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. Halsted, B. D. 1899. Mycological Notes -V. Bull. Torrey Bot. Club 26:72-78. Lieneman, C. 1929. A host index to the North American species of the genus Cercospora. Ann. Mo. Bot. Gard. 16:1-52. McKay, M. B., and Pool, V. W. 1918. Field studies of Cercospora beticola. Phytopathology 8:119-136. Milat, M.-L., Prangé, T., Ducrot, P.-H., Tabet, J.-C., Einhorn, J., Blein, J.-P., and Lallemand, J. Y. 1992. Structures of the beticolins, the yellow toxins produced by Cercospora beticola. J. Am. Chem. Soc. 114:1478-1479. Nagel, C. A. 1938. The longevity of Cercospora beticola in soil. Phytopathology 28:342-350. Poggi, E. M. 1930. The German sugar beet industry. Econ. Geogr. 6:81-93. Pons, N., and Sutton, B. C. 1988. Cercospora and similar fungi on yams (Dioscorea spp.). Mycol, Pap. 1-78. Pool, V. W., and McKay, M. B. 1916. Climatic conditions as related to Cercospora beticola. J. Agric. Res. 6:21-60. Saccardo, P. A. 1876. Fungi veneti novi vel critici. Series V. Nuovo G. Bot. Ital. 8:162-211. Saccardo, P. A. 1886. Pages 456-457 in: Sylloge Fungorum IV. Schlösser, E. 1962. Über eine biologisch aktiv Sybstanz aus Cercospora beticola. Phytopathol. Z. 44:295312. Schmidt, E. W. 1928. Untersuchungen über die Cercospora-Blattfleckenkrankheit der Zuckerrübe. Z. Parasitenkd. 1:100-137.
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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. Smith, G. A., and Ruppel, E. G. 1971. Cercospora leaf spot as a predisposing factor in storage rot of sugar beet roots. Phytopathology 61:1485-1487. Sutton, B. C., and Pons, N. 1991. Proposal to conserve Cercospora Fresenius (Fungi). Taxon 40:643-646. Van Cleef, E. 1915. The sugar beet in Germany, with special attention to its relation to climate. Bull. Am. Geogr. Soc. 47:241-258. Vestal, E. F., and Bell, F. G. 1931. A preliminary study of some environmental factors on the spread of Cercospora leaf spot and yield in checked and drilled sugar beets. Am. J. Bot. 18:705-716. von Th체men, F. 1886. Die Bek채mpfung der Pilzkrankheiten unserer Culturgew채chse. Faesy Verlag, Wien.