Management of Colletotrichum orbiculare: History
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Contributor:
Takshay Patel
,
Lina M. Quesada-Ocampo
,
Todd C. Wehner
,
Bed Prakash Bhatta
,
Edgar Correa
,
Subas Malla

The fungus Colletotrichum orbiculare causes watermelon anthracnose and is an important pathogen of watermelon in the United States, causing a significant impact on yield and quality of the produce. The application of fungicides as preventative and post-occurrence control measures is currently being deployed by growers. Further study of the genetic and molecular basis of anthracnose resistance will help in guiding future watermelon breeding strategies. Several conserved virulence factors (effectors) in C. orbiculare have been reported to interact with the host, at times impairing the host immune machinery. 

  • anthracnose
  • Colletotrichum orbiculare
  • watermelon

1. Disease Management

Field management practices for anthracnose include planting disease-free seed material, deep plowing of crop residue immediately after harvest, crop rotation with non-cucurbit crops for a minimum of 1 year (2 to 3 years is optimum), avoiding usage of farm machinery among fields when the foliage is wet, fungicide applications with effective active ingredients such as quinone outside inhibitors (QoIs), and resistant plant cultivars [1]. To reduce fruit damage by anthracnose, growers are recommended to avoid mechanical injury to fruits, inspect for infected fruits during harvest and discard them, disinfect the fruit surface with chlorinated water, and refrigerate the fruit after harvest to prevent or delay anthracnose development postharvest [1].

2. Host Resistance

Host resistance screening was conducted either on cotyledons [2] or the two- to four-true-leaf stage [3][4][5][6][7][8]. The disease inoculum used for the seedling screening varied from 2.5 × 103 [8] to 5 × 105 [5] conidial spores/mL. The incubation time also varied from 3 to 14 days post-inoculation (DPI). A recent study reported the optimum inoculum concentration and DPI for screening two- to four-leaf-stage seedlings for race 2 anthracnose resistance [4].
In 1937, Layton started breeding for anthracnose resistance and identified sources of resistance to develop commercial cultivars. Five cultivars from Africa with high resistance to anthracnose were identified, out of which three had edible fruit and desired horticultural traits [9]. The three cultivars were named Africa 8, 9, and 13, and were further used as parents. Homozygous anthracnose-resistant selections from Africa 8, 9, and 13 were crossed with commercial cultivars Iowa Belle and Iowa King and a few other cultivars [9]. The commercial Iowa cultivars were wilt-resistant, large-fruited, and crisp-fleshed. The first widely accepted anthracnose-resistant watermelon cultivars were ‘Congo’ (1949), ‘Fairfax’ (1953), and ‘Charleston Gray’ (1955), released by Andrus [8][10]. Charleston Gray, Congo, and Fairfax are resistant to races 1 and 3 but susceptible to race 2 [11]. Cultivars resistant to race 1 were also resistant to race 3 [8][12].
Resistance to race 2 was first found in a citron, W695, which was also resistant to races 1 and 3 [8]. PI 326515 was the first PI reported to have resistance only to race 2 [7]. More resistance sources to race 2 including PI 189225, 271775, 271778, and 512385 were identified [3][6]. Resistance to anthracnose race 2 was also identified in Citrullus colocynthis, designated as R309 [13]. Interestingly, two studies found that resistance in Citrullus colocynthis, R309, did not follow the single gene inheritance and was suggested to be multigenic [13]. These studies suggested that a dominant single gene confers major resistance, but there are other genes contributing to the phenotype. R309 has been the only source of multigenic resistance; no other multigenic resistance sources have been reported.
The first inheritance work on anthracnose resistance was performed in 1937 [9]. Resistance to race 1 is dominant over susceptibility and segregates as a single gene. Resistance to races 1 and 3 is controlled by the same gene, Ar-1 [8]. Inheritance of race 2 resistance is like race 1 resistance, dominant and segregating as a single gene [7]. In Korea, Jang et al. used a biparental population, ‘DrHS7250’ (female parent, resistant breeding line) and ‘Oto9491’ (male parent, susceptible breeding line), to identify a C. orbiculare race 1-resistance quantitative trait locus (QTL) on chromosome 8 and further conducted transcriptomics via RNAseq on the parents to identify a coiled-coil (CC)–nucleotide-binding site (NBS)–leucine-rich repeat (LRR) gene in the QTL region that conferred resistance to the disease [14]. They hypothesized that residue 18 of a conserved motif, IxxLPxSxxxLYNLQTLxL, could govern resistance in ‘DrHs7250’. An independent study conducted in the U.S. using a biparental mapping population, ‘Charleston Gray’ (female parent, resistant) and ‘New Hampshire Midget’ (male parent, susceptible), found a major C. orbiculare race 1-resistance QTL in the same region on chromosome 8 [15]. A PACE SNP marker designed from the SNP marker CL 14-27-9, identified earlier [14], was also the diagnostic marker for the QTL (LOD = 14.06) in the study. Even though the resistance source for the breeding line ‘DrHS7250’ was not reported, it seemed that both ‘DrHS7250’ and ‘Charleston Gray’ may have the same resistance gene for C. orbiculare race 1. Both studies in different watermelon resistance sources validated that the race 1 anthracnose resistance is governed by a single dominant gene. Even today, anthracnose is a problem and a major research priority in watermelon [16]. Most of the current commercial cultivars with anthracnose resistance were developed by private industry (Table 1). These commercial cultivars have intermediate to high levels of resistance to anthracnose race 1, and some descriptions do not specify the race. Many hybrid watermelon cultivars are resistant to races 1 and 2B and susceptible to race 2 [1]. The SNP marker CL 14-27-9 could be utilized as a diagnostic marker to develop race 1-resistant cultivars via marker-assisted selection in watermelon breeding programs.
Table 1. Anthracnose-resistant cultivars of watermelon.
Cultivar Level of Resistance Race Company
SSX8585 High 1 Sakata, Yokohama, Japan
Valentino High 1 Sakata, Yokohama, Japan
Belmont Intermediate 1 Sakata, Yokohama, Japan
Sweet Treasure Intermediate 1 Sakata, Yokohama, Japan
Fascination Intermediate 1 Syngenta, Basel, Switzerland
Melody Intermediate 1 Syngenta, Basel, Switzerland
Excursion Intermediate 1 Syngenta, Basel, Switzerland
Captivation Intermediate 1 Syngenta, Basel, Switzerland
Cooperstown High 1 Seminis, St. Louis, MO, USA
Majestic High ? † Seminis, St. Louis, MO, USA
Road Trip High ? Seminis, St. Louis, MO, USA
Santa Matilde High 1 Seminis, St. Louis, MO, USA
HMX 1925 Intermediate 1 HM Clause, Davis, CA, USA
Maistros F1 High 1 HM Clause, Davis, CA, USA
Accomplice High 1 HM Clause, Davis, CA, USA
Millennium High 1 HM Clause, Davis, CA, USA

3. Crop Protection

Growers often use fungicides to manage watermelon anthracnose throughout the growing season. Fungicides can be applied preventatively if cost-effective, or application should be started with the occurrence of the symptoms in a 5-to-10-day interval. If disease severity is high or environmental conditions are conducive to disease (wet weather), growers will use the shorter application interval. Effective fungicide active ingredients for managing watermelon anthracnose include compounds in group 11: trifloxystrobin, azoxystrobin, pyraclostrobin, fluoxastrobin; group 7: boscalid, fluxapyroxad; group 3: difenoconazole; group M05: chlorothalonil; and group M03: mancozeb [17][18]. Group 11 fungicides correspond to quinone outside inhibitors (QoIs), group 7 fungicides correspond to succinate dehydrogenase inhibitors (SDHIs), group 3 fungicides correspond to demethylation inhibitors (DMIs), and M05 and M03 have multi-site contact activity. Products commonly recommended for watermelon anthracnose control include ‘Kocide 3000’ (Copper Hydroxide), ‘Pristine’ (pyraclostrobin, boscalid), ‘Cabrio’ (pyraclostrobin), ‘Quadris Top’ (azoxystrobin, difenoconazole), ‘Bravo WeatherStik’ (chlorothalonil), and ‘TopGuard EQ’ (azoxystrobin) [17][19][20][21].

This entry is adapted from the peer-reviewed paper 10.3390/horticulturae9101132

References

  1. Keinath, A.P. Anthracnose. In Compendium of Cucurbit Diseases and Pests, 2nd ed.; Keinath, A.P., Wintermantel, W.M., Zitter, T.A., Eds.; The American Phytopathological Society: St. Paul, MN, USA, 2017; pp. 54–55.
  2. Wasilwa, L.; Correll, J.; Morelock, T.; McNew, R. Reexamination of races of the cucurbit anthracnose pathogen Colletotrichum orbiculare. Phytopathology 1993, 83, 1190–1198.
  3. Boyhan, G.; Norton, J.; Abrahams, B.; Wen, H. A new source of resistance to anthracnose (Race 2) in watermelon. HortScience 1994, 29, 111–112.
  4. Correa, E.; Crosby, K.; Malla, S. Optimizing a seedling screening method for anthracnose resistance in watermelon. Plant Health Prog. 2021, 22, 536–543.
  5. Keinath, A.P. Identification of races of Colletotrichum orbiculare on muskmelon in South Carolina. Plant Health Prog. 2015, 16, 88–89.
  6. Sowell, G., Jr.; Rhodes, B.; Norton, J. New sources of resistance to watermelon anthracnose . J. Am. Soc. Hortic. Sci. 1980, 105, 197–199.
  7. Suvanprakorn, K.; Norton, J. Inheritance of resistance to race 2 anthracnose in watermelon. J. Am. Soc. Hortic. Sci. 1980, 106, 862–865.
  8. Winstead, N.; Goode, M.; Barham, W. Resistance in watermelon to Colletotrichum lagenarium races 1, 2, and 3. Plant Dis. Rep. 1959, 43, 570–577.
  9. Layton, D.V. The Parasitism of Colletotrichum lagenarium (Pass.) Ell. and Halst.; Research Bulletin 223; Agricultural Experiment Station, Iowa State College of Agriculture and Mechanic Arts: Ames, IA, USA, 1937; pp. 37–67.
  10. Andrus, C.F. New watermelon varieties: Bring new life to that industry. Seed World 1955, 4, 36–40.
  11. Goode, M.J. Physiological specialization in Colletotrichum lagenarium. Phytopathology 1958, 48, 79–83.
  12. Jenkins, S.F.; Winstead, N. Glomerella magna, cause of a new anthracnose of cucurbits. Phytopathology 1964, 54, 452–454.
  13. Love, S.; Rhodes, B. Single gene control of anthracnose resistance in Citrullus? Cucurbit Genet. Coop. Rep. 1988, 11, 64–67.
  14. Jang, Y.J.; Seo, M.; Hersh, C.P.; Rhee, S.-J.; Kim, Y.; Lee, G.P. An evolutionarily conserved non-synonymous SNP in a leucine-rich repeat domain determines anthracnose resistance in watermelon. Theor. Appl. Genet. 2019, 132, 473–488.
  15. Bhatta, B.P.; Patel, T.; Correa, E.; Wehner, T.C.; Crosby, K.M.; Thomson, M.J.; Metz, R.; Wang, S.; Brun, M.; Johnson, C.D.; et al. Dissection of race 1 anthracnose resistance in a watermelon (Citrullus lanatus var. lanatus) biparental mapping population. Euphytica 2022, 218, 157.
  16. Kousik, C.S.; Brusca, J.; Turechek, W.W. Diseases and disease management strategies take top research priority in the Watermelon Research and Development Group members survey (2014 to 2015). Plant Health Prog. 2016, 17, 53–58.
  17. FRAC. FRAC Code List ©*2018: Fungicides Sorted by Mode of Action (Including FRAC Code Numbering); Fungicide Resistance Action Committee: Brussels, Belgium, 2018.
  18. Adams, M.L.; Noël, N.A.; Collins, H.; Quesada-Ocampo, L.M. Evaluation of fungicides for control of anthracnose on cucumber, Clinton 2017. Plant Dis. Manag. Rep. 2018, 12, V099.
  19. Egel, D.S.; Marchino, C. Evaluation of systemic fungicide timing for the control of anthracnose on watermelon, 2017. Plant Dis. Manag. Rep. 2018, 12, V049.
  20. Everts, K.L.; Korir, R.C. Evaluation of fungicides for management of foliar diseases on watermelon, 2016. Plant Dis. Manag. Rep. 2017, 11, V022.
  21. Everts, K.L.; Korir, R.C. Evaluation of fungicide programs for management of foliar diseases on watermelon, 2017. Plant Dis. Manag. Rep. 2018, 12, V039.
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