Abstract
In this study, the diversity of leaf-associated microorganisms of the native Andean ericaceous plants Gaultheria pumila and Empetrum rubrum was screened to identify and characterize microorganisms with plant growth promotion and biocontrol capability against the phytopathogenic fungus Botrytis cinerea affecting Vaccinium corymbosum cultivars. Microbial strains with biocontrol potential against Botrytis cinerea were selected, and in vivo tests were performed to evaluate the biocontrol activity of the selected strains. The fungi Epicoccum nigrum (strains HFE11 and HFG20), Epicoccum layuense (strain HFG13), and Aspergillus sp. (strain HFG1), the yeasts Aureobasidium pullulans (strains BFG22 and BFG24) Sporobolomyces roseus (strains BFE10 and BFE11), and the bacteria Bacillus mycoides (strains BFE4 and BFE14), Bacillus sp. (strain BFG8), Pseudomonas fluorescens (strain BFE6), and Pseudomonas sp. (strain BFG21) were isolated. In vitro biocontrol activity of the selected strains (BFE14, BFE6, and HFG13) showed inhibition percentages ranging from 60 to 80%. Most of the isolates were able to produce Exopolysaccharides, Siderophore, Indole-3-acetic acid, P-solubilization and Ammonia to different levels. The in vivo experiments showed that the inoculation of the isolates BFG22, BFE6, and HFG13 on V. corymbosum leaves before infection avoids severe damage to the infected tissues. Additionally, BFG22 decreases the lipid peroxidation levels (malondialdehyde 36% lower) when the leaves were infected with B. cinerea. Our results provide evidence of beneficial traits of microorganisms inhabiting the phyllosphere of native Ericaceae which can be used as microbial inoculants in agricultural production. These beneficial effects enhance plant growth and avoid damage by B. cinerea in V. corymbosum cultivars.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abadi V, Sepehri M, Rahmani H, Dolatabad H, Shamshiripour M, Khatabi B (2021) Diversity and abundance of culturable nitrogen-fixing bacteria in the phyllosphere of maize. J Appl Microbiol 131:898–912. https://doi.org/10.1111/jam.14975
Andrews J, Buck J (2002) Adhesion of yeasts to leaf surfaces, pp 53–68
Arnon D (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1. https://doi.org/10.1104/pp.24.1.1
Arun KD, Sabarinathan KG, Gomathy M, Kannan R, Balachandar D (2020) Mitigation of drought stress in rice crop with plant growth-promoting abiotic stress-tolerant rice phyllosphere bacteria. J Basic Microbiol 60:768–786. https://doi.org/10.1002/jobm.202000011
Azeem S et al (2022) Characterization and survival of broad-spectrum biocontrol agents against phytopathogenic fungi. Rev Argent Microbiol 54(3):233–242. https://doi.org/10.1016/j.ram.2021.10.005
Aziz U et al (2021) Toward a molecular understanding of rhizosphere, phyllosphere, and spermosphere interactions in plant growth and stress response. Crit Rev Plant Sci 40:479–500. https://doi.org/10.1080/07352689.2022.2031728
Bhattacharyya C et al (2020) Evaluation of plant growth promotion properties and induction of antioxidative defense mechanism by tea rhizobacteria of Darjeeling, India. Sci Rep 10:1–19. https://doi.org/10.1038/s41598-020-72439-z
Boukaew S, Prasertsan P, Troulet C, Bardin MJB (2017) Biological control of tomato gray mold caused by Botrytis cinerea by using Streptomyces spp. BioControl 62:793–803. https://doi.org/10.1007/s10526-017-9825-9
Branda SS, Vik Å, Friedman L, Kolter R (2005) Biofilms: the matrix revisited. Trends Microbiol 13:20–26. https://doi.org/10.1016/j.tim.2004.11.006
Bric JM, Bostock RM, Silverstone SE (1991) Rapid in situ assay for indoleacetic acid production by bacteria immobilized on a nitrocellulose membrane. Appl Environ Microbiol 57:535–538. https://doi.org/10.1128/aem.57.2.535-538.1991
Castro L, Blázquez ML, González F, Muñoz JAJM (2020) Bioleaching of phosphate minerals using Aspergillus niger: recovery of copper and rare earth elements. Metals 10:978. https://doi.org/10.3390/met10070978
Chen J, Hu K-X, Hou X-Q, Guo S-X (2011) Endophytic fungi assemblages from 10 Dendrobium medicinal plants (Orchidaceae). World J Microbiol Biotechnol 27:1009–1016. https://doi.org/10.1007/s11274-010-0544-y
Chen P-H, Chen R-Y, Chou J-Y (2018) Screening and evaluation of yeast antagonists for biological control of Botrytis cinerea on strawberry fruits. Mycobiology 46:33–46. https://doi.org/10.1080/12298093.2018.1454013
Committee CB (2021) https://comitedearandanos.cl/.
Copeland JK, Yuan L, Layeghifard M, Wang PW, Guttman DS (2015) Seasonal community succession of the phyllosphere microbiome. Mol Plant Microbe Interact 28:274–285. https://doi.org/10.1094/MPMI-10-14-0331-FI
de Vries FT, Griffiths RI, Knight CG, Nicolitch O, Williams A (2020) Harnessing rhizosphere microbiomes for drought-resilient crop production. Science 368:270–274. https://doi.org/10.1126/science.aaz5192
Del Frari G, Cabral A, Nascimento T, Boavida Ferreira R, Oliveira H (2019) Epicoccum layuense a potential biological control agent of esca-associated fungi in grapevine. PloS One 14:e0213273. https://doi.org/10.1371/journal.pone.0213273
Dell’Amico E, Cavalca L, Andreoni V (2008) Improvement of Brassica napus growth under cadmium stress by cadmium-resistant rhizobacteria. Soil Biol Biochem 40:74–84. https://doi.org/10.1016/j.soilbio.2007.06.024
Du Z, Bramlage WJ (1992) Modified thiobarbituric acid assay for measuring lipid oxidation in sugar-rich plant tissue extracts. J Agric Food Chem 40:1566–1570. https://doi.org/10.1021/jf00021a018
Egamberdieva D, Wirth S, Behrendt U, Ahmad P, Berg G (2017) Antimicrobial activity of medicinal plants correlates with the proportion of antagonistic endophytes. Front Microbiol 8:199. https://doi.org/10.3389/fmicb.2017.00199
Elias F, Woyessa D, Muleta D (2016) Phosphate solubilization potential of rhizosphere fungi isolated from plants in Jimma Zone, Southwest Ethiopia. Int J Microbiol 2016. https://doi.org/10.1155/2016/5472601
Etesami H, Maheshwari DK (2018) Use of plant growth promoting rhizobacteria (PGPRs) with multiple plant growth promoting traits in stress agriculture: action mechanisms and future prospects. Ecotoxicol Environ Saf 156:225–246. https://doi.org/10.1016/j.ecoenv.2018.03.013
Fan X et al (2019) Microenvironmental interplay predominated by beneficial Aspergillus abates fungal pathogen incidence in paddy environment. Environ Sci Technol 53:13042–13052. https://doi.org/10.1021/acs.est.9b04616
Ferreira CM, Vilas-Boas Â, Sousa CA, Soares HM, Soares EV (2019) Comparison of five bacterial strains producing siderophores with ability to chelate iron under alkaline conditions. AMB Expr 9:1–12. https://doi.org/10.1186/s13568-019-0796-3
Freeman D, Falkiner F, Keane C (1989) New method for detecting slime production by coagulase negative staphylococci. J Clin Pathol 42:872–874. https://doi.org/10.1136/jcp.42.8.872
Garcia-Gonzales R et al (2018) Development and characterization of microsatellite markers in Gaultheria pumila Lf.(Ericaceae). Biol Res 51. https://doi.org/10.1186/s40659-018-0193-4
Godoy R, Marín C (2019) Mycorrhizal studies in temperate rainforests of Southern Chile. In: Mycorrhizal Fungi in South America. Springer, pp 315–341
Haelewaters D, Urbina H, Brown S, Newerth-Henson S, Aime M (2021) Isolation and molecular characterization of the romaine lettuce phylloplane mycobiome. J Fungi (Basel) 7:277. https://doi.org/10.3390/jof7040277
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. In: Nucleic acids symposium series. Information Retrieval Ltd., c1979-c2000., London, pp 95–98
Hankin L, Anagnostakis S (1975) The use of solid media for detection of enzyme production by fungi. Mycologia 67:597–607. https://doi.org/10.1080/00275514.1975.12019782
Hardoim PR et al (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320. https://doi.org/10.1128/MMBR.00050-14
Hassan EA, Mostafa YS, Alamri S, Hashem M, Nafady NA (2021) Biosafe management of Botrytis grey mold of strawberry fruit by novel bioagents. Plants (Basel) 10:2737. https://doi.org/10.3390/plants10122737
Henriquez JM, Lusk C (2005) Facilitation of Nothofagus antarctica (Fagaceae) seedlings by the prostrate shrub Empetrum rubrum (Empetraceae) on glacial moraines in Patagonia. Austral Ecol 30:877–882. https://doi.org/10.1111/j.1442-9993.2005.01531.x
Herrera H, Novotná A, Ortiz J, Soto J, Arriagada C (2020a) Isolation and identification of plant growth-promoting bacteria from rhizomes of Arachnitis uniflora, a fully mycoheterotrophic plant in southern Chile. Appl Soil Ecol 149:103512. https://doi.org/10.1016/j.apsoil.2020.103512
Herrera H, Sanhueza T, Martiarena R, Valadares R, Fuentes A, Arriagada C (2020b) Mycorrhizal fungi isolated from native terrestrial orchids from region of La Araucanía, Southern Chile. Microorganisms 8:1120. https://doi.org/10.3390/microorganisms8081120
Herrera H et al (2022) Root-associated endophytes isolated from juvenile Ulex europaeus L.(Fabaceae) plants colonizing rural areas in South-Central Chile. Plant and Soil 474:1–13. https://doi.org/10.1007/s11104-022-05324-5
Hildebrand P, McRae K, Lu X (2001) Factors affecting flower infection and disease severity of lowbush blueberry by Botrytis cinerea. Can J Plant Pathol 23:364–370. https://doi.org/10.1080/07060660109506957
Hiscox J, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1334. https://doi.org/10.1139/b79-163
Jabborova D, Enakiev Y, Sulaymanov K, Kadirova D, Ali A, Annapurna K (2021) Plant growth promoting bacteria Bacillus subtilis promote growth and physiological parameters of Zingiber officinale Roscoe. Plant Sci Today 8:66–71. https://doi.org/10.14719/pst.2021.8.1.997
Jamali H, Sharma A, Srivastava AK (2020) Biocontrol potential of Bacillus subtilis RH5 against sheath blight of rice caused by Rhizoctonia solani. J Basic Microbiol 60:268–280. https://doi.org/10.1002/jobm.201900347
Janakiev T, Dimkić I, Bojić S, Fira D, Stanković S, Berić T (2020) Bacterial communities of plum phyllosphere and characterization of indigenous antagonistic Bacillus thuringiensis R3/3 isolate. J Appl Microbiol 128:528–543. https://doi.org/10.1111/jam.14488
Júnior PSPC et al (2020) Endophytic bacteria of garlic roots promote growth of micropropagated meristems. Microbiol Res 241:126585
Kasana RC, Salwan R, Dhar H, Dutt S, Gulati A (2008) A rapid and easy method for the detection of microbial cellulases on agar plates using Gram’s iodine. Curr Microbiol 57:503–507. https://doi.org/10.1007/s00284-008-9276-8
Knief C et al (2012) Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. ISME J 6:1378–1390. https://doi.org/10.1038/ismej.2011.192
Krimm U, Abanda-Nkpwatt D, Schwab W, Schreiber LJFME (2005) Epiphytic microorganisms on strawberry plants (Fragaria ananassa cv. Elsanta): identification of bacterial isolates and analysis of their interaction with leaf surfaces. FEMS Microbiol Ecol 53:483–492. https://doi.org/10.1016/j.femsec.2005.02.004
Kumar D, Kumar L, Nagar S, Raina C, Parshad R, Gupta VK (2012) Screening, isolation and production of lipase/esterase producing Bacillus sp. strain DVL2 and its potential evaluation in esterification and resolution reactions. Arch Appl Sci Res 4:1763–1770
Kwon J-H, Cheon M-G, Choi O, Kim J (2011) First report of Botrytis cinerea as a postharvest pathogen of blueberry in Korea. Mycobiology 39:52–53. https://doi.org/10.4489/MYCO.2011.39.1.052
Laforest-Lapointe I, Messier C, Kembel SW (2016) Tree phyllosphere bacterial communities: exploring the magnitude of intra-and inter-individual variation among host species. PeerJ 4:e2367. https://doi.org/10.7717/peerj.2367
Larkin MA et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. https://doi.org/10.1093/bioinformatics/btm404
Lealem F, Gashe B (1994) Amylase production by a Gram-positive bacterium isolated from fermenting tef (Eragrostis tef). J Appl Bacteriol 77:348–352. https://doi.org/10.1111/j.1365-2672.1994.tb03084.x
Leveau J (2019) A brief from the leaf: latest research to inform our understanding of the phyllosphere microbiome. Curr Opin Microbiol 49:41–49. https://doi.org/10.1016/j.mib.2019.10.002
Lidon FC et al (2012) Fungistatic action of Aureobasidium pullulans on Penicillium expansum in “Rocha” pear: implications for oxidative stress during fruit storage. Int J Pest Manag 58:41–52. https://doi.org/10.1080/09670874.2011.645515
Lukashe NS, Mupambwa HA, Green E, Mnkeni PN (2019) Inoculation of fly ash amended vermicompost with phosphate solubilizing bacteria (Pseudomonas fluorescens) and its influence on vermi-degradation, nutrient release and biological activity. Waste Manag 83:14–22. https://doi.org/10.1016/j.wasman.2018.10.038
Marques AP, Pires C, Moreira H, Rangel AO, Castro PM (2010) Assessment of the plant growth promotion abilities of six bacterial isolates using Zea mays as indicator plant. Soil Biol Biochem 42:1229–1235. https://doi.org/10.1016/j.soilbio.2010.04.014
Mendes R, Garbeva P, Raaijmakers JM (2013) The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev 37:634–663. https://doi.org/10.1111/1574-6976.12028
Meriño-Gergichevich C, Reyes-Díaz M, Guerrero J, Ondrasek G (2017) Physiological and nutritional responses in two highbush blueberry cultivars exposed to deficiency and excess of boron. J Soil Sci Plant Nutr 17:307–318. https://doi.org/10.4067/S0718-95162017005000024
Mieres-Castro D et al (2019) Antioxidant activity and the isolation of polyphenols and new iridoids from Chilean Gaultheria phillyreifolia and G. poeppigii berries. Food Chem 291:167–179. https://doi.org/10.1016/j.foodchem.2019.04.019
Mina D, Pereira JA, Lino-Neto T, Baptista P (2020) Screening the olive tree phyllosphere: search and find potential antagonists against Pseudomonas savastanoi pv. savastanoi. Front Microbiol 11:2051. https://doi.org/10.3389/fmicb.2020.02051
Mitter B, Pfaffenbichler N, Sessitsch A (2016) Plant–microbe partnerships in 2020. J Microbial Biotechnol 9:635–640. https://doi.org/10.1111/1751-7915.12382
Mueller UG, Sachs JL (2015) Engineering microbiomes to improve plant and animal health. Trends Microbiol 23:606–617. https://doi.org/10.1016/j.tim.2015.07.009
Muñoz G, Orlando J, Zuñiga-Feest AJP (2021) Plants colonizing volcanic deposits: root adaptations and effects on rhizosphere microorganisms. Plant and Soil 461:265–279. https://doi.org/10.1007/s11104-020-04783-y
Nautiyal C (1999) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 170:265–270. https://doi.org/10.1111/j.1574-6968.1999.tb13383.x
Ngah N, Thomas RL, Shaw MW, Fellowes MD (2018) Asymptomatic host plant infection by the widespread pathogen Botrytis cinerea alters the life histories, behaviors, and interactions of an aphid and its natural enemies. Insects 9:80. https://doi.org/10.3390/insects9030080
Oyarzún P, Cornejo P, Gómez-Alonso S, Ruiz A (2020) Influence of profiles and concentrations of phenolic compounds in the coloration and antioxidant properties of Gaultheria poeppigii Fruits from Southern Chile. Plant Foods Hum Nutr 75:532–539. https://doi.org/10.1007/s11130-020-00843-x
Panstruga R, Kuhn H (2019) Mutual interplay between phytopathogenic powdery mildew fungi and other microorganisms. Mol Plant Pathol 20:463–470. https://doi.org/10.1111/mpp.12771
Parsek MR, Fuqua C (2004) Biofilms 2003: emerging themes and challenges in studies of surface-associated microbial life. J Bacteriol 186:4427–4440. https://doi.org/10.1128/JB.186.14.4427-4440.2004
Peng X et al (2018) Yeasts from Nanfeng mandarin plants: occurrence, diversity and capability to produce indole-3-acetic acid. Biotechnol Biotechnol Equip 32:1496–1506. https://doi.org/10.1080/13102818.2018.1487337
Pietrowska E, Różalska S, Kaźmierczak A, Nawrocka J, Małolepsza U (2015) Reactive oxygen and nitrogen (ROS and RNS) species generation and cell death in tomato suspension cultures—Botrytis cinerea interaction. Protoplasma 252:307–319. https://doi.org/10.1007/s00709-014-0680-6
Prussin AJ, Marr LCJM (2015) Sources of airborne microorganisms in the built environment. Microbiome 3:1–10. https://doi.org/10.1186/s40168-015-0144-z
Rathnayake R, Savocchia S, Schmidtke L, Steel CJ (2018) Characterisation of Aureobasidium pullulans isolates from Vitis vinifera and potential biocontrol activity for the management of bitter rot of grapes. Eur J Plant Pathol 151:593–611. https://doi.org/10.1007/s10658-017-1397-0
Rivera S, Zoffoli JP, Latorre B (2013) Infection risk and critical period for the postharvest control of gray mold (Botrytis cinerea) on blueberry in Chile. Plant Dis 97:1069–1074. https://doi.org/10.1094/PDIS-12-12-1112-RE
Rosenberg E, Zilber-Rosenberg I (2016) Microbes drive evolution of animals and plants: the hologenome concept. mBio 7:e01395–e01315. https://doi.org/10.1128/mBio.01395-15
Saha M et al (2016) Microbial siderophores and their potential applications: a review. Environ Sci Pollut Res 23:3984–3999. https://doi.org/10.1007/s11356-015-4294-0
Sautua F, Baron C, Pérez-Hernández O, Carmona MA (2019) First report of resistance to carbendazim and procymidone in Botrytis cinerea from strawberry, blueberry and tomato in Argentina. Crop Prot 125:104879. https://doi.org/10.1016/j.cropro.2019.104879
Soto J et al (2019) Enhanced arsenic tolerance in Triticum aestivum inoculated with arsenic-resistant and plant growth promoter microorganisms from a heavy metal-polluted soil. Microorganisms 7:348. https://doi.org/10.3390/microorganisms7090348
Streletskii R, Kachalkin A, Glushakova A, Yurkov A, Vladimir V (2019) Yeasts producing zeatin. PeerJ 7:e6474
Sturz A, Christie B, Matheson BG (1998) Associations of bacterial endophyte populations from red clover and potato crops with potential for beneficial allelopathy. Can J Microbiol 44:162–167. https://doi.org/10.1139/w97-146
Sun P-F, Chien I-A, Xiao H-S, Fang W-T, Hsu C-H, Chou J-Y (2019) Intra specific variation in plant growth-promoting traits of Aureobasidium pullulans. Chiang Mai J Sci 46:15–31
Tahir M et al (2020) Inoculation of pqqE gene inhabiting Pantoea and Pseudomonas strains improves the growth and grain yield of wheat with a reduced amount of chemical fertilizer. J Appl Microbiol 129:575–589. https://doi.org/10.1111/jam.14630
Tani A et al (2012) High-throughput identification and screening of novel Methylobacterium species using whole-cell MALDI-TOF/MS analysis. PloS One 7:e40784
Teillier S, Escobar F (2013) Revisión del género Gaultheria L.(Ericaceae) en Chile. Gayana Bot 70:136–153. https://doi.org/10.4067/S0717-66432013000100014
Vasquez P, Baldomá J, Wright E, Pérez A, de Sesar MD, Pérez B (2007) First report of blueberry Botrytis blight in Buenos Aires, Entre Ríos, and Córdoba, Argentina. Plant Dis 91:639–639. https://doi.org/10.1094/PDIS-91-5-0639C
Villagra E et al (2014) Morphometric and phytochemical characterization of chaura fruits (Gaultheria pumila): a native Chilean berry with commercial potential. Biol Res 47:1–8. https://doi.org/10.1186/0717-6287-47-26
Wang L, Hu J, Li D, Reymick OO, Tan X, Tao NJSH (2022) Isolation and control of Botrytis cinerea in postharvest green pepper fruit. Sci Hortic 302:111159. https://doi.org/10.1016/j.scienta.2022.111159
Wang X et al (2020) A biocontrol strain of Pseudomonas aeruginosa CQ-40 promote growth and control Botrytis cinerea in tomato. Pathogens 10:22. https://doi.org/10.3390/pathogens10010022
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols 18:315–322
Xiao H-S et al (2019) Phenotypic plasticity in Aureobasidium pullulans isolates. Int J Agric Biol 22:167–177. https://doi.org/10.17957/IJAB/15.1047
Yalage Don S, Schmidtke L, Gambetta J, Steel C (2020) Aureobasidium pullulans volatilome identified by a novel, quantitative approach employing SPME-GC-MS, suppressed Botrytis cinerea and Alternaria alternata in vitro. Sci Rep 10:1–13. https://doi.org/10.1038/s41598-020-61471-8
Yoshida S, Hiradate S, Koitabashi M, Kamo T, Tsushima S (2017) Phyllosphere Methylobacterium bacteria contain UVA-absorbing compounds. J Photochem Photobiol B Biol 167:168–175. https://doi.org/10.1016/j.jphotobiol.2016.12.019
Zhang D, Spadaro D, Valente S, Garibaldi A, Gullino M (2012) Cloning, characterization, expression and antifungal activity of an alkaline serine protease of Aureobasidium pullulans PL5 involved in the biological control of postharvest pathogens. Int J Food Microbiol 153:453–464. https://doi.org/10.1016/j.ijfoodmicro.2011.12.016
Zhang J, Plowman JE, Tian B, Clerens S, On S (2021) Application of MALDI-TOF analysis to reveal diversity and dynamics of winemaking yeast species in wild-fermented, organically produced, New Zealand Pinot Noir wine. Food Microbiol 99:103824
Zhang Q et al (2019) Endophytic bacterial communities associated with roots and leaves of plants growing in Chilean extreme environments. Sci Rep 9:1–12. https://doi.org/10.1038/s41598-019-41160-x
Zhang X, Gao Z, Zhang M, Jing F, Du J, Zhang L (2016) Analysis of endophytic actinobacteria species diversity in the stem of Gynura cusimbua by 16S rRNA gene clone library. Microbiology 85:379–385. https://doi.org/10.1134/S0026261716030176
Zheng M, Shi J, Shi J, Wang Q, Li Y (2013) Antimicrobial effects of volatiles produced by two antagonistic Bacillus strains on the anthracnose pathogen in postharvest mangos. Biol Control 65:200–206
Zheng M et al (2018) Degradation of Macondo 252 oil by endophytic Pseudomonas putida. J Environ Chem Eng 6:643–648. https://doi.org/10.1016/j.jece.2017.12.071
Zhu H, Li S, Hu Z, Liu G (2018) Molecular characterization of eukaryotic algal communities in the tropical phyllosphere based on real-time sequencing of the 18S rDNA gene. BMC Plant Biol 18:1–14. https://doi.org/10.1186/s12870-018-1588-7
Zilda DS et al (2012) Screening of thermostable protease producing microorganisms isolated from Indonesian hotspring. Bull Marine Fish Postharvest Biotechnol 7:105–114. https://doi.org/10.15578/squalen.v7i3.5
Acknowledgements
This study is dedicated for the memory of Prof. Domingo Contreras Fernandez (1952–2021), Chilean botanist, unforgettable friend and from whom the authors learned much that could not have been learned elsewhere.
Funding
This research was funded by the “Fondo Nacional de Desarrollo Científico y Tecnológico” of Chile, grant number 1211857.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
ESM 1
(DOCX 13 kb)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Sanhueza, T., Herrera, H. & Arriagada, C. Contribution of Leaf-Associated Microorganisms from Native Andean Ericaceae against Botrytis cinerea in Vaccinium corymbosum Cultivars. J Soil Sci Plant Nutr 23, 2637–2650 (2023). https://doi.org/10.1007/s42729-023-01220-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42729-023-01220-8