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British Society for Plant Pathology Presidential Meeting, 22 September 2009, Museum of Natural History, Oxford, UK
The influence of three individuals was strongly felt at this year’s joint MBPP and BSPP Presidential meetings, even though none of them were able to attend. Charles Darwin, for whom 2009 was both his bicentenary and the 150th anniversary of the publication of On the Origin of Species, provided inspiration for the theme of the BSPP presidential meeting, in addition to the cornerstone for the conceptual framework for the entire field of modern biology. The writings of Reverend Thomas Malthus, and in particular his account of the tension between population growth and resource availability in The Principle of Population, which strongly influenced both Darwin and Russell Wallace in their discoveries of Natural Selection, continue to cast a shadow over the globe, even in 2009. The third individual was Norman Borlaug, whose work on developing high-yield crop varieties is credited with saving billions of people from a Malthusian food crisis in the late Twentieth Century, and who sadly died shortly before these meetings, was honoured by organiser Pari Skamnioti’s opening address at the MBPP as the ‘Father of the Green Revolution’.
The MBPP meeting attracted approximately 100 delegates and 25 scheduled (14 female) speakers. Pari Skamnioti’s introductory tribute to Norman Borlaug was the first of many presentations by these young and emerging scientists to be placed firmly in the global context of the potential impact of plant pathology research in the developed and developing world. Easing the human impact of plant diseases, such as Magnaporthe oryzae which causes losses to rice sufficient to feed 600 million people each year, in the context of food security and rapid world population growth, expected to hit 10 billion people by 2050 (Tom Mentlak and Lauren Ryder, both University of Exeter), underpinned much of the research and was an obvious motivation for many speakers. More specific impacts on the developing world were emphasised in work such as that on threats to African plants due to palm vascular disease (Hefni Rusli, University of Bath) – and lethal yellowing of coconut palm by phytoplasmas (Philip Swarbrick, University of Nottingham).
Most of the major classes of plant pathogen were represented in the presentations of the MBPP speakers. Most of the presented oomycete pathogen research was focused on effector proteins, produced by the pathogen to manipulate the host in some way. Liliana Cano (The Sainsbury Laboratory) spoke about the advantages of next generation sequencing and the insights gained into the evolution of effectors in the Phytophthora species ipomoeae and mirabilis. Susan Breen (SCRI) described her work cloning the P. infestans effector Avr2 and identifying its binding targets by yeast-2-hybrid screens. Screening effector targets in yeast was also the subject of Sarat Bimandham’s (University of Warwick) presentation concerning Hyaloperonospora arabidopsidis ef fector funct ion. Effectors were also a key topic in the fungal work presented: Tom Mentlak (University of Exeter) in particular spoke about lysin motifs in M. oryzae effectors, and their interaction with chitin. Work on the fundamental biochemistry of fungi was presented by Muhammad Badaruddin (University of Exeter), who described the role of glycogen metabolism in turgor pressure generation for M. oryzae, and by Francesca Stefanato (University of Freiburg), who detailed the contribution of the BcatrB ABC-transporter to virulence in Botrytis cinerea by exporting plant defence compounds.
Not all fungal pathogens are damaging purely in terms of causing disease on the plant. Fusarium graminarium, which causes wheat head scab, is largely a problem to humans due to production of the mycotoxin deoxynivalenol (DON). In presentations on this organism, Jens Due Jensen (University of Copenhagen) spoke about his work on the relationship between oxidative stress and DON production, and Andrew Beacham (Rothamsted) described the use of deletion mutants to investigate hotspots of virulence-related genes on the genome. Contrastingly, Lauren Ryder (University of Exeter) spoke about a hexoseaminidase mutant of the rhizosphere fungus Trichoderma hamatum, that actually enhances host plant growth.
Genome sequencing has greatly accelerated research on phytopathogens, and bacteria in particular. Sonia Humphris (SCRI) spoke about the emerging threat of Dickeya spp. in Scotland, and the comparative sequencing efforts underway to understand the differences between strains. Also from Scotland, Jo Fyans (University of Dundee) described her work investigating the influence of the Tat and Type VI secretion systems on Streptomyces pathogenicity. Systems level work is perhaps more tractable with bacteria than some other pathogens, and Arantza Rico (University of Oxford) spoke about her metabolic profiling study of the response of the tomato apoplast to Pseudomonas syringae infection. In contrast to these free-living bacteria, Philip Swarbrick and Melanie Tuffen (both University of Nottingham) gave accounts of the impact of Phytoplasmas, which are obligate parasites of plant phloem, spread by insect vectors. Philip described the impact of these pathogens on developing world crops, and the difficulties of diagnosing and controlling infection, while Melanie presented her work on the physiological changes induced in a model system infected by Phytoplasma. Although genomics, bioinformatics and computational biology provided much support for several of the talks at the meeting, only Aziz Mithani (University of Oxford) presented almost purely on computational biology. He described Rahnuma, a web-based service that facilitates comparisons between biological networks, potentially revealing the differential functional capabilities of individual pathogens.
The pathogens did not get it all their own way in the presentations, however. Helen Lovell (University of the West of England), establishing a theme of considering interactions involving pathogens in the context of their environment, gave a P. H. Gregory prize-winning presentation on her work that demonstrated DNA transformation of the genomic island PPHGI-1 between strains of P. syringae, in planta. This work is the first empirical evidence for lateral gene transfer in the host environment, long suspected to be an important factor in the development and spread of pathogenicity genes among phytopathogenic bacteria. Helen Fones (University of Oxford) and Christopher Burt (John Innes Centre) each provided a plant’s perspective on the pathogen’s environment. Helen, in her work on hyperaccumulation of toxic metals as a defence mechanism in the brassica Thlaspi caerulescens, and Christopher in his work on the mapping of eyespot resistance in wheat. Bill Truman (University of Exeter) overcame multiple equipment failures during his presentation to speak on the interplay between plant hormone signalling pathways, their impact on host resistance, particularly via auxin and indole synthetic pathways, and their effect on systemic acquired resistance.
Host resistance is not a perfect defence: interactions with the pathogen and the wider environment are complex, and the variation in and distribution of pathogen populations makes them formidable opponents to overcome. Presentations by Sonia Humphris and Philip Swarbrick addressed this problem directly, and Hefni Rusli (University of Bath) and Nichola Hawkins (Rothamsted) also considered this issue for diagnostic tools in the Fusarium oxysporum/Elaeis guineensis system and the evolution of Rhynchosporium secalis populations under the selective pressure of fungicide use, respectively. The persistence and spread of bacterial plant pathogens in the environment by adherence to non-host organisms was a feature of presentations by Sonia Humphris (Dickeya attachment to wild weeks), and by Frederico Dorati (University of Reading), who described the attachment of P. syringae to nematodes and insects as a potential dispersal technique for this pathogen. In the day’s only presentation on viral pathogens, the effect of environmental factors on symptom development in mushroom virus X infection was described by Coimhe Archibald-Fleming (Teagasc).
By the beginning of the BSPP meeting the next day, delegate numbers had swollen to around 150 to hear the keynote presentation from the director of the International Rice Research Institute (IRRI), Robert Ziegler. The difficulties of ensuring global food security were evident in his clear account of the central role of rice in the life of billions, and the threat that plant diseases present to this security. Until 2002, rice production outstripped demand, coincident with its record low prices, but yield per hectare is reaching a plateau. The resultant rising cost of rice threatens poverty and undernourishment for large numbers of people. Though hybrid rice has transformed China’s food security and increased yields by around 20%, reemerging old pathogens and new problems such as false smut and white backed planthopper are serious issues for agriculture. Ziegler however presented an optimistic vision of the future, citing the simultaneous revolutions in communications, biology, and computational power as a cause for hope in the developing world. He described the IRRI’s huge gene bank, containing over 110,000 cultivar accessions (which they eventually hope to sequence), as a resource for genetic modification and transgenics to help overcome the problems impacting on food security, and stressed the need to inform policy makers about the utility of these techniques, and the many decade time-scales for breeding resistant cultivars. He also emphasised that GM technology is not a solution on its own, and that an integrated approach to agriculture, with attention paid to farming systems and not just the crop plant in isolation, is necessary to ensure food security.
The rice blast fungus Magnaporthe oryzae is a pathogen of great economic and social impact, and Nick Talbot (University of Exeter) presented recent work from his group on the fundamental understanding of a key early stage in its infection process: appressorium formation and development. His group have identified cell checkpoints that control commitment of the pathogen’s production of the appressorium, which physically penetrates the host cell. They used an ingenious approach involving temperature-sensitive pathogen mutants that arrest the cell at distinct points in the cell cycle, so determining that mitotic entry is both necessary and sufficient for appressorium differentiation, and that disruption of septation does not halt morphogenesis, but does prevent plant infection.
Gero Steinberg, also of the University of Exeter, spoke about the role played by the class XVII myosins of the fungus Ustilago maydis in pathogen growth and virulence. Myosins are actin-associated mechanoenzymes that ‘walk’ along the cytoskeleton, and the fungal variants are virulence factors involved in cell wall biosynthesis. His group’s work focused on the Mcs1 class XVII myosin, mutants of which cause the hypha to ‘balloon’ inside the host. They used a selective laser cell-bleaching technique to demonstrate both that the Mcs1 protein was delivered to the hyphal tip, and that it does not itself ‘walk’ the actin cytoskeleton, but is carried there by another myosin. Mcs1 appears to participate in apical tethering of secretory chitosomes at the hyphal tip, mediating the forces leading to exocytosis by a complex ‘tug-of-war’- like interaction between the actin filament and the cell membrane.
Ian Toth from SCRI gave a thorough historical overview of the evolutionary and human history of bacteria, covering the scientific and philosophical developments of evolution in the 19th and 20th centuries before returning to modernity with the creation of the (semi-)synthetic organism Mycoplasma laboratorium. He described his group’s comparative genomics work on plant pathogenic enterobacteria, including Pectobacterium and Dickeya species, and the concept of ‘core’ and ‘accessory’ genomes. The ‘accessory’ genomes of phytopathogens include groups of genes for functions such as nitrogen fixation and phytotoxin synthesis, and include functions that seem to enable environmental persistence, rather than virulence. The persistence of phytopathogens on wild plants and the attachment of human pathogens to crop plants are now major lines of work being taken forward at the institute. Ian ended with a warning that, while sequence data may be cheap, and getting progressively cheaper, its analysis remains relatively expensive, and informatics infrastructure development is critical for this kind of work.
Howard Atkinson, of the University of Leeds, presented his group’s nematode work. The economic impact of nematodes on agriculture is great: they cause 80% of the worldwide cost of crop damage. His group have identified clusters of Longidorus genes that are expressed with dissimilar seasonality, apparently timed to host root development, and by qPCR have also found differential expression of pharyngeal gland products during host invasion. Howard proposed RNAi targeting of the genes encoding those products that are essential for invasion as a potential nematode control mechanism, and also an alternative approach to control involving expression by the plant of a short peptide that disrupts nematode chemoreception. This latter approach is currently being tested in the UK’s only GM field trial, and he expanded on the issues of transgenics by emphasising steady progress via a ser ies of safe approaches, using molecules that are already present in humans, while noting – as did Robert Ziegler – that GM is an effective and powerful tool for plant pathologists, but not a panacea.
Paul Birch (University of Dundee) drew a direct line from Darwin to his current work via a letter written to T. H. Farrar in which he declared that the development of a ‘fungus-proof potato’ would be a ‘benefaction to mankind’. The fungus in question was actually the oomycete Phytophthora infestans, which still causes over $3 billion of damage and loss each year, and whose genome was recently sequenced. The emerging highly virulent ‘blue 13’ strain of P. infestans is an increasing problem in Europe, and the genome sequence has provided insights into how this pathogen is able rapidly and repeatedly to overcome bred resistance. In addition to delineating the effector complement of the organism, the genome sequence has revealed a ‘two speed’ structure in which the ‘highspeed’ region is proposed to permit rapid assortment and development of virulence-related functions. Paul’s group, having already identified the Avr2 effector, are searching for its target in the host, and for sources of durable resistance to P. infestans in potato, particularly to the new ‘blue 13’ strain.
Ralph Panstruga (University of Cologne) continued the theme of host resistance by describing his work on barley Mlo mutant-mediated resistance to Blumeria graminis. This is an unusual kind of resistance, being conferred by the absence, rather than the presence of the resistance gene: a plant-specific integral membrane protein, but this modality has now also been seen in pea, tomato and Arabidopsis. The known mutants are thought mostly to be anthropogenically-derived due to agricultural selection, and provide protection against host cell entry in barley. The resistance doesn’t appear to operate via defence signalling, (e.g. by salicylic acid, jasmonate or ethene), but rather by modification of indole metabolic pathway s , and the accumulation of indolic secondary metabolites was found to be a requirement for resistance in single Mlo mutants (though intriguingly not in Mlo2/Mlo6/Mlo12 triple mutants). Ralph’s group suspects that at least one additional pathway contributes to Mlo resistance, and are using forward genetic screens to attempt to identify it, or them.
Frank Takken (University of Amsterdam) gave a presentation with the intriguing title of “How to Resist a Resistance Gene”, considering mainly the NB-LRR innate im munity receptor type, in the I-2 : F. oxysporum model pathosystem. Frank’s group has split the NB and LRR domains to demonstrate that both sections of the protein are required to activate the host hypersensitive response. By threading the I-2 NB-LRR on a known homologous structure, and transcomplementing domain mutants they have developed a model of NB-LRR activation with structurally distinct ‘on’, ‘off’ and ‘intermediate’ states, based on the presence or absence of a pathogen effector. Their model pathogen F. oxysporum secretes small, cysteine-rich Six (secreted in xylem) proteins, which are clustered on a single chromosome in the pathogen; Six3 interacts with the I-2 NB-LRR. They suspect this chromosome to be mobile among isolates, and have demonstrated its transfer in vitro, suggesting that host specificity determination, and potentially pathogenicity, are transferable characteristics.
Juriaan Ton (Rothamsted) described the priming and sensitisation of Arabidopsis defence, in which the plant is made ‘ready’ to combat infection by exposure to pathogen attack, or to compounds such as insect-induced volatiles. This ‘priming’ boosts the efficiency of a number of layers of host defence. In particular Ralph’s group are screening Arabidopsis for mutants that are not primed by beta-aminobutyric acid (BABA), a primer of SA-independent defence by callose deposition that is likely involved in a number of defence pathways. They identified ibi1 and ibi2 mutants, which had changes in an aspartyl tRNA synthetase, and hypothesise that BABA acts as an aspartate mimic when causing priming via a pathway including ibi1. They find that priming defence in this way has a cost, albeit low, to the host that appears to be outweighed by the benefits of resistance in a hostile environment.
James Brown (John Innes Centre) declared an ambitious aim to improve resistance to all diseases simultaneously by plant breeding. This has historically been a critical factor in ensuring global food security, and taking a lead from Darwin’s account of pigeons, he framed breeding as an evolutionary process contending that a detailed knowledge of pathology and genetics are useful, but not necessary, for plant breeding. In particular, he proposed that plant breeding in the absence of an understanding of the underlying system can trump a detailed understanding of the disease process for generating resistance in the plant, and questioned whether efforts would be better spent on association genetics and finding genetic markers of resistance, rather than investigating the underlying molecular causes and mechanisms of disease. However, he supports the use of genetic modification to tackle resistance mechanisms directly in situations where it might work better than breeding, such as when selection is slow, breeding is very difficult or even impossible, or when there are few genes in the germplasm.
The President’s Address by Sarah Gurr closed the meeting. She began with a brief autobiographical discursion, demonstrating the truth in Darwin’s maxim that “the species that survives [“¦] is the one that is the most adaptable to change. “ Sarah described the formative influence of reading widely at an early age, with particular reference to Woodham Smith and Large’s works on the potato famine and the advance of fungi. After jobs in a mortuary and on a ferry, she began work on fungicides at Shell, leading to a PhD at Imperial College (by whom she was later awarded the Huxley Medal) on the ambitious topic of the “biochemical basis of biotrophy in oomycetes”. Her scientific career continued to encompass a wide range of pathogens, including Phytophthora infestans, Globodera rostochiensis, Blumeria graminis and Septoria, in collaboration with many familiar and eminent names such as Jim Duncan, Kim Hammond- Kosack, and Tim Carver. In 1994, Sarah was appointed as the first female lecturer in Plant Sciences, as the Shepherdess of Somerville College, and managed to feature in the Morse episode “Numbers Awake”. While at Oxford, and balancing a hefty workload on the second most popular undergraduate course after animal behaviour, a young family, and improvised lab equipment, a pivotal scientific moment came when working on Magnaporthe oryzae functional genomics. Sarah described some of her group’s influential and extensive work on M. oryzae, focusing on the role of cutinases in preparing spore attachment to the host, and their role in signalling for appressorium formation. These signalling cues are effectively integrated in biological logic gates, and the effects propagate downstream via the AGC kinase Sta1. Sarah summarised some recent work of the laboratory on Sta1, demonstrating that it is a virulence determinant involved in a number of key processes such as homeostasis of the environment and regulation of stress. In closing, Sarah emphasised the importance of the diverse collaborative environment of the university, and returned to the importance of plant pathology research for the future benefit of humankind, drawing comparisons between the research budgets and global impacts of some high-profile diseases, and the same metrics for plant diseases and plant pathology: plant pathology research is not proportionately funded.
It seems suitable to end on the theme highlighted by Sarah Gurr of the responsibility of plant pathologists to the rest of the world, with comments from Robert Ziegler and Thomas Malthus, one of the conference’s unseen influences. Robert ended his keynote address with a message that, on the evidence of the MBPP presentations, has already been taken on board by many of the young researchers: that any scientist with a social conscience can ask fundamental questions of nature for practical reasons, that have great scientific impact, and also impact on the lives of the poor. Malthus, from two centuries ago, also gives us hope that we can make a difference through our research: “[The] main peculiarity which distinguishes man from other animals, is the means of his support, is the power which he possesses of very greatly increasing these means”.
Plant Pathology Programme, SCRI, Errol Road, Invergowrie, Dundee DD2 5DA