NOXious gases and the unpredictability of emerging plant pathogens under climate change

This is the final version of the article. Available from BioMed Central via the DOI in this record.Emerging pathogens of crops threaten food security and are increasingly problematic due to intensive agriculture and high volumes of trade and transport in plants and plant products. The ability to predict pathogen risk to agricultural regions would therefore be valuable. However, predictions are complicated by multi-faceted relationships between crops, their pathogens, and climate change. Climate change is related to industrialization, which has brought not only a rise in greenhouse gas emissions but also an increase in other atmospheric pollutants. Here, we consider the implications of rising levels of reactive nitrogen gases and their manifold interactions with crops and crop diseases

Presence of ice-nucleating Pseudomonas on wheat leaves promotes Septoria tritici blotch disease (Zymoseptoria tritici) via a mutually beneficial interaction

This is the final version. Available on open access from Nature ResearchZymoseptoria tritici causes Septoria tritici blotch (STB) of wheat, an economically important disease causing yield losses of up to 10% despite the use of fungicides and resistant cultivars. Z. tritici infection is symptomless for around 10 days, during which time the fungus grows randomly across the leaf surface prior to entry through stomata. Wounded leaves show faster, more extensive STB, suggesting that wounds facilitate fungal entry. Wheat leaves also host epiphytic bacteria; these include ice-nucleating (INA+) bacteria, which induce frost damage at warmer temperatures than it otherwise occurs. Here, STB is shown to be more rapid and severe when wheat is exposed to both INA+ bacteria and sub-zero temperatures. This suggests that ice-nucleation-induced wounding of the wheat leaf provides additional openings for fungal entry. INA+ bacterial populations are shown to benefit from the presence of Z. tritici, indicating that this microbial interaction is mutualistic. Finally, control of INA+ bacteria is shown to reduce STB.Medical Research Council (MRC)British Ecological Societ

A role for the asexual spores in infection of Fraxinus excelsior by the ash-dieback fungus Hymenoscyphus fraxineus

This is the final version of the article. Available from Springer Nature via the DOI in this record.There is another ORE record for this article: http://hdl.handle.net/10871/33324The invasive pathogen, ash dieback fungus Hymenoscyphus fraxineus, is spreading rapidly across Europe. It shows high levels of outcrossing and limited population structure, even at the epidemic front. The anamorphic (asexual) form produces prolific conidia, thought to function solely as spermatia (male gametes), facilitating gene flow between sympatric strains. Here, we show that conidia are capable of germination on ash leaves and in vitro, and can infect seedlings via leaves or soil. In leaves, germlings form structures resembling fruiting bodies. Additionally, H. fraxineus colonises ash debris and grows in soil in the absence of ash tissues. We propose an amended life-cycle in which wind-dispersed, insectvectored or water-spread conidia infect ash and may sporulate in planta, as well as in forest debris. This amplifies inoculum levels of different strains in ash stands. In combination with their function as spermatia, conidia thus act to maximise gene flow between sympatric strains, including those originally present at low inoculum. Such mixing increases evolutionary potential, as well as enhancing the likelihood of gene introgression from closely-related strains or assimilation of further genetic diversity from parental Asian populations. This scenario increases the adaptability of H. fraxineus to new climates and, indeed, onto new host species.This work was funded by a grant from the BBSRC to the Nornex Consortium, BBS/E/J/000CA523, in association with DEFRA. We thank Dr Chris Thornton for useful discussions concerning fungal pathogens of soil and Dr Sreedhar Kilaru for kindly providing primers

The current status of the elemental defense hypothesis in relation to pathogens

This is the final version of the article. Available from Frontiers Media via the DOI in this record.Metal hyperaccumulating plants are able to accumulate exceptionally high concentrations of metals, such as zinc, nickel, or cadmium, in their aerial tissues. These metals reach concentrations that would be toxic to most other plant species. This trait has evolved multiple times independently in the plant kingdom. Recent studies have provided new insight into the ecological and evolutionary significance of this trait, by showing that some metal hyperaccumulating plants can use high concentrations of accumulated metals to defend themselves against attack by pathogenic microorganisms and herbivores. Here, we review the evidence that metal hyperaccumulation acts as a defensive trait in plants, with particular emphasis on plant-pathogen interactions. We discuss the mechanisms by which defense against pathogens might have driven the evolution of metal hyperaccumulation, including the interaction of this trait with other forms of defense. In particular, we consider how physiological adaptations and fitness costs associated with metal hyperaccumulation could have resulted in trade-offs between metal hyperaccumulation and other defenses. Drawing on current understanding of the population ecology of metal hyperaccumulator plants, we consider the conditions that might have been necessary for metal hyperaccumulation to be selected as a defensive trait, and discuss the likelihood that these were fulfilled. Based on these conditions, we propose a possible scenario for the evolution of metal hyperaccumulation, in which selective pressure for resistance to pathogens or herbivores, combined with gene flow from non-metallicolous populations, increases the likelihood that the metal hyperaccumulating trait becomes established in plant populations.This work was supported by an award to Gail M. Preston from the John Fell Fund, University of Oxford, by funding from the Natural Environment Research Council (grant number NER/S/A/2006/14187), and by a Marie Curie Intra-European Fellowship awarded to Anja C. Hörger

A role for the asexual spores in infection of Fraxinus excelsior by the ash-dieback fungus Hymenoscyphus fraxineus

This is the final version of the article. Available from Springer Nature via the DOI in this record.There is another ORE record for this article: http://hdl.handle.net/10871/23613The invasive pathogen, ash dieback fungus Hymenoscyphus fraxineus, is spreading rapidly across Europe. It shows high levels of outcrossing and limited population structure, even at the epidemic front. The anamorphic (asexual) form produces prolific conidia, thought to function solely as spermatia (malegametes), facilitating gene flow between sympatric strains. Here, we show that conidia are capable of germination on ash leaves and in vitro, and can infect seedlings via leaves or soil. In leaves, germlings form structures resembling fruiting bodies. Additionally, H. fraxineus colonises ash debris and grows in soil in the absence of ash tissues. We propose an amended life-cycle in which wind-dispersed, insectvectored or water-spread conidia infect ash and may sporulate in planta, as well as in forest debris. This amplifies inoculum levels of different strains in ash stands. In combination with their function as spermatia, conidia thus act to maximise gene flow between sympatric strains, including those originally present at low inoculum. Such mixing increases evolutionary potential, as well as enhancing the likelihood of gene introgression from closely-related strains or assimilation of further genetic diversity from parental Asian populations. This scenario increases the adaptability of H. fraxineus to new climates and, indeed, onto new host species.This work was fund by a grant from the BBSRC to the Nornex Consortium, BBS/E/J/000CA523, in association with DEFRA

The infiltration-centrifugation technique for extraction of apoplastic fluid from plant leaves using Phaseolus vulgaris as an example

This is the final version of the article. Available from JoVE via the DOI in this record.The apoplast is a distinct extracellular compartment in plant tissues that lies outside the plasma membrane and includes the cell wall. The apoplastic compartment of plant leaves is the site of several important biological processes, including cell wall formation, cellular nutrient and water uptake and export, plant-endophyte interactions and defence responses to pathogens. The infiltration-centrifugation method is well established as a robust technique for the analysis of the soluble apoplast composition of various plant species. The fluid obtained by this method is commonly known as apoplast washing fluid (AWF). The following protocol describes an optimized vacuum infiltration and centrifugation method for AWF extraction from Phaseolus vulgaris (French bean) cv. Tendergreen leaves. The limitations of this method and the optimization of the protocol for other plant species are discussed. Recovered AWF can be used in a wide range of downstream experiments that seek to characterize the composition of the apoplast and how it varies in response to plant species and genotype, plant development and environmental conditions, or to determine how microorganisms grow in apoplast fluid and respond to changes in its composition.This work was supported by grants BB/J016012/1 and BB/E007872/1 from the UK Biotechnology and Biological Sciences Research Council (BBSRC) to Gail Preston

A new mechanistic model of weather-dependent Septoria tritici blotch disease risk

This is the final version. Available on open access from the Royal Society via the DOI in this record.Data accessibility: All data and code associated with this work are available as supplementary material or on Github (https://github.com/thomaschaloner/A_new_mechanistic_model_of_weather-dependent_Septoria_tritici_blotch_disease_risk), respectively.We present a new mechanistic model for predicting Septoria tritici blotch (STB) disease, parameterized with experimentally derived data for temperature- and wetness-dependent germination, growth and death of the causal agent, Zymoseptoria tritici. The output of this model (A) was compared with observed disease data for UK wheat over the period 2002-2016. In addition, we compared the output of a second model (B), in which experimentally derived parameters were replaced by a modified version of a published Z. tritici thermal performance equation, with the same observed disease data. Neither model predicted observed annual disease, but model A was able to differentiate UK regions with differing average disease risks over the entire period. The greatest limitations of both models are: broad spatial resolution of the climate data, and lack of host parameters. Model B is further limited by its lack of explicitly defined pathogen death, leading to a cumulative overestimation of disease over the course of the growing season. Comparison of models A and B demonstrates the importance of accounting for the temperature-dependency of pathogen processes important in the initiation and progression of disease. However, effective modelling of STB will probably require similar experimentally derived parameters for host and environmental factors, completing the disease triangle. This article is part of the theme issue 'Modelling infectious disease outbreaks in humans, animals and plants: approaches and important themes'. This issue is linked with the subsequent theme issue 'Modelling infectious disease outbreaks in humans, animals and plants: epidemic forecasting and control'

A role for random, humidity-dependent epiphytic growth prior to invasion of wheat by Zymoseptoria tritici

This is the final version of the article.Available from Elsevier via the doi in this record.Zymoseptoria tritici causes Septoria leaf blotch of wheat. The prevailing paradigm of the Z. tritici-wheat interaction assumes fungal ingress through stomata within 24–48 h, followed by days of symptomless infection. This is extrapolated from studies testing the mode of fungal ingress under optimal infection conditions. Here, we explicitly assess the timing of entry, using GFP-tagged Z. tritici. We show that early entry is comparatively rare, and extended epiphytic growth possible. We test the hypotheses that our data diverge from earlier studies due to: i. random ingress of Z. tritici into the leaf, with some early entry events; ii. previous reliance upon fungal stains, combined with poor attachment of Z. tritici to the leaf, leading to increased likelihood of observing internal versus external growth, compared to using GFP; iii. use of exceptionally high humidity to promote entry in previous studies. We combine computer simulation of leaf-surface growth with thousands of in planta observations to demonstrate that while spores germinate rapidly on the leaf, over 95% of fungi remain epiphytic, growing randomly over the leaf for ten days or more. We show that epiphytic fungi are easily detached from leaves by rinsing and that humidity promotes epiphytic growth, increasing infection rates. Together, these results explain why epiphytic growth has been dismissed and early ingress assumed. The prolonged epiphytic phase should inform studies of pathogenicity and virulence mutants, disease control strategies, and interpretation of the observed low in planta growth, metabolic quiescence and evasion of plant defences by Zymoseptoria during symptomless infection.HF, CE, WK and SG were funded by BBSRC grant: and JC by a BSPP summer studentship

Epiphytic proliferation of Zymoseptoria tritici isolates on resistant wheat leaves

This is the author accepted manuscript. The final version is available on open access from the DOI in this recordThe wheat pathogen Zymoseptoria tritici is capable of a long period of pre-invasive epiphytic growth. Studies have shown that virulent isolates vary in the extent, duration and growth form of this epiphytic growth, and the fungus has been observed to undergo behaviours such as asexual reproduction by budding and vegetative fusion of hyphae on the leaf surface. This epiphytic colonisation has been investigated very little during interactions in which an isolate of Z. tritici is unable to colonise the apoplast, as occurs during avirulence. However, avirulent isolates have been seen to undergo sexual crosses in the absense of leaf penetration, and it is widely accepted that the main point of distinction between virulent and avirulent isolates occurs at the point of attempted leaf penetration or attempted apoplastic growth, which fails in the avirulent case. In this work, we describe extensive epiphytic growth in three isolates which are unable or have very limited ability to invade the leaf, and show that growth form is as variable as for fully virulent isolates. We demonstrate that during certain interactions, Z. tritici isolates rarely invade the leaf and form pycnidia, but induce necrosis and are able to achieve higher epiphytic biomass than virulent isolates during asymptomatic growth, and may undergo very extensive asexual reproduction on the leaf surface. These findings have implications for open questions such as whether and how Z. tritici obtains nutrients on the leaf surface and the nature of its interaction with wheat defences.UK Research and InnovationBiotechnology and Biological Sciences Research Council (BBSRC