Contribution to the characterization of the seed endophyte microbiome of Argania spinosa across geographical locations in Central Morocco using metagenomic approaches.
[en] Microbial endophytes are microorganisms that live inside plants, and some of them play important yet understudied roles in plant health, growth, and adaptation to environmental conditions. Their diversity within plants has traditionally been underestimated due to the limitations of culture-dependent techniques. Metagenomic profiling provides a culture-independent approach to characterize entire microbial communities. The argan tree (Argania spinosa) is ecologically and economically important in Morocco, yet its seed endophyte microbiome remains unexplored. This study aimed to compare the bacterial and fungal endophyte communities associated with argan seeds collected from six sites across Morocco using Illumina MiSeq sequencing of the 16S rRNA gene and ITS regions, respectively. Bacterial DNA was extracted from surface-sterilized seeds and amplified using universal primers, while fungal DNA was isolated directly from seeds. Bioinformatics analysis of sequencing data identified taxonomic profiles at the phylum to genus levels. The results indicated that bacterial communities were dominated by the genus Rhodoligotrophos, while fungal communities exhibited varying degrees of dominance between Ascomycota and Basidiomycota depending on site, with Penicillium being the most abundant overall. Distinct site-specific profiles were observed, with Pseudomonas, Bacillus, and Aspergillus present across multiple locations. Alpha diversity indices revealed variation in endophyte richness between seed sources. In conclusion, this first exploration of the argan seed endophyte microbiome demonstrated environmental influence on community structure. While facing limitations due to small sample sizes and lack of ecological metadata, it provides a foundation for future mechanistic investigations into how specific endophyte-host interactions shape argan adaptation across Morocco's diverse landscapes.
Research Center/Unit :
TERRA Research Centre. Plant Sciences - ULiège
Disciplines :
Agriculture & agronomy
Author, co-author :
Sohaib, Hourfane; Laboratory of Life and Health Sciences, Faculty of Medicine and Pharmacy of Tangier, University Abdelmalek Essaâdi, Tetouan, Morocco
Fays, Morgan; Phytopathology, Microbial and Molecular Farming Lab, Centre D'Etudes et Recherche Appliquée-Haute Ecole Provinciale du Hainaut Condorcet, Ath, Belgium
Khatib, Abderrezzak; Laboratory of Life and Health Sciences, Faculty of Medicine and Pharmacy of Tangier, University Abdelmalek Essaâdi, Tetouan, Morocco
Rivière, John; Laboratory of Biotechnology and Applied Biology, Haute Ecole Provinciale de Hainaut-Condorcet, Ath, Hainaut, Belgium
El Aouad, Noureddine; Laboratory of Life and Health Sciences, Faculty of Medicine and Pharmacy of Tangier, University Abdelmalek Essaâdi, Tetouan, Morocco
Desoignies, Nicolas ; Université de Liège - ULiège > Département GxABT ; Phytopathology, Microbial and Molecular Farming Lab, Centre D'Etudes et Recherche Appliquée-Haute Ecole Provinciale du Hainaut Condorcet, Ath, Belgium
Language :
English
Title :
Contribution to the characterization of the seed endophyte microbiome of Argania spinosa across geographical locations in Central Morocco using metagenomic approaches.
The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This study was financially supported by the Government of Belgium through the \u201CAcad\u00E9mie de Recherche et d\u2019Enseignement Sup\u00E9rieur (ARES)\u201D at the \u201CHaute \u00C9cole Provinciale de Hainaut-Condorcet (HEPH-C).\u201D
Abdallah N. Saadi A. Shakoor A. Merouane A. Della N. M. Gul Z. et al. (2019). Diversity of endophytic fungal community associated to the roots of Argania spinosa (L.) Skeels growing in the arid and semi-arid regions of Algeria. Acta Agric. Slov. 114, 103–111. doi: 10.14720/aas.2019.114.1.12
Abdel-Baky N. (1998). Three Cladosporium spp. as promising biological control candidates for controlling whiteflies (Bemisia spp.) in Egypt. Pak. J. Biol. Sci. 1, 188–195. doi: 10.3923/pjbs.1998.188.195
Adeleke B. S. Ayangbenro A. S. Babalola O. O. (2021a). Bacterial community structure of the sunflower (Helianthus annuus) endosphere. Plant Signal. Behav. 16:1974217. doi: 10.1080/15592324.2021.1974217, PMID: 34590546
Adeleke B. S. Ayangbenro A. S. Babalola O. O. (2021b). Genomic analysis of endophytic Bacillus cereus T4S and its plant growth-promoting traits. Plan. Theory 10:1776. doi: 10.3390/plants10091776, PMID: 34579311
Albayrak Ç. B. (2019). Bacillus species as biocontrol agents for fungal plant pathogens. Bacilli Agrobiotechnol. 2, 239–265. doi: 10.1007/978-3-030-15175-1_13
Al-Dohail M. A. Hashim R. Aliyu-Paiko M. (2011). Evaluating the use of Lactobacillus acidophilus as a biocontrol agent against common pathogenic bacteria and the effects on the haematology parameters and histopathology in African catfish Clarias gariepinus juveniles. Aquac. Res. 42, 196–209. doi: 10.1111/j.1365-2109.2010.02606.x
Alijani Z. Amini J. Ashengroph M. Bahramnejad B. (2019). Antifungal activity of volatile compounds produced by Staphylococcus sciuri strain MarR44 and its potential for the biocontrol of Colletotrichum nymphaeae, causal agent strawberry anthracnose. Int. J. Food Microbiol. 307:108276. doi: 10.1016/j.ijfoodmicro.2019.108276, PMID: 31408741
Aloo B. N. Makumba B. Mbega E. R. (2019). The potential of Bacilli rhizobacteria for sustainable crop production and environmental sustainability. Microbiol. Res. 219, 26–39. doi: 10.1016/j.micres.2018.10.011, PMID: 30642464
Alsharari S. S. Galal F. H. Seufi A. M. (2022). Composition and diversity of the Culturable endophytic Community of six Stress-Tolerant Dessert Plants Grown in stressful soil in a hot Dry Desert region. J. Fungi 8:241. doi: 10.3390/jof8030241, PMID: 35330243
Amplicon P. Clean-Up P. Index P. (2013). 16S Metagenomic Sequencing Library Preparation, Illumina: San Diego, CA, USA. p. 21.
Arshad M. Saleem M. Hussain S. (2007). Perspectives of bacterial ACC deaminase in phytoremediation. Trends Biotechnol. 25, 356–362. doi: 10.1016/j.tibtech.2007.05.005, PMID: 17573137
Atallah O. O. Mazrou Y. S. Atia M. M. Nehela Y. Abdelrhim A. S. Nader M. M. (2022). Polyphasic characterization of four aspergillus species as potential biocontrol agents for white mold disease of bean. J Fungi 8:626. doi: 10.3390/jof8060626, PMID: 35736109
Atehnkeng J. Ojiambo P. Ikotun T. Sikora R. Cotty P. Bandyopadhyay R. (2008). Evaluation of atoxigenic isolates of aspergillus flavus as potential biocontrol agents for aflatoxin in maize. Food Addit. Contam. 25, 1264–1271. doi: 10.1080/02652030802112635
Auguie B. Antonov A. Auguie M. B. (2017). “Package ‘gridExtra’” in Miscellaneous Functions for “Grid” Graphics, 9.
Balogun F. O. Abdulsalam R. A. Ojo A. O. Cason E. (2023). Chemical characterization and metagenomic identification of endophytic microbiome from south African sunflower (Helianthus annuus). Seeds 11:988. doi: 10.3390/microorganisms11040988
Bhatt K. Suyal D. Kumar S. Singh K. Goswami P. (2022). New insights into engineered plant-microbe interactions for pesticide removal. Chemosphere 309:136635. doi: 10.1016/j.chemosphere.2022.136635, PMID: 36183882
Blacutt A. Ginnan N. Dang T. Bodaghi S. Vidalakis G. Ruegger P. et al. (2020). An in vitro pipeline for screening and selection of citrus-associated microbiota with potential anti-“Candidatus Liberibacter asiaticus” properties. Appl. Environ. Microbiol. 86:e02883-19. doi: 10.1128/AEM.02883-19
Bloemberg G. V. Lugtenberg B. J. (2001). Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr. Opin. Plant Biol. 4, 343–350. doi: 10.1016/S1369-5266(00)00183-7, PMID: 11418345
Bomfim C. S. G. Da Silva V. B. Cursino L. H. S. Mattos W. D. S. Santos J. C. S. De Souza L. S. B. et al. (2020). Endophytic bacteria naturally inhabiting commercial maize seeds occupy different niches and are efficient plant growth-promoting agents. Symbiosis 81, 255–269. doi: 10.1007/s13199-020-00701-z
Boughalleb-M’Hamdi N. Salem I. B. M’Hamdi M. (2018). Evaluation of the efficiency of Trichoderma, Penicillium, and aspergillus species as biological control agents against four soil-borne fungi of melon and watermelon. Egypt. J. Biol. Pest Control 28, 1–12. doi: 10.1186/s41938-017-0010-3
Callahan B. J. Mcmurdie P. J. Rosen M. J. Han A. W. Johnson A. J. A. Holmes S. P. (2016). DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583. doi: 10.1038/nmeth.3869, PMID: 27214047
Carr N. T. (2008). Using Microsoft excel® to calculate descriptive statistics and create graphs. Lang. Assess. Q. 5, 43–62. doi: 10.1080/15434300701776336
Carruthers F. Shum-Thomas T. Conner A. Mahanty H. (1995). The significance of antibiotic production by Pseudomonas aureofaciens PA 147-2 for biological control of Phytophthora megasperma root rot of asparagus. Plant Soil 170, 339–344. doi: 10.1007/BF00010487
Cebrián E. Núñez F. Gálvez F. J. Delgado J. Bermúdez E. Rodríguez M. (2020). Selection and evaluation of Staphylococcus xylosus as a biocontrol agent against toxigenic moulds in a dry-cured ham model system. Microorganisms 8:793. doi: 10.3390/microorganisms8060793, PMID: 32466433
Challacombe J. F. Hesse C. N. Bramer L. M. Mccue L. A. Lipton M. Purvine S. et al. (2019). Genomes and secretomes of Ascomycota fungi reveal diverse functions in plant biomass decomposition and pathogenesis. BMC Genomics 20, 1–27. doi: 10.1186/s12864-019-6358-x
Chausali N. Saxena J. (2022). “Role of Bacillus species in alleviating biotic stress in crops” in Bacilli in Agrobiotechnology: Plant Stress Tolerance, Bioremediation, and Bioprospecting. ed. Z. de Ruiter (Midtown Manhattan, New York City, USA: Springer), 365–391.
Chen K. Tian Z. He H. Long C.-A. Jiang F. (2020). Bacillus species as potential biocontrol agents against citrus diseases. Biol. Control 151:104419. doi: 10.1016/j.biocontrol.2020.104419
Choi O. Kim J. Kim J.-G. Jeong Y. Moon J. S. Park C. S. et al. (2008). Pyrroloquinoline quinone is a plant growth promotion factor produced by Pseudomonas fluorescens B16. Plant Physiol. 146, 657–668. doi: 10.1104/pp.107.112748, PMID: 18055583
D’errico G. Aloj V. Flematti G. R. Sivasithamparam K. Worth C. M. Lombardi N. et al. (2021). Metabolites of a Drechslera sp. endophyte with potential as biocontrol and bioremediation agent. Nat. Prod. Res. 35, 4508–4516. doi: 10.1080/14786419.2020.1737058, PMID: 32159387
David V. Terrat S. Herzine K. Claisse O. Rousseaux S. Tourdot-Maréchal R. et al. (2014). High-throughput sequencing of amplicons for monitoring yeast biodiversity in must and during alcoholic fermentation. J. Ind. Microbiol. Biotechnol. 41, 811–821. doi: 10.1007/s10295-014-1427-2, PMID: 24659178
Debbab A. Aly H. A. Edrada-Ebel R. Müller W. E. G. Mosaddak M. Hakiki A. et al. (2009). Bioactive secondary metabolites from the endophytic fungus Chaetomium sp. isolated from Salvia officinalis growing in Morocco. Biotechnol. Agron. Soc. Environ. 13, 229–234.
Deng S.-K. Chen G.-Q. Chen Q. Cai S. Yao L. He J. et al. (2014). Rhodoligotrophos jinshengii sp. nov., isolated from activated sludge. Int. J. Syst. Evol. Microbiol. 64, 3325–3330. doi: 10.1099/ijs.0.066050-0, PMID: 25002364
Droby S. Vinokur V. Weiss B. Cohen L. Daus A. Goldschmidt E. et al. (2002). Induction of resistance to Penicillium digitatum in grapefruit by the yeast biocontrol agent Candida oleophila. Phytopathology 92, 393–399. doi: 10.1094/PHYTO.2002.92.4.393, PMID: 18942952
Edgar R. C. Haas B. J. Clemente J. C. Quince C. Knight R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200. doi: 10.1093/bioinformatics/btr381, PMID: 21700674
Fira D. Dimkić I. Berić T. Lozo J. Stanković S. (2018). Biological control of plant pathogens by Bacillus species. J. Biotechnol. 285, 44–55. doi: 10.1016/j.jbiotec.2018.07.044
Fukuda W. Yamada K. Miyoshi Y. Okuno H. Atomi H. Imanaka T. (2012). Rhodoligotrophos appendicifer gen. Nov., sp. nov., an appendaged bacterium isolated from a freshwater Antarctic Lake. Int. J. Syst. Evol. Microbiol. 62, 1945–1950. doi: 10.1099/ijs.0.032953-0, PMID: 22003040
Gandrud C. (2018). Reproducible Research with R and R Studio. Boca Raton: Chapman and Hall/CRC. p. 313.
Ganoudi M. Calonne-Salmon M. Ibriz M. Declerck S. (2021). In vitro mycorrhization of Argania spinosa L. using germinated seeds. Symbiosis 85, 57–68. doi: 10.1007/s13199-021-00790-4
Glick B. R. (2012). Plant growth-promoting Bacteria: mechanisms and applications. Scientifica 2012:963401, 1–15. doi: 10.6064/2012/963401
Gupta G. Parihar S. S. Ahirwar N. K. Snehi S. K. Singh V. (2015). Plant growth promoting rhizobacteria (PGPR): current and future prospects for development of sustainable agriculture. J Microb Biochem Technol 7, 096–102. doi: 10.4172/1948-5948.1000188
Hamilton C. E. Bauerle T. L. (2012). A new currency for mutualism? Fungal endophytes alter antioxidant activity in hosts responding to drought. Fungal Divers. 54, 39–49. doi: 10.1007/s13225-012-0156-y
Hammer Ø. Harper D. Ryan P. (2001). PAST: Palaeontological statistics software package for education and data analysis, version 4.03. Palaeontol. Electron. 4:9.
Hardoim P. R. Van Overbeek L. S. Van Elsas J. D. (2008). Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol. 16, 463–471. doi: 10.1016/j.tim.2008.07.008, PMID: 18789693
Hashem A. H. Attia M. S. Kandil E. K. Fawzi M. M. Abdelrahman A. S. Khader M. S. et al. (2023). Bioactive compounds and biomedical applications of endophytic fungi: a recent review. Microb. Cell Factories 22:107. doi: 10.1186/s12934-023-02118-x, PMID: 37280587
Hassa J. Maus I. Off S. Pühler A. Scherer P. Klocke M. et al. (2018). Metagenome, metatranscriptome, and metaproteome approaches unraveled compositions and functional relationships of microbial communities residing in biogas plants. Appl. Microbiol. Biotechnol. 102, 5045–5063. doi: 10.1007/s00253-018-8976-7, PMID: 29713790
Higa T. Parr J. F. (1994). Beneficial and effective microorganisms for a sustainable agriculture and environment. Int. Nat. Farm. Res. Center Atami. 1:16.
Hunziker L. Bönisch D. Groenhagen U. Bailly A. Schulz S. Weisskopf L. (2015). Pseudomonas strains naturally associated with potato plants produce volatiles with high potential for inhibition of Phytophthora infestans. Appl. Environ. Microbiol. 81, 821–830. doi: 10.1128/AEM.02999-14, PMID: 25398872
Imane C. Laila S. Jamal A. (2018). Endophytic Fungi isolated from Crocus sativus L. (saffron) as a source of bioactive secondary metabolites. Pharm. J. 10, 1143–1148. doi: 10.5530/pj.2018.6.195
Islam M. T. (2022). Current status and future prospects of Cladosporium sp., a biocontrol agent for sustainable plant protection. Biocontrol Sci. 27, 185–191. doi: 10.4265/bio.27.185, PMID: 36567114
Jeong S. Kim T.-M. Choi B. Kim Y. Kim E. (2021). Invasive Lactuca serriola seeds contain endophytic bacteria that contribute to drought tolerance. Sci. Rep. 11:13307. doi: 10.1038/s41598-021-92706-x, PMID: 34172799
Johnston-Monje D. Raizada M. N. (2011). Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology. PLoS One 6:e20396. doi: 10.1371/journal.pone.0020396, PMID: 21673982
Kharazian Z. A. Jouzani G. S. Aghdasi M. Khorvash M. Zamani M. Mohammadzadeh H. (2017). Biocontrol potential of Lactobacillus strains isolated from corn silages against some plant pathogenic fungi. Biol. Control 110, 33–43. doi: 10.1016/j.biocontrol.2017.04.004
Kurt Menke G. Smith R. Jr. Pirelli L. John Van Hoesen G. (2016). Mastering QGIS. Birmingham, UK: Packt Publishing Ltd.
Laihonen M. Saikkonen K. Helander M. Vázquez De Aldana B. R. Zabalgogeazcoa I. Fuchs B. (2022). Epichloë endophyte-promoted seed pathogen increases host grass resistance against insect herbivory. Front. Microbiol. 12:786619. doi: 10.3389/fmicb.2021.786619, PMID: 35087489
Leitão A. L. Enguita F. J. (2016). Gibberellins in Penicillium strains: challenges for endophyte-plant host interactions under salinity stress. Microbiol. Res. 183, 8–18. doi: 10.1016/j.micres.2015.11.004, PMID: 26805614
Li H.-Y. Wei D.-Q. Shen M. Zhou Z.-P. (2012). Endophytes and their role in phytoremediation. Fungal Divers. 54, 11–18. doi: 10.1007/s13225-012-0165-x
Liu Y.-L. Meng D. Li R.-R. Gu P.-F. Fan X.-Y. Huang Z.-S. et al. (2019). Rhodoligotrophos defluvii sp. nov., isolated from activated sludge. Int. J. Syst. Evol. Microbiol. 69, 3830–3836. doi: 10.1099/ijsem.0.003691, PMID: 31502947
Mapelli F. Riva V. Vergani L. Choukrallah R. Borin S. (2020). Unveiling the microbiota diversity of the xerophyte Argania spinosa L. skeels root system and residuesphere. Microb. Ecol. 80, 822–836. doi: 10.1007/s00248-020-01543-4, PMID: 32583006
Martin M. (2011). Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. journal 17, 10–12. doi: 10.14806/ej.17.1.200
Mastretta C. Taghavi S. Van Der Lelie D. Mengoni A. Galardi F. Gonnelli C. et al. (2009). Endophytic bacteria from seeds of Nicotiana tabacum can reduce cadmium phytotoxicity. Int. J. Phytoremediation 11, 251–267. doi: 10.1080/15226510802432678
Mechqoq H. El Yaagoubi M. El Hamdaoui A. Momchilova S. Da Silva Almeida J. R. G. Msanda F. et al. (2021a). Ethnobotany, phytochemistry and biological properties of argan tree (Argania spinosa (L.) Skeels) (Sapotaceae) – a review. J. Ethnopharmacol. 281:114528. doi: 10.1016/j.jep.2021.114528, PMID: 34418509
Mechqoq H. El Yaagoubi M. Momchilova S. Msanda F. El Aouad N. (2021b). Comparative study on yields and quality parameters of argan oils extracted by conventional and green extraction techniques. Grain Oil Sci Technol 4, 125–130. doi: 10.1016/j.gaost.2021.08.002
Michavila G. Adler C. De Gregorio P. R. Lami M. J. Caram Di Santo M. C. Zenoff A. M. et al. (2017). Pseudomonas protegens CS 1 from the lemon phyllosphere as a candidate for citrus canker biocontrol agent. Plant Biol. 19, 608–617. doi: 10.1111/plb.12556
Miransari M. (2012). “Role of phytohormone signaling during stress” in Environmental Adaptations and Stress Tolerance of Plants in the Era of Climate Change. eds. Ahmad P. Prasad M. N. V. (Midtown Manhattan, New York City, USA: AbtinBerkeh Scientific Ltd), 381–393.
Moore F. P. Barac T. Borremans B. Oeyen L. Vangronsveld J. Van Der Lelie D. et al. (2006). Endophytic bacterial diversity in poplar trees growing on a BTEX-contaminated site: the characterisation of isolates with potential to enhance phytoremediation. Syst. Appl. Microbiol. 29, 539–556. doi: 10.1016/j.syapm.2005.11.012, PMID: 16919907
Morris E. K. Caruso T. Buscot F. Fischer M. Hancock C. Maier T. S. et al. (2014). Choosing and using diversity indices: insights for ecological applications from the German biodiversity Exploratories. Ecol. Evol. 4, 3514–3524. doi: 10.1002/ece3.1155, PMID: 25478144
Msanda F. El Aboudi A. Peltier J.-P. (2005). Biodiversité et biogéographie de l'arganeraie marocaine. Cahiers Agric. 14, 357–364.
Pal G. Kumar K. Verma A. Verma S. K. (2022). Seed inhabiting bacterial endophytes of maize promote seedling establishment and provide protection against fungal disease. Microbiol. Res. 255:126926. doi: 10.1016/j.micres.2021.126926, PMID: 34856481
Petrini O. (1991). “Fungal endophytes of tree leaves” in Microbial Ecology of Leaves. eds. Andrews J. H. Hirano S. S. (Midtown Manhattan, New York City, USA: Springer), 179–197.
Petrović M. Janakiev T. Grbić M. L. Unković N. Stević T. Vukićević S. et al. (2023). Insights into endophytic and Rhizospheric Bacteria of five sugar beet hybrids in terms of their diversity, plant-growth promoting, and biocontrol properties. Microb. Ecol. 87:19. doi: 10.1007/s00248-023-02329-0
Pistori J. F. Simionato A. S. Navarro M. O. Andreata M. F. Santos I. M. Meneguim L. et al. (2018). Low-molecular-weight metabolites produced by Pseudomonas aeruginosa as an alternative to control Huanglongbing in Citrus sinensis cv. Valencia. Trop. Plant Pathol. 43, 289–296. doi: 10.1007/s40858-018-0231-3
Porras-Alfaro A. Bayman P. (2011). Hidden fungi, emergent properties: endophytes and microbiomes. Annu. Rev. Phytopathol. 49, 291–315. doi: 10.1146/annurev-phyto-080508-081831
Price L. B. Liu C. M. Melendez J. H. Frankel Y. M. Engelthaler D. Aziz M. et al. (2009). Community analysis of chronic wound bacteria using 16S rRNA gene-based pyrosequencing: impact of diabetes and antibiotics on chronic wound microbiota. PLoS One 4:e6462. doi: 10.1371/journal.pone.0006462, PMID: 19649281
Quattrini M. Bernardi C. Stuknytė M. Masotti F. Passera A. Ricci G. et al. (2018). Functional characterization of Lactobacillus plantarum ITEM 17215: a potential biocontrol agent of fungi with plant growth promoting traits, able to enhance the nutritional value of cereal products. Food Res. Int. 106, 936–944. doi: 10.1016/j.foodres.2018.01.074, PMID: 29580007
Radhakrishnan R. Khan A. L. Lee I.-J. (2013). Endophytic fungal pre-treatments of seeds alleviates salinity stress effects in soybean plants. J. Microbiol. 51, 850–857. doi: 10.1007/s12275-013-3168-8, PMID: 24385364
Redman R. S. Kim Y. O. Woodward C. J. Greer C. Espino L. Doty S. L. et al. (2011). Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: a strategy for mitigating impacts of climate change. PLoS One 6:e14823. doi: 10.1371/journal.pone.0014823, PMID: 21750695
Reed B. M. Tanprasert P. (1995). Detection and control of bacterial contaminants of plant tissue cultures. A review of recent literature. Plant Tissue Cul. Biotechnol. 1, 137–142.
Rim S. O. Roy M. Jeon J. Montecillo J. A. V. Park S.-C. Bae H. (2021). Diversity and communities of fungal endophytes from four Pinus species in Korea. Forests 12:302. doi: 10.3390/f12030302
Rosenblueth M. Martínez-Romero E. (2006). Bacterial endophytes and their interactions with hosts. Mol. Plant-Microbe Interact. 19, 827–837. doi: 10.1094/MPMI-19-0827
Roswell M. Dushoff J. Winfree R. (2021). A conceptual guide to measuring species diversity. Oikos 130, 321–338. doi: 10.1111/oik.07202
Santos L. F. Olivares F. L. (2021). Plant microbiome structure and benefits for sustainable agriculture. Curr. Plant Biol. 26:100198. doi: 10.1016/j.cpb.2021.100198
Santoyo G. Orozco-Mosqueda M. D. C. Govindappa M. (2012). Mechanisms of biocontrol and plant growth-promoting activity in soil bacterial species of Bacillus and Pseudomonas: a review. Biocontrol Sci. Tech. 22, 855–872. doi: 10.1080/09583157.2012.694413
Senanayake I. C. Pem D. Rathnayaka A. R. Wijesinghe S. N. Tibpromma S. Wanasinghe D. N. et al. (2022). Predicting global numbers of teleomorphic ascomycetes. Fungal Divers. 114, 237–278. doi: 10.1007/s13225-022-00498-w
Singh R. K. Singh P. Guo D.-J. Sharma A. Li D.-P. Li X. et al. (2021). Root-derived endophytic diazotrophic bacteria Pantoea cypripedii AF1 and Kosakonia arachidis EF1 promote nitrogen assimilation and growth in sugarcane. Front. Microbiol. 12:774707. doi: 10.3389/fmicb.2021.774707, PMID: 34975800
Taylor M. W. Tsai P. Anfang N. Ross H. A. Goddard M. R. (2014). Pyrosequencing reveals regional differences in fruit-associated fungal communities. Environ. Microbiol. 16, 2848–2858. doi: 10.1111/1462-2920.12456, PMID: 24650123
Thukral A. K. (2017). A review on measurement of alpha diversity in biology. Agric. Res. J. 54, 1–10. doi: 10.5958/2395-146X.2017.00001.1
Ting A. Abidin C. M. R. Z. Hamid N. H. Azzam G. Salim H. (2023). Uncovering the microbiota of bagworm Metisa plana (Lepidoptera: Psychidae) in oil palm plantations in Malaysia. Trop. Life Sci. Res. 34:185. doi: 10.21315/tlsr2023.34.1.11
Toju H. Tanabe A. S. Yamamoto S. Sato H. (2012). High-coverage ITS primers for the DNA-based identification of ascomycetes and basidiomycetes in environmental samples. PLoS One 7:e40863. doi: 10.1371/journal.pone.0040863, PMID: 22808280
Tran H. Ficke A. Asiimwe T. Höfte M. Raaijmakers J. M. (2007). Role of the cyclic lipopeptide massetolide a in biological control of Phytophthora infestans and in colonization of tomato plants by Pseudomonas fluorescens. New Phytol. 175, 731–742. doi: 10.1111/j.1469-8137.2007.02138.x
Trivedi P. Spann T. Wang N. (2011). Isolation and characterization of beneficial bacteria associated with citrus roots in Florida. Microb. Ecol. 62, 324–336. doi: 10.1007/s00248-011-9822-y, PMID: 21360139
Truyens S. Beckers B. Thijs S. Weyens N. Cuypers A. Vangronsveld J. (2016). Cadmium-induced and trans-generational changes in the cultivable and total seed endophytic community of Arabidopsis thaliana. Plant Biol. 18, 376–381. doi: 10.1111/plb.12415, PMID: 26577608
Truyens S. Jambon I. Croes S. Janssen J. Weyens N. Mench M. et al. (2014). The effect of long-term cd and Ni exposure on seed endophytes of Agrostis capillaris and their potential application in phytoremediation of metal-contaminated soils. Int. J. Phytoremediation 16, 643–659. doi: 10.1080/15226514.2013.837027, PMID: 24933875
Truyens S. Weyens N. Cuypers A. Vangronsveld J. (2015). Bacterial seed endophytes: genera, vertical transmission and interaction with plants. Environ. Microbiol. Rep. 7, 40–50. doi: 10.1111/1758-2229.12181
Unnamalai N. Gnanamanickam S. (1984). Pseudomonas fluorescens is an antagonist to Xanthomonas citri (Hasse) dye, the incitant of citrus canker. Curr. Sci India 53, 703–704.
Valero-Mora P. M. (2010). ggplot2: elegant graphics for data analysis. J. Stat. Softw. 35, 1–3. doi: 10.18637/jss.v035.b01
Villamizar S. Ferro J. A. Caicedo J. C. Alves L. (2020). Bactericidal effect of entomopathogenic bacterium Pseudomonas entomophila against Xanthomonas citri reduces citrus canker disease severity. Front. Microbiol. 11:1431. doi: 10.3389/fmicb.2020.01431, PMID: 32670251
Waller F. Achatz B. Baltruschat H. Fodor J. Becker K. Fischer M. et al. (2005). The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc. Natl. Acad. Sci. 102, 13386–13391. doi: 10.1073/pnas.0504423102, PMID: 16174735
Wani A. K. Akhtar N. Singh R. Chopra C. Kakade P. Borde M. et al. (2022). Prospects of advanced metagenomics and meta-omics in the investigation of phytomicrobiome to forecast beneficial and pathogenic response. Mol. Biol. Rep. 49, 12165–12179. doi: 10.1007/s11033-022-07936-7, PMID: 36169892
Weller D. M. (2007). Pseudomonas biocontrol agents of soilborne pathogens: looking back over 30 years. Phytopathology 97, 250–256. doi: 10.1094/PHYTO-97-2-0250, PMID: 18944383
Wright J. S. (2002). Plant diversity in tropical forests: a review of mechanisms of species coexistence. Oecologia 130, 1–14. doi: 10.1007/s004420100809, PMID: 28547014
Xiong D. S. Yang Y. B. Hu B. Y. Miao C. P. Wang Y. L. Zou J. M. et al. (2021). Myrothins A–F from endophytic fungus Myrothecium sp. BS-31 harbored in panax notoginseng. Chem. Biodivers. 18:e2000964. doi: 10.1002/cbdv.202000964, PMID: 33533151
Yang F. Huang M. Li C. Wu X. Fang L. (2022). Vegetation restoration increases the diversity of bacterial communities in deep soils. Appl. Soil Ecol. 180:104631. doi: 10.1016/j.apsoil.2022.104631
Yu X. L. Hu X. Y. Wang X. X. Zhang X. Y. Du K. B. (2022). A protocol specialized for microbial DNA extraction from living poplar wood. Notulae Botanicae Horti Agrobotanici Cluj Napoca 50, –12822. doi: 10.15835/nbha50312822
Zhang J. Kobert K. Flouri T. Stamatakis A. (2014). PEAR: a fast and accurate Illumina paired-end reAd mergeR. Bioinformatics 30, 614–620. doi: 10.1093/bioinformatics/btt593, PMID: 24142950
