relationships. A further two independently segregating loci, AvrRvi1 and AvrRvi6, identified in previous studies, were mapped by inference based on their known linkage to SSR markers. The clustering of avirulence genes in V. inaequalis reflecting the clustering of resistance genes in Malus suggests this pathosystem is a classical example of an “arms race” between host and pathogen. This also seems to apply to the narrow spectrum scab resistance genes, which may imply a larger role in plant defense for these genes than has been assumed to date
The RPi-mcd1 Locus from Solanum microdontum Involved in Resistance to Phytophthora infestans, Causing a Delay in Infection, Maps on Potato Chromosome 4 in a Cluster of NBS-LRR Genes
Tan, M.Y.A. ; Hutten, R.C.B. ; Celis Gamboa, B.C. ; Park, T.H. ; Niks, R.E. ; Visser, R.G.F. ; Eck, H.J. van - \ 2008
Molecular Plant-Microbe Interactions 21 (2008)7. - ISSN 0894-0282 - p. 909 - 918.
late blight resistance - broad-spectrum resistance - quantitative trait loci - foliage maturity type - field-resistance - hypersensitive response - durable resistance - linkage maps - r-genes - bulbocastanum
The distinction between field resistance and resistance based on resistance (R) genes has been proven valid for many plant¿pathogen interactions. This distinction does not seem to be valid for the interaction between potato and late blight. In this study, a locus involved in late blight resistance, derived from Solanum microdontum, provides additional evidence for this lack of distinction. The resistance is associated with a hypersensitive response and results in a delay of infection of approximately 1 to 2 weeks. Both a quantitative as well as a qualitative genetic approach were used, based on data from a field assay. Quantitative trait locus (QTL) analysis identified a QTL on chromosome 4 after correction of the resistance data for plant maturity. A qualitative genetic analysis resulted in the positioning of this locus on the short arm of chromosome 4 in between amplified fragment length polymorphism marker pCTmACG_310 and cleaved amplified polymorphic sequence markers TG339 and T0703. This position coincides with a conserved Phytophthora R gene cluster which includes R2, R2-like, RPi-blb3, and RPi-abpt. This implies that RPi-mcd1 is the fifth R gene of this nucleotide-binding site leucine-rich repeat cluster. The implications of our results on R-gene-based and field resistance are discussed
The Rpi-blb2 gene from Solanum bulbocastanum is a Mi-1 gene homolog conferring broadspectrum late blight resistance in potato
Vossen, E.A.G. van der; Gross, J. ; Sikkema, A. ; Muskens, M. ; Wouters, T.C.A.E. ; Wolters, P. ; Pereira, A.B. ; Allefs, S. - \ 2005
The Plant Journal 44 (2005)2. - ISSN 0960-7412 - p. 208 - 222.
root-knot nematodes - disease-resistance - phytophthora-infestans - cell-death - durable resistance - cultivated potato - virus-resistance - tolerance gene - iii effector - tomato
The necessity to develop potato and tomato crops that possess durable resistance against the oomycete pathogen Phytophthora infestans is increasing as more virulent, crop-specialized and pesticide resistant strains of the pathogen are rapidly emerging. Here, we describe the positional cloning of the Solanum bulbocastanum-derived Rpi-blb2 gene, which even when present in a potato background confers broad-spectrum late blight resistance. The Rpi-blb2 locus was initially mapped in several tetraploid backcross populations, derived from highly resistant complex interspecific hybrids designated ABPT (an acronym of the four Solanum species involved:S. acaule, S. bulbocastanum, S. phureja and S. tuberosum), to the same region on chromosome 6 as the Mi-1 gene from tomato, which confers resistance to nematodes, aphids and white flies. Due to suppression of recombination in the tetraploid material, fine mapping was carried out in a diploid intraspecific S. bulbocastanum F1 population. Bacterial artificial chromosome (BAC) libraries, generated from a diploid ABPT-derived clone and from the resistant S. bulbocastanum parent clone, were screened with markers linked to resistance in order to generate a physical map of the Rpi-blb2 locus. Molecular analyses of both ABPT- and S. bulbocastanum¿derived BAC clones spanning the Rpi-blb2 locus showed it to harbor at least 15 Mi-1 gene homologs (MiGHs). Of these, five were genetically determined to be candidates for Rpi-blb2. Complementation analyses showed that one ABPT- and one S. bulbocastanum-derived MiGH were able to complement the susceptible phenotype in both S. tuberosum and tomato. Sequence analyses of both genes showed them to be identical. The Rpi-blb2 protein shares 82% sequence identity to the Mi-1 protein. Significant expansion of the Rpi-blb2 locus compared to the Mi-1 locus indicates that intrachromosomal recombination or unequal crossing over has played an important role in the evolution of the Rpi-blb2 locus. The contrasting evolutionary dynamics of the Rpi-blb2/Mi-1 loci in the two related genomes may reflect the opposite evolutionary potentials of the interacting pathogens
Stability of partial resistance in potato cultivars exposed to aggressive strains of Phytophthora infestans
Flier, W.G. ; Bosch, G.B.M. van den; Turkensteen, L.J. - \ 2003
Plant Pathology 52 (2003)3. - ISSN 0032-0862 - p. 326 - 337.
late blight - differential interaction - durable resistance - field-resistance - tuber rot - r-genes - netherlands - populations - host - diversity
Potato cultivars were evaluated for their resistance responses to aggressive strains of Phytophthora infestans in field and laboratory experiments. Analysis of variance revealed differential cultivar-by-isolate interactions for both foliar and tuber blight resistance. Differential responses occur as revealed by specific susceptibilities of cultivars to certain pathogen genotypes and changing rank order. In general, severity of late blight epidemics as observed in the haulms did not correlate well with foliar blight resistance ratings as presented in the National List of Recommended Potato Varieties. No significant correlation was found between tuber blight incidence under field conditions and the tuber blight rating in the National List. Also, there was no relation between the field and laboratory tuber blight resistance assessments. A significant association was demonstrated between late blight infection in the foliage and tuber blight incidence under field conditions. The presence of differential interaction, independent of R-gene-based resistance, indicates some adaptation of P. infestans to partial resistance and consequently adverse effects on the stability and durability of partial resistance to potato late blight