Skip to main content
SpringerLink
Log in

The Bacterial and Fungal Microbiota of the Mexican Rubiaceae Family Medicinal Plant Bouvardia ternifolia

  • Plant Microbe Interactions
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Bouvardia ternifolia is a medicinal plant considered a source of therapeutic compounds, like the antitumoral cyclohexapeptide bouvardin. It is known that large number of secondary metabolites produced by plants results from the interaction of the host and adjacent or embedded microorganisms. Using high-throughput DNA sequencing of V3-16S and V5-18S ribosomal gene libraries, we characterized the endophytic, endophytic + epiphyte bacterial, and fungal communities associated to flowers, leaves, stems, and roots, as well as the rhizosphere. The Proteobacteria (average 80.7%) and Actinobacteria (average 14.7%) were the most abundant bacterial phyla, while Leotiomycetes (average 54.8%) and Dothideomycetes (average 27.4%) were the most abundant fungal classes. Differential abundance for the bacterial endophyte group showed a predominance of Erwinia, Propionibacterium, and Microbacterium genera, while Sclerotinia, Coccomyces, and Calycina genera predominated for fungi. The predictive metagenome analysis for bacteria showed significative abundance of pathways for secondary metabolite production, while a FUNguild analysis revealed the presence of pathotroph, symbiotroph, and saprotrophs in the fungal community. Intra and inter copresence and mutual exclusion interactions were identified for bacterial and fungal kingdoms in the endophyte communities. This work provides a description of the diversity and composition of bacterial and fungal microorganisms living in flowers, leaves, stems, roots, and the rhizosphere of this medicinal plant; thus, it paves the way towards an integral understanding in the production of therapeutic metabolites.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

source of the endophytes. Asterisks indicate taxa with similar abundance: g_Sphingomonas*, Sphingomonas wittichii species; g_Aureobasidium**, Aureobasidium pullulans; g_Sclerotinia***, Sclerotinia trifoliorum; and g_Cladosporium****, Cladosporium albugolaibachiiNc14. Absolute counts are in Supplementary Table S6

Fig. 5
Fig. 6

Similar content being viewed by others

Availability of Data and Material

The sequence and corresponding mapping files for all samples used in this study were deposited in the NCBI BioSample repository (accession number: PRJNA703940), https://www.ncbi.nlm.nih.gov/sra/PRJNA703940.

Code availability

Not applicable.

References

  1. Müller DB, Vogel C, Bai Y, Vorholt JA (2016) The plant microbiota: systems-level insights and perspectives. Annu Rev Genet 50:211–234. https://doi.org/10.1146/annurev-genet-120215-034952

    Article  CAS  PubMed  Google Scholar 

  2. Bulgarelli D, Schlaeppi K, Spaepen S et al (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838. https://doi.org/10.1146/annurev-arplant-050312-120106

    Article  CAS  PubMed  Google Scholar 

  3. Jurić S, Sopko Stracenski K, Król-Kilińska Ż et al (2020) The enhancement of plant secondary metabolites content in Lactuca sativa L. by encapsulated bioactive agents. Sci Rep 10:3737. https://doi.org/10.1038/s41598-020-60690-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Köberl M, Schmidt R, Ramadan EM et al (2013) The microbiome of medicinal plants: diversity and importance for plant growth, quality and health. Front Microbiol 4:4. https://doi.org/10.3389/fmicb.2013.00400

    Article  Google Scholar 

  5. Nair DN, Padmavathy S (2014) Impact of endophytic microorganisms on plants, environment and humans. Sci World J 2014:1–11. https://doi.org/10.1155/2014/250693

    Article  Google Scholar 

  6. Srivastava SK, Singh NK (2020) General overview of medicinal and aromatic plants : a review. J Med Plants Stud 8:91–93

    Google Scholar 

  7. Heinrich M, Ankli A, Frei B et al (1998) Medicinal plants in Mexico: Healers’ consensus and cultural importance. Soc Sci Med 47:1859–1871. https://doi.org/10.1016/S0277-9536(98)00181-6

    Article  CAS  PubMed  Google Scholar 

  8. Espejo A, López-Ferrari AR (2009) Catalogo Taxonomico de Especies. Cap Nat México Vol. I

  9. Correll DS& MCJ (1970) Manual of the vascular plants of Texas. Univ Texas Dallas, Richardson 1–1881

  10. Jiménez-Ferrer JE, Pérez-Terán YY, Román-Ramos R, Tortoriello J (2005) Antitoxin activity of plants used in Mexican traditional medicine against scorpion poisoning. Phytomedicine 12:116–122. https://doi.org/10.1016/J.PHYMED.2003.10.001

    Article  PubMed  Google Scholar 

  11. Shivanand DJ, Hoffmann JJ, Torrance SJ et al (1977) Bouvardin and deoxybouvardin, antitumor cyclic hexapeptides from bouvardia ternifolia (Rubiaceae). J Am Chem Soc 99:8040–8044. https://doi.org/10.1021/ja00466a043

    Article  Google Scholar 

  12. Perez GRM, Perez GC, Perez GS, Zavala SMA (1998) Effect of triterpenoids of Bouvardia terniflora on blood sugar levels of normal and alloxan diabetic mice. Phytomedicine 5:475–478. https://doi.org/10.1016/S0944-7113(98)80045-7

    Article  CAS  Google Scholar 

  13. García-Morales G, Huerta-Reyes M, González-Cortazar M et al (2015) Anti-inflammatory, antioxidant and anti-acetylcholinesterase activities of Bouvardia ternifolia: potential implications in Alzheimer’s disease. Arch Pharm Res 38:1369–1379. https://doi.org/10.1007/s12272-015-0587-6

    Article  CAS  PubMed  Google Scholar 

  14. Gouda S, Das G, Sen SK et al (2016) Endophytes: a treasure house of bioactive compounds of medicinal importance. Front Microbiol 7:1–8. https://doi.org/10.3389/fmicb.2016.01538

    Article  Google Scholar 

  15. Bredow C, Azevedo JL, Pamphile JA et al (2015) In silico analysis of the 16S rRNA gene of endophytic bacteria, isolated from the aerial parts and seeds of important agricultural crops. Genet Mol Res 14:9703–9721. https://doi.org/10.4238/2015.August.19.3

    Article  CAS  PubMed  Google Scholar 

  16. Kottek M, Grieser J, Beck C et al (2006) World map of the Köppen-Geiger climate classification updated. Meteorol Zeitschrift 259–263. https://doi.org/10.1127/0941-2948/2006/0130

  17. Araújo WL, Maccheroni W, Aguilar-Vildoso CI et al (2001) Variability and interactions between endophytic bacteria and fungi isolated from leaf tissues of citrus rootstocks. Can J Microbiol 47:229–236. https://doi.org/10.1139/W00-146

    Article  PubMed  Google Scholar 

  18. Fierer N, Hamady M, Lauber CL, Knight R (2008) The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc Natl Acad Sci 105:17994–17999. https://doi.org/10.1073/pnas.0807920105

    Article  PubMed  PubMed Central  Google Scholar 

  19. Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Segata N, Izard J, Waldron L et al (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60. https://doi.org/10.1186/gb-2011-12-6-r60

    Article  PubMed  PubMed Central  Google Scholar 

  21. Nguyen NH, Song Z, Bates ST et al (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248. https://doi.org/10.1016/j.funeco.2015.06.006

    Article  Google Scholar 

  22. Suga T, Kimura T, Inahashi Y et al (2018) Hamuramicins A and B, 22-membered macrolides, produced by an endophytic actinomycete Allostreptomyces sp. K12–0794. J Antibiot (Tokyo) 71:619–625. https://doi.org/10.1038/s41429-018-0055-x

    Article  CAS  Google Scholar 

  23. Sasaki T, Igarashi Y, Saito N, Furumai T (2001) TPU-0031-A and B, new antibiotics of the novobiocin group produced by Streptomyces sp. TP-A0556. J Antibiot (Tokyo) 54:441–447. https://doi.org/10.7164/antibiotics.54.441

    Article  CAS  Google Scholar 

  24. Goulart MC, Cueva-Yesquén LG, Attili-Angelis D, Fantinatti-Garboggini F (2019) Endophytic bacteria from Passiflora incarnata L. leaves with genetic potential for flavonoid biosynthesis. Microb Probiotics Agric Syst 127–139. https://doi.org/10.1007/978-3-030-17597-9_8

  25. Liu H, Wang J, Zhao J et al (2009) Isoquinoline alkaloids from Macleaya cordata active against plant microbial pathogens. Nat Prod Commun 4:1934578X0900401. https://doi.org/10.1177/1934578X0900401120

    Article  Google Scholar 

  26. Zhou JY, Sun K, Chen F et al (2018) Endophytic pseudomonas induces metabolic flux changes that enhance medicinal sesquiterpenoid accumulation in Atractylodes lancea. Plant Physiol Biochem 130:473–481. https://doi.org/10.1016/j.plaphy.2018.07.016

    Article  CAS  PubMed  Google Scholar 

  27. Lòpez-Fernàndez S, Compant S, Vrhovsek U et al (2016) Grapevine colonization by endophytic bacteria shifts secondary metabolism and suggests activation of defense pathways. Plant Soil 405:155–175. https://doi.org/10.1007/s11104-015-2631-1

    Article  CAS  Google Scholar 

  28. Mori T, Awakawa T, Shimomura K et al (2016) Structural insight into the enzymatic formation of bacterial stilbene. Cell Chem Biol 23:1468–1479. https://doi.org/10.1016/j.chembiol.2016.10.010

    Article  CAS  PubMed  Google Scholar 

  29. Singh S, Pandey SS, Shanker K, Kalra A (2020) Endophytes enhance the production of root alkaloids ajmalicine and serpentine by modulating the terpenoid indole alkaloid pathway in Catharanthus roseus roots. J Appl Microbiol 128:1128–1142. https://doi.org/10.1111/jam.14546

    Article  CAS  PubMed  Google Scholar 

  30. Mastan A, Rane D, Dastager SG, Vivek Babu CS (2020) Plant probiotic bacterial endophyte, Alcaligenes faecalis, modulates plant growth and forskolin biosynthesis in Coleus forskohlii. Probiotics Antimicrob Proteins 12:481–493. https://doi.org/10.1007/s12602-019-09582-1

    Article  CAS  PubMed  Google Scholar 

  31. Zhu X, Ni X, Gatheruwaigi M et al (2016) Biodegradation of mixed PAHS by PAH-degrading endophytic bacteria. Int J Environ Res Public Health 13. https://doi.org/10.3390/ijerph13080805

  32. Grossetête S, Labedan B, Lespinet O (2010) FUNGIpath: a tool to assess fungal metabolic pathways predicted by orthology. BMC Genomics 11. https://doi.org/10.1186/1471-2164-11-81

  33. Saikkonen K, Mikola J, Helander M et al (2015) Endophytic phyllosphere fungi and nutrient cycling in terrestrial ecosystems. Curr Sci 109:121–126

    Google Scholar 

  34. Jia M, Chen L, Xin H-L et al (2016) A friendly relationship between endophytic fungi and medicinal plants: a systematic review. Front Microbiol 7:906. https://doi.org/10.3389/fmicb.2016.00906

    Article  PubMed  PubMed Central  Google Scholar 

  35. Martínez-Diz MdelP, Andrés-Sodupe M, Bujanda R et al (2019) Soil-plant compartments affect fungal microbiome diversity and composition in grapevine. Fungal Ecol 41:234–244. https://doi.org/10.1016/j.funeco.2019.07.003

    Article  Google Scholar 

  36. Reazin C, Baird R, Clark S, Jumpponen A (2019) Chestnuts bred for blight resistance depart nursery with distinct fungal rhizobiomes. Mycorrhiza 29:313–324. https://doi.org/10.1007/s00572-019-00897-z

    Article  CAS  PubMed  Google Scholar 

  37. Gafni A, Calderon CE, Harris R et al (2015) Biological control of the cucurbit powdery mildew pathogen Podosphaera xanthii by means of the epiphytic fungus Pseudozyma aphidis and parasitism as a mode of action. Front Plant Sci 6:132. https://doi.org/10.3389/fpls.2015.00132

    Article  PubMed  PubMed Central  Google Scholar 

  38. Osono T, Bhatta BK, Takeda H (2004) Phyllosphere fungi on living and decomposing leaves of giant dogwood. Mycoscience 45:35–41. https://doi.org/10.1007/S10267-003-0155-7

    Article  Google Scholar 

  39. Li Y, Li Z, Arafat Y, Lin W (2020) Studies on fungal communities and functional guilds shift in tea continuous cropping soils by high-throughput sequencing. Ann Microbiol 70:7. https://doi.org/10.1186/s13213-020-01555-y

    Article  CAS  Google Scholar 

  40. Qian X, Li X, Li H, Zhang D (2021) Floral fungal-bacterial community structure and co-occurrence patterns in four sympatric island plant species. Fungal Biol 125:49–61. https://doi.org/10.1016/j.funbio.2020.10.004

    Article  CAS  PubMed  Google Scholar 

  41. Hassani MA, Durán P, Hacquard S (2018) Microbial interactions within the plant holobiont. Microbiome 6:58. https://doi.org/10.1186/s40168-018-0445-0

    Article  PubMed  PubMed Central  Google Scholar 

  42. Agler MT, Ruhe J, Kroll S et al (2016) Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLoS Biol 14:e1002352. https://doi.org/10.1371/journal.pbio.1002352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Chowdhury EK, Jeon J, Rim SO et al (2017) Composition, diversity and bioactivity of culturable bacterial endophytes in mountain-cultivated ginseng in Korea. Sci Rep 7:1–10. https://doi.org/10.1038/s41598-017-10280-7

    Article  CAS  Google Scholar 

  44. Zhang B, Zhang J, Liu Y et al (2018) Co-occurrence patterns of soybean rhizosphere microbiome at a continental scale. Soil Biol Biochem 118:178–186. https://doi.org/10.1016/j.soilbio.2017.12.011

    Article  CAS  Google Scholar 

  45. Han LL, Wang JT, Yang SH et al (2017) Temporal dynamics of fungal communities in soybean rhizosphere. J Soils Sediments 17:491–498. https://doi.org/10.1007/s11368-016-1534-y

    Article  CAS  Google Scholar 

  46. Campisano A, Ometto L, Compant S et al (2014) Interkingdom transfer of the acne-causing agent, propionibacterium acnes, from human to grapevine. Mol Biol Evol 31:1059–1065. https://doi.org/10.1093/molbev/msu075

    Article  CAS  PubMed  Google Scholar 

  47. Bogas AC, Ferreira AJ, Araújo WL et al (2015) Endophytic bacterial diversity in the phyllosphere of Amazon Paullinia cupana associated with asymptomatic and symptomatic anthracnose. Springerplus 4:258. https://doi.org/10.1186/s40064-015-1037-0

    Article  PubMed  PubMed Central  Google Scholar 

  48. Santoyo G, Moreno-Hagelsieb G, del Carmen O-M, Glick BR (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99. https://doi.org/10.1016/j.micres.2015.11.008

    Article  CAS  PubMed  Google Scholar 

  49. Ouertani R, Ouertani A, Mahjoubi M et al (2020) New plant growth-promoting, chromium-detoxifying microbacterium species isolated from a tannery wastewater: performance and genomic insights. Front Bioeng Biotechnol 8:521. https://doi.org/10.3389/fbioe.2020.00521

    Article  PubMed  PubMed Central  Google Scholar 

  50. Wang W, Zhai Y, Cao L et al (2016) Illumina-based analysis of core actinobacteriome in roots, stems, and grains of rice. Microbiol Res 190:12–18. https://doi.org/10.1016/j.micres.2016.05.003

    Article  PubMed  Google Scholar 

  51. Manirajan BA, Maisinger C, Ratering S et al (2018) Diversity, specificity, co-occurrence and hub taxa of the bacterial–fungal pollen microbiome. FEMS Microbiol Ecol 94:112. https://doi.org/10.1093/femsec/fiy112

    Article  CAS  Google Scholar 

  52. Valverde A, De Maayer P, Oberholster T et al (2016) Specific microbial communities associate with the rhizosphere of Welwitschia mirabilis, a living fossil. PLoS ONE 11:e0153353. https://doi.org/10.1371/journal.pone.0153353

    Article  PubMed  PubMed Central  Google Scholar 

  53. Li J, Zhao GZ, Huang HY et al (2010) Pseudonocardia rhizophila sp. nov., a novel actinomycete isolated from a rhizosphere soil. Antonie van Leeuwenhoek. Int J Gen Mol Microbiol 98:77–83. https://doi.org/10.1007/s10482-010-9431-7

    Article  CAS  Google Scholar 

  54. Khan AL, Asaf S, Al-Rawahi A et al (2017) Rhizospheric microbial communities associated with wild and cultivated frankincense producing Boswellia sacra tree. PLoS ONE 12:e0186939. https://doi.org/10.1371/journal.pone.0186939

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. He H, Xing J, Liu C et al (2015) Actinoplanes rhizophilus sp. Nov., an actinomycete isolated from the rhizosphere of Sansevieria trifasciata prain. Int J Syst Evol Microbiol 65:4763–4768. https://doi.org/10.1099/ijsem.0.000646

    Article  CAS  PubMed  Google Scholar 

  56. Afzal I, Shinwari ZK, Sikandar S, Shahzad S (2019) Plant beneficial endophytic bacteria: mechanisms, diversity, host range and genetic determinants. Microbiol Res 221:36–49. https://doi.org/10.1016/j.micres.2019.02.001

    Article  CAS  PubMed  Google Scholar 

  57. Ramírez-Bahena M-H, Salazar S, Cuesta MJ et al (2016) Erwinia endophytica sp. nov., isolated from potato (Solanum tuberosum L.) stems. Int J Syst Evol Microbiol 66:975–981. https://doi.org/10.1099/ijsem.0.000820

    Article  CAS  PubMed  Google Scholar 

  58. Zhang H, Li YQ, Xiao M et al (2019) Description of Paracoccus endophyticus sp. nov., isolated from gastrodia elata blume. Int J Syst Evol Microbiol 69:261–265. https://doi.org/10.1099/ijsem.0.003142

    Article  CAS  PubMed  Google Scholar 

  59. Sun LN, Zhang YF, He LY et al (2010) Genetic diversity and characterization of heavy metal-resistant-endophytic bacteria from two copper-tolerant plant species on copper mine wasteland. Bioresour Technol 101:501–509. https://doi.org/10.1016/j.biortech.2009.08.011

    Article  CAS  PubMed  Google Scholar 

  60. Kämpfer P, Lai WA, Arun AB et al (2012) Paracoccus rhizosphaerae sp. nov., isolated from the rhizosphere of the plant Crossostephium chinense (L.) Makino (Seremban). Int J Syst Evol Microbiol 62:2750–2756. https://doi.org/10.1099/ijs.0.039057-0

    Article  CAS  PubMed  Google Scholar 

  61. Liu X, Zhang S, Jiang Q et al (2016) Using community analysis to explore bacterial indicators for disease suppression of tobacco bacterial wilt. Sci Rep 6:1–11. https://doi.org/10.1038/srep36773

    Article  CAS  Google Scholar 

  62. Dai Y, Liu R, Zhou Y et al (2020) Fire Phoenix facilitates phytoremediation of PAH-Cd co-contaminated soil through promotion of beneficial rhizosphere bacterial communities. Environ Int 136. https://doi.org/10.1016/j.envint.2019.105421

  63. Madhaiyan M, Alex THH, Te NS et al (2015) Leaf-residing Methylobacterium species fix nitrogen and promote biomass and seed production in Jatropha curcas. Biotechnol Biofuels 8:222. https://doi.org/10.1186/s13068-015-0404-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Dourado MN, Aparecida Camargo Neves A, Santos DS, Araújo WL (2015) Biotechnological and agronomic potential of endophytic pink-pigmented methylotrophic Methylobacterium spp. Biomed Res Int 2015:1–19. https://doi.org/10.1155/2015/909016

    Article  CAS  Google Scholar 

  65. Chaintreuil C, Giraud E, Prin Y et al (2000) Photosynthetic bradyrhizobia are natural endophytes of the African wild rice Oryza breviligulata. Appl Environ Microbiol 66:5437–5447. https://doi.org/10.1128/AEM.66.12.5437-5447.2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Khan AL, Waqas M, Asaf S et al (2017) Plant growth-promoting endophyte Sphingomonas sp. LK11 alleviates salinity stress in Solanum pimpinellifolium. Environ Exp Bot 133:58–69. https://doi.org/10.1016/j.envexpbot.2016.09.009

    Article  CAS  Google Scholar 

  67. Dhole A (2018) Non-rhizobial endophytes in root nodules. MOJ Biol Med 3. https://doi.org/10.15406/mojbm.2018.03.00064

  68. Mano H, Morisaki H (2008) Endophytic bacteria in the rice plant. Microbes Env 23:109–117. https://doi.org/10.1264/jsme2.23.109

    Article  Google Scholar 

  69. Srinivas A, Sasikala C, Ramana CV (2014) Rhodoplanes oryzae sp. nov., a phototrophic alphaproteobacterium isolated from the rhizosphere soil of paddy. Int J Syst Evol Microbiol 64:2198–2203. https://doi.org/10.1099/ijs.0.063347-0

    Article  CAS  PubMed  Google Scholar 

  70. Pontonio E, Di Cagno R, Tarraf W et al (2018) Dynamic and assembly of epiphyte and endophyte lactic acid bacteria during the life cycle of Origanum vulgare L. Front Microbiol 9:1372. https://doi.org/10.3389/fmicb.2018.01372

    Article  PubMed  PubMed Central  Google Scholar 

  71. Shehata HR, Lyons EM, Jordan KS, Raizada MN (2016) Bacterial endophytes from wild and ancient maize are able to suppress the fungal pathogen Sclerotinia homoeocarpa. J Appl Microbiol 120:756–769. https://doi.org/10.1111/jam.13050

    Article  CAS  PubMed  Google Scholar 

  72. Ansary WR, Prince FRK, Haque E et al (2018) Endophytic Bacillus spp. from medicinal plants inhibit mycelial growth of Sclerotinia sclerotiorum and promote plant growth. Zeitschrift fur Naturforsch - Sect C J Biosci 73:247–256. https://doi.org/10.1515/znc-2018-0002

    Article  CAS  Google Scholar 

  73. McMullin DR, Tanney JB, McDonald KP, Miller JD (2019) Phthalides produced by Coccomyces strobi (Rhytismataceae, Rhytismatales) isolated from needles of Pinus strobus. Phytochem Lett 29:17–24. https://doi.org/10.1016/j.phytol.2018.10.016

    Article  CAS  Google Scholar 

  74. Osono T, Hirose D (2009) Effects of prior decomposition of Camellia japonica leaf litter by an endophytic fungus on the subsequent decomposition by fungal colonizers. Mycoscience 50:52–55. https://doi.org/10.1007/s10267-008-0442-4

    Article  Google Scholar 

  75. Jumpponen A, Mattson KG, Trappe JM (1998) Mycorrhizal functioning of Phialocephala fortinii with Pinus contorta on glacier forefront soil: Interactions with soil nitrogen and organic matter. Mycorrhiza 7:261–265. https://doi.org/10.1007/s005720050190

    Article  CAS  PubMed  Google Scholar 

  76. DIGITAL.CSIC: The endophytic mycobiota of the grass Dactylis glomerata. https://digital.csic.es/handle/10261/17021. Accessed 8 Feb 2021

  77. Chaure P, Gurr SJ, Spanu P (2000) Stable transformation of Erysiphe graminis, an obligate biotrophic pathogen of barley. Nat Biotechnol 18:205–207. https://doi.org/10.1038/72666

    Article  CAS  PubMed  Google Scholar 

  78. Singh UP, Singh HB (1983) Development of Erysiphe pisi on susceptible and resistant cultivars of pea. Trans Br Mycol Soc 81:275–278. https://doi.org/10.1016/s0007-1536(83)80079-5

    Article  Google Scholar 

  79. Bensch K, Braun U, Groenewald JZ, Crous PW (2012) The genus cladosporium. Stud Mycol 72:1–401. https://doi.org/10.3114/sim0003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Cheewangkoon R, Groenewald JZ, Summerell BA et al (2009) Myrtaceae, a cache of fungal biodiversity. Persoonia Mol Phylogeny Evol Fungi 23:55–85. https://doi.org/10.3767/003158509X474752

    Article  CAS  Google Scholar 

  81. Vidal A, Parada R, Mendoza L, Cotoras M (2020) Endophytic fungi isolated from plants growing in Central Andean Precordillera of Chile with antifungal activity against botrytis cinerea. J Fungi 6:1–14. https://doi.org/10.3390/jof6030149

    Article  CAS  Google Scholar 

  82. Isaeva OV, Glushakova AM, Garbuz SA et al (2010) Endophytic yeast fungi in plant storage tissues. Biol Bull 37:26–34. https://doi.org/10.1134/S1062359010010048

    Article  CAS  Google Scholar 

  83. Basha H, Ramanujam B (2015) Growth promotion effect of Pichia guilliermondii in chilli and biocontrol potential of Hanseniaspora uvarum against Colletotrichum capsici causing fruit rot. Biocontrol Sci Technol 25:185–206. https://doi.org/10.1080/09583157.2014.968092

    Article  Google Scholar 

  84. Joubert PM, Doty SL (2018) Endophytic yeasts: biology, ecology and applications. Endophytes of Forest Trees. Springer, Cham, pp 3–14

    Chapter  Google Scholar 

  85. Ramos HP, Braun GH, Pupo MT, Said S (2010) Antimicrobial activity from endophytic fungi Arthrinium state of Apiospora montagnei Sacc. and Papulaspora immersa. Brazilian Arch Biol Technol 53:629–632. https://doi.org/10.1590/S1516-89132010000300017

    Article  Google Scholar 

  86. Wang Z, Li M, Ju W et al (2020) The entomophagous caterpillar fungus Ophiocordyceps sinensis is consumed by its lepidopteran host as a plant endophyte. Fungal Ecol 47:100989. https://doi.org/10.1016/j.funeco.2020.100989

    Article  Google Scholar 

  87. Arie T (2019) Fusarium diseases of cultivated plants, control, diagnosis, and molecular and genetic studies. J Pestic Sci 44:275. https://doi.org/10.1584/JPESTICS.J19-03

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Liu HX, Liu WZ, Chen YC et al (2016) Cytotoxic trichothecene macrolides from the endophyte fungus Myrothecium roridum. J Asian Nat Prod Res 18:684–689. https://doi.org/10.1080/10286020.2015.1134505

    Article  CAS  PubMed  Google Scholar 

  89. Nicoletti R, Di Vaio C, Cirillo C (2020) Endophytic fungi of olive tree. Microorganisms 8:1321. https://doi.org/10.3390/microorganisms8091321

    Article  CAS  PubMed Central  Google Scholar 

  90. Larkin BG, Hunt LS, Ramsey PW (2012) Foliar nutrients shape fungal endophyte communities in Western white pine (Pinus monticola) with implications for white-tailed deer herbivory. Fungal Ecol 5:252–260. https://doi.org/10.1016/j.funeco.2011.11.002

    Article  Google Scholar 

Download references

Acknowledgements

We thank CONACyT Doctoral Fellowships for LEV-F (336296) and FH-Q (291236. We are grateful to Rodrigo García-Gutiérrez and Antonia López-Salazar for excellent technical support and Viridiana Rosas-Ocegueda for administrative assistance. We thank Rosa María Pineda Mendoza and Raquel Galvan Villanueva (ENCB-IPN) for technical support on plant taxonomic identification. We recognize the support of the B. Sc. summer students Isabel Montserrat-Cortez de la Puente (2015) and Mariana Román-Reyes (2016) for the development of this work. Jaime García-Mena (19815) is a Fellow from the Sistema Nacional de Investigadores (Mexico).

Funding

This work was financed by the Cinvestav, FONCICYT 2 267416, CONACYT-BMBF-267416 for RS and JGM and CONACyT-163235 INFR-2011–01 for JGM.

Author information

Authors and Affiliations

  1. Departamento de Genética y Biología Molecular, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (Cinvestav), Avenida Instituto Politécnico Nacional 2508, 07360, Ciudad de México, Mexico

    Loan Edel Villalobos-Flores, Samuel David Espinosa-Torres, Fernando Hernández-Quiroz, Alberto Piña-Escobedo & Jaime García-Mena

  2. Laboratorio de Posgrado de Operaciones Unitarias, Escuela Superior de Ingeniería Química E Industrias Extractivas del Instituto Politécnico Nacional, Unidad Profesional Adolfo López Mateos, 07738, Ciudad de México, Mexico

    Yair Cruz-Narváez

  3. Max Volmer Laboratorium Für Biophysikalische Chemie Technische Universität Berlin, Technische Universität Berlin, Str. des 17. Juni 135/Sekr. PC-14, 10623, Berlin, Germany

    Francisco Velázquez-Escobar

  4. Department of Chemistry, Institut Für Chemie, Technische Universität Berlin, Sekr. TC 2, Straße des 17. Juni 124, 10623, Berlin, Germany

    Roderich Süssmuth

Authors
  1. Loan Edel Villalobos-Flores
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Samuel David Espinosa-Torres
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fernando Hernández-Quiroz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alberto Piña-Escobedo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yair Cruz-Narváez
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Francisco Velázquez-Escobar
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Roderich Süssmuth
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jaime García-Mena
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization: Francisco Velázquez-Escobar, Roderich Süssmuth, and Jaime García-Mena. Methods: Loan Edel Villalobos-Flores, Samuel David Espinosa-Torres, Alberto Piña-Escobedo, and Yair Cruz-Narváez. Software: Loan Edel Villalobos-Flores and Fernando Hernández-Quiroz. Validation: Loan Edel Villalobos-Flores and Jaime García-Mena. Formal analysis and investigation: Loan Edel Villalobos-Flores, Fernando Hernández-Quiroz, Francisco Velázquez-Escobar, Roderich Süssmuth, and Jaime García-Mena. Data curation: Loan Edel Villalobos-Flores, Samuel David Espinosa-Torres, and Jaime García-Mena. Writing—original draft preparation: Loan Edel Villalobos-Flores and Jaime García-Mena. Writing—review and editing: Loan Edel Villalobos-Flores, Yair Cruz-Narváez, Francisco Velázquez-Escobar, Roderich Süssmuth, and Jaime García-Mena. Visualization: Loan Edel Villalobos-Flores. Funding acquisition: Francisco Velázquez-Escobar, Roderich Süssmuth, and Jaime García-Mena. Resources: Yair Cruz-Narváez and Jaime García-Mena. Supervision: Jaime García-Mena. Project administration: Jaime García-Mena.

Corresponding author

Correspondence to Jaime García-Mena.

Ethics declarations

Ethics Approval

Not applicable.

Consent to Participate

Not applicable.

Consent for Publication

Not applicable.

Conflict of Interest

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Villalobos-Flores, L.E., Espinosa-Torres, S.D., Hernández-Quiroz, F. et al. The Bacterial and Fungal Microbiota of the Mexican Rubiaceae Family Medicinal Plant Bouvardia ternifolia. Microb Ecol 84, 510–526 (2022). https://doi.org/10.1007/s00248-021-01871-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-021-01871-z

Keywords

Search

Navigation