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Crop-destroying fungal and oomycete pathogens challenge food security
Fungal Genetics and Biology 74 (2015) 62–64
Contents lists available at ScienceDirect
Fungal Genetics and Biology journal homepage: www.elsevier.com/locate/yfgbi
Video Article
Crop-destroying fungal and oomycete pathogens challenge food security Daniel P. Bebber a, Sarah J. Gurr a,b,⇑ a b
School of Biosciences, University of Exeter, Stocker Road, Exeter EX4 4QD, UK Rothamsted Research, North Wyke, EX20 2SB, UK
a r t i c l e
i n f o
Article history: Received 3 September 2014 Accepted 13 October 2014 Available online 20 October 2014 Keywords: Agriculture Food security Climate change
a b s t r a c t Of the various crop pests and pathogens which blight our harvests, it is the fungi and oomycetes which are the most widely-dispersed groups and which lead the global invasion of agriculture. Here, we highlight the rapid growth in fungal and oomycete disease incidence and spread across the globe. We draw attention to the need for improved disease surveillance and for more sustainable agricultural intensification and consider the economic and humanitarian costs of fungal and oomycete diseases. Ó 2014 Published by Elsevier Inc.
1. Introduction An ever-expanding human population compels us to intensify crop production to match the increasing global demand for food. With a total population of 9.2 billion and thus another projected 2.2 billion more mouths to feed by 2050, we will need to produce an extra 200,000 billion calories per annum (pa). In addition, we will need to ensure a better geographic food spread to meet this increasing demand. Global food security (GFS) is further challenged by the spread of pathogens via trade and transport (Anderson et al., 2004; Brown and Hovmøller, 2002; Bebber et al., 2014a). Aside from such socio-economic issues, various ‘‘abiotic’’ threats challenge GFS. These include water crises, spiralling energy costs, land degradation, volatile political conditions and climate change. GFS is further threatened by crop losses due to pest and pathogen attack. These ‘‘biotic’’ agents of disease include viruses, bacteria, fungi, oomycetes and insects (hereafter named pathogens). Such cropdestroyers account for persistent yield losses of up to 20% of the world’s harvest, with a further 10% loss post-harvest (Oerke, 2006; Flood, 2010). In years of severe epidemic outbreaks, total harvests can be lost to disease. Of these ‘‘biotic’’ threats, it is the fungi and oomycetes that pose the greatest to global food security (Fisher et al., 2012). Resource-rich farming practices, such as the planting of vast hectarages of genetically uniform crops increase the challenge. These crops are often guarded by a few inbred disAbbreviations: GFS, global food security; pa, per annum; GDP, gross domestic product. ⇑ Corresponding author at: School of Biosciences, University of Exeter, Stocker Road, Exeter EX4 4QD, UK. E-mail address: [email protected] (S.J. Gurr). http://dx.doi.org/10.1016/j.fgb.2014.10.012 1087-1845/Ó 2014 Published by Elsevier Inc.
ease resistance genes and further protected by application of antifungals that may have only a single target site in the pathogen. Moreover, this practice favours pathogens with short generation times, and especially those which can then produce prolific numbers of spores. Even more alarmingly, recent detailed molecular analysis has revealed how remarkably ‘‘plastic’’ the genetic blueprint of these microbes can be (Haas et al., 2009). Such agricultural practices favour emergence of aggressive variants of existing pathogens, which can overcome plant defences and/or become fungicide resistant.
2. The growing threat of crop pathogens to global food security A series of meta-analyses interrogating large data sets has revealed some stark facts about the growing threat of pathogens to crop security. Firstly, a global analysis of pathogen distributions shows that a country’s ability to monitor and report accurately its pathogen load increases with per capita gross domestic product (GDP), but also relates to a country’s research capacity and expenditure (Bebber et al., 2014a). This poses a major challenge to development of pathogen control strategies in poorer nations. This study then used this information to generate an unbiased model, which revealed that total crop production and crop diversity are the most reliable predictors of pathogen threat (Bebber et al., 2014a). Using these predictors, the study revealed, rather surprisingly, that a greater number of pathogens is found on islands than is present in land-locked or coastal countries. An important next step towards developing cost-efficient and successful crop-disease management strategies is our ability to predict future pathogen distributions. This challenge was most
D.P. Bebber, S.J. Gurr / Fungal Genetics and Biology 74 (2015) 62–64
recently addressed in another meta-analysis study (Bebber et al., 2014b). Consistent with earlier findings (Fisher et al., 2012), the study confirmed that fungal and oomycete pathogens lead the global invasion of agricultural crops. We tracked the movement of pathogens globally and over a period of 50 years, revealing that, in many countries, the number of diseases caused ot fungal and oomycete pathogens increased over time (Video 1).
Video 1. Movie showing observational data records of fungal and oomycete plant diseases over the past 50 years. The scale bar is the number of fungi/oomycetes plant diseases reported in the CABI Distribution Maps of Plant Diseases published between 2000 and 2011.
Interestingly, most pathogens remain strongly regionalized and their distribution correlates significantly with their plant host, climate, latitude and socio-economic conditions (Bebber et al., 2014b). However, the study showed that a subset of pathogens has invaded new territories at an unprecedented rate. Indeed, these pathogens are predicted to reach all available hosts by mid-century in many economically important countries. Amongst these pathogens certain leaf spot fungi and the powdery mildews (Fig. 1) lead the advancing front (Bebber et al., 2014b). The situation gets even more challenging as recent results show that plant pathogenic fungi and oomycetes, generally, are moving polewards. Due to climate change, it was predicted that these pathogens are marching towards the poles, at a rate of some 8 km pa (Bebber et al., 2013), thereby posing new challenges for disease control, particularly in the northern hemisphere. 3. Conclusion In this article, we have considered some recent work that has demonstrated that climate change has likely caused a global shift in the distribution of crop pathogens, including fungi and oomycetes. Of the various crop pathogens, it is a subset of fungi that are the most pervasive and thus pose a more immediate challenge to global food security. How shall we meet the upcoming challenges? Here, we highlight some very specific action points, including the need for more research and training and a more defined route for such data to influence robust policy decisions:
63
(i) Pathogen biology: More fundamental research on the biology and a better understanding of molecular mechanisms underpinning the various infection strategies of our major crop pathogens is required. For example, we need a greater knowledge and better understanding of the key features in a pathogen’s genome which drive the emergence of new aggressive variants. Understanding the cell biology of their interaction with the host may reveal novel fungicide targets, and enable us to fight the pathogen before disease is established. (ii) New antifungals: Better understanding of the pathogen’s biology and infection strategies may help to identify the ‘‘Achilles heel’’ and lead to development of new broad spectrum, low-dose and low-ecological-impact antifungals. It appears important to decreased reliance on single-target site chemistries. Furthermore, agreements on international protocols for rotational use of extant fungicides have to be found to limit emergence of fungicide resistance. These goals require tighter collaborations between academia, industry and governments. (iii) Pathogen detection and monitoring: We need to be able to recognize disease at very early stages. Thus, development of antibody and molecular-marker based technologies to detect pathogens emerging in virgin lands and on new hosts is required. We need methods to track pathogen populations, both temporally and spatially. This will enable more comprehensive disease forecasting and better predictive epidemiological models. Care has to be taken to ensure that developing countries profit from such achievements. This could be done by establishing global quarantine and pathogen monitoring networks. (iv) Crop perspective: We must enable our crop plants to cope with pathogen attack better. We recommend, breeding plants to carry several stacked monogenic disease resistance genes or using better broad spectrum resistance, as well as exploiting quantitative trait loci in high yielding varieties. We need to be less reliant on high yield harvests derived from vast monocultures of monogenetically disease resistant crops, which stand in jeopardy of attack by planting mixed cultivars. More effort needs to be expended on bio-protection and the hunt for plant defence activators to boost disease immunity in crops. Finally, we must evaluate carefully the use of transgenic plants in agriculture. (v) Awareness: Crop pathogens are a severe challenge to global societies, and it is important that the public is aware of the impact of crop disease on food security. We must redress the imbalance of research funds spent on human versus crop diseases. This need is illustrated by the fact that the spend on research on HIV/AIDs or Malaria exceeds that on malnu-
Fig. 1. Barley powdery mildew fungus Blumeria graminis f. sp. hordei. (A) Colony formation on an infected leaf; and a healthy leaf. Scale bar is 0.5 cm. (B) Scanning electron micrograph of chains of asexual spores (conidia) comprising the colonies. Scale bar is 100 lm.
64
D.P. Bebber, S.J. Gurr / Fungal Genetics and Biology 74 (2015) 62–64
trition (of which plant disease is a but a tiny fraction), by 730- and 430 times, respectively (Skamnioti and Gurr, 2009). (vi) Succession: Finally, we must realize that fighting crop pathogens is a long term ongoing battle. We have to train the next generation of scientists in more holistic and integrative approaches to global food security. We need to hone their skills in epidemiology, climate forecasting, global pathogen surveillance and ensure that they well-informed in hostpathogen biology.
Acknowledgments DB is a Senior Research Fellow at Exeter University. SG gratefully acknowledges BBSRC funding. Data for the video were abstracted from the CABI Distribution Maps of Plant Diseases. Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.fgb.2014.10.012.
References Anderson, P.K., Cunningham, A.A., Patel, N.G., Morales, F.J., Epstein, P.R., Daszak, P., 2004. Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol. Evol. 19, 535–544. Bebber, D.P., Ramotowski, M.A.T., Gurr, S.J., 2013. Crop pests and pathogens move polewards in a warming world. Nat. Clim. Change 3, 985–988. Bebber, D.P., Holmes, T., Smith, D., Gurr, S.J., 2014a. Economic and physical determinants of the global distributions of crop pests and pathogens. New Phytol. 202, 901–910. Bebber, D.P., Holmes, T., Gurr, S.J., 2014b. The global spread of crops pests and pathogens. Global Ecol. Biogeogr.. http://dx.doi.org/10.1111/geb.12214. Brown, J.K.M., Hovmøller, M.S., 2002. Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297, 537–541. Fisher, M.C., Henk, D.A., Briggs, C.J., Brownstein, J.S., Madoff, L.C., McCraw, S.L., Gurr, S.J., 2012. Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186–194. Flood, J., 2010. The importance of plant health to food security. Food Sec. 2, 215– 231. Haas, B.J. et al., 2009. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461, 393–398. Oerke, E.-C., 2006. Crop losses to pests. J. Agric. Sci. 144, 31–43. Skamnioti, P., Gurr, S.J., 2009. Against the grain: safeguarding rice from rice blast disease. Trends Biotechnol. 27, 141–150.
Contents lists available at ScienceDirect
Fungal Genetics and Biology journal homepage: www.elsevier.com/locate/yfgbi
Video Article
Crop-destroying fungal and oomycete pathogens challenge food security Daniel P. Bebber a, Sarah J. Gurr a,b,⇑ a b
School of Biosciences, University of Exeter, Stocker Road, Exeter EX4 4QD, UK Rothamsted Research, North Wyke, EX20 2SB, UK
a r t i c l e
i n f o
Article history: Received 3 September 2014 Accepted 13 October 2014 Available online 20 October 2014 Keywords: Agriculture Food security Climate change
a b s t r a c t Of the various crop pests and pathogens which blight our harvests, it is the fungi and oomycetes which are the most widely-dispersed groups and which lead the global invasion of agriculture. Here, we highlight the rapid growth in fungal and oomycete disease incidence and spread across the globe. We draw attention to the need for improved disease surveillance and for more sustainable agricultural intensification and consider the economic and humanitarian costs of fungal and oomycete diseases. Ó 2014 Published by Elsevier Inc.
1. Introduction An ever-expanding human population compels us to intensify crop production to match the increasing global demand for food. With a total population of 9.2 billion and thus another projected 2.2 billion more mouths to feed by 2050, we will need to produce an extra 200,000 billion calories per annum (pa). In addition, we will need to ensure a better geographic food spread to meet this increasing demand. Global food security (GFS) is further challenged by the spread of pathogens via trade and transport (Anderson et al., 2004; Brown and Hovmøller, 2002; Bebber et al., 2014a). Aside from such socio-economic issues, various ‘‘abiotic’’ threats challenge GFS. These include water crises, spiralling energy costs, land degradation, volatile political conditions and climate change. GFS is further threatened by crop losses due to pest and pathogen attack. These ‘‘biotic’’ agents of disease include viruses, bacteria, fungi, oomycetes and insects (hereafter named pathogens). Such cropdestroyers account for persistent yield losses of up to 20% of the world’s harvest, with a further 10% loss post-harvest (Oerke, 2006; Flood, 2010). In years of severe epidemic outbreaks, total harvests can be lost to disease. Of these ‘‘biotic’’ threats, it is the fungi and oomycetes that pose the greatest to global food security (Fisher et al., 2012). Resource-rich farming practices, such as the planting of vast hectarages of genetically uniform crops increase the challenge. These crops are often guarded by a few inbred disAbbreviations: GFS, global food security; pa, per annum; GDP, gross domestic product. ⇑ Corresponding author at: School of Biosciences, University of Exeter, Stocker Road, Exeter EX4 4QD, UK. E-mail address: [email protected] (S.J. Gurr). http://dx.doi.org/10.1016/j.fgb.2014.10.012 1087-1845/Ó 2014 Published by Elsevier Inc.
ease resistance genes and further protected by application of antifungals that may have only a single target site in the pathogen. Moreover, this practice favours pathogens with short generation times, and especially those which can then produce prolific numbers of spores. Even more alarmingly, recent detailed molecular analysis has revealed how remarkably ‘‘plastic’’ the genetic blueprint of these microbes can be (Haas et al., 2009). Such agricultural practices favour emergence of aggressive variants of existing pathogens, which can overcome plant defences and/or become fungicide resistant.
2. The growing threat of crop pathogens to global food security A series of meta-analyses interrogating large data sets has revealed some stark facts about the growing threat of pathogens to crop security. Firstly, a global analysis of pathogen distributions shows that a country’s ability to monitor and report accurately its pathogen load increases with per capita gross domestic product (GDP), but also relates to a country’s research capacity and expenditure (Bebber et al., 2014a). This poses a major challenge to development of pathogen control strategies in poorer nations. This study then used this information to generate an unbiased model, which revealed that total crop production and crop diversity are the most reliable predictors of pathogen threat (Bebber et al., 2014a). Using these predictors, the study revealed, rather surprisingly, that a greater number of pathogens is found on islands than is present in land-locked or coastal countries. An important next step towards developing cost-efficient and successful crop-disease management strategies is our ability to predict future pathogen distributions. This challenge was most
D.P. Bebber, S.J. Gurr / Fungal Genetics and Biology 74 (2015) 62–64
recently addressed in another meta-analysis study (Bebber et al., 2014b). Consistent with earlier findings (Fisher et al., 2012), the study confirmed that fungal and oomycete pathogens lead the global invasion of agricultural crops. We tracked the movement of pathogens globally and over a period of 50 years, revealing that, in many countries, the number of diseases caused ot fungal and oomycete pathogens increased over time (Video 1).
Video 1. Movie showing observational data records of fungal and oomycete plant diseases over the past 50 years. The scale bar is the number of fungi/oomycetes plant diseases reported in the CABI Distribution Maps of Plant Diseases published between 2000 and 2011.
Interestingly, most pathogens remain strongly regionalized and their distribution correlates significantly with their plant host, climate, latitude and socio-economic conditions (Bebber et al., 2014b). However, the study showed that a subset of pathogens has invaded new territories at an unprecedented rate. Indeed, these pathogens are predicted to reach all available hosts by mid-century in many economically important countries. Amongst these pathogens certain leaf spot fungi and the powdery mildews (Fig. 1) lead the advancing front (Bebber et al., 2014b). The situation gets even more challenging as recent results show that plant pathogenic fungi and oomycetes, generally, are moving polewards. Due to climate change, it was predicted that these pathogens are marching towards the poles, at a rate of some 8 km pa (Bebber et al., 2013), thereby posing new challenges for disease control, particularly in the northern hemisphere. 3. Conclusion In this article, we have considered some recent work that has demonstrated that climate change has likely caused a global shift in the distribution of crop pathogens, including fungi and oomycetes. Of the various crop pathogens, it is a subset of fungi that are the most pervasive and thus pose a more immediate challenge to global food security. How shall we meet the upcoming challenges? Here, we highlight some very specific action points, including the need for more research and training and a more defined route for such data to influence robust policy decisions:
63
(i) Pathogen biology: More fundamental research on the biology and a better understanding of molecular mechanisms underpinning the various infection strategies of our major crop pathogens is required. For example, we need a greater knowledge and better understanding of the key features in a pathogen’s genome which drive the emergence of new aggressive variants. Understanding the cell biology of their interaction with the host may reveal novel fungicide targets, and enable us to fight the pathogen before disease is established. (ii) New antifungals: Better understanding of the pathogen’s biology and infection strategies may help to identify the ‘‘Achilles heel’’ and lead to development of new broad spectrum, low-dose and low-ecological-impact antifungals. It appears important to decreased reliance on single-target site chemistries. Furthermore, agreements on international protocols for rotational use of extant fungicides have to be found to limit emergence of fungicide resistance. These goals require tighter collaborations between academia, industry and governments. (iii) Pathogen detection and monitoring: We need to be able to recognize disease at very early stages. Thus, development of antibody and molecular-marker based technologies to detect pathogens emerging in virgin lands and on new hosts is required. We need methods to track pathogen populations, both temporally and spatially. This will enable more comprehensive disease forecasting and better predictive epidemiological models. Care has to be taken to ensure that developing countries profit from such achievements. This could be done by establishing global quarantine and pathogen monitoring networks. (iv) Crop perspective: We must enable our crop plants to cope with pathogen attack better. We recommend, breeding plants to carry several stacked monogenic disease resistance genes or using better broad spectrum resistance, as well as exploiting quantitative trait loci in high yielding varieties. We need to be less reliant on high yield harvests derived from vast monocultures of monogenetically disease resistant crops, which stand in jeopardy of attack by planting mixed cultivars. More effort needs to be expended on bio-protection and the hunt for plant defence activators to boost disease immunity in crops. Finally, we must evaluate carefully the use of transgenic plants in agriculture. (v) Awareness: Crop pathogens are a severe challenge to global societies, and it is important that the public is aware of the impact of crop disease on food security. We must redress the imbalance of research funds spent on human versus crop diseases. This need is illustrated by the fact that the spend on research on HIV/AIDs or Malaria exceeds that on malnu-
Fig. 1. Barley powdery mildew fungus Blumeria graminis f. sp. hordei. (A) Colony formation on an infected leaf; and a healthy leaf. Scale bar is 0.5 cm. (B) Scanning electron micrograph of chains of asexual spores (conidia) comprising the colonies. Scale bar is 100 lm.
64
D.P. Bebber, S.J. Gurr / Fungal Genetics and Biology 74 (2015) 62–64
trition (of which plant disease is a but a tiny fraction), by 730- and 430 times, respectively (Skamnioti and Gurr, 2009). (vi) Succession: Finally, we must realize that fighting crop pathogens is a long term ongoing battle. We have to train the next generation of scientists in more holistic and integrative approaches to global food security. We need to hone their skills in epidemiology, climate forecasting, global pathogen surveillance and ensure that they well-informed in hostpathogen biology.
Acknowledgments DB is a Senior Research Fellow at Exeter University. SG gratefully acknowledges BBSRC funding. Data for the video were abstracted from the CABI Distribution Maps of Plant Diseases. Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.fgb.2014.10.012.
References Anderson, P.K., Cunningham, A.A., Patel, N.G., Morales, F.J., Epstein, P.R., Daszak, P., 2004. Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol. Evol. 19, 535–544. Bebber, D.P., Ramotowski, M.A.T., Gurr, S.J., 2013. Crop pests and pathogens move polewards in a warming world. Nat. Clim. Change 3, 985–988. Bebber, D.P., Holmes, T., Smith, D., Gurr, S.J., 2014a. Economic and physical determinants of the global distributions of crop pests and pathogens. New Phytol. 202, 901–910. Bebber, D.P., Holmes, T., Gurr, S.J., 2014b. The global spread of crops pests and pathogens. Global Ecol. Biogeogr.. http://dx.doi.org/10.1111/geb.12214. Brown, J.K.M., Hovmøller, M.S., 2002. Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297, 537–541. Fisher, M.C., Henk, D.A., Briggs, C.J., Brownstein, J.S., Madoff, L.C., McCraw, S.L., Gurr, S.J., 2012. Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186–194. Flood, J., 2010. The importance of plant health to food security. Food Sec. 2, 215– 231. Haas, B.J. et al., 2009. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461, 393–398. Oerke, E.-C., 2006. Crop losses to pests. J. Agric. Sci. 144, 31–43. Skamnioti, P., Gurr, S.J., 2009. Against the grain: safeguarding rice from rice blast disease. Trends Biotechnol. 27, 141–150.