Cercospora Leaf Spot of Sugar Beet and Related Species

Preface Cercospora leaf spot (CLS) of sugar beet has been a high-impact and persistent problem for the beet sugar industry since the causal agent Cercospora beticola was first described in 1876. For well over a century, scientists have confronted this problem and have expended considerable resources on the management of CLS of sugar beet and related crop species.

This volume, Cercospora Leaf Spot of Sugar Beet and Related Species, is the first book to merge the information on past and current research efforts, which are directed toward understanding and managing CLS of sugar beet and its relatives. The concept for this publication originated during the First International Symposium of Cercospora Leaf Spot of Sugar Beet held in conjunction with the annual APS meeting at Quebec City, Quebec, Canada, in 2006. This volume should serve as a source of information on CLS for current and future researchers, students, and the beet sugar industry. We also hope that it serves as a basis for discussion within the scientific community on current and emerging ideas in the management of CLS on sugar beet and related species.

The volume begins with introductory information on the history of sugar beet as source of sugar, emergence of CLS as a problem, ecology, and the epidemiology of the disease.

Under the section “Biology of Cercospora beticola,” the first subsection deals with taxonomic information including speciation and host range of C. beticola, mating types, and vegetative compatibility. The subsection on ecology and epidemiology presents information on survival, spore trapping, dispersal, and primary infection. Other subjects presented here encompass the relationship of C. beticola with host plants and fungal antagonists and CLS of vegetable crops in the Chenopodiaceae. The final subsection offers information of Cercospora toxins, with references to specific aspects of cercosporin and beticolin. The final section deals with management of Cercospora leaf spot of sugar beet.

In the the subsection, “Traditional and Novel Breeding for Host Plant Resistance,” different approaches in breeding for resistance against C. beticola are discussed. Other topics in this subsection include a historical review of breeding for resistance to C. beticola in North America, strategies for the development of resistance to cercosporin, and the use of the Cercospora CFP toxin pump gene to improve resistance in crop plant species. Under the subsection “Fungicide Resistance,” the genetics of fungicide resistance in Cercospora and Mycosphaerella are presented, as well as U.S. and European perspectives of fungicide resistance. The final part of this subsection presents information on sensitivity of C. beticola to foliar fungicides. The final subsection is “Disease Management.” This begins with an integrated pest management approach, followed by CLS prediction models as a basis for managing C. beticola in North America.

Recommendations for timing fungicide applications in sugar beet are discussed in the next chapter, followed by information on management in sugar beets using fungicides with disease-tolerant cultivars. The final chapter on integrated management of CLS includes novel information on biological control of C. beticola and CLS of sugar beet. iii

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On behalf of all the contributing authors, the editors would like to acknowledge invaluable help that was provided by Beth Redlin of the USDA-Agricultural Research Service, Sidney, Montana. Beth played a very significant in role in the organization of the First International Symposium of Cercospora Leaf Sport of Sugar Beet that was held at Quebec City, Quebec, Canada, in 2006. She provided hours of editorial assistance in compiling, checking, and organizing the manuscripts in preparation of this volume. We acknowledge and appreciate the editing of the manuscripts and excellent suggestions by Robert M. Harveson and Carl A. Bradley. We also would like to acknowledge financial assistance that was provided for the symposium by the Beet Sugar Development Foundation and SESVanderHave as well as the USDA-ARS which also provided additional aid for the publication of this book. Finally, we would like to express our sincere thanks to all at the APS Press and the Editorial Board for agreeing to and providing guidance for publication of this Book.

Robert T. Lartey John J. Weiland Lee Panella Pedro Crous Carol Windels

Contents Part I: Introduction to Cercospora 1. A Brief History of Cercospora Leaf Spot of Sugar Beet .........................................1 Robert T. Lartey, John J. Weiland, and Lee Panella 2. Ecology and Epidemiology of Cercospora beticola ...............................................7 Gary D. Franc

Part II: Biology of Cercospora beticola A) Taxonomy 3. Cercospora Speciation and Host Range ................................................................21 Johannes Z. Groenewald, Marizeth Groenewald, Uwe Braun, and Pedro W. Crous 4. Mating Type Genes in Cercospora beticola and Allied Species...........................39 Marizeth Groenewald, Johannes Z. Groenewald, and Pedro W. Crous 5. Vegetative Compatibility Groups in Cercospora beticola ....................................55 Maddalena Moretti, Marco Saracchi, and Gandolfina Farina B) Ecology and Epidemiology 6. Survival, Spore Trapping, Dispersal, and Primary Infection Site for Cercospora beticola in Sugar Beet ..................................................................67 M. F. R. Khan and J. Khan 7. Relations of Cercospora beticola with Host Plants and Fungal Antagonists........77 Robert T. Lartey, Soumitra Ghoshroy, TheCan Caesar-TonThat, Andrew W. Lenssen, and Robert G. Evans 8. Cercospora Leaf Spot of Vegetable Crops in the Chenopodiaceae .......................91 Steven T. Koike, Lindsey J. du Toit, and George S. Abawi C) Toxins of Cercospora 9. Cercosporin Production in Cercospora and Related Anamorphs of Mycosphaerella .................................................................................................97 Stephen B. Goodwin and Larry D. Dunkle 10. The Role of Cercosporin in the Virulence of Cercospora spp. to Plant Hosts....109 John J. Weiland, Kuang-Ren Chung, and Jeffrey C. Suttle vii

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11. Beticolins: Chemistry and Biological Activities .................................................119 Marie-Louise Milat, Thierry PrangĂŠ, Sabine Wiedemann-Merdinoglu, and Jean-Pierre Blein

Part III: Management of the Cercospora Leaf Spot of Sugar Beet A) Traditional and Novel Breeding for Host Plant Resistance 12. Conventional and Novel Approaches in Breeding for Resistance to Cercospora beticola in Sugar Beet..................................................................129 Bernd Holtschulte, Wolfgang Mechelke, and Dietmar J. Stahl 13. The History of Public Breeding for Resistance to Cercospora Leaf Spot in North America .................................................................................................141 Lee Panella and J. Mitchell McGrath 14. Strategies for the Development of Resistance to Cercosporin, a Toxin Produced by Cercospora Species...........................................................157 Margaret E. Daub, Sonia Herrero, and Tanya V. Taylor 15. Innovative Strategies for Improving Leaf Spot Disease Resistance in Sugar Beet .......................................................................................................173 Robert G. Upchurch and L. David Kuykendall B) Fungicide Resistance 16. Genetics of Fungicide Resistance in Cercospora and Mycosphaerella ..............179 L. E. Hanson 17. Fungicide Resistance of Cercospora beticola in Europe ....................................189 George S. Karaoglanidis and Philippos M. Ioannidis 18. Sensitivity of Cercospora beticola to Foliar Fungicides in the Red River Valley of North Dakota and Minnesota ...................................213 Gary A. Secor, Viviana V. Rivera-Varas, Neil C. Gudmestad, and John J. Weiland C) Disease Management 19. Quaternary Concept of Integrated Pest Management (IPM) Developed for the Control of Cercospora Leaf Spot in Sugar Beet.......................................223 Peter F. J. Wolf and J.-A.Verreet 20. Cercospora Leaf Spot Prediction Models in North America...............................235 Carol E. Windels 21. Uniform Recommendation for Timing Fungicide Applications to Control Cercospora beticola on Sugar Beet in the Red River Valley.............251 M. F. R. Khan and J. Khan 22. Control of Cercospora Leaf Spot and Powdery Mildew of Sugar Beet with Fungicides and Tolerant Cultivars...............................................................259 Philippos M. Ioannidis and George S. Karaoglanidis 23. Integrated Management of Cercospora Leaf Spot ...............................................275 B. J. Jacobsen Index..................................................................................................................................285

Chapter 1

Brief History of Cercospora Leaf Spot of Sugar Beet Robert T. Lartey, John J. Weiland, and Lee Panella Sugar beet (Beta vulgaris L.), as it is known today, was developed from the beet root (Runkelrübe), which is most likely a native of the humid parts of western and southern Asia. Although the beet was probably known as early as 500 B.C., it was first cultivated for sugar in Europe in the eighteenth century (Van Cleef 1915). According to Van Cleef, uncertainty remains about the westward movement of the beet to Europe. What is certain is that it arrived in Europe via the Mediterranean countries through Egypt. Long before its cultivation as an alternate source of sugar, beet was harvested as a vegetable and for medicinal use. The cultivation of sugar beet as an alternative source of sugar is attributed to the work of Andreas Siegmund Marggraf in the 1740s and his student Franz Karl Achard, who is credited with building the first sugar factory (Fabrik) in Cunern, near Breslau (Polish Wroclaw), Schlesia, in 1801 (Van Cleef 1915; Coons 1949).

Following Nelson’s victory in the Napoleonic war (1800–1815) at Trafalgar in 1805, continental Europe was cut off from the West Indies’ cane sugar by an English blockade.

By 1806, cane sugar had virtually disappeared from European shops. In 1811, as the story goes, Napoleon Bonaparte was presented with two loaves of sugar made from sugar beet.

Napoleon was so impressed that he decreed that 32,000 hectares of French land should be planted with beets and provided the assistance needed to get factories established. Sugar beet factories subsequently were established in France, Germany, Austria, Russia, and Denmark. This was the advent of the beet sugar industry in Europe. By the turn of the century, the proportion of the world’s beet crop used for sugar production rose from 14% in 1853 to 65% by 1900 (Poggi 1930).

Early attempts to establish a sugar industry in the United States in 1837 met with failure (Coons 1949). Indeed, according to Coons, the first beet sugar factory in the United States was established in Northampton, Massachusetts, in 1837 but was shut down within three years. The subsequent success of the industry in the United States was probably due to the efforts of Charles Goessmann, a German chemist at the Massachusetts Agricultural College, the predecessor of the University of Massachusetts (Adams 1999). Goessmann conducted the first scientific experiments on sugar beet culture in the United States between 1870 and 1874, establishing and strongly advocating conditions under which sugar beet could be cultivated profitably in the United States. The first successful sugar beet-based sugar factory was built at Alvarado, California, in 1870, rebuilt in 1879, and modernized in 1936 (Coons 1949).

Cercospora beticola Sacc., the causal agent of Cercospora leaf spot (CLS) of sugar beet and other cultivated and wild Beta spp., was first described as a species of the genus Cercospora by Saccardo (1876). The typification of Cercospora has been clouded in 1

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controversy (Crous and Braun 2003). The creation of the genus Cercospora is credited to Fresenius in 1863, who used this generic name to describe four passalora-like fungal species with pluriseptate conidia, viz., C. apii Fres., C. chenopodii Fres., C. penicillata (Ces.) Fres. (≡ Passalora penicillata Ces.), and C. ferruginea Fuckel, implying that a lectotypification is necessary (Lieneman 1929; Crous and Braun 2003). Pons and Sutton (1988) attributed the name Cercospora to Fuckel in 1863, and designated C. ferruginea Fuckel as the only species cited in the original publication (= ‘holotype’). Sutton and Pons (1991) acknowledged that Fuckel used C. ferruginea to describe a single species in his Fungi Rhenani exsiccati earlier in 1863. They, however, suggested that Fresenius probably communicated the unpublished generic name Cercospora “in litteris” to Fuckel. Indeed, according to Lieneman (1929) and Crous and Braun (2003), Fuckel provided a full description of the new genus Cercospora in 1863 with reference to Fresenius (‘Genus Cercospora Fres. Passalora valde affinis est, sed constanter sporidiis multiseptatis differt’). Furthermore, Cercospora penicillata (Ces.) Fres. (≡ Passalora penicillata Ces.) was the only species connected with the original description of Cercospora. Thus the latter species, which is identical with Cercospora depazeoides (Desm.) Sacc., must be considered the type species of Cercospora. C. depazeoides is a true Cercospora s.str. on Sambucus spp. congeneric with C. apii.

C. beticola likely originated in central Europe and the Mediterranean area (Groenewald et al. 2005). Before the beginning of the twentieth century, investigators gave various names to fungal pathogens that caused leaf spot diseases of sugar beet and related plants which, based on their descriptions, probably were C. beticola (Chupp 1954). Certainly some of these pathogens, including C. flagelliformis on Beta cicla and C. spinaciae on Chenopodium polyspermum, were reclassified as C. beticola. Yet Chupp (1954) still considered the Cercospora species to be plant host species-, genus-, or family-specific.

However, recent evidence has shown that the host range of some Cercospora species, including C. beticola, goes beyond plant families (Crous and Braun 2003; Groenewald et al. 2006). For example, C. beticola is now known to infect species within the genera Malva, Spinacia, Limonium, and Apium, all belonging to different plant families (Groenewald et al. 2006).

According to Saccardo (1886), on page 456 of his Sylloge Fungorum IV, early geographical distribution of C. beticola included Italy, Gallia (France), Austria, Germany, Lusitania (Portugal), America boreali (North America), and America australi (South America). Ten years after description of the genus, CLS was described as one of the most destructive diseases of sugar beet in Germany (von Thümen 1886). Outbreaks of CLS grew more severe in 1878 and drew serious attention in Europe. von Thümen (1886) described the severity of the disease in 1878, a year characterized by exceptionally high precipitation. He observed as many as 80 lesions of Cercospora leaf spot on a single sugar beet leaf. Meanwhile in the United States, Atkinson (1892) provided early information about the disease by reporting on the ongoing work of Pammel, a botanist at Iowa who was studying the life history of fungi, including C. beticola. By 1895, the disease was described as a serious problem in the United States (Halsted 1895). Thus, within three decades of establishment of the sugar beet industry in the United States and two decades of description of the species C. beticola by Saccordo in Italy, the pathogen appeared to have become a serious problem of the sugar beet industry worldwide.

One of the earliest descriptions of Cercospora leaf spot “Blattfleckenkrankheit der Zuckerrübe” of sugar beet was provided by von Thümen (1886). He described the disease, survival, dispersal, pathogenesis, and detailed descriptions of the symptoms. Additional descriptions of the Cercospora leaf spot symptoms were given by Halsted (1895), who also provided the first known photographic descriptions of the disease (Fig. 1).

Brief History of Cercospora Leaf Spot of Sugar Beet / 3

Early in the twentieth century, Pool and McKay (1916) conducted extensive experiments to identify climatic conditions favorable for infection of sugar beet by C. beticola.

They showed how production of conidia is influenced by temperature and relative humidity. In 1918, they continued investigating environmental requirements for CLS as well as pathogen survival, inoculum source, and disease pathogenesis (McKay and Pool 1918). In experiments on host range, they provided information that identified other beets and some common weeds as hosts of C. beticola. They also concluded that C. beticola is spread locally by air, insects and irrigation water, suggesting therefore a minimum distance of at least 100 yards between a new cropping and a non-rotating crop as a cultural control practice. Finally, they provided information on the effects of CLS on yield (beet weight and percent sugar). Vestal and Bell (1931) examined and provided information on environmental factors (air, soil temperature, humidity, light, wind, soil moisture, and evaporation) as they relate to CLS and yield (number of harvested beets, beet weight, percent sugar, and purity). Important information on long-term survival of C. beticola was provided by Nagel (1938), who studied longevity of C. beticola and stated that it could survive in sterile and field soils for 27 and 20 months, respectively. Later, Smith and Ruppel (1971) determined that further losses from CLS occur after harvest because C. beticola predisposes roots to storage rot. At least two toxins are produced by C. beticola. First is cercosporin, the perylenequinone photosensitizing toxin produced by Cercospora species that is implicated in the development of symptoms (Daub 1982; Daub and Ehrenschaft 2000), which was observed in culture as early as 1928 by Schmidt (1928). The other consists of the non-hostspecific nonpeptidic toxins produced by C. beticola. These yellow compounds were first described as “gelben factor” (GF) by Schlösser (1962). The toxins were subsequently

Fig. 1. Early photographic image of Cercospora leaf spot of sugar beet by B. D. Halsted; an engraving image from a sun print of a severely infected sugar beet leaf. (Reprinted from Halsted, B. D. 1895. Notes on Agriculture (I.). Science, New Series 1:376-379.)

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referred to as Cercospora beticola toxins (CBT) and finally named beticolin by Milat et al.

(1992). As a final point, original work by Smith and Gaskill (1970) on the genetic components of resistance to CLS confirmed that host plant resistance was controlled by at least four major genes and additional minor genes, all sensitive to environmental variation. von Thümen (1886) was first to recommend controls for CLS based on his own extensive research. Prominent among these were removal of infected plant tissues and rotation with nonhost crops. In the United States, Halsted (1899) experimented with different formulations of Bordeaux mixtures to control CLS. Evidence of attempts to select resistant varieties also were provided by Halsted (1895), who remarked, “There seems to be no respect shown for any variety of beets, for the writer (referring to himself) has made special visit to the trial grounds of large seed growers, and all sorts of beets, from the oldest to the newest kinds, were found with their foliage about equally injured.”

Well over a century after the description of C. beticola by Saccardo (1876), CLS continues to be the most important foliar disease of sugar beet. However, the comprehensive historical research conducted over the past century has laid the foundation for modern research on CLS and its management, which is further described in this volume.

Literature Cited Adams, D. L. 1999. Charles Anthony Goessmann–A leader in American agricultural chemistry. N. Engl.

Assoc. Chem. Teachers J. 18:8-11.

Atkinson, G. F. 1892. Botany at the experiment stations. Science 20:328-330.

Chupp, C. 1954. A monograph of the fungus genus Cercospora. The Author, Ithaca, NY. Coons, G. H. 1949. The sugar beet: Product of science. Sci. Mon. 68:149-164.

Crous, P. W., and Braun, U. 2003. Mycosphaerella and its anamorphs. 1. Names published in Cercospora and Passalora. Centraalbureau voor Schimmelcultures, Utrecht, The Netherlands.

Daub, M. E. 1982. Cercosporin, a photosensitizing toxin from Cercospora species. Phytopathology 72: 370-374.

Daub, M. E., and Ehrenschaft, M. 2000. The photoactivated Cercospora toxin cercosporin: Contributions to plant disease and fundamental biology. Ann. Rev. Phytopathol. 38:461-490.

Groenewald, M., Groenewald, J. Z., and Crous, P. W. 2005. Distinct species exist within the Cercospora apii morphotype. Phytopathology 95:951-959.

Groenewald, M., Groenewald, J. Z., Braun, U., and Crous, P. W. 2006. Host range of Cercospora apii and C. beticola, and description of C. apiicola, a novel species from celery. Mycologia 98:275-285.

Halsted, B. D. 1895. Notes on Agriculture (I.). Science, New Series 1:376-379.

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Brief History of Cercospora Leaf Spot of Sugar Beet / 5

Smith, G. A., and Gaskill, J. O. 1970. Inheritance of resistance to Cercospora leaf spot in sugarbeet. J. Am. Soc. Sugarbeet Technol. 16:172-180.

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