Biocontrol of Diplodia bulgarica, the causal agent of apple canker, using Trichoderma zelobreve.
Biological control
Culture filtrate
Endophytic fungus
In vivo assay
Wettable powder formulation
Journal
Archives of microbiology
ISSN: 1432-072X
Titre abrégé: Arch Microbiol
Pays: Germany
ID NLM: 0410427
Informations de publication
Date de publication:
24 Feb 2024
24 Feb 2024
Historique:
received:
30
11
2023
accepted:
17
01
2024
revised:
16
01
2024
medline:
24
2
2024
pubmed:
24
2
2024
entrez:
24
2
2024
Statut:
epublish
Résumé
Apple (Malus domestica Borkh) is one of the most consumed and nutritious fruits. Iran is one of the main producers of the apple in the world. Diplodia bulgarica is the major causal agent of apple tree decline in Iran. Biological control is a nature-friendly approach to plant disease management. Trichoderma zelobreve was isolated from apple trees infected with Diplodia bulgarica in West Azarbaijan province of Iran. The results showed that T. zelobreve strongly inhibited the colony growth of D. bulgarica. In vivo assay on detached branches of apple tree cv. Golden Delicious using T. zelobreve mycelial plug showed that canker length/stem length (CL/SL) and canker perimeter/stem perimeter (CP/SP) indices decreased by 76 and 69%, respectively, 21 days after inoculation. Additionally, wettable powder formulation (WPF) containing the antagonistic fungus "T. zelobreve" decreased CL and CP/SP by 75 and 67%, respectively, 6 months after inoculation. Moreover, canker progress curves and the area under the disease progress curve (AUDPC) supported these findings. The growth temperatures of the antagonist and pathogen were similar, indicating the adaptation of T. zelobreve for biocontrol of apple canker caused by D. bulgarica. The results also showed that T. zelobreve-based WPF stored at 25 °C assure excellent shelf life at least 4 months, allowing the bioproduct to be stored at room temperature, which is a great advantage and cost-effective option.
Identifiants
pubmed: 38396230
doi: 10.1007/s00203-024-03852-5
pii: 10.1007/s00203-024-03852-5
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
120Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Adams G, Roux J, Wingfield M (2006) Cytospora species (Ascomycota, Diaporthales, Valsaceae): introduced and native pathogens of trees in South Africa. Australas Plant Pathol 35:521–548. https://doi.org/10.1071/AP06058
doi: 10.1071/AP06058
Arzanlou M, Bakhshi M (2012) ITS-rDNA sequence differentiates a new lineage of Diplodia associated with canker disease of apple in Iran. Plant Pathol Quar J Fungal Biol 2:132–141. https://doi.org/10.5943/ppq/2/2/6
doi: 10.5943/ppq/2/2/6
Ashkan M (1994) Introducing Leucostoma cincta, the causal agent of canker disease apple trees in Tehran. Iran J Plant Pathol 30:40–43
Azizbekyan RR (2019) Biological preparations for the protection of agricultural plants. Appl Biochem Microbiol 55(8):816–823. https://doi.org/10.1134/S0003683819080027
doi: 10.1134/S0003683819080027
Berninger T, González López Ó, Bejarano A, Preininger C, Sessitsch A (2018) Maintenance and assessment of cell viability in formulation of non-sporulating bacterial inoculants. Microb Biotechnol 11(2):277–301. https://doi.org/10.1111/1751-7915.12880
doi: 10.1111/1751-7915.12880
pubmed: 29205959
Boyetchko S, Pedersen E, Punja Z, Reddy MS (1999) Formulations of biopesticides. In: Hall FR, Menn JJ (eds) Biopesticides: use and delivery. Humana Press, Totowa, pp 487–508
Broeckx G, Vandenheuvel D, Claes IJJ, Lebeer S, Kiekens F (2016) Drying techniques of probiotic bacteria as an important step towards the development of novel pharmabiotics. Int J Pharm 505:303–318. https://doi.org/10.1016/j.ijpharm.2016.04.002
doi: 10.1016/j.ijpharm.2016.04.002
pubmed: 27050865
Brown EA, Britton K (1986) Botryosphaeria diseases of apple and peach in the southeastern United States. Plant Dis 70:480–484. https://doi.org/10.1094/PD-70-480
doi: 10.1094/PD-70-480
Campbell CL, Madden LV (1990) Introduction to plant disease epidemiology. Wiley, New York
Carbone I, Kohn LM (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91(3):553–556. https://doi.org/10.1080/00275514.1999.12061051
doi: 10.1080/00275514.1999.12061051
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552. https://doi.org/10.1093/oxfordjournals.molbev.a026334
doi: 10.1093/oxfordjournals.molbev.a026334
pubmed: 10742046
Chaverri P, Branco-Rocha F, Jaklitsch W, Gazis R, Degenkolb T, Samuels GJ (2015) Systematics of the Trichoderma harzianum species complex and the re-identification of commercial biocontrol strains. Mycologia 107(3):558–590. https://doi.org/10.3852/14-147
doi: 10.3852/14-147
pubmed: 25661720
pmcid: 4885665
Chen K, Zhuang WY (2017) Three new soil-inhabiting species of Trichoderma in the Stromaticum clade with test of their antagonism to pathogens. Curr Microbiol 74:1049–1060. https://doi.org/10.1007/s00284-017-1282-2
doi: 10.1007/s00284-017-1282-2
pubmed: 28631173
de Lima FB, Félix C, Osório N, Alves A, Vitorino R, Domingues P, da Silva Ribeiro RT, Esteves AC (2017) Trichoderma harzianum T1A constitutively secretes proteins involved in the biological control of Guignardia citricarpa. Biol Control 106:99–109. https://doi.org/10.1016/j.biocontrol.2017.01.003
doi: 10.1016/j.biocontrol.2017.01.003
Dennis C, Webster J (1971a) Antagonistic properties of species-groups of Trichoderma: III. Hyphal interaction. Trans Br Mycol Soc 57:363–369. https://doi.org/10.1016/S0007-1536(71)80050-5
doi: 10.1016/S0007-1536(71)80050-5
Dennis C, Webster J (1971b) Antagonistic properties of species-groups of Trichoderma: II. Production of volatile antibiotics. Trans Br Mycol Soc 57(1):41–48. https://doi.org/10.1016/S0007-1536(71)80078-5
doi: 10.1016/S0007-1536(71)80078-5
Elad Y, Chet I, Henis Y (1982) Degradation of plant pathogenic fungi by Trichoderma harzianum. Can J Microbiol 28:719–725. https://doi.org/10.1139/m82-110
doi: 10.1139/m82-110
Elad Y, Chet I, Boyle P, Henis Y (1983) Parasitism of Trichoderma spp. on Rhizoctonia solani and Sclerotium rolfsii: scanning electron microscopy and fluorescence microscopy. Phytopathology 73:85–88. https://doi.org/10.1094/Phyto-73-85
doi: 10.1094/Phyto-73-85
FAOSTAT (2019) Food and Agriculture Organization of the United Nations. http://www.fao.org/faostat/en/#data/QC/visualize
Farhadi S, Moieni A, Safaie N, Sabet MS, Salehi M (2020) Fungal cell wall and methyl-β-cyclodextrin synergistically enhance paclitaxel biosynthesis and secretion in Corylus avellana cell suspension culture. Sci Rep 10:5427. https://doi.org/10.1038/s41598-020-62196-4
doi: 10.1038/s41598-020-62196-4
pubmed: 32214149
pmcid: 7096423
Gams W, Bissett J (2002) Morphology and identification of Trichoderma. In: Kubicek CP, Harman GE (eds) Trichoderma and Gliocladium: basic biology, taxonomy and genetics. Taylor & Francis Ltd, London, pp 3–31
Gerhauser C (2008) Cancer chemopreventive potential of apples, apple juice, and apple components. Planta Med 74:1608–1624. https://doi.org/10.1055/s-0028-1088300
doi: 10.1055/s-0028-1088300
pubmed: 18855307
Gu X, Wang R, Sun Q, Wu B, Sun JZ (2020) Four new species of Trichoderma in the Harzianum clade from northern China. MycoKeys 73:109. https://doi.org/10.3897/mycokeys.73.51424
doi: 10.3897/mycokeys.73.51424
pubmed: 33117081
pmcid: 7561617
Hanifeh S, Zafari D, Soleimani MJ (2017) Reaction of some apple cultivars to Diplodia bulgarica in Iran. Mycosphere 8(2):1253–1260. https://doi.org/10.5943/mycosphere/8/2/9
doi: 10.5943/mycosphere/8/2/9
Harman GE (2006) Overview of mechanisms and uses of Trichoderma spp. Phytopathology 96(2):190–194. https://doi.org/10.1094/PHYTO-96-0190
doi: 10.1094/PHYTO-96-0190
pubmed: 18943924
Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species—opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2(1):43–56. https://doi.org/10.1038/nrmicro797
doi: 10.1038/nrmicro797
pubmed: 15035008
Huson DH, Scornavacca C (2012) Dendroscope 3: an interactive tool for rooted phylogenetic trees and networks. Syst Biol 61:1061–1067. https://doi.org/10.1093/sysbio/sys062
doi: 10.1093/sysbio/sys062
pubmed: 22780991
Jaklitsch WM, Voglmayr H (2015) Biodiversity of Trichoderma (Hypocreaceae) in southern Europe and Macaronesia. Stud Mycol 80:1–87. https://doi.org/10.1016/j.simyco.2014.11.001
doi: 10.1016/j.simyco.2014.11.001
pubmed: 26955191
pmcid: 4779795
Jaklitsch WM, Komon M, Kubicek CP, Druzhinina IS (2005) Hypocrea voglmayrii sp. nov. from the Austrian Alps represents a new phylogenetic clade in Hypocrea/Trichoderma. Mycologia 97:1365–1378. https://doi.org/10.1080/15572536.2006.11832743
doi: 10.1080/15572536.2006.11832743
pubmed: 16722227
Jeyarajan R, Ramakrishnan G, Dinakaran D, Sridar R (1994) Development of products of Trichoderma viride and Bacillus subtilis for biocontrol of root rot diseases. In: Biotechnology in India, pp 25–36
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010
doi: 10.1093/molbev/mst010
pubmed: 23329690
pmcid: 3603318
Kexiang G, Xiaoguang L, Yonghong L, Tianbo Z, Shuliang W (2002) Potential of Trichoderma harzianum and T. atroviride to control Botryosphaeria berengeriana f. sp. piricola, the cause of apple ring rot. J Phytopathol 150:271–276. https://doi.org/10.1046/j.1439-0434.2002.00754.x
doi: 10.1046/j.1439-0434.2002.00754.x
Knowles A (2008) Recent developments of safer formulations of agrochemicals. Environmentalist 28:35–44. https://doi.org/10.1007/s10669-007-9045-4
doi: 10.1007/s10669-007-9045-4
Köhl J, Kolnaar R, Ravensberg WJ (2019) Mode of action of microbial biological control agents against plant diseases: relevance beyond efficacy. Front Plant Sci 10:845. https://doi.org/10.3389/fpls.2019.00845
doi: 10.3389/fpls.2019.00845
pubmed: 31379891
pmcid: 6658832
Larget B, Simon DL (1999) Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Mol Biol Evol 16:750–759. https://doi.org/10.1093/oxfordjournals.molbev.a026160
doi: 10.1093/oxfordjournals.molbev.a026160
Leggett M, Leland J, Kellar KL, Epp B (2011) Formulation of microbial biocontrol agents—an industrial perspective. Can J Plant Pathol 33:101–107. https://doi.org/10.1080/07060661.2011.563050
doi: 10.1080/07060661.2011.563050
Li Z, Gao X, Kang Z, Huang L, Fan D, Yan X, Kang Z (2016) Saccharothrix yanglingensis strain Hhs. 015 is a promising biocontrol agent on apple valsa canker. Plant Dis 100(2):510–514. https://doi.org/10.1094/PDIS-02-15-0190-RE
doi: 10.1094/PDIS-02-15-0190-RE
pubmed: 30694140
Liu YJJ, Whelen S, Benjamin DH (1999) Phylogenetic relationships among ascomycetes: evidence from an RNA polymerase II subunit. Mol Biol Evol 16:1799–1808. https://doi.org/10.1093/oxfordjournals.molbev.a026092
doi: 10.1093/oxfordjournals.molbev.a026092
pubmed: 10605121
Maciag T, Krzyzanowska DM, Jafra S, Siwinska J, Czajkowski R (2020) The Great Five—an artificial bacterial consortium with antagonistic activity towards Pectobacterium spp. and Dickeya spp.: formulation, shelf life, and the ability to prevent soft rot of potato in storage. Appl Microbiol Biotechnol 104(10):4547–4561. https://doi.org/10.1007/s00253-020-10550-x
doi: 10.1007/s00253-020-10550-x
pubmed: 32215712
pmcid: 7190590
Maruyama CR, Bilesky-José N, de Lima R, Fraceto LF (2020) Encapsulation of Trichoderma harzianum preserves enzymatic activity and enhances the potential for biological control. Front Bioeng Biotechnol 8:225. https://doi.org/10.3389/fbioe.2020.00225
doi: 10.3389/fbioe.2020.00225
pubmed: 32269991
pmcid: 7110528
Mehrabi M, Mohammadi Goltapeh E, Fotouhifar K (2011) Studies on Cytospora canker disease of apple trees in Semirom region of Iran. J Agric Techol 7:967–982
Mondal P, Singh A, Sarkar DJ, Dubey SC, Kumar A (2020) Trichoderma harzianum formulations based on a biopolymeric hydrogel, ZnSO
doi: 10.5958/2249-524X.2020.00001.1
Mukherjee PK, Mendoza-Mendoza A, Zeilinger S, Horwitz BA (2022) Mycoparasitism as a mechanism of Trichoderma-mediated suppression of plant diseases. Fungal Biol Rev 39:15–33. https://doi.org/10.1016/j.fbr.2021.11.004
doi: 10.1016/j.fbr.2021.11.004
Nabi SU, Sheikh MA, Raja WH, Mir JI, Sharma OC, Singh DB, Yousuf N, Shafi M, Khan KA, Yadav MK, Kamil D (2020) Morphological and molecular characterization of Diplodia spp. associated with apple canker disease in India. Crop Prot 137:105238. https://doi.org/10.1016/j.cropro.2020.105238
doi: 10.1016/j.cropro.2020.105238
Nourian A, Salehi M, Safaie N, Khelghatibana F, Abdollahzadeh J (2021) Fungal canker agents in apple production hubs of Iran. Sci Rep 11:22646. https://doi.org/10.1038/s41598-021-02245-8
doi: 10.1038/s41598-021-02245-8
pubmed: 34811444
pmcid: 8608896
Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden
Patocka J, Bhardwaj K, Klimova B, Nepovimova E, Wu Q, Landi M, Kuca K, Valis M, Wu W (2020) Malus domestica: a review on nutritional features, chemical composition. Tradit Med Value Plants 9(11):1408. https://doi.org/10.3390/plants9111408
doi: 10.3390/plants9111408
Phillips AJL, Lopes J, Abdollahzadeh J, Bobev S, Alves A (2012) Resolving the Diplodia complex on apple and other Rosaceae hosts. Persoonia 29:29–38. https://doi.org/10.3767/003158512X658899
doi: 10.3767/003158512X658899
pubmed: 23606763
pmcid: 3589793
Poveda J (2021) Trichoderma as biocontrol agent against pests: new uses for a mycoparasite. Biol Control 159:104634. https://doi.org/10.1016/j.biocontrol.2021.104634
doi: 10.1016/j.biocontrol.2021.104634
Proffer T, Jones A (1989) A new canker disease of apple caused by Leucostoma cincta and other fungi associated with cankers on apple in Michigan. Plant Dis 73:508–514
doi: 10.1094/PD-73-0508
Qiao M, Du X, Zhang Z, Xu JP, Yu ZF (2018) Three new species of soil-inhabiting Trichoderma from southwest China. Mycokeys 44:63–80. https://doi.org/10.3897/mycokeys.44.30295
doi: 10.3897/mycokeys.44.30295
Qin WT, Zhuang WY (2016) Seven wood-inhabiting new species of the genus Trichoderma (Fungi, Ascomycota) in Viride clade. Sci Rep 6:27074. https://doi.org/10.1038/srep27074
doi: 10.1038/srep27074
pubmed: 27245694
pmcid: 4888246
Qin G, Tian S, Xu Y (2004) Biocontrol of postharvest diseases on sweet cherries by four antagonistic yeasts in different storage conditions. Postharvest Biol Technol 31(1):51–58. https://doi.org/10.1016/S0925-5214(03)00130-3
doi: 10.1016/S0925-5214(03)00130-3
Ram V, Sharma IM (2010) Isolation, identification and evaluation of potential biocontrol agents against major cankers in apple. J Biol Control 24:343–348. https://doi.org/10.18311/jbc/2010/3583
doi: 10.18311/jbc/2010/3583
Rhodes DJ (1993) Formulation of biological control agents. In: Jones DG (ed) Exploitation of microorganisms. Springer, Dordrecht, pp 411–439. https://doi.org/10.1007/978-94-011-1532-2_16
doi: 10.1007/978-94-011-1532-2_16
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. https://doi.org/10.1093/bioinformatics/btg180
doi: 10.1093/bioinformatics/btg180
pubmed: 12912839
Salehi M, Moieni A, Safaie N (2018) Elicitors derived from hazel (Corylus avellana L.) cell suspension culture enhance growth and paclitaxel production of Epicoccum nigrum. Sci Rep 8:12053. https://doi.org/10.1038/s41598-018-29762-3
doi: 10.1038/s41598-018-29762-3
pubmed: 30104672
pmcid: 6089963
Salehi M, Moieni A, Safaie N, Farhadi S (2019) Elicitors derived from endophytic fungi Chaetomium globosum and Paraconiothyrium brasiliense enhance paclitaxel production in Corylus avellana cell suspension culture. Plant Cell Tissue Organ Cult 136(1):161–171. https://doi.org/10.1007/s11240-018-1503-9
doi: 10.1007/s11240-018-1503-9
Stephens JHG, Rask HM (2000) Inoculant production and formulation. Field Crops Res 65(2–3):249–258. https://doi.org/10.1016/S0378-4290(99)00090-8
doi: 10.1016/S0378-4290(99)00090-8
Sun JZ, Liu XZ, Jeewon R, Li YL, Lin CG, Tian Q, Zhao Q, XiaoXP HKD, Nilthong S (2019a) Fifteen fungicolous ascomycetes on edible and medicinal mushrooms in China and Thailand. AJOM 2(1):129–169. https://doi.org/10.5943/ajom/2/1/7
doi: 10.5943/ajom/2/1/7
Sun JZ, Liu XZ, McKenzie EH, Jeewon R, Liu JK, Zhang XL, Zhao Q, Hyde KD (2019b) Fungicolous fungi: terminology, diversity, distribution, evolution, and species checklist. Fungal Divers 95(1):337–430. https://doi.org/10.1007/s13225-019-00422-9
doi: 10.1007/s13225-019-00422-9
Tariq M, Khan A, Asif M, Khan F, Ansari T, Shariq M, Siddiqui MA (2020) Biological control: a sustainable and practical approach for plant disease management. Acta Agric Scand B Soil Plant Sci 70(6):507–524. https://doi.org/10.1080/09064710.2020.1784262
doi: 10.1080/09064710.2020.1784262
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protoc Guide Methods Appl 18(1):315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
doi: 10.1016/B978-0-12-372180-8.50042-1
Xin YF, Shang JJ (2005) Bio-control trials of Chaetomium spirale ND35 against apple canker. J for Res 16:121–124. https://doi.org/10.1007/BF02857904
doi: 10.1007/BF02857904
Zheng XR, Zhang MJ, Shang XL, Fang SZ, Chen FM (2020) Stem canker on Cyclocarya paliurus is caused by Botryosphaeria dothidea. Plant Dis 104(4):1032–1040. https://doi.org/10.1094/PDIS-11-18-1990-RE
doi: 10.1094/PDIS-11-18-1990-RE
pubmed: 31999219