Abstract
Strawberry seedlings from greenhouses in different districts of Beijing started showing symptoms of black root rot in 2014, and the diseased plants were collected between 2015 and 2017. Forty-six Dactylonectria isolates were obtained from the root samples, among which five representative isolates were further identified based on morphological characteristics and multi-locus sequence of four loci, internal transcribed spacer region of nuclear rDNA (ITS), β-tubulin (tub2), histone H3 (his3) and translation elongation factor 1-alpha (tef1). Amongst them, three isolates were identified as D. novozelandica, one was D. torresensis and one D. pauciseptata. Pathogenicity tests confirmed that all isolates were pathogenic to strawberry (cultivar Benihope) and produced black root rot symptoms. This study is the first report of Dactylonectria species causing black root rot of strawberries in China, as well as D. novozelandica and D. pauciseptata in the world.
Similar content being viewed by others
References
Adhikari TB, Hodges CS, Louws FJ (2013) First report of Cylindrocarpon sp. associated with root rot disease of strawberry in North Carolina. Plant Dis 97:1251
Aiello D, Guarnaccia V, Epifani F, Perrone G, Polizzi G (2015) ‘Cylindrocarpon’and Ilyonectria species causing root and crown rot disease of potted Laurustinus plants in Italy. J Phytopathol 163:675–680
Berkeley GH, Lauderthomson I (1934) Root rots of strawberry in Britain the “black lesion” type of strawberry root rot. Journal of Pomology and Horticultural Science 12:222–246
Botha A, Denman S, Lamprecht SC, Mazzola M, Crous PW (2003) Characterisation and pathogenicity of Rhizoctonia isolates associated with black root rot of strawberries in the Western Cape Province, South Africa. Australas Plant Pathol 32:195–201
Cabral A, Groenewald JZ, Rego C, Oliveira H, Crous PW (2012a) Cylindrocarpon root rot: multi-gene analysis reveals novel species within the Ilyonectria radicicola species complex. Mycol Prog 11:655–688
Cabral A, Rego C, Nascimento T, Oliveira H, Groenewald JZ, Crous PW (2012b) Multi-gene analysis and morphology reveal novel Ilyonectria species associated with black foot disease of grapevines. Fungal Biol-UK 116:62–80
Carlucci A, Lops F, Mostert L, Halleen F, Raimondo ML (2017) Occurrence fungi causing black foot on young grapevines and nursery rootstock plants in Italy. Phytopathol Mediterr 56:10–39
Chaverri P, Salgado C, Hirooka Y, Rossman AY, Samuels GJ (2011) Delimitation of Neonectria and Cylindrocarpon (Nectriaceae, Hypocreales, Ascomycota) and related genera with Cylindrocarpon-like anamorphs. Stud Mycol 68:57–78
Chen TA, Rich AE (1962) The role of Pratylenchus penetrans in the development of strawberry black root rot. Plant Dis Rptr 46:839–843
Crous PW, Groenewald JZ, Risede JM, Hywel-Jones NL (2004) Calonectria species and their Cylindrocladium anamorphs: species with sphaeropedunculate vesicles. Stud Mycol 50:415–429
Cubero OF, Crespo A, Fatehi J, Bridge PD (1999) DNA extraction and PCR amplification method suitable for fresh, herbarium stored, lichenized, and other fungi. Plant Syst Evol 216:243–249
De Hoog GS, Gerrits van den Ende AHG (1998) Molecular diagnostics of clinical strains of filamentous Basidiomycetes. Mycoses 41:183–189
Dinler H, Benlioglu S, Benlioglu K (2018) Rhizoctonia fragariae causes black root rot on strawberry seedlings in Turkey. Australasian Plant Dis Notes 13:23
Fang XL, Phillips D, Li H, Sivasithamparam K, Barbetti MJ (2011) Severity of crown and root diseases of strawberry and associated fungal and oomycete pathogens in Western Australia. Australas Plant Pathol 40:109–119
Glass NL, Donaldson G (1995) Development of primer sets designed for use with PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol 61:1323–1330
Golzar H, Phillips D, Mack S (2007) Occurrence of strawberry root and crown rot in Western Australia. Australas Plant Dis Notes 2:145–147
Gordillo A, Decock C (2017) Cylindrocarpon-like (Ascomycota, Hypocreales) species from the Amazonian rain forests in Ecuador: additions to Campylocarpon and Dactylonectria. Cryptogamie Mycol 38:409–434
Halleen F, Schroers H-J, Groenewald JZ, Crous PW (2004) Novel species of Cylindrocarpon (Neonectria) and Campylocarpon gen. nov. associated with black foot disease of grapevines (Vitis spp.). Stud Mycol 50:431–455
Hu YJ, Zhang RQ (2012) Identification and pathogenicity test of strawberry root rot pathogens in Yantai. Northern Horticulture 10:141–144
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780
Koike ST (2008) Crown rot of strawberry caused by Macrophomina phaseolina in California. Plant Dis 92:1253–1253
LaMondia JA (2004) Strawberry black root rot. Advances in Strawberry Research 23:1–10
Lawrence DP, Nouri MT, Trouillas FP (2019) Taxonomy and multi-locus phylogeny of cylindrocarpon-like species associated with diseased roots of grapevine and other fruit and nut crops in California. FUSE (fungal Systematics and Evolution) 4:59–75
Li WJ, Zhang XY, Pei WH, Zheng GW (2020) First report of root rot caused by Dactylonectria torresensis on Bletilla striata (Baiji) in Yunnan, China. Plant Dis. https://doi.org/10.1094/PDIS-10-20-2166-PDN
Lombard L, van der Merwe NA, Groenewald JZ, Crous PW (2014) Lineages in Nectriaceae: re-evaluating the generic status of Ilyonectria and allied genera. Phytopathol Mediterr 53:515–532
Lu JZ, Ehsani R, Shi YY, Abdulridha J, de Castro AI, Xu YJ (2017) Field detection of anthracnose crown rot in strawberry using spectroscopy technology. Comput Electron Agric 135:289–299
Maas JL (1998) Compendium of strawberry diseases. 2nd ed. The Amer Phytopathol Soc, St. Paul, Minn
Manici LM, Caputo F, Baruzzi G (2005) Additional experiences to elucidate the microbial component of soil suppressiveness towards strawberry black root rot complex. Ann Appl Biol 146:421–431
Manici LM, Kelderer M, Caputo F, Saccà ML, Nicoletti F, Topp AR, Mazzola M (2018) Involvement of Dactylonectria and Ilyonectria spp. in tree decline affecting multi-generation apple orchards. Plant Soil 425:217–230
Martin FN, Bull CT (2002) Biological approaches for control of root pathogens of strawberry. Phytopathology 92:1356–1362
Mason-Gamer RJ, Kellogg EA (1996) Testing for phylogenetic conflict among molecular data sets in the tribe Triticeae (Gramineae). Syst Biol 45:524–545
Mazzola M (1998) Elucidation of the microbial complex having a causal role in the development of apple replant disease in Washington. Phytopathology 88:930–938
McKinney HH (1923) Helminthosporium disease of wheat. J Agric Res 26:195–218
Ministry of Agriculture of the People’s Republic of China (2018) The sown area and yield of vegetables, watermelons, muskmelons, strawberries and potatoes all over the country in 2016. China Vegetables 2018:18
Morocko I, Fatehi J, Gerhardson B (2006) Gnomonia fragariae, a cause of strawberry root rot and petiole blight. Eur J Plant Pathol 114:235–244
Nirenberg HI (1981) A simplified method to identify Fusarium spp. occurring on wheat. Can J Bot 59:1599–1609
O’Donnell K, Cigelnik E (1997) Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Mol Phylogenet Evol 7:103–116
O’Donnell K, Kistler HC, Cigelnik E, Ploetz RC (1998) Multiple evolutionary origins of the fungus causing Panama disease of banana: concordant evidence from nuclear and mitochondrial gene genealogies. Proc Natl Acad Sci USA 95:2044–2049
Parkinson LE, Shivas RG, Dann EK (2017) Pathogenicity of Nectriaceous fungi on avocado in Australia. Phytopathology 107:1479–1485
Piperkova N, Cabral A, Mohamedova M, Milusheva S, Oliveira H (2017) First report of Dactylonectria pauciseptata associated with black foot of grapevine and root rot of plum in Bulgaria. Plant Dis 101:2146
Rossman AY, Samuels GJ, Rogerson CT, Lowen R (1999) Genera of Bionectriaceae, Hypocreaceae and Nectriaceae (Hypocreales, Ascomycetes). Stud Mycol 42:1–260
Shen T, Wang C, Yang H, Deng Z, Wang S, Shen B, Shen Q (2016) Identification, solid-state fermentation and biocontrol effects of Streptomyces hygroscopicus B04 on strawberry root rot. Appl Soil Ecol 103:36–43
Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16:1114–1116
Swofford DL (2003) PAUP*: phylogenetic analysis using parsimony. Version 4.0 b10. Sunderland, Massachusetts: Sinauer
Tamura K, Stecher G, Peterson D, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
Tewoldemedhin YT, Mazzola M, Mostert L, McLeod A (2011) Cylindrocarpon species associated with apple tree roots in South Africa and their quantification using real-time PCR. Eur J Plant Pathol 129:637–651
Van Hemelrijck W, Ceustermans A, Van Campenhout J, Lieten P, Bylemans D (2016) Crown rot in strawberry caused by Pestalotiopsis. VIII International Strawberry Symposium 1156:781–786
Weber RW, Entrop AP (2017) Dactylonectria torresensis as the main component of the black root rot complex of strawberries and raspberries in northern Germany. Erwerbs-Obstbau 59:157–169
White TJ, Bruns T, Lee SJWT, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols: A guide to methods and applications. Academic Press, San Diego, pp 315–322
Yaseen T, Ahmed Y, D’Onghia AM, Digiaro M (2012) First report of Cylindrocarpon pauciseptatum associated with root rot and decline of peach in southern Italy (Apulia region). Plant Dis 96:764
Yuen GY, Schroth MN, Weinhold AR, Hancock JG (1991) Effects of soil fumigation with methyl bromide and chloropicrin on root health and yield of strawberry. Plant Dis 75:416–420
Zhang XM, Lu XH, Tian GL, Jiao XL, Gao WW (2019) First report of Dactylonectria novozelandica associated with rusty root of Panax quinquefolius in China. Plant Dis PDIS-01. https://doi.org/10.1094/PDIS-01-19-0009-PDN
Zhang Y, Liu ZP, Wei YM, Shang QX, Li YQ, Zhao XY (2015) Identification of the strawberry root rot pathogen in Changping District Beijing. Chin Agric Sci Bull 31:278–284
Zhao Y, Qian HW, Xu PC, Huang JG, Jiang ZJ (2016) Isolation and identification of pathogen of strawberry root rot in Qingdao. China Plant Protection 36(43–46):82
Zhu XQ, Song ZL, Pei DL (2017) Isolation and identification of strawberry root rot pathogen in Shangqiu, Henan Province. J Plant Prot 44:349–350
Zong J, Wang Q, Ma X, Qi CH, Yu JS, Chen QJ, Wang JY (2018) The development status and problems of strawberry industry in Beijing. China Vegetables 2018:14–18
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Chen, Q., Yin, S.L., Zhang, X.G. et al. Dactylonectria species associated with black root rot of strawberry in China. Australasian Plant Pathol. 50, 501–511 (2021). https://doi.org/10.1007/s13313-021-00804-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13313-021-00804-1