Marssonina Leaf Blotch of Apple - A Growing Problem in South-Eastern New York

Dr. Srdjan Acimovic and Daniel J. Donahue

Excessive rain in New York and the rest of the Eastern US experienced in the second half of both the 2017 and 2018 growing seasons favored the development of Marssonina Leaf Blotch (MLB), a disease caused by Marssonina coronaria (sexual stage Diplocarpon mali). In early September 2017, in the lower-Hudson Valley and south NY we found MLB late in the summer in more than several apple orchards on Mutsu, Honeycrisp, NY-1 (SnapDragon), NY-2 (RubyFrost), Gala, Red Delicious, Golden Delicious, Pristine, Grimes Golden, Northern Spy, Stayman Winesap, Tompkins King, and others. The alarming outcome was defoliation of lower part of the tree crowns, especially where moisture due to heavy dew or sprinkler irrigation was present up until midday. When we examined the structures from round, brown to grey leaf spots of this disease (Fig. 1A, C), we found typical Marssonina sp. fungal spores originating from spore groups called acervuli (Fig. 1B). In 2017, leaves of Mutsu, Honeycrisp, Winesap, NY-1, NY-2 were microscopically examined. Defoliation of the lower part of the crown in 2017 was associated with orchards where fungicide cover sprays were not applied as frequently as the weather patterns required. In 2018, from mid-September up until Mid-October, new reports of apple tree defoliation started coming in. The most affected cultivars were Rome, Mutsu, Goldrush, Honeycrisp, Ginger Golds, Williams' Pride and others. Again, we detected the two-celled fungal spores typical for Marssonina sp. in leaf spots (Fig. 1B).

In 2017, we focused our efforts on pathogen isolation from the infected leaf samples and performed a dozen of isolation attempts and different methods. After preliminary molecular analyses of isolated fungi and two-gene sequencing that was done for recovered fungal isolates, the results came negative, indicating that we were not successful in isolating M. coronaria. However, when we tried the last test option, i.e. when we extracted total DNA from leaves  showing MLB (containing mix of both fungal and plant DNA) and conducted a molecular method called PCR with previously published primers (Oberhänsli et al. 2014), we got positive identification of M. coronaria. However, this was not a good result as plant pathologist always aims to isolate the fungus i.e. causal organism of a disease in a pure culture and replicate pathogenicity test by inoculating healthy leaves of apple to prove 100% the result obtained by PCR detection. It is known in literature that M. coronaria is difficult to isolate (Lee et al. 2011), especially from samples collected at the end of the growing season when many saprophytic fungi live on the leaf surface and inhabit dead blotches caused initially by M. coronaria. This makes it very challenging to isolate this pathogen and for identification efforts to be completed. We are continuing our efforts in 2018 to confirm this species in NY by isolation and reliable diagnostic methods.

In recent years and in the past, MLB outbreaks in USA were reported in New York, Pennsylvania, Wisconsin. Disease is also known in Canada, Brazil, Panama, India, China, Taiwan, Korea, Japan, and several European countries (Romania, Italy, Germany, Austria, Switzerland). In Europe the most susceptible cultivars are Topaz, Jonagold, Gala, Golden Delicious and Luna. In Asia, the most affected is Fuji. Usually, the cultivars that are resistant to apple scab are more susceptible to MLB (Lebleu, 2015). MLB is a problem in both conventional and organic apple orchards, especially when reduced spray programs are attempted in a year very frequent rains during summer. MLB leaf symptoms express as grey to brown large round spots (blotches) that can coalesce in time, or are sometimes in a form of more dispersed smaller spots on more resistant cultivars (Fig. 1C). First symptoms are usually visible at the end of August and beginning of September. When leaf infections become severe due to lack of fungicide cover sprays, they lead to leaf yellowing and lower crown defoliation (Fig. 2A). Apple leaf symptoms are more prevalent then symptoms on fruit, which we haven't found in NY (Fig. 2B and C). MLB leads to defoliation of apple trees during late summer if cover sprays with fungicides are not applied at shorter spray intervals, in alignment with frequent rains events. During 2018, the disease started expressing in NY around 5-15 September. Most affected were the blocks where summer cover sprays with fungicides were not tightened, i.e. applied at shorter intervals than in a normal year, to re-cover after frequent rains we got in July, August and September.

Even though, the primary host for M. coronaria is apple (Malus pumila), other species such as Malus baccata and Chaenomeles spp. are also known to host in this fungus and serve as inoculum sources. M. coronaria overwinters in fallen leaves on the orchard floor (EPPO 2013). Ascospores cause first infections in spring. They form in the overwintered cup-like fungal structures that form on the leaf litter from last year. It is not known whether apothecia can form in NY conditions. It has been reported that in Korea apothecia do not form and that the fungus overwinters as asexual spores (conidia) on fallen leaves (Back and Jung 2014). Nevertheless, ascospores are inoculum for primary infections while, conidia are asexual spores produced in acervuli. Acervuli are plate-like spore groups visible as small round specks after leaf epidermis is ruptured by pushing spore masses. Conidia can cause several secondary infections during the season. To express as blotch, leaf infections require extended period of moisture i.e. leaf wetness, high relative air humidity, and temperatures between 20 to 25°C (EPPO, 2013). It seems that in Europe and probably in NY as well, infections start sometime in May or around first or second week of June. Typical symptoms usually express 40 - 45 days after the infection (Lee et al. 2011). In the orchard, spores disseminate by rain and wind. Trade with nursery material that bears infected leaves allows introduction of MLB in new distant regions. Since apple fruit are rarely infected, introduction by infected fruit into new orchards or regions is probably of low risk (EPPO, 2013).

There are no labelled fungicides for control of Marssonina Leaf Blotch (MLB) on apple in New York (NY). Various researchers indicate that thiophanate-methyl (Topsin-M), DMI fungicides such as Inspire Super (contains difenoconazole, Frac group 3), QoI trifloxystrobin (Flint), and Merivon which combines an SDHI fungicide fluxapyroxad (FRAC group 7) and QoI pyraclostrobin (FRAC Group 11), are effective on Marssonina fungal species on apple and/or poplar. However, none of these fungicides have labelled use for M. coronaria on apples so far in the USA. EBDC fungicides such as mancozeb (Manzate) or metiram (Polyram) are effective but have no labelled use for MLB in apple in the USA and are of very limited utility due to limitation of 77 days pre-harvest interval (PHI). Recent study in China has showed that DMI-s such as tebuconazole, hexaconazole, propiconazole, alone or DMI tebuconazole + benziothiazolinone (from a group of isothiazolinones) were very effective when applied at 20-day intervals, from early July - late August (Dang et al. 2017). The same authors report that Bordeaux mix + tebuconazole, Bordeaux mix + propiconazole, or Bordeaux mix + tebuconazole + benziothiazolinone alternated at 25 days were very effective (Dang et al. 2017). Except Bordeaux mix, none of these fungicide have label for use on apples in USA. However, in general, Marssonina has low sensitivity to copper fungicides (Li Y., The Connecticut Agricultural Experiment Station, personal communication). Other fungicides used in other countries of the world for this fungus include carbendazim (benzimidazol, FRAC group 1), QoI kresoxim-methyl, and DMI-s flusilazol and prochloraz. However, none of these fungicides have current labels for use on apples except Sovran (kresoxim-methyl), which is not labelled for M. coronaria. The main problems with all the above mentioned single-site fungicides is loss of their efficacy due to development of resistance in M. coronaria populations and unacceptable accumulation of residues in fruit (Dang et al. 2017). In terms of organic apple production where this pathogen can have a devastating impact, it is essential to prune the tree crown to facilitate good air circulation and to eliminate leaf litter as the major infection source. Hence, the same recommendations to reduce overwintering apple scab inoculum by degrading leaf litter would help here. If you had a high incidence of MLB, you should reduce inoculum size by promoting biological processes of degradation of leaf litter in fall, spring, or both in fall and spring. The aim of this practice is to quicken the degradation of leaf litter by promoting the activity of microorganisms and worms on and in the soil. In conventional orchards, spray apple leaves on the tree with urea just 1-2 days before the major leaf drop in fall (first severe frost) or as leaf litter on the orchard floor. When leaves are on the branches you will have better coverage with urea. Make sure this practice is done late enough in fall and start of winter to avoid promoting any late growth with sprayed nitrogen. If spraying leaf litter on the ground, the best time is to apply urea in late winter but before bud break. Turn air deflectors of your air-blast sprayer downward and/or turn off top nozzles to allow spray mist to lift loose leaves and coat them with urea. Use rate of 40 lbs of urea / A in 100 gals of water. Once done, you must wash and rinse well your spray equipment since urea can wear up any rubber parts, washers, and gaskets in the sprayer, especially the pump diaphragm. In organic apple orchards urea is not allowed. When ground is without snow cover and it is not muddy, use flail mower to shred leaves to smaller peaces instead. This method can also be used in conventional apple orchards. If practical, rake leaves into row middles from under the trees and remove leaf piles with flail mower mode for scalping the sod (Cox, 2016). Instead of urea, lime can be applied in both organic and conventional orchards at a rate of 2.5 tons/A. If lime is used, it is better to apply it after the leaf drop in fall or early in the winter. Lime increases pH or basicity of soil, thus promoting microbial activity and litter breakdown. Reduction of MLB inoculum with above specified practices does not mean you do not need to spray against MLB next summer. Enough inoculum can always be present in the orchard to cause infection. However, inoculum reduction secures better efficacy of your fungicide sprays and reduces the overall chance for severe MLB infections. Recent research from Germany shows that in organic orchards 10-12 sprays per year of each of the following products: acid clay Myco-Sin, Myco-Sin + sulfur, Funguran (copper hydroxide), Curatio (lime sulfur), or sulfur alone, provide relatively good control if the first spray application is started around 10-12 June (Bohr et al. 2018). These treatments allowed only 4-15% of MLB incidence in 2017 and 5-25% in 2018 efficacy trials. To better time fungicide sprays for maximum efficacy in MLB control in both conventional and organic orchards, use of RIMpro's Marssonina prediction model that is based on 10-day weather forecast is highly recommended and especially helpful in orchards that had severe MLB outbreaks in the past (RIMpro B.V., Zoelmond, Netherlands). More information about this model can be found by here: https://www.rimpro.eu/faces/index.xhtml?faces-redirect=true by clicking on the button "Create a new RIMpro account."

Literature

Agnello et al. (2017): 2017 Cornell Pest Management Guidelines for Commercial Tree Fruit Production. Chapter 6, Disease Management, 6.2.2 Orchard Sanitation for High-inoculum Orchards. Pg. 60.

Back, C.-G., and Jung, H.-Y. 2014. Biological characterization of Marssonina coronaria infecting apple trees in Korea. Korean J. Mycol. 42:183-190.

Bohr et al. 2018: Symptom occurrence and disease management of Marssonina blotch. 18th International Conference on Organic Fruit-Growing: Proceedings of the Conference, 19-21 February 2018, Hohenheim, Germany.

Cox K. (2016): Having Fungi Yet? Fungicide Update for NY, Scaffolds Vol. 25, No. 1, March 21, 2016, Geneva, NY.

Dang, J. L., Gleason, M. L., Niu, C. K., Liu, X., Guo, Y. Z., Zhang, R., et al. 2016. Effects of Fungicides and Spray Application Interval on Controlling Marssonina Blotch of Apple in the Loess Plateau Region of China. Plant Dis. 101:568-575.

EPPO. (2013-103). Diplocarpon mali (anamorph: Marssonina coronaria) - Marssonina blotch of apple. European and Mediterranean Plant Protection Organization ,Paris, France:

Lebleu, F. 2015. Chute des feuilles causée par Marssonina - Une menace pour l'arboriculture fruitière biologique/ Falling leaves caused by Marssonina - A threat to organic fruit arboriculture. Arboriculture and special crops FiBL, Switzerland.

Lee et al. 2011: Biological Characterization of Marssonina coronaria Associated with Apple Blotch Disease. Mycobiology. 39: 200-205.

Oberhänsli, T., Vorley, T., Tamm, L., and Schärer, H. J. 2014. Development of a quantitative PCR for improved detection of Marssonina coronaria in field samples. In Proceeding of the 16th International Conference on Organic Fruit-Growing Conference, p. 17-19.

Rosenberger, D. (2005): Jump Starting Apple Scab Control Programs in High-Inoculum Orchards. Available also at: http://www.scaffolds.entomology.cornell.edu/2005/050321.html

Sutton, D. K., MacHardy, W. E. & Lord, W. G. (2000): Effects of Shredding or Treating Apple Leaf Litter with Urea on Ascospore Dose of Venturia inaequalis and Disease Buildup. Plant Disease, 84(12), pp.1319-1326.

This paper was supported by the Cornell Cooperative Extension ENYCHP Challenge Fund Grant Proposal titled "Confirm the Presence and Distribution of a New Apple Disease in Eastern New York".