The John Innes Centre Publications Repository contains details of all publications resulting from our researchers.
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Population structure of the ash dieback pathogen, Hymenoscyphus fraxineus, in relation to its mode of arrival in the UK
Plant Pathology (10.1111/ppa.12762) 12762
Publisher's version: 10.1111/ppa.12762
ID: 57264read more
The ash dieback fungus, Hymenoscyphus fraxineus, a destructive, alien pathogen of common ash (Fraxinus excelsior), has spread across Europe over the past 25 years and was first observed in the UK in 2012. To investigate the relationship of the pathogen's population structure to its mode of arrival, isolates were obtained from locations in England and Wales, either where established natural populations of ash had been infected by wind-dispersed ascospores or where the fungus had been introduced on imported planting stock. Population structure was determined by tests for vegetative compatibility (VC), mating type and single-nucleotide polymorphisms (SNPs). VC heterogeneity was high at all locations, with 96% of isolate pairings being incompatible. Frequencies of the MAT1-1-1 and MAT1-2-1 idiomorphs were approximately equal, consistent with H. fraxineus being an obligate outbreeder. Most SNP variation occurred within study location and there was little genetic differentiation between the two types of location in the UK, or between pathogen populations in the UK and continental Europe. There was modest differentiation between UK subpopulations, consistent with genetic variation between source populations in continental Europe. However, there was no evidence of strong founder effects, indicating that numerous individuals of H. fraxineus initiated infection at each location, regardless of the route of pathogen transmission. The ssRNA virus HfMV1 was present at moderate to high frequencies in all UK subpopulations. The results imply that management of an introduced plant pathogen requires action against its spread at the continental level involving coordinated efforts by European countries.
Plant Biotechnology Journal (Plant Biotechnol J. 2017 Apr 24. doi: 10.1111/pbi.12749. [Epub ahead of print]) doi: 10.1111/pbi.12749
Publisher's version: 10.1111/pbi.12749
ID: 56109read more
Zinc (Zn) is essential for all life forms, including humans. It is estimated that around two billion people are deficient in their Zn intake. Human dietary Zn intake relies heavily on plants, which in many developing countries consists mainly of cereals. The inner part of cereal grain, the endosperm, is the part that is eaten after milling but contains only a quarter of the total grain Zn. Here we present results demonstrating that endosperm Zn content can be enhanced through expression of a transporter responsible for vacuolar Zn accumulation in cereals. The barley (Hordeum vulgare) vacuolar Zn transporter HvMTP1 was expressed under the control of the endosperm-specific D-hordein promoter. Transformed plants exhibited no significant change in growth but had higher total grain Zn concentration, as measured by ICP-OES, compared to parental controls. Compared with Zn, transformants had smaller increases in concentrations of Cu and Mn but not Fe. Staining grain cross-sections with the Zn-specific stain DTZ revealed a significant enhancement of Zn accumulation in the endosperm of two of three transformed lines, a result confirmed by ICP-OES in the endosperm of dissected grain. Synchrotron X-ray fluorescence analysis of longitudinal grain sections demonstrated a redistribution of grain Zn from aleurone to endosperm. We argue that this proof-of-principle study provides the basis of a strategy for biofortification of cereal endosperm with Zn. This article is protected by copyright. All rights reserved.
Early molecular signatures of responses of wheat to Zymoseptoria tritici in compatible and incompatible interactions
Plant Pathology (-) -
Publisher's version: 10.1111/ppa.12633
ID: 55181read more
Zymoseptoria tritici, the causal agent of Septoria tritici blotch, a serious foliar disease of wheat, is a necrotrophic pathogen which undergoes a long latent period. Emergence of insensitivity to fungicides and pesticide reduction policies mean there is a pressing need to understand Septoria and control it through greater varietal resistance. Stb6 and Stb15, the most common qualitative resistance genes in modern wheat cultivars, determine specific resistance to avirulent fungal genotypes following a gene-for-gene relationship. We investigated compatible and incompatible interactions of wheat with Z. tritici using eight combinations of cultivars and isolates, with the aim of identifying molecular responses which could be used as markers for disease resistance during the early, symptomless phase of colonisation. The accumulation of TaMPK3 was estimated using Western blotting and the expression of genes implicated in gene-for-gene interactions of plants with a wide range of other pathogens was measured by qRT-PCR during the pre-symptomatic stages of infection. Production of TaMPK3 and expression of most of the genes responded to inoculation with Z. tritici but varied considerably between experimental replicates. There was no significant difference, however, between compatible and incompatible interactions in any of the responses tested. These results demonstrate that the molecular biology of the gene-for-gene interaction between wheat and Septoria is unlike that in many other plant diseases, indicate that environmental conditions may strongly influence early responses of wheat to infection byZ. tritici, and emphasise the importance of including both compatible and incompatible interactions when investigating the biology of this complex pathosystem.
Molecular plant pathology (18) 276-292
Publisher's version: 10.1111/mpp.12482
ID: 55442read more
An association genetics analysis was conducted to investigate the genetics of resistance to Septoria tritici blotch, caused by the fungus Zymoseptoria tritici (alternatively Mycosphaerella graminicola), in cultivars and breeding lines of wheat (Triticum aestivum) used in the UK between 1860 and 2000. The population was tested with Diversity Array Technology (DArT) and simple-sequence repeat (SSR or microsatellite) markers. The lines formed a single population with no evidence for subdivision, because there were several common ancestors of large parts of the pedigree. Quantitative trait loci (QTLs) controlling Septoria resistance were postulated on 11 chromosomes, but 38% of variation was not explained by the identified QTLs. Calculation of best linear unbiased predictions (BLUPs) identified lineages of spring and winter wheat carrying different alleles for resistance and susceptibility. Abundant variation in Septoria resistance may be exploited by crossing well-adapted cultivars in different lineages to achieve transgressive segregation and thus breed for potentially durable quantitative resistance, whereas phenotypic selection for polygenic quantitative resistance should be effective in breeding cultivars with increased resistance. The most potent allele reducing susceptibility to Septoria, on chromosome arm 6AL, was associated with reduced leaf size. Genes which increase susceptibility to Septoria may have been introduced inadvertently into UK wheat breeding programmes from cultivars used to increase yield, rust resistance and eyespot resistance between the 1950s and 1980s. This indicates the need to consider trade-offs in plant breeding when numerous traits are important and to be cautious about the use of non-adapted germplasm.
Proposal for a unified nomenclature for target-site mutations associated with resistance to fungicides.
Pest management science (72) 1449-59
Publisher's version: 10.1002/ps.4301
ID: 56678read more
Evolved resistance to fungicides is a major problem limiting our ability to control agricultural, medical and veterinary pathogens and is frequently associated with substitutions in the amino acid sequence of the target protein. The convention for describing amino acid substitutions is to cite the wild-type amino acid, the codon number and the new amino acid, using the one-letter amino acid code. It has frequently been observed that orthologous amino acid mutations have been selected in different species by fungicides from the same mode of action class, but the amino acids have different numbers. These differences in numbering arise from the different lengths of the proteins in each species. The purpose of the present paper is to propose a system for unifying the labelling of amino acids in fungicide target proteins. To do this we have produced alignments between fungicide target proteins of relevant species fitted to a well-studied 'archetype' species. Orthologous amino acids in all species are then assigned numerical 'labels' based on the position of the amino acid in the archetype protein. © 2016 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.
Increased yield stability of field-grown winter barley (Hordeum vulgare L.) varietal mixtures through ecological processes
Crop Protection (85) 1-8
Publisher's version: doi:10.1016/j.cropro.2016.03.001
ID: 53086read more
Crop variety mixtures have the potential to increase yield stability in highly variable and unpredictable environments, yet knowledge of the specific mechanisms underlying enhanced yield stability has been limited. Ecological processes in genetically diverse crops were investigated by conducting field trials with winter barley varieties (Hordeum vulgare), grown as monocultures or as three-way mixtures in fungicide treated and untreated plots at three sites. Mixtures achieved yields comparable to the best performing monocultures whilst enhancing yield stability despite being subject to multiple predicted and unpredicted abiotic and biotic stresses including brown rust (Puccinia hordei) and lodging. There was compensation through competitive release because the most competitive variety overyielded in mixtures thereby compensating for less competitive varieties. Facilitation was also identified as an important ecological process within mixtures by reducing lodging. This study indicates that crop varietal mixtures have the capacity to stabilise productivity even when environmental conditions and stresses are not predicted in advance. Varietal mixtures provide a means of increasing crop genetic diversity without the need for extensive breeding efforts. They may confer enhanced resilience to environmental stresses and thus be a desirable component of future cropping systems for sustainable arable farming.
Reduction of Growth and Reproduction of the Biotrophic Fungus Blumeria graminis in the Presence of a Necrotrophic Pathogen.
Frontiers in Plant Science (Biotrophic plant-microbe interactions ) doi-10.3389/fpls.2016.00742
Publisher's version: 10.3389/fpls.2016.00742
ID: 53287read more
Crops are attacked by many potential pathogens with differing life-history traits, which raises the question of whether or not the outcome of infection by one pathogen may be modulated by a change in the host environment brought on by infection by another pathogen. We investigated the host-mediated interaction between the biotroph Blumeria graminis f.sp. tritici (Bgt), the powdery mildew pathogen of wheat, and the necrotroph Zymoseptoria tritici, which has a long latent, endophytic phase following which it switches to a necrotrophic phase, resulting in the disease symptoms of Septoria tritici blotch. Both diseases are potentially severe in humid temperate climates and are controlled by fungicides and by growing wheat varieties with partial resistance. The compatible interaction between Z. tritici and the host reduced the number, size, and reproductive capacity of mildew colonies that a normally virulent Bgt isolate would produce but did not significantly alter the early development of Bgt on the leaf. The effect on virulent Bgt was elicited only by viable spores of Z. tritici. Notably, this effect was seen before the necrotic foliar symptoms induced by Z. tritici were visible, which implies there is a physiological interaction during the latent, endophytic period of Z. tritici, which either takes place directly between this fungus and Bgt or is mediated by the wheat leaf. Information on how different pathogens interact in host plants may allow plant breeders and others to improve the design of screening trials and selection of germplasm.
Molecular markers for tracking the origin and worldwide distribution of invasive strains of Puccinia striiformis
Ecology and Evolution (6) 27902804
Publisher's version: 10.1002/ece3.2069
ID: 52832read more
Investigating the origin and dispersal pathways is instrumental to mitigate threats and economic and environmental consequences of invasive crop pathogens. In the case of Puccinia striiformis causing yellow rust on wheat, a number of economically important invasions have been reported, e.g., the spreading of two aggressive and high temperature adapted strains to three continents since 2000. The combination of sequence-characterized amplified region (SCAR) markers, which were developed from two specific AFLP fragments, differentiated the two invasive strains, PstS1 and PstS2 from all other P. striiformis strains investigated at a worldwide level. The application of the SCAR markers on 566 isolates showed that PstS1 was present in East Africa in the early 1980s and then detected in the Americas in 2000 and in Australia in 2002. PstS2 which evolved from PstS1 became widespread in the Middle East and Central Asia. In 2000, PstS2 was detected in Europe, where it never became prevalent. Additional SSR genotyping and virulence phenotyping revealed 10 and six variants, respectively, within PstS1 and PstS2, demonstrating the evolutionary potential of the pathogen. Overall, the results suggested East Africa as the most plausible origin of the two invasive strains. The SCAR markers developed in the present study provide a rapid, inexpensive, and efficient tool to track the distribution of P. striiformis invasive strains, PstS1 and PstS2.
Evolution of the EKA family of powdery mildew avirulence-effector genes from the ORF 1 of a LINE retrotransposon.
BMC Genomics (16) 917
Publisher's version: 10.1186/s12864-015-2185-x
ID: 52122read more
The Avrk1 and Avra10 avirulence (AVR) genes encode effectors that increase the pathogenicity of the fungus Blumeria graminis f.sp. hordei (Bgh), the powdery mildew pathogen, in susceptible barley plants. In resistant barley, MLK1 and MLA10 resistance proteins recognize the presence of AVRK1 and AVRA10, eliciting the hypersensitive response typical of gene for gene interactions. Avrk1 and Avra10 have more than 1350 homologues in Bgh genome, forming the EKA (Effectors homologous to Avr k 1 and Avr a 10) gene family.
FUNCTIONAL ECOLOGY (30) 649-657
Publisher's version: 10.1111/1365-2435.12552
ID: 53675read more
Experiments were conducted on the role of intra- and inter-genotypic competition in ecological processes operating at the population scale in diseased plant populations. Combinations of Arabidopsis thaliana genotypes showing variation for phenotypic traits relating to competitive ability and pathogen compatibility were infected with the oomycete Hyaloperonospora arabidopsidis and Turnip yellows virus in separate experiments. Plant fitness and competitive ability were estimated from phenotypic measurements. Pathogen-induced reduction in competitive ability for susceptible genotypes increased the competitive ability of resistant genotypes, resulting in maintenance of yield via competitive release. The two diseases had different effects on competitive interactions between plants. In experiments involving the oomycete, the highest yields were produced by mixtures of two weakly competing genotypes. The Arabidopsis model system has elucidated the ecological processes by which compensatory competitive interactions can increase the buffering capacity of plant populations under pathogen attack. Highly competitive genotypes may not maximize the productivity of the population as a whole, as they may over-yield at the expense of less competitive, more productive genotypes. The specific outcomes of competitive interactions cannot be generalized because they depend on the disease and the host genotypes.
Fungal Genetics and Biology (79) 33-41
Publisher's version: 10.1016/j.fgb.2015.04.017
ID: 53717read more
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.
Contribution of the drought tolerance-related Stress-responsive NAC 1 transcription factor to resistance of barley to Ramularia leaf spot
Molecular Plant Pathology (16) 201209
Publisher's version: 10.1111/mpp.12173
ID: 48192read more
NAC proteins are plant transcription factors that are involved in tolerance of abiotic and biotic stress as well as many developmental processes. Stress-responsive NAC 1 (SNAC1) transcription factor is involved in drought tolerance in barley and rice but it was not previously known to have a role in disease resistance. Transgenic over-expression of HvSNAC1 in barley cv. Golden Promise reduced the severity of Ramularia leaf spot (RLS), caused by the fungus Ramularia collo-cygni, but had no effect on disease symptoms caused by Fusarium culmorum, Oculimacula yallundae (eyespot), Blumeria graminis f. sp. hordei (powdery mildew), or Magnaporthe oryzae (blast). The HvSNAC1 transcript was weakly induced in the RLS-susceptible cv. Golden Promise during the latter stages of R. collo-cygni symptom development when infected leaves were senescing. Potential mechanisms controlling HvSNAC1-mediated resistance to RLS were investigated. Gene expression analysis revealed no difference in constitutive levels of antioxidant transcripts in either of the over-expression lines compared to cv. Golden Promise nor was any difference in stomatal conductance or sensitivity to reactive oxygen species-induced cell death observed. Over-expression of HvSNAC1 delayed dark-induced leaf senescence. It is proposed that mechanisms controlled by HvSNAC1 that are involved in tolerance to abiotic stress and inhibit senescence also confer resistance to R. collo-cygni and suppress RLS symptoms. This provides further evidence for an association between abiotic stress and senescence in barley and the development of RLS.
Molecular Plant Pathology (15) 304-14
Publisher's version: 10.1111/mpp.12093
ID: 47571read more
Powdery mildew is an important disease of cereals, affecting both grain yield and end-use quality. The causal agent of powdery mildew on cereals, Blumeria graminis, has been classified into eight formae speciales (ff.spp.), infecting crops and wild grasses. Advances in research on host specificity and resistance, and on pathogen phylogeny and origins, have brought aspects of the subspecific classification system of B.?graminis into ff.spp. into question, because it is based on adaptation to certain hosts rather than strict host specialization. Cereals therefore cannot be considered as typical non-hosts to non-adapted ff.spp. We introduce the term 'non-adapted resistance' of cereals to inappropriate ff.spp. of B.?graminis, which involves both pathogen-associated molecular pattern-triggered immunity (PTI) and effector-triggered immunity (ETI). There is no clear distinction between the mechanisms of resistance to adapted and non-adapted ff.spp. Molecular evolutionary data suggest that the taxonomic grouping of B.?graminis into different ff.spp. is not consistent with the phylogeny of the fungus. Imprecise estimates of mutation rates and the lack of genetic variation in introduced populations may explain the uncertainty with regard to divergence times, in the Miocene or Holocene epochs, of ff.spp. of B.?graminis which infect cereal crop species. We propose that most evidence favours divergence in the Holocene, during the course of early agriculture. We also propose that the forma specialis concept should be retained for B.?graminis pathogenic on cultivated cereals to include clades of the fungus which are strongly specialized to these hosts, i.e. ff.spp. hordei, secalis and tritici, as well as avenae from cultivated A.?sativa, and that the forma specialis concept should no longer be applied to B.?graminis from most wild grasses.
A trade off between mlo resistance to powdery mildew and increased susceptibility of barley to a newly important disease, Ramularia leaf spot.
Journal of Experimental Botany (65) 1025-37
Publisher's version: 10.1093/jxb/ert452
ID: 47570read more
Ramularia leaf spot (RLS), caused by the fungus Ramularia collo-cygni, is a serious, recently emerged disease of barley in Europe and other temperate regions. This study investigated the trade off between strong resistance to powdery mildew conferred by mlo mutant alleles and increased susceptibility to RLS. In field trials and seedling tests, the presence of mlo alleles increased severity of RLS. Genetic analysis of a doubled-haploid population identified one quantitative trait locus for susceptibility to RLS, colocalizing with the mlo-11 allele for mildew resistance. The effect of mlo-11 on RLS severity was environmentally sensitive. Analysis of near-isogenic lines of different mlo mutations in various genetic backgrounds confirmed that mlo alleles increased RLS severity in seedlings and adult plants. For mlo resistance to mildew to be fully effective, the genes ROR1 and ROR2 are required. RLS symptoms were significantly reduced on mlo-5 ror double mutants but fungal DNA levels remained as high as in mlo-5 single mutants, implying that ror alleles modify the transition of the fungus from endophytism to necrotrophy. These results indicate that the widespread use of mlo resistance to control mildew may have inadvertently stimulated the emergence of RLS as a major disease of barley.
Plant Pathology (62 (Suppl. 1)) 1-1
Publisher's version: 10.1111/ppa.12124
ID: 46454read more
no abstract available
Plant Pathology (62) 8395.
Publisher's version: 10.1111/ppa.12163
ID: 46455read more
The fitness costs of disease resistance in plants are reviewed and their relevance to plant breeding is discussed. An important theme of current research is that plant defence is closely integrated into pathways that regulate growth and development in plants, so mutations in genes with central locations in defence networks often have numerous pleiotropic effects. There is increasing evidence that resistance to one disease involves trade-offs with responses to other bio-antagonists; the numerous pleiotropic effects of mlo resistance to powdery mildew of barley are discussed as an example. There is a striking contrast between the low costs of resistance in most crop diseases and the sometimes high costs of resistance in model systems studied in fundamental research. It is suggested that, through natural and artificial selection over thousands of years, farmers and more recently plant breeders have selected alleles which maximize the benefits and minimize the costs of resistance. There is sometimes substantial genotype-by-environment interaction in fitness costs, which makes experiments on fitness in plants especially challenging, but it is essential to understand these interactions to appreciate the relevance of fitness costs and trade-offs to crops in field conditions. It is proposed that in the great majority of cases, in which it is not feasible to investigate fitness costs and their interactions with the environment in depth, plant breeding is an efficient way of incorporating genes with benefits which exceed any costs into commercially successful cultivars of arable crops.
Plant Pathology (62) 115121.
Publisher's version: 10.1111/ppa.12165
ID: 46456read more
Breeding of arable crops such as wheat has led to substantial improvements in yield, quality of produce, traits of agronomic value and resistance to disease and abiotic stress. Resistance to many diseases and pests of wheat has improved through a combination of innovation by breeders, driven by competition, and independent assessment of cultivars in Recommended List trials. In addition to pleiotropic effects of resistance genes, two further limitations on breeding for disease resistance are linkage drag and competition drag. Linkage drag, the slow rate of decline of linkage disequilibrium between closely linked genes, can be especially significant in wheat, particularly after the introgression of chromosome segments from related wild grasses. For example it slowed the deployment of the Pch1 gene for resistance to eyespot in leading cultivars because Pch1 is on a chromosome segment that also reduces yield. Linkage drag also inhibited the use of Pm16 for resistance to powdery mildew. Competition drag can be described as the delay in the deployment of a useful gene because of the additional time needed to raise yield and quality to the standard of the current market-leading cultivars. This is exemplified by the near-absence of resistance to Soil-borne cereal mosaic virus in most modern varieties, despite no evidence for detrimental pleiotropic effects. Changes in agricultural practice and regulation of pesticides are increasing demand for durable resistance to disease but wherever possible, improvement of resistance should not constrain selection for yield which remains the most significant trait in leading wheat cultivars for the UK.
Annals of Botany (112) 1439-1447
Publisher's version: 10.1093/aob/met209
ID: 43572read more
Quantitative trait loci for partial resistance to Pseudomonas syringae pv. maculicola in Arabidopsis thaliana.
Molecular Plant Pathology (14) 828-837
Publisher's version: 10.1111/mpp.12043
ID: 42042read more
Long-distance dispersal and its influence on adaptation to host resistance in a heterogeneous landscape
Plant Pathology (62) 9-20
Publisher's version: 10.1111/j.1365-3059.2012.02621.x
ID: 40361read more
The 'Green Revolution' dwarfing genes play a role in disease resistance in Triticum aestivum and Hordeum vulgare
Journal of Experimental Botany (63) 1271-1283
Publisher's version: 10.1093/jxb/err350
ID: 39657read more
Spatial heterogeneity, frequency-dependent selection and polymorphism in host-parasite interactions.
BMC Evolutionary Biology (11) 319
Publisher's version: 10.1186/1471-2148-11-319
ID: 40117read more
Breeding for resistance as a component of integrated crop disease control and sustainable food protection
ID: 39577read more
Annual Reviews in Phytopathology (49) 345-67
Publisher's version: 10.1146/annurev-phyto-072910-095301
ID: 39537read more