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Characterizing members of the Cladosporium cladosporioides species complex as fruit rot pathogens of red raspberries in the mid-Atlantic and co-occurrence with Drosophila suzukii (spotted wing drosophila)

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Abstract

Fruit rot, primarily caused by Botrytis cinerea, is a major driver of pre- and post-harvest yield losses in fall red raspberries in the Mid-Atlantic. Recent observations indicate that Cladosporium fruit rot may also reduce yields. In a two-year survey of two Maryland farms, 1–30% of fall-bearing red raspberry fruit exhibited Cladosporium fruit rot (CFR) symptoms pre-harvest and symptoms developed post-harvest in 16% of fruit harvested when under-ripe and 51% of fruit harvested red ripe. Cladosporium cladosporioides and C. pseudocladosporioides were identified based on BLAST analysis of TEF-1α and actin gene regions, but determinations against voucher specimen sequences were not always congruent with phylogenetic analyses; sequences from many isolates matched C. anthropophilum voucher sequences still labeled as C. cladosporioides. Isolates of all three species caused fruit rot on non-wounded drupes (33–66%) and incidence increased when drupes were wounded (50–100%) (P < 0.05). In the field, 21–33% of CFR-affected fruit were infested with D. suzukii larvae; Cladosporium propagules were recovered from frass of 25–71% of larvae and determined to be C. cladosporioides or C. pseudocladosporioides, conspecific with fruit-derived isolates. Further, frass-derived isolates of both species initiated rot, with similar incidence to raspberry-derived isolates (P > 0.05). This first description of Cladosporium fruit rot of red raspberry in the Mid-Atlantic provides an expansive perspective on CFR pre- and post-harvest biology as well as pathogen diversity. Several lines of evidence point to linkages between CFR and D. suzukii epidemiology which require further exploration.

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Acknowledgements

We would like to acknowledge Bryan Butler and collaborating growers for their support in conducting field surveys; Maggie Lewis for providing assistance in D. suzukii identification and isolation of larval gut fungi; Lisa Castlebury for assistance with phylogenetic analyses; the North American Blackberry and Raspberry Growers Association for providing funding for the project; and the University of Maryland, College Park, for providing start up support for this project.

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Correspondence to Cassandra L. Swett.

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12600_2019_734_MOESM1_ESM.jpg

S1 Fig. Most likely tree inferred from an analysis of elongation factor with a 80-taxon alignment of a section of the Cladosporium cladosporioides species complex. Tree generated with 200 heuristic best tree searches using Garli 2.01 using a model and partitioning scheme generated by PartitionFinder2 (S2 Table). Bipartitions receiving ≥70% bootstrap support in Garli and ≥ 0.95 posterior probability in MrBayes 3.2.6 are indicated. Sequence accessions and culture collections are listed in S1 Table. (JPG 1165 kb)

12600_2019_734_MOESM2_ESM.jpg

S2 Fig. Most likely tree inferred from an analysis of actin with a 80-taxon alignment of a section of the Cladosporium cladosporioides species complex. Tree generated with 200 heuristic best tree searches using Garli 2.01 using a model and partitioning scheme generated by PartitionFinder2 (S2 Table). Bipartitions receiving ≥70% bootstrap support in Garli and ≥ 0.95 posterior probability in MrBayes 3.2.6 are indicated. Sequence accessions and culture collections are listed in S1 Table. (JPG 967 kb)

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Swett, C.L., Hamby, K.A., Hellman, E.M. et al. Characterizing members of the Cladosporium cladosporioides species complex as fruit rot pathogens of red raspberries in the mid-Atlantic and co-occurrence with Drosophila suzukii (spotted wing drosophila). Phytoparasitica 47, 415–428 (2019). https://doi.org/10.1007/s12600-019-00734-1

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