Potato Late Blight Disease Caused by Phytophthora infestans: Comparison
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Please note this is a comparison between Version 2 by Camila Xu and Version 1 by Florian Martini.

Phytophthora infestans (Mont.) de Bary, 1876 is the oomycete responsible for potato late blight disease, generally recognized as the worst pathogen of potato. 

  • Phytophthora infestans
  • potato late blight disease
  • oomycete

1. Introduction

Potato (Solanum tuberosum L., 1753) is recognized as the third most significant crop for global human consumption [1]. With an annual production exceeding 350 million tons harvested over an estimated area of 19 million hectares [1[1][2],2], it holds the top position among non-cereal crops in terms of yield [3]. The versatility of potato in human diets, coupled with its high edible biomass reaching up to 80% [2], makes it a vital contributor to food security across the globe [1]. Indeed, S. tuberosum gained success in the food habits of numerous populations thanks to both the facilities of its cultivation [4,5][4][5] and significant source of energy and essential metabolites (macro and micronutrients) it provides [6,7][6][7]. In a world where the population is projected to exceed 9 billion people by 2050 [8], meeting the increased demand for high-quality food will be crucial, and potato will definitely play a major role. Given these reasons, efforts focusing on the management of its pests, including late blight disease, have become strongly promoted topics.
Phytophthora infestans (Mont.) de Bary, 1876, is generally recognized as the worst pathogen of potato [9]. The first strains originally came from Central America, more specifically, from the Toluca Valley, Mexico [10,11][10][11]. After spreading across the United States, they migrated to Europe and eventually expanded worldwide. In fact, potato late blight caused the devastating Irish famine in the 1850s, resulting in the deaths of over 1 million people and forcing many others to migrate from Ireland [12]. This event spurred scientists to start studying plant diseases, leading to the birth of phytopathology as a scientific field on its own [13]. From now on, in order to effectively combat a plant pathogen, it is crucial to accurately describe it. This requires a thorough understanding of both its taxonomy and biology.
The genus Phytophthora encompasses over one hundred species [14]. The majority have been identified as plant pathogens [15] causing various diseases around the world. They belong to the clade of oomycetes; these are eukaryotic microorganisms, part of the kingdom of the Chromista [16,17][16][17]. They are usually referred to as “pseudo-fungi” because of some shared similarities they exhibit with fungi, such as the mode of nutrition and comparable morphology [18]. Nonetheless, oomycetes phylogenetically diverged from Eumycetes and differ notably by the content of their cell wall (cellulose instead of chitin) [19,20][19][20].
Among those, Phytophthora infestans was probably the first species to be observed and classified. It is commonly known to cause both potato and tomato late blight disease [21,22][21][22]. Potato late blight is widely recognized as the most severe and problematic disease affecting potatoes. It does not only affect the foliage of potato plants but also the tubers, both before and after harvest [23]. When the environmental conditions are suitable for its optimal development (i.e., relative humidity superior to 90% and temperature between 15 et 25 °C) [24], late blight can devastate a whole field of potato within a matter of days [25,26][25][26]. As a consequence, the annual costs associated with both managing and mitigating the losses caused by P. infestans were estimated around USD 6 billion in 2015 [23,26,27][23][26][27].
P. infestans’ life cycle is achieved throughout two pathways. Since this organism is known to be heterothallic, sexual reproduction requires the meeting of two different mating types, namely A1 and A2 [21]. Mating actions lead to the formation of diploid oospores, which establish genetic variations within the populations. Genetic recombination occurring during sexual reproduction is a key phenomenon for the apparition of new resistant or virulent populations [28]. In addition, oospores also constitute survival structures able to persist in soil for relatively long periods of time. Nevertheless, asexual multiplication is most commonly used for dissemination of the disease across the fields [18]. Indeed, along with its mycelial growth, P. infestans develops sporangia [24]. Sporangia can either directly germinate to infect plant tissues when temperatures are relatively high (around 20–25 °C) or release motile zoospores produced within them at lower temperatures (between 10 and 15 °C) [26,29][26][29]. Zoospores are biflagellate cells that need moisture to swim towards new hosts and participate in additional infection.
At the early stage of infection, spores germinate at the surface of plant tissues by creating appressoria that are able to enter into host cells. It is the biotrophic phase during which the first symptoms appear: a white felting starts progressing on the abaxial side of the leaves [30]. Later on, the pseudofungi switches to the necrotrophic phase and feeds itself by absorbing plant cellular content [30]. This initiates necrosis during advanced stages of the infection. It ends up blocking photosynthesis and slowing down tuberization. The combination of both these trophic stages is called hemibiotrophy [29]. Globally, the pathogen survives thus by the persistence of its mycelium but disseminates thanks to the density of its spores [19]. Infected plants and tubers are therefore the primary source of inoculum. This is why discarding infected tissues remains the first prophylactic action useful to avoid potato late blight outbreaks.
While certain lineages (such as US-1, US-8 [31], or EU-13 [32]) have gained legendary status over the years because of their persistence across different parts of the world [33], new strains of P. infestans are rapidly emerging [34]. These appear to be more virulent, develop resistances to previously effective substances (e.g., phenylamides as metalaxyl) [35,36,37][35][36][37] or show reduced sensitivity towards others (fluazinam) [38]. They also reproduce faster and spread more rapidly across fields than before [39]. The emergence of these new pathovars is making the fight against potato late blight disease more relevant and urgent than ever. Taking that into consideration, innovative ways for the management of both old and new strains must be encouraged.
Current global food production heavily relies on intensive agriculture practices along with extensive use of fungicides [40]. The efficacy of these synthetic substances starts to fail because pathogens populations are developing strategies to overcome inhibition properties and became resistant throughout the years [41,42][41][42]. In addition, out of over 4 million tons of pesticide produced in 2019 (all chemical families considered), it is estimated that only 0.1% effectively reached the intended target [43]. Consequently, the majority of these chemicals end up in soils, water bodies, or into the atmosphere, contributing to pollution, altering species distribution, and causing the destruction of ecosystems [44]. Moreover, the residues of synthetic pesticides also pose significant risks to human and animal health because they accumulate in tissues and have been associated with various health issues such as cancer, mutagenicity, hepatotoxicity, neurotoxicity, nephrotoxicity, and infertility on both livestock and wild animals [45].
In response to these challenges, there is an urgent need to implement more sustainable and environmentally friendly agricultural practices. Cultural, harvesting and storage methods act as the first lines of action for integrated pest management (IPM) by limiting the dissemination and survival of pathogens [46]. In the case of potato, while numerous cultivars exist, only a limited number of them are grown on a large scale and are valorized by the industry. As it currently stands, the market leaders have been selected based on other criteria such as the yields, the organoleptic properties, and the size and shape of tubers [47]. This has made their growing hardly possible without chemical control [48]. Yet, varietal selection also plays a significant role in disease management [49]. Many studies have demonstrated the effectiveness of resistant varieties exhibiting reduced or even no symptoms of either foliage or tuber late blight [50,51,52,53][50][51][52][53]. Besides this, among alternative tools, natural molecules including plants metabolites are emerging. Their use in the frame of IPM recently introduced the notion of biocontrol, recently promoted by European legislation [54].
References
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2. Haverkort, A.J.; Struik, P.C. Yield Levels of Potato Crops: Recent Achievements and Future Prospects. Field Crops Res. 2015, 182, 76–85. [CrossRef]
3. Raymundo, R.; Asseng, S.; Robertson, R.; Petsakos, A.; Hoogenboom, G.; Quiroz, R.; Hareau, G.; Wolf, J. Climate Change Impact on Global Potato Production. Eur. J. Agron. 2018, 100, 87–98. [CrossRef]
4. Djaman, K.; Koudahe, K.; Koubodana, H.D.; Saibou, A.; Essah, S. Tillage Practices in Potato (Solanum tuberosum L.) Production: A Review. Am. J. Potato Res. 2022, 99, 1–12. [CrossRef]
5. Haverkort, A.J. Ecology of Potato Cropping Systems in Relation to Latitude and Altitude. Agric. Syst. 1990, 32, 251–272. [CrossRef]
6. Dupuis, J.H.; Liu, Q. Potato Starch: A Review of Physicochemical, Functional and Nutritional Properties. Am. J. Potato Res. 2019, 96, 127–138. [CrossRef]
7. Navarre, D.A.; Goyer, A.; Shakya, R. Chapter 14—Nutritional Value of Potatoes: Vitamin, Phytonutrient, and Mineral Content. In Advances in Potato Chemistry and Technology; Singh, J., Kaur, L., Eds.; Washington State University: Prosser, WA, USA, 2009; pp. 395–424, ISBN 978-0-12-374349-7.
8. Godfray, H.C.J.; Beddington, J.R.; Crute, I.R.; Haddad, L.; Lawrence, D.; Muir, J.F.; Pretty, J.; Robinson, S.; Thomas, S.M.; Toulmin, C. Food Security: The Challenge of Feeding 9 Billion People. Science 2010, 327, 812–818. [CrossRef]
9. Cooke, D.E.L.; Drenth, A.; Duncan, J.M.; Wagels, G.; Brasier, C.M. A Molecular Phylogeny of Phytophthora and Related Oomycetes. Fungal Genet. Biol. 2000, 30, 17–32. [CrossRef]
10. Kroon, L.P.N.M.; Brouwer, H.; de Cock, A.W.A.M.; Govers, F. The Genus Phytophthora Anno 2012. Phytopathology 2012, 102, 348–364. [CrossRef]
11. Sogin, M.L.; Silberman, J.D. Evolution of the Protists and Protistan Parasites from the Perspective of Molecular Systematics. Int. J. Parasitol. 1998, 28, 11–20. [CrossRef]
12. Crous, P.W.; Rossman, A.Y.; Aime, M.C.; Allen, W.C.; Burgess, T.; Groenewald, J.Z.; Castlebury, L.A. Names of Phytopathogenic Fungi: A Practical Guide. Phytopathology 2021, 111, 1500–1508. [CrossRef]
13. Carlile, M.J. The Success of the Hypha and Mycelium. In The Growing Fungus; Gow, N.A.R., Gadd, G.M., Eds.; Springer: Dordrecht, The Netherlands, 1995; pp. 3–19, ISBN 978-0-585-27576-5.
14. Werner, S.; Steiner, U.; Becher, R.; Kortekamp, A.; Zyprian, E.; Deising, H.B. Chitin Synthesis during in Planta Growth and Asexual Propagation of the Cellulosic Oomycete and Obligate Biotrophic Grapevine Pathogen Plasmopara Viticola. FEMS Microbiol. Lett. 2002, 208, 169–173. [CrossRef] [PubMed]
15. Chérif, M.; Benhamou, N.; Belanger, R. Occurrence of Cellulose and Chitin in the Hyphal Walls of Pythium Ultimum: A Comparative Study with Other Plant Pathogenic Fungi. Can. J. Microbiol. 2011, 39, 213–222. [CrossRef]
16. Ivanov, A.A.; Ukladov, E.O.; Golubeva, T.S. Phytophthora infestans: An Overview of Methods and Attempts to Combat Late Blight. J. Fungi 2021, 7, 1071. [CrossRef]
17. Goss, E.M.; Tabima, J.F.; Cooke, D.E.L.; Restrepo, S.; Fry, W.E.; Forbes, G.A.; Fieland, V.J.; Cardenas, M.; Grünwald, N.J. The Irish Potato Famine Pathogen Phytophthora infestans Originated in Central Mexico Rather than the Andes. Proc. Natl. Acad. Sci. USA 2014, 111, 8791–8796. [CrossRef] [PubMed]
18. Grünwald, N.J.; Flier, W.G. The Biology of Phytophthora infestans at Its Center of Orgin. Annu. Rev. Phytopathol. 2005, 43, 171–190. [CrossRef] [PubMed]
19. Ristaino, J.B. Tracking Historic Migrations of the Irish Potato Famine Pathogen, Phytophthora infestans. Microbes Infect. 2002, 4, 1369–1377. [CrossRef]
20. Schumann, G.L.; D’Arcy, C.J. CHAPTER 1: The Irish Potato Famine: The Birth of Plant Pathology. In Hungry Planet: Stories of Plant Diseases; General Plant Pathology; The American Phytopathological Society: Saint Paul, MN, USA, 2017; pp. 1–19, ISBN 978-0-89054-490-7.
21. Nowicki, M.; Foolad, M.R.; Nowakowska, M.; Kozik, E.U. Potato and Tomato Late Blight Caused by Phytophthora infestans: An Overview of Pathology and Resistance Breeding. Plant Dis. 2012, 96, 4–17. [CrossRef]
22. Fawke, S.; Doumane, M.; Schornack, S. Oomycete Interactions with Plants: Infection Strategies and Resistance Principles. Microbiol. Mol. Biol. Rev. 2015, 79, 263–280. [CrossRef]
23. Fry, W.E.; Birch, P.R.J.; Judelson, H.S.; Grünwald, N.J.; Danies, G.; Everts, K.L.; Gevens, A.J.; Gugino, B.K.; Johnson, D.A.; Johnson, S.B.; et al. Five Reasons to Consider Phytophthora infestans a Reemerging Pathogen. Phytopathology 2015, 105, 966–981. [CrossRef]
24. Olanya, M.; Anwar, M.; He, Z.; Larkin, R.; Honeycutt, C. Survival Potential of Phytophthora infestans Sporangia in Relation to Environmental Factors and Late Blight Occurrence. J. Plant Prot. Res. 2016, 56, 73–81. [CrossRef]
25. Hagman, J.E.; Mårtensson, A.; Grandin, U. Cultivation Practices and Potato Cultivars Suitable for Organic Potato Production. Potato Res. 2009, 52, 319–330. [CrossRef]
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33. Fry, W.E. Phytophthora infestans: New Tools (and Old Ones) Lead to New Understanding and Precision Management. Annu. Rev. Phytopathol. 2016, 54, 529–547. [CrossRef]
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37. Elansky, S.; Pobedinskaya, M.A.; Kokaeva, L.; Statsyuk, N.; Dyakov, Y.T. Phytophthora infestans Populations from the European Part of Russia: Genotypic Structure and Metalaxyl Resistance. J. Plant Pathol. 2015, 97, 449–456. [CrossRef]
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46. Tsedaley, B. Late Blight of Potato (Phytophthora infestans) Biology, Economic Importance and Its Management Approaches. J. Biol. Agric. Healthc. 2014, 4, 215–225.
47. Forbes, G.A. Using Host Resistance to Manage Potato Late Blight with Particular Reference to Developing Countries. Potato Res. 2012, 55, 205–216. [CrossRef]
48. Runno-Paurson, E.; Williams, I.H.; Metspalu, L.; Kaart, T.; Mänd, M. Current Potato Varieties Are Too Susceptible to Late Blight to Be Grown without Chemical Control under North-East European Conditions. Acta Agric. Scand. Sect. B—Soil Plant Sci. 2013, 63, 80–88. [CrossRef]
49. Haverkort, A.J.; Boonekamp, P.M.; Hutten, R.; Jacobsen, E.; Lotz, L.A.P.; Kessel, G.J.T.; Visser, R.G.F.; van der Vossen, E.A.G. Societal Costs of Late Blight in Potato and Prospects of Durable Resistance Through Cisgenic Modification. Potato Res. 2008, 51, 47–57. [CrossRef]
50. Kefelegn, H.; Chala, A.; Kassa, B.; Pananjay, G.; Tiwari, K. Evaluation of Different Potato Variety and Fungicide Combinations for the Management of Potato Late Blight (Phytophthora infestans) in Southern Ethiopia. Int. J. Life Sci. 2012, 1, 8–15.
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References

  1. Devaux, A.; Goffart, J.-P.; Petsakos, A.; Kromann, P.; Gatto, M.; Okello, J.; Suarez, V.; Hareau, G. Global Food Security, Contributions from Sustainable Potato Agri-Food Systems. In The Potato Crop: Its Agricultural, Nutritional and Social Contribution to Humankind; Campos, H., Ortiz, O., Eds.; Springer International Publishing: Cham, Swizerland, 2020; pp. 3–35. ISBN 978-3-03028-683-5.
  2. Haverkort, A.J.; Struik, P.C. Yield Levels of Potato Crops: Recent Achievements and Future Prospects. Field Crops Res. 2015, 182, 76–85.
  3. Raymundo, R.; Asseng, S.; Robertson, R.; Petsakos, A.; Hoogenboom, G.; Quiroz, R.; Hareau, G.; Wolf, J. Climate Change Impact on Global Potato Production. Eur. J. Agron. 2018, 100, 87–98.
  4. Djaman, K.; Koudahe, K.; Koubodana, H.D.; Saibou, A.; Essah, S. Tillage Practices in Potato (Solanum tuberosum L.) Production: A Review. Am. J. Potato Res. 2022, 99, 1–12.
  5. Haverkort, A.J. Ecology of Potato Cropping Systems in Relation to Latitude and Altitude. Agric. Syst. 1990, 32, 251–272.
  6. Dupuis, J.H.; Liu, Q. Potato Starch: A Review of Physicochemical, Functional and Nutritional Properties. Am. J. Potato Res. 2019, 96, 127–138.
  7. Navarre, D.A.; Goyer, A.; Shakya, R. Chapter 14—Nutritional Value of Potatoes: Vitamin, Phytonutrient, and Mineral Content. In Advances in Potato Chemistry and Technology; Singh, J., Kaur, L., Eds.; Washington State University: Prosser, WA, USA, 2009; pp. 395–424. ISBN 978-0-12-374349-7.
  8. Godfray, H.C.J.; Beddington, J.R.; Crute, I.R.; Haddad, L.; Lawrence, D.; Muir, J.F.; Pretty, J.; Robinson, S.; Thomas, S.M.; Toulmin, C. Food Security: The Challenge of Feeding 9 Billion People. Science 2010, 327, 812–818.
  9. Cooke, D.E.L.; Drenth, A.; Duncan, J.M.; Wagels, G.; Brasier, C.M. A Molecular Phylogeny of Phytophthora and Related Oomycetes. Fungal Genet. Biol. 2000, 30, 17–32.
  10. Kroon, L.P.N.M.; Brouwer, H.; de Cock, A.W.A.M.; Govers, F. The Genus Phytophthora Anno 2012. Phytopathology 2012, 102, 348–364.
  11. Sogin, M.L.; Silberman, J.D. Evolution of the Protists and Protistan Parasites from the Perspective of Molecular Systematics. Int. J. Parasitol. 1998, 28, 11–20.
  12. Crous, P.W.; Rossman, A.Y.; Aime, M.C.; Allen, W.C.; Burgess, T.; Groenewald, J.Z.; Castlebury, L.A. Names of Phytopathogenic Fungi: A Practical Guide. Phytopathology 2021, 111, 1500–1508.
  13. Carlile, M.J. The Success of the Hypha and Mycelium. In The Growing Fungus; Gow, N.A.R., Gadd, G.M., Eds.; Springer: Dordrecht, The Netherlands, 1995; pp. 3–19. ISBN 978-0-585-27576-5.
  14. Werner, S.; Steiner, U.; Becher, R.; Kortekamp, A.; Zyprian, E.; Deising, H.B. Chitin Synthesis during in Planta Growth and Asexual Propagation of the Cellulosic Oomycete and Obligate Biotrophic Grapevine Pathogen Plasmopara Viticola. FEMS Microbiol. Lett. 2002, 208, 169–173.
  15. Chérif, M.; Benhamou, N.; Belanger, R. Occurrence of Cellulose and Chitin in the Hyphal Walls of Pythium Ultimum: A Comparative Study with Other Plant Pathogenic Fungi. Can. J. Microbiol. 2011, 39, 213–222.
  16. Ivanov, A.A.; Ukladov, E.O.; Golubeva, T.S. Phytophthora infestans: An Overview of Methods and Attempts to Combat Late Blight. J. Fungi 2021, 7, 1071.
  17. Goss, E.M.; Tabima, J.F.; Cooke, D.E.L.; Restrepo, S.; Fry, W.E.; Forbes, G.A.; Fieland, V.J.; Cardenas, M.; Grünwald, N.J. The Irish Potato Famine Pathogen Phytophthora infestans Originated in Central Mexico Rather than the Andes. Proc. Natl. Acad. Sci. USA 2014, 111, 8791–8796.
  18. Grünwald, N.J.; Flier, W.G. The Biology of Phytophthora infestans at Its Center of Orgin. Annu. Rev. Phytopathol. 2005, 43, 171–190.
  19. Ristaino, J.B. Tracking Historic Migrations of the Irish Potato Famine Pathogen, Phytophthora infestans. Microbes Infect. 2002, 4, 1369–1377.
  20. Schumann, G.L.; D’Arcy, C.J. CHAPTER 1: The Irish Potato Famine: The Birth of Plant Pathology. In Hungry Planet: Stories of Plant Diseases; General Plant Pathology; The American Phytopathological Society: Saint Paul, MN, USA, 2017; pp. 1–19. ISBN 978-0-89054-490-7.
  21. Nowicki, M.; Foolad, M.R.; Nowakowska, M.; Kozik, E.U. Potato and Tomato Late Blight Caused by Phytophthora infestans: An Overview of Pathology and Resistance Breeding. Plant Dis. 2012, 96, 4–17.
  22. Fawke, S.; Doumane, M.; Schornack, S. Oomycete Interactions with Plants: Infection Strategies and Resistance Principles. Microbiol. Mol. Biol. Rev. 2015, 79, 263–280.
  23. Fry, W.E.; Birch, P.R.J.; Judelson, H.S.; Grünwald, N.J.; Danies, G.; Everts, K.L.; Gevens, A.J.; Gugino, B.K.; Johnson, D.A.; Johnson, S.B.; et al. Five Reasons to Consider Phytophthora infestans a Reemerging Pathogen. Phytopathology 2015, 105, 966–981.
  24. Olanya, M.; Anwar, M.; He, Z.; Larkin, R.; Honeycutt, C. Survival Potential of Phytophthora infestans Sporangia in Relation to Environmental Factors and Late Blight Occurrence. J. Plant Prot. Res. 2016, 56, 73–81.
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