{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,12]],"date-time":"2026-02-12T07:58:11Z","timestamp":1770883091732,"version":"3.50.1"},"reference-count":49,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2021,9,16]],"date-time":"2021-09-16T00:00:00Z","timestamp":1631750400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["SuberControl (PTDC\/ASP-SIL\/28635\/2017)"],"award-info":[{"award-number":["SuberControl (PTDC\/ASP-SIL\/28635\/2017)"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["BioISI (UIDB\/04046\/2020)"],"award-info":[{"award-number":["BioISI (UIDB\/04046\/2020)"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["CIMO (UIDB\/00690\/2020)"],"award-info":[{"award-number":["CIMO (UIDB\/00690\/2020)"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Plant growth promoting rhizobacteria (PGPR) are in increasing demand due to their role in promoting sustainable practices, not only in agriculture but also in forestry. Keeping in mind the future application of PGPR for increasing cork oak sustainability, the aim of this study was to find cork oak PGPR isolates with increased nutrient solubilisation traits, able to promote root morphological changes and\/or antagonize cork oak bark phytopathogens. Soils from three cork oak forests with distinct bioclimates (humid, semi-humid and semi-arid) were used for isolating bacteria. From the 7634 colony-forming units, 323 bacterial isolates were biochemically assayed for PGPR traits (siderophores production, phosphate solubilizing and organic acids production), and 51 were found to display all these traits. These PGPR were able to induce root morphological changes on Arabidopsis thaliana, like suppression of primary root growth, increase of lateral roots or root hairs formation. However, the most proficient PGPR displayed specific ability in changing a single root morphological trait. This ability was related not only to bacterial genotype, but also with the environment where bacteria thrived and isolation temperature. Bacteria from semi-arid environments (mainly Bacillus megaterium isolates) could hold a promising tool to enhance plant development. Other isolates (Serratia quinivorens or B. cereus) could be further explored for biocontrol purposes.<\/jats:p>","DOI":"10.3390\/microorganisms9091973","type":"journal-article","created":{"date-parts":[[2021,9,18]],"date-time":"2021-09-18T00:13:47Z","timestamp":1631924027000},"page":"1973","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["Cork Oak Forests Soil Bacteria: Potential for Sustainable Agroforest Production"],"prefix":"10.3390","volume":"9","author":[{"given":"Francisca","family":"Reis","sequence":"first","affiliation":[{"name":"Plant Functional Biology Centre, BioSystems and Integrative Sciences Institute (BioISI), Campus de Gualtar, University of Minho, 4710-057 Braga, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0009-0006-2618-0101","authenticated-orcid":false,"given":"Ana Jo\u00e3o","family":"Pereira","sequence":"additional","affiliation":[{"name":"Plant Functional Biology Centre, BioSystems and Integrative Sciences Institute (BioISI), Campus de Gualtar, University of Minho, 4710-057 Braga, Portugal"}]},{"given":"Rui M.","family":"Tavares","sequence":"additional","affiliation":[{"name":"Plant Functional Biology Centre, BioSystems and Integrative Sciences Institute (BioISI), Campus de Gualtar, University of Minho, 4710-057 Braga, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6331-3731","authenticated-orcid":false,"given":"Paula","family":"Baptista","sequence":"additional","affiliation":[{"name":"Centro de Investiga\u00e7\u00e3o de Montanha (CIMO), Instituto Polit\u00e9cnico de Bragan\u00e7a, Campus de Santa Apol\u00f3nia, 5300-253 Bragan\u00e7a, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1385-4799","authenticated-orcid":false,"given":"Teresa","family":"Lino-Neto","sequence":"additional","affiliation":[{"name":"Plant Functional Biology Centre, BioSystems and Integrative Sciences Institute (BioISI), Campus de Gualtar, University of Minho, 4710-057 Braga, Portugal"}]}],"member":"1968","published-online":{"date-parts":[[2021,9,16]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1016\/j.japb.2017.05.004","article-title":"Why does Quercus suber species decline in Mediterranean areas?","volume":"10","author":"Kim","year":"2017","journal-title":"J. Asia Pac. Biodivers."},{"key":"ref_2","unstructured":"(2020, November 01). APCOR. Available online: https:\/\/www.apcor.pt\/wp-content\/uploads\/2019\/12\/boletim_estatistico_apcor_2019.pdf."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1890\/100084","article-title":"Mediterranean cork oak savannas require human use to sustain biodiversity and ecosystem services","volume":"9","author":"Bugalho","year":"2011","journal-title":"Front. Ecol. Environ."},{"key":"ref_4","first-page":"73","article-title":"Climate effects on stem radial growth of Quercus suber L.: Does tree size matter?","volume":"92","author":"Mendes","year":"2018","journal-title":"Int. J. For. Res."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1051\/forest:2006040","article-title":"Interactive effects of drought and pathogens in forest trees","volume":"63","author":"Nageleisen","year":"2006","journal-title":"Ann. For. Sci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"2184","DOI":"10.1094\/PDIS-03-16-0408-FE","article-title":"Endemic and emerging pathogens threatening cork oak trees: Management options for conserving a unique forest ecosystem","volume":"100","author":"Moricca","year":"2016","journal-title":"Plant Dis."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Hodkinson, T., Doohan, F., Saunders, M., and Murphy, B. (2019). The influence of endophytes on cork oak forests under a changing climate. Endophytes for a Growing World, Cambridge University Press.","DOI":"10.1017\/9781108607667"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1473","DOI":"10.3389\/fpls.2018.01473","article-title":"Plant growth-promoting rhizobacteria: Context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture","volume":"9","author":"Backer","year":"2018","journal-title":"Front. Plant Sci."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/j.foreco.2018.12.002","article-title":"The rhizosphere microbiome: A key component of sustainable cork oak forests in trouble","volume":"434","author":"Maghnia","year":"2019","journal-title":"For. Ecol. Manag."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Meena, R.S., Kumar, S., Datta, R., Lal, R., Vijayakumar, V., Brtnicky, M., Sharma, M.P., Yadav, G.S., Jhariya, M.K., and Jangir, C.K. (2020). Impact of Agrochemicals on Soil Microbiota and Management: A Review. Land, 9.","DOI":"10.3390\/land9020034"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Bevivino, A., Paganin, P., Bacci, G., Florio, A., Pellicer, M.S., Papaleo, M.C., Mengoni, A., Ledda, L., Fani, R., and Benedetti, A. (2014). Soil bacterial community response to differences in agricultural management along with seasonal changes in a mediterranean region. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0105515"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/j.apsoil.2019.05.031","article-title":"Climatic impacts on the bacterial community profiles of cork oak soils","volume":"143","author":"Reis","year":"2019","journal-title":"Appl. Soil Ecol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"e00063-16","DOI":"10.1128\/MMBR.00063-16","article-title":"Forest soil bacteria: Diversity, involvement in ecosystem processes, and response to global change","volume":"81","author":"Baldrian","year":"2017","journal-title":"Microbiol. Mol. Biol. Rev."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"038","DOI":"10.29328\/journal.jpsp.1001004","article-title":"Antagonistic features displayed by plant growth-promoting rhizobacteria (PGPR): A Review","volume":"1","author":"Tariq","year":"2017","journal-title":"J. Plant Sci. Phytopathol."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Etesami, H., and Adl, S.M. (2020). Plant Growth-Promoting Rhizobacteria (PGPR) and Their Action Mechanisms in Availability of Nutrients to Plants, Springer.","DOI":"10.1007\/978-981-15-2576-6_9"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1007\/s00572-021-01027-4","article-title":"Bacteria could help ectomycorrhizae establishment under climate variations","volume":"21","author":"Reis","year":"2021","journal-title":"Mycorrhiza"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1007\/s00572-018-0832-1","article-title":"Ectomycorrhizal fungal diversity and community structure associated with cork oak in different landscapes","volume":"28","author":"Reis","year":"2018","journal-title":"Mycorrhiza"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1434","DOI":"10.1016\/j.egypro.2015.07.790","article-title":"Isolation and characterization of the native Rhizobia under hyper-salt edaphic conditions in Ouargla (southeast Algeria)","volume":"74","author":"Sobti","year":"2015","journal-title":"Energy Procedia"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1007\/BF00369386","article-title":"Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria","volume":"12","author":"Alexander","year":"1991","journal-title":"Biol. Fertil. Soils"},{"key":"ref_20","first-page":"362","article-title":"Mobilization of Phosphorus in Soil Connection with the Vital Activity of Some Microbial Species","volume":"17","author":"Pikovskaya","year":"1948","journal-title":"Microbiology"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1007\/s002840010259","article-title":"An efficient method for qualitative screening of phosphate-solubilizing bacteria","volume":"43","author":"Mehta","year":"2001","journal-title":"Curr. Microbiol."},{"key":"ref_22","first-page":"141","article-title":"Characterization of plant growth-promoting rhizobacteria associated with chickpea (Cicer arietinum L.)","volume":"1","author":"Joseph","year":"2012","journal-title":"Int. J. Plant Prod."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1111\/j.1472-765X.1989.tb00262.x","article-title":"Rapid extraction of bacterial genomic DNA with guanidium thiocyanate","volume":"8","author":"Pitcher","year":"1989","journal-title":"Lett. Appl. Microbiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"3233","DOI":"10.1128\/aem.63.8.3233-3241.1997","article-title":"Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients","volume":"63","author":"Heuer","year":"1997","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1007\/s13199-010-0066-2","article-title":"Plant growth-promoting rhizobacteria modulate root-system architecture in Arabidopsis thaliana through volatile organic compound","volume":"51","year":"2010","journal-title":"Symbiosis"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Costa, D., Tavares, R.M., Baptista, P., and Lino-Neto, T. (2020). Cork oak endophytic fungi as potential biocontrol agents against Biscogniauxia mediterranea and Diplodia corticola. J. Fungi, 6.","DOI":"10.3390\/jof6040287"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1016\/j.biocontrol.2006.07.017","article-title":"Screening rhizobacteria for biological control of Fusarium root and crown rot of sorghum in Ethiopia","volume":"40","author":"Idris","year":"2007","journal-title":"Biol. Control"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"11030","DOI":"10.1073\/pnas.0404206101","article-title":"Prospects for inferring very large phylogenies by using the neighbor-joining method","volume":"101","author":"Tamura","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1547","DOI":"10.1093\/molbev\/msy096","article-title":"MEGA X: Molecular evolutionary genetics analysis across computing platforms","volume":"35","author":"Kumar","year":"2018","journal-title":"Mol. Biol. Evol."},{"key":"ref_30","first-page":"406","article-title":"The neighborneighbor-joining method: A new method for reconstructing phlylogenetic trees","volume":"4","author":"Saitou","year":"1987","journal-title":"Mol. Biol. Evol."},{"key":"ref_31","unstructured":"Brock, T.D., Madigan, M.T., Martinko, J.M., and Parker, J. (1994). Biology of Microorganisms, Prentice-Hall. [8th ed.]."},{"key":"ref_32","first-page":"10","article-title":"Differential effects of a Bacillus megaterium strain on Lactuca sativa plant growth depending on the origin of the arbuscular mycorrhizal fungus coinoculated: Physiologic and biochemical traits","volume":"27","author":"Aroca","year":"2007","journal-title":"J. Plant Growth Regul."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"212","DOI":"10.1111\/1758-2229.12130","article-title":"Spore formation in Bacillus subtilis","volume":"6","author":"Tan","year":"2013","journal-title":"Environ. Microbiol. Rep."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Salazar-Badillo, F., Salas-Mu\u00f1oz, S., Mauricio-Castillo, J., S\u00e1enz-Mata, J., Mendoza, A., Nieto Jacobo, M., and Steyaert, J. (2017). The rhizospheres of arid and semi-arid ecosystems are a source of microorganisms with growth-promoting potential. Advances in PGPR Research, CABI.","DOI":"10.1079\/9781786390325.0187"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.jare.2011.11.003","article-title":"Diversity of bacteria nesting the plant cover of north Sinai deserts, Egypt","volume":"4","author":"Hanna","year":"2013","journal-title":"J. Adv. Res."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1007\/s10725-020-00571-x","article-title":"Crosstalk amongst phytohormones from planta and PGPR under biotic and abiotic stresses","volume":"90","author":"Khan","year":"2020","journal-title":"Plant Growth Regul."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"11","DOI":"10.3389\/fpls.2019.00011","article-title":"Auxin modulated initiation of lateral roots is linked to pericycle cell length in maize","volume":"10","author":"Salguero","year":"2019","journal-title":"Front. Plant Sci."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Xie, L., Chen, F., Du, H., Zhang, X., Wang, X., Yao, G., and Xu, B. (2020). Graphene oxide and indole-3-acetic acid cotreatment regulates the root growth of Brassica napus L. via multiple phytohormone pathways. BMC Plant Biol., 20.","DOI":"10.1186\/s12870-020-2308-7"},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Jahn, L., Hofmann, U., and Ludwig-M\u00fcller, J. (2021). Indole-3-Acetic acid is synthesized by the endophyte Cyanodermella asteris via a tryptophan-dependent and -independent way and mediates the interaction with a non-host plant. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22052651"},{"key":"ref_40","first-page":"103","article-title":"Indole-3-acetic acid production and effect on sprouting of yam (Dioscorea rotundata L.) minisetts by Bacillus subtilis isolated from culturable cowdung microflora","volume":"56","author":"Swain","year":"2007","journal-title":"Pol. J. Microbiol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1007\/s11104-008-9754-6","article-title":"Isolation and characterization of phosphate solubilizing rhizobacteria to improve plant health of tomato","volume":"316","author":"Hariprasad","year":"2009","journal-title":"Plant Soil"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1143","DOI":"10.1007\/s00253-007-0909-9","article-title":"Plant-growth-promoting compounds produced by two agronomically important strains of Azospirillum brasilense, and implications for inoculant formulation","volume":"75","author":"Perrig","year":"2007","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"356","DOI":"10.3389\/fpls.2013.00356","article-title":"Plant growth-promoting rhizobacteria and root system functioning","volume":"4","author":"Vacheron","year":"2013","journal-title":"Front. Plant Sci."},{"key":"ref_44","first-page":"1","article-title":"Portraying mechanics of plant growth promoting rhizobacteria (PGPR): A review","volume":"2","author":"Goswami","year":"2016","journal-title":"Cogent Food Agric."},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Siddiqui, Z.A. (2005). Biosynthesis of Antibiotics by PGPR and its Relation in Biocontrol of Plant Diseases. PGPR: Biocontrol and Biofertilization, Springer.","DOI":"10.1007\/1-4020-4152-7"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1016\/j.biocontrol.2017.10.010","article-title":"Plant growth promoting and inducible antifungal activities of irrigation well water-bacteria","volume":"117","author":"Tabli","year":"2018","journal-title":"Biol. Control"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"126389","DOI":"10.1016\/j.micres.2019.126389","article-title":"Functional characterization of potential PGPR exhibiting broad-spectrum antifungal activity","volume":"232","author":"Ali","year":"2019","journal-title":"Microbiol. Res."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1007\/s10658-005-4753-4","article-title":"Antagonistic rhizoplane bacteria induce diverse morphological alterations in Peronosporomycete hyphae during in vitro interaction","volume":"112","author":"Deora","year":"2005","journal-title":"Eur. J. Plant Pathol."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Basu, A., Prasad, P., Das, S.N., Kalam, S., Sayyed, R.Z., Reddy, M.S., and El Enshasy, H. (2021). Plant Growth Promoting Rhizobacteria (PGPR) as Green Bioinoculants: Recent Developments, Constraints, and Prospects. Sustainability, 13.","DOI":"10.3390\/su13031140"}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/9\/9\/1973\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:00:59Z","timestamp":1760166059000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/9\/9\/1973"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,9,16]]},"references-count":49,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2021,9]]}},"alternative-id":["microorganisms9091973"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms9091973","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,9,16]]}}}