Advertisement

Actinobacteria and Their Role as Plant Probiotics

  • Esther MenendezEmail author
  • Lorena Carro
Chapter
Part of the Soil Biology book series (SOILBIOL, volume 55)

Abstract

Actinobacteria is one of the largest phyla within the domain Bacteria. This phylum comprises more than 400 genera heterogeneously distributed in up to 50 families, 20 orders and 6 classes, being composed with very diverse groups of microorganisms. Members included within this phylum were recovered from a wide range of aquatic and terrestrial environments and also from a huge number of higher organisms, including plants. Actinobacteria inhabiting soils and plants are well known as producers of bioactive molecules and as biocontrol agents, possessing antimicrobial activities mostly against pathogenic fungi and/or bacteria. Moreover, some of them have the capacity to exert beneficial effects on plant growth and development via different plant growth-promoting mechanisms, i.e., phytohormones biosynthesis, siderophore production, and phosphate solubilization, among others. The available genomic data revealed that members belonging to this phylum have a huge potential as Plant Probiotic Actinobacteria. A plethora of studies reported the isolation and identification of plant endophytic actinobacteria possessing those features and also their performance under controlled conditions. However, few studies show the effects of the inoculation of these actinobacteria on real field conditions. In this chapter, we will provide an overview of the available data on the Actinobacteria displaying plant growth-promoting features, particularly in the ones that already had applications in agriculture. Together with a correct taxonomic classification, we will present evidence that the Plant Probiotic Actinobacteria should be considered as a source of bacterial candidates that will be important for a future sustainable agriculture.

References

  1. Adekambi BRW, Hanrahan F, Delcher AL et al (2011) Core gene set as the basis of multilocus sequence analysis of the subclass Actinobacteridae. PLoS One 6(3):e14792.  https://doi.org/10.1371/journal.pone.0014792 PubMedPubMedCentralCrossRefGoogle Scholar
  2. Alekhya G, Gopalakrishnan S (2017) Biological control and plant growth-promotion traits of Streptomyces species under greenhouse and field conditions in chickpea. Agric Res 6(4):410–420CrossRefGoogle Scholar
  3. Alvarez-Pérez JM, González-García S, Cobos R et al (2017) Using endophytic and rhizospheric actinobacteria from grapevine plants to reduce fungal graft infections in nurseries that lead to young grapevine decline. App Environ Microbiol 83:24.  https://doi.org/10.1128/AEM.01564-17 CrossRefGoogle Scholar
  4. Anwar S, Ali B, Sajid I (2016) Screening of rhizospheric Actinomycetes for various in-vitro and in-vivo plant growth promoting (PGP) traits and for agroactive compounds. Front Microbiol 7:1334PubMedPubMedCentralCrossRefGoogle Scholar
  5. Araujo R, Kaewkla O, Franco CM (2017) Endophytic actinobacteria: beneficial partners for sustainable agriculture. In: Maheshwari D (ed) Endophytes: biology and biotechnology, Sustainable development and biodiversity, vol 15. Springer, Cham, pp 171–192CrossRefGoogle Scholar
  6. Bal HB, Das S, Dangar TK et al (2013) ACC deaminase and IAA producing growth promoting bacteria from the rhizosphere soil of tropical rice plants. J Basic Microbiol 53:972–984PubMedCrossRefGoogle Scholar
  7. Banik A, Mukhopadhaya SK, Dangar TK (2016) Characterization of N2-fixing plant growth promoting endophytic and epiphytic bacterial community of Indian cultivated and wild rice (Oryza spp.) genotypes. Planta 243:799–812PubMedCrossRefGoogle Scholar
  8. Barka EA, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C, Klenk H-P, Clément C, Ouhdouch Y, van Wezel GP (2015) Taxonomy, physiology, and natural products of Actinobacteria. Microbiol Mol Biol Rev 80(1):1–43PubMedPubMedCentralCrossRefGoogle Scholar
  9. Beijerinck MW (1901) Über oligonitrophile Mikroben. Zentr Bakt Parasitenk Infektionskrank Hyg, Abt II 7:561–582Google Scholar
  10. Bertani I, Abbruscato P, Piffanelli P et al (2016) Rice bacterial endophytes: isolation of a collection, identification of beneficial strains and microbiome analysis. Environ Microbiol Rep 8:388–398PubMedCrossRefGoogle Scholar
  11. Cardinale M, Ratering S, Suarez C et al (2015) Paradox of plant growth promotion potential of rhizobacteria and their actual promotion effect on growth of barley (Hordeum vulgare L.) under salt stress. Microbiol Res 181:22–32PubMedCrossRefGoogle Scholar
  12. Carro L (2010) Avances en la sistemática del genéro Micromonospora: estudio de cepas aisladas de la rizosfera y nódulos de Pisum sativum. PhD ThesisGoogle Scholar
  13. Carro L, Nouiuoi I (2017) Taxonomy and systematics of plant probiotic bacteria in the genomic era. AIMS Microbiol 3(3):383–412PubMedPubMedCentralCrossRefGoogle Scholar
  14. Carro L, Sproer C, Alonso P et al (2012) Diversity of Micromonospora strains isolated from nitrogen fixing nodules and rhizosphere of Pisum sativum analyzed by multilocus sequence analysis. Syst Appl Microbiol 35:73–80PubMedCrossRefGoogle Scholar
  15. Carro L, Pujic P, Alloisio N et al (2015) Alnus peptides modify membrane porosity and induce the release of nitrogen rich metabolites from nitrogen-fixing Frankia. ISME J 9:1723–1733PubMedPubMedCentralCrossRefGoogle Scholar
  16. Carro L, Riesco R, Spröer C et al (2016a) Micromonospora luteifusca sp. nov. isolated from cultivated Pisum sativum. Syst Appl Microbiol 39:237–242PubMedCrossRefGoogle Scholar
  17. Carro L, Riesco R, Sproër C et al (2016b) Micromonospora ureilytica sp. nov., Micromonospora noduli sp. nov. and Micromonospora vinacea sp. nov., isolated from Pisum sativum nodules. Int J Syst Evol Microbiol 66:3509–3514PubMedCrossRefGoogle Scholar
  18. Carro L, Nouoioui I, Sangal V et al (2018a) Genome-based classification of micromonosporae with a focus on their biotechnological and ecological potential. Sci Rep 8:525PubMedPubMedCentralCrossRefGoogle Scholar
  19. Carro L, Veyisoglu A, Riesco R et al (2018b) Micromonospora phytophila sp. nov. and Micromonospora luteiviridis sp. nov., isolated as natural inhabitants of plant nodules. Int J Syst Evol Microbiol 68:248–253PubMedCrossRefGoogle Scholar
  20. Cavalier-Smith T (2002) The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial megaclassification. Int J Syst Evol Microbiol 52:7–76PubMedCrossRefGoogle Scholar
  21. Conn VM, Walker AR, Franco CM (2008) Endophytic actinobacteria induce defense pathways in Arabidopsis thaliana. Mol Plant Microbe Interact 21(2):208–218.  https://doi.org/10.1094/MPMI-21-2-0208 PubMedCrossRefGoogle Scholar
  22. Curtis SM, Norton I, Everest GJ et al (2018) Kribbella podocarpi sp. nov., isolated from the leaves of a yellowwood tree (Podocarpus latifolius). Antonie Van Leeuwenhoek 111(6):875–882.  https://doi.org/10.1007/s10482-017-0984-6 PubMedCrossRefGoogle Scholar
  23. Damodharan K, Palaniyandi SA, Le B et al (2018) Streptomyces sp. strain SK68, isolated from peanut rhizosphere, promotes growth and alleviates salt stress in tomato (Solanum lycopersicum cv. Micro-Tom). J Microbiol 56:753–759.  https://doi.org/10.1007/s12275-018-8120-5 PubMedCrossRefGoogle Scholar
  24. Diagne N, Arumugam K, Ngom M et al (2013) Use of Frankia and actinorhizal plants for degraded lands reclamation. Biomed Res Int 2013:948258.  https://doi.org/10.1155/2013/948258 PubMedPubMedCentralCrossRefGoogle Scholar
  25. El-Tarabily KA, Nassar AH, Hardy GSJ, Sivasithamparam K (2009) Plant growth promotion and biological control of Pythium aphanidermatum, a pathogen of cucumber, by endophytic actinomycetes. J App Microbiol 106(1):13–26CrossRefGoogle Scholar
  26. Fabri S, Caucas V, Abril A (1996) Infectivity and effectiveness of different strains of Frankia spp. on Atriplex cordobensis plants. Rev Argent Microbiol 28:31–38PubMedGoogle Scholar
  27. Fernández-González AJ, Martínez-Hidalgo P, Cobo-Díaz JF et al (2017) The rhizosphere microbiome of burned holm-oak: potential role of the genus Arthrobacter in the recovery of burned soils. Sci Rep 7(1):6008PubMedPubMedCentralCrossRefGoogle Scholar
  28. Francis IM, Stes E, Zhang Y, Rangel D, Audenaert K, Vereecke D (2016) Mining the genome of Rhodococcus fascians, a plant growth-promoting bacterium gone astray. N Biotechnol 33(5):706–717.  https://doi.org/10.1016/j.nbt.2016.01.009 PubMedCrossRefGoogle Scholar
  29. Ganapathy A, Natesan S (2018) Metabolic potential and biotechnological importance of plant associated endophytic Actinobacteria. In: Gupta V, Rodriguz-Couto S (eds) New and future developments in microbial biotechnology and bioengineering. Elsevier, Amsterdam, pp 207–224CrossRefGoogle Scholar
  30. Garcia LC, Martínez-Molina E, Trujillo ME (2010) Micromonospora pisi sp. nov., isolated from root nodules of Pisum sativum. Int J Syst Evol Microbiol 60:331–337PubMedCrossRefGoogle Scholar
  31. Ghodhbane-Gtari F, Nouioui I, Hezbri K et al (2018) The plant-growth-promoting actinobacteria of the genus Nocardia induces root nodule formation in Casuarina glauca. Antonie Van Leeuwenhoek 112(1):75–90.  https://doi.org/10.1007/s10482-018-1147-0 PubMedCrossRefGoogle Scholar
  32. Golinska P, Wypij M, Agarkar G et al (2015) Endophytic actinobacteria of medicinal plants: diversity and bioactivity. Antonie Van Leeuwenhoek 108(2):267–289PubMedPubMedCentralCrossRefGoogle Scholar
  33. Goudjal Y, Toumatia O, Yekkour A et al (2014) Biocontrol of Rhizoctonia solani damping-off and promotion of tomato plant growth by endophytic actinomycetes isolated from native plants of Algerian Sahara. Microbiol Res 169:59–65PubMedCrossRefGoogle Scholar
  34. Hamdali H, Hafidi M, Virolle MJ, Ouhdouch Y (2008a) Rock phosphate-solubilizing Actinomycetes: screening for plant growth-promoting activities. World J Microbiol Biotechnol 24(11):2565–2575CrossRefGoogle Scholar
  35. Hamdali H, Hafidi M, Virolle MJ, Ouhdouch Y (2008b) Growth promotion and protection against damping-off of wheat by two rock phosphate solubilizing actinomycetes in a P-deficient soil under greenhouse conditions. App Soil Ecol 40(3):510–517CrossRefGoogle Scholar
  36. Hill C, Guarner F, Reid G et al (2014) Expert consensus document: the international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 11:506–514PubMedCrossRefGoogle Scholar
  37. Janssen PH (2006) Identifying the dominant soil bacteria taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72:1719–1728PubMedPubMedCentralCrossRefGoogle Scholar
  38. Jiang ZK, Pan Z, Li FN et al (2017) Marmoricola endophyticus sp. nov., an endophytic actinobacterium isolated from Thespesia populnea. Int J Syst Evol Microbiol 67:4379–4384PubMedCrossRefGoogle Scholar
  39. Jog R, Pandya M, Nareshkumar G, Rajkumar S (2014) Mechanism of phosphate solubilization and antifungal activity of Streptomyces spp. isolated from wheat roots and rhizosphere and their application in improving plant growth. Microbiology 160(4):778–788PubMedCrossRefGoogle Scholar
  40. Kaewkla O, Franco CMM (2018) Actinomycetospora callitridis sp. nov., an endophytic actinobacterium isolated from the surface-sterilised root of an Australian native pine tree. Antonie Van Leeuwenhoek 112(3):331–337.  https://doi.org/10.1007/s10482-018-1162-1 PubMedCrossRefGoogle Scholar
  41. Kaewkla O, Thamchaipenet A, Franco CM (2017) Micromonospora terminaliae sp. nov., an endo phytic actinobacterium isolated from the surface-sterilized stem of the medicinal plant Terminalia mucronata. Int J Syst Evol Microbiol 67:225–230PubMedCrossRefGoogle Scholar
  42. Kämpfer P, Glaeser SP, McInroy JA et al (2016) Nocardioides zeicaulis sp. nov., an endophyte actinobacterium of maize. Int J Syst Evol Microbiol 67:225–230Google Scholar
  43. Kang SM, Asaf S, Kim SJ et al (2016) Complete genome sequence of plant growth-promoting bacterium Leifsonia xyli SE134, a possible gibberellin and auxin producer. J Biotechnol 239:34–38.  https://doi.org/10.1016/j.jbiotec.2016.10.004 PubMedCrossRefGoogle Scholar
  44. Khan MA, Ullah I, Waqas M et al (2018) Halo-tolerant rhizospheric Arthrobacter woluwensis AK1 mitigates salt stress and induces physio-hormonal changes and expression of GmST1 and GmLAX3 in soybean. Symbiosis 77(1):9–21.  https://doi.org/10.1007/s13199-018-0562-3 CrossRefGoogle Scholar
  45. Kim WI, Cho WK, Kim SN et al (2011) Genetic diversity of cultivable plant growth-promoting rhizobacteria in Korea. J Microbiol Biotechnol 21:777–790PubMedCrossRefGoogle Scholar
  46. Kirby BM, Meyers PR (2010) Micromonospora tulbaghiae sp. nov., isolated from the leaves of wild garlic, Tulbaghia violacea. Int J Syst Evol Microbiol 60:1328–1333PubMedCrossRefGoogle Scholar
  47. Kittiwongwattana C, Thanaboripat D, Laosinwattana C et al (2015) Micromonospora oryzae sp. nov., isolated from roots of upland rice. Int J Syst Evol Microbiol 65:3818–3823PubMedCrossRefGoogle Scholar
  48. König H (2012) Class III. Coriobacteriia class. nov. In: Goodfellow M, Kämpfer P, Busse HJ, Trujillo ME, Suzuki KI, Ludwig W, Whitman WB (eds) Bergey’s manual of systematic bacteriology, The Actinobacteria, part B, vol 5, 2nd edn. Springer, New York, p 1968Google Scholar
  49. Kuncharoen N, Pittayakhajonwut P, Tanasupawat S (2018) Micromonospora globbae sp. nov., an endophytic actinomycete isolated from roots of Globba winitii C. H. Wright. Int J Syst Evol Microbiol 68:1073–1077PubMedCrossRefGoogle Scholar
  50. Li L, Tang YL, Wei B et al (2013) Micromonospora sonneratiae sp. nov., isolated from a root of Sonneratia apetala. Int J Syst Evol Microbiol 63:2383–2388PubMedCrossRefGoogle Scholar
  51. Li L, Ma JB, Abdalla Mohamad O et al (2015) Phytoactinopolyspora endophytica gen. nov., sp. nov., a halotolerant filamentous actinomycete isolated from the roots of Glycyrrhiza uralensis F. Int J Syst Evol Microbiol 65:2671–2677PubMedCrossRefGoogle Scholar
  52. Li L, Li YQ, Fu YS et al (2018a) Nesterenkonia endophytica sp. nov., isolated from roots of Glycyrrhiza uralensis. Int J Syst Evol Microbiol 68(8):2659–2663.  https://doi.org/10.1099/ijsem.0.002905 PubMedCrossRefGoogle Scholar
  53. Li X, Lai X, Gan L et al (2018b) Streptomyces geranii sp. nov., a novel endophytic actinobacterium isolated from root of Geranium carolinianum L. Int J Syst Evol Microbiol 68(8):2562–2567.  https://doi.org/10.1099/ijsem.0.002876 PubMedCrossRefGoogle Scholar
  54. Li X, Wang Z, Lu F et al (2018c) Actinocorallia populi sp. nov., an endophytic actinomycete isolated from a root of Populus adenopoda (Maxim.). Int J Syst Evol Microbiol. 68(7):2325–2330.  https://doi.org/10.1099/ijsem.0.002840 PubMedCrossRefGoogle Scholar
  55. Li FN, Tuo L, Lee SM et al (2018d) Amnibacterium endophyticum sp. nov., an endophytic actino bacterium isolated from Aegiceras corniculatum. Int J Syst Evol Microbiol 68(4):1327–1332.  https://doi.org/10.1099/ijsem.0.002676 PubMedCrossRefGoogle Scholar
  56. Lin L, Guo W, Xing Y, Zhang X, Li Z, Hu C, Li S, Li Y, An Q (2012) The actinobacterium Microbacterium sp. 16SH accepts pBBR1-based pPROBE vectors, forms biofilms, invades roots, and fixes N2 associated with micropropagated sugarcane plants. Appl Microbiol Biotechnol 93(3):1185–1195PubMedCrossRefGoogle Scholar
  57. Liu N, Wang H, Liu M et al (2009) Streptomyces alni sp. nov., a daidzein-producing endophyte isolated from a root of Alnus nepalensis D. Don. Int J Syst Evol Microbiol 59:254–258PubMedCrossRefGoogle Scholar
  58. Lozi R (1994) Actinomycetes as plant pathogens. Eur J Plant Path 100:179–200CrossRefGoogle Scholar
  59. Ludwig W, Euzéby J, Whitman WB (2012) Class IV. Nitriliruptoria class. nov. In: Goodfellow M, Kämpfer P, Busse HJ, Trujillo ME, Suzuki KI, Ludwig W, Whitman WB (eds) Bergey’s manual of systematic bacteriology, The Actinobacteria, part B, vol 5, 2nd edn. Springer, New York, p 1968Google Scholar
  60. Martínez-Hidalgo P, Galindo-Villardón P, Trujillo ME et al (2014) Micromonospora from nitrogen fixing nodules of alfalfa (Medicago sativa L.). A new promising plant probiotic bacteria. Sci Rep 4:6389PubMedPubMedCentralCrossRefGoogle Scholar
  61. Misk A, Franco C (2011) Biocontrol of chickpea root rot using endophytic actinobacteria. BioControl 56(5):811–822CrossRefGoogle Scholar
  62. Ngom M, Gray K, Diagne N et al (2016) Symbiotic performance of diverse Frankia strains on salt-stressed Casuarina glauca and Casuarina equisetifolia plants. Front Plant Sci 7:1331.  https://doi.org/10.3389/fpls.2016.01331 PubMedPubMedCentralCrossRefGoogle Scholar
  63. Normand P, Nouioui I, Pujic P et al (2018) Frankia canadensis sp. nov., isolated from root nodules of Alnus incana subspecies rugosa. Int J Syst Evol Microbiol 68(9):3001–3011.  https://doi.org/10.1099/ijsem.0.002939 PubMedCrossRefGoogle Scholar
  64. Norris PR (2012) Class II. Acidimicrobiia class. nov. In: Goodfellow M, Kämpfer P, Busse HJ, Trujillo ME, Suzuki KI, Ludwig W, Whitman WB (eds) Bergey’s manual of systematic bac teriology, The Actinobacteria, part B, vol 5, 2nd edn. Springer, New York, p 1968Google Scholar
  65. Nouioui I, Ghodhbane-Gtari F, Jando M et al (2018a) Frankia torreyi sp. nov., the first actinobacterium of the genus Frankia Brunchorst 1886, 174AL isolated in axenic culture. Antonie Van Leeuwenhoek.  https://doi.org/10.1007/s10482-018-1131-8 PubMedCrossRefGoogle Scholar
  66. Nouioui I, Ghodhbane-Gtari F, Rhode M et al (2018b) Frankia irregularis sp. nov., an actinobacterium unable to nodulate its original host, Casuarina equisetifolia, but effectively nodulates members of the actinorhizal Rhamnales. Int J Syst Evol Microbiol 68(9):2883–2914.  https://doi.org/10.1099/ijsem.0.002914 PubMedCrossRefGoogle Scholar
  67. Nouioui I, Carro L, García-López M, Meier-Kolthoff JP, Woyke T, Kyrpides NC, Pukall R, Klenk H-P, Goodfellow M, Göker M (2018c) Genome-based taxonomic classification of the phylum Actinobacteria. Front Microbiol 9:2007PubMedPubMedCentralCrossRefGoogle Scholar
  68. Palaniyandi SA, Yang SH, Zhang L, Suh JW (2013) Effects of actinobacteria on plant disease suppression and growth promotion. App Microbiol Biotech 97(22):9621–9636CrossRefGoogle Scholar
  69. Palaniyandi SA, Damodharan K, Yang SH, Suh JW (2014) Streptomyces sp. strain PGPA39 alleviates salt stress and promotes growth of ‘Micro Tom’ tomato plants. J Appl Microbiol 117(3):766–773PubMedCrossRefGoogle Scholar
  70. Palazzini JM, Ramirez ML, Torres AM, Chulze SN (2007) Potential biocontrol agents for Fusarium head blight and deoxynivalenol production in wheat. Crop Prot 26(11):1702–1710CrossRefGoogle Scholar
  71. Palazzini JM, Yerkovich N, Alberione E et al (2017) An integrated dual strategy to control Fusarium graminearum sensu stricto by the biocontrol agent Streptomyces sp. RC 87B under field conditions. Plant Gene 9:13–18CrossRefGoogle Scholar
  72. Passari AK, Mishra VK, Singh G et al (2017) Insights into the functionality of endophytic actinobacteria with a focus on their biosynthetic potential and secondary metabolites production. Sci Rep 7(1):11809PubMedPubMedCentralCrossRefGoogle Scholar
  73. Patel JK, Madaan S, Archana G (2018) Antibiotic producing endophytic Streptomyces spp. colonize above-ground plant parts and promote shoot growth in multiple healthy and pathogen-challenged cereal crops. Microbiol Res 215:36–45.  https://doi.org/10.1016/j.micres.2018.06.003 PubMedCrossRefGoogle Scholar
  74. Paterson J, Jahanshah G, Li Y et al (2017) The contribution of genome mining strategies to the understanding of active principles of PGPR strains. FEMS Microbiol Ecol 93(3):fiw249.  https://doi.org/10.1093/femsec/fiw249 PubMedCrossRefGoogle Scholar
  75. Qin S, Zhao GZ, Li J et al (2009) Jiangella alba sp. nov., an endophytic actinomycete isolated from the stem of Maytenus austroyunnanensis. Int J Syst Evol Microbiol 59:2162–2165PubMedCrossRefGoogle Scholar
  76. Rachniyom H, Matsumoto A, Inahashi Y et al (2018) Actinomadura barringtoniae sp. nov., an endophytic actinomycete isolated from the roots of Barringtonia acutangula (L.) Gaertn. Int J Syst Evol Microbiol 68(5):1584–1590.  https://doi.org/10.1099/ijsem.0.002714 PubMedCrossRefGoogle Scholar
  77. Raja A, Prabakarana P (2011) Actinomycetes and drug-an overview. Am J Drug Discov Dev 1:75–84.  https://doi.org/10.3923/ajdd.2011.75.84 CrossRefGoogle Scholar
  78. Remali J, Sarmin NM, Ng CL et al (2017) Genomic characterization of a new endophytic Streptomyces kebangsaanensis identifies biosynthetic pathway gene clusters for novel phenazine antibiotic production. Peer J 5:e3738.  https://doi.org/10.7717/peerj.3738 PubMedCrossRefGoogle Scholar
  79. Roman-Ponce B, Wang D, Vasquez-Murrieta MS et al (2016) Kocuria arsenatis sp. nov., an arsenic-resistant endophytic actinobacterium associated with Prosopis laegivata grown on high-arsenic-polluted mine tailing. Int J Syst Evol Microbiol 66:1027–1033PubMedCrossRefGoogle Scholar
  80. Sakdapetsiri C, Ngaemthao W, Suriyachadkun C et al (2018) Actinomycetospora endophytica sp. nov., isolated from wild orchid (Podochilus microphyllus Lindl.) in Thailand. Int J Syst Evol Microbiol 68(9):3017–3021.  https://doi.org/10.1099/ijsem.0.002938 PubMedCrossRefGoogle Scholar
  81. Salomon MV, Purpora R, Bottini R et al (2016) Rhizosphere associated bacteria trigger accumulation of terpenes in leaves of Vitis vinifera L. cv. Malbec that protect cells against reactive oxygen species. Plant Physiol Biochem 106:295–304PubMedCrossRefGoogle Scholar
  82. Schwachtje J, Karojet S, Kunz S et al (2012) Plant-growth promoting effect of newly isolated rhizobacteria varies between two Arabidopsis ecotypes. Plant Signal Behav 7:623–627PubMedPubMedCentralCrossRefGoogle Scholar
  83. Sen A, Daubin V, Abrouk D et al (2014) Phylogeny of the class Actinobacteria revisited in the light of complete genomes. The orders ‘Frankiales’ and Micrococcales should be split into coherent entities: proposal of Frankiales ord. nov., Geodermatophilales ord. nov., Acidothermales ord. nov. and Nakamurellales ord. nov. Int J Syst Evol Microbiol 64:3821–3832PubMedCrossRefGoogle Scholar
  84. Sharma M, Mishra V, Rau N, Sharma RS (2016) Increased iron-stress resilience of maize through inoculation of siderophore-producing Arthrobacter globiformis from mine. J Basic Microbiol 56(7):719–735.  https://doi.org/10.1002/jobm.201500450 PubMedCrossRefGoogle Scholar
  85. Shen Y, Zhang Y, Liu C et al (2014) Micromonospora zeae sp. nov., a novel endophytic actinomycete isolated from corn root (Zea mays L.). J Antibiot (Tokyo) 67(11):739–743.  https://doi.org/10.1038/ja.2014.54 CrossRefGoogle Scholar
  86. Singh R, Dubey AK (2018) Diversity and applications of endophytic actinobacteria of plants in special and other ecological niches. Front Microbiol 9:1767PubMedPubMedCentralCrossRefGoogle Scholar
  87. Soe KM, Bhromsiri A, Karladee D, Yamakawa T (2012) Effects of endophytic actinomycetes and Bradyrhizobium japonicum strains on growth, nodulation, nitrogen fixation and seed weight of different soybean varieties. Soil Sci Plant Nutr 58:319–325CrossRefGoogle Scholar
  88. Solans M (2007) Discaria trinervis-Frankia symbiosis promotion by saprophytic actinomycetes. J Basic Microbiol 47:243–250PubMedCrossRefGoogle Scholar
  89. Stackebrandt E, Rainey FA, Ward-Rainey NL (1997) Proposal for a new hierarchic classification system, Actinobacteria classis nov. Int J Syst Bacteriol 47:479–491CrossRefGoogle Scholar
  90. Sun Y, Chen HH, Sun HM et al (2017) Naumannella huperziae sp. nov., an endophytic actinobacterium isolated from Huperzia serrata (Thunb.). Int J Syst Evol Microbiol 67:1867–1872PubMedCrossRefGoogle Scholar
  91. Suzuki KI (2012) Class V. Rubrobacteria class. nov. In: Goodfellow M, Kämpfer P, Busse HJ, Trujillo ME, Suzuki KI, Ludwig W, Whitman WB (eds) Bergey’s manual of systematic bacteriology, The Actinobacteria, part B, vol 5, 2nd edn. Springer, New York, p 1968Google Scholar
  92. Suzuki KI, Whitman WB (2012) Class VI. Thermoleophilia class. nov. In: Goodfellow M, Kämpfer P, Busse HJ, Trujillo ME, Suzuki KI, Ludwig W, Whitman WB (eds) Bergey’s manual of systematic bacteriology, The Actinobacteria, part B, vol 5, 2nd edn. Springer, New York, p 1968Google Scholar
  93. Thawai C (2015) Micromonospora costi sp. nov., isolated from a leaf of Costus speciosus. Int J Syst Evol Microbiol 65:1456–1461PubMedCrossRefGoogle Scholar
  94. Trujillo ME, Alonso-Vega P, Rodriguez R et al (2010) The genus Micromonospora is widespread in legume root nodules: the example of Lupinus angustifolius. ISME J 4:1265–1281PubMedCrossRefGoogle Scholar
  95. Trujillo ME, Bacigalupe R, Pujic P et al (2014) Genome features of the endophytic actinobacterium Micromonospora lupini strain Lupac 08: on the process of adaptation to an endophytic life style? PLoS One 9(9):e108522.  https://doi.org/10.1371/journal.pone.0108522 PubMedPubMedCentralCrossRefGoogle Scholar
  96. Trujillo ME, Riesco R, Benito P et al (2015) Endophytic Actinobacteria and the interaction of Micromonospora and Nitrogen fixing plants. Front Microbiol 6:1341.  https://doi.org/10.3389/fmicb.2015.01341 PubMedPubMedCentralCrossRefGoogle Scholar
  97. Tuo L, Yan XR, Li FN et al (2018) Brachybacterium endophyticum sp. nov., a novel endophytic actinobacterium isolated from bark of Scutellaria baicalensis Georgi. Int J Syst Evol Microbiol 68(11):3563–3568.  https://doi.org/10.1099/ijsem.0.003032 PubMedCrossRefGoogle Scholar
  98. Upadhyay SK, Singh JS, Saxena AK et al (2012) Impact of PGPR inoculation on growth and antioxidant status of wheat under saline conditions. Plant Biol 14:605–611PubMedCrossRefGoogle Scholar
  99. Valetti L, Iriarte L, Fabra A (2018) Growth promotion of rapeseed (Brassica napus) associated with the inoculation of phosphate solubilizing bacteria. App Soil Ecol 132:1–10CrossRefGoogle Scholar
  100. Viaene T, Langendries S, Beirinck S et al (2016) Streptomyces as a plant’s best friend? FEMS Microbiol Ecol 92(8):fiw119.  https://doi.org/10.1093/femsec/fiw119 PubMedCrossRefGoogle Scholar
  101. Wang HF, Li L, Zhang YG et al (2015) Arthrobacter endophyticus sp. nov., an endophytic actino bacterium isolated from root of Salsola affinis C. A. Mey. Int J Syst Evol Microbiol 65:2154–2160PubMedCrossRefGoogle Scholar
  102. Wang R, Zhang H, Sun L et al (2017) Microbial community composition is related to soil biological and chemical properties and bacterial wilt outbreak. Sci Rep 7:343.  https://doi.org/10.1038/s41598-017-00472-6 PubMedCrossRefGoogle Scholar
  103. Wang Z, Tian J, Li X et al (2018a) Streptomyces dioscori sp. nov., a novel endophytic actinobacterium isolated from bulbil of Dioscorea bulbifera L. Curr Microbiol 75(10):1384–1390.  https://doi.org/10.1007/s00284-018-1534-9 PubMedCrossRefGoogle Scholar
  104. Wang Z, Jiang B, Li X et al (2018b) Streptomyces populi sp. nov., a novel endophytic actinobacterium isolated from stem of Populus adenopoda Maxim. Int J Syst Evol Microbiol 68(8):2568–2573.  https://doi.org/10.1099/ijsem.0.002877 PubMedCrossRefGoogle Scholar
  105. Wei L, Ouyang S, Wang Y et al (2014) Solirubrobacter phytolaccae sp. nov., an endophytic bac terium isolated from roots of Phytolacca acinosa Roxb. Int J Syst Evol Microbiol 64:858–862PubMedCrossRefGoogle Scholar
  106. Yan X, Li Y, Wang N, Chen Y et al (2018) Streptomyces ginkgonis sp. nov., an endophyte from Ginkgo biloba. Antonie Van Leeuwenhoek 111(6):891–896.  https://doi.org/10.1007/s10482-017-0987-3 PubMedCrossRefGoogle Scholar
  107. Yandigeri MS, Meena KK, Singh D et al (2012) Drought-tolerant endophytic actinobacteria promote growth of wheat (Triticum aestivum) under water stress conditions. Plant Growth Regul 68(3):411–420CrossRefGoogle Scholar
  108. Zhang Y, Liu H, Zhang X et al (2014) Micromonospora violae sp. nov., isolated from a root of Viola philippica Car. Antonie van Leeuwenhoek 106:219–225PubMedCrossRefGoogle Scholar
  109. Zhang YG, Wang HF, Alkhalifah DHM (2018) Glycomyces anabasis sp. nov., a novel endophytic actinobacterium isolated from roots of Anabasis aphylla L. Int J Syst Evol Microbiol 68(4):1285–1290.  https://doi.org/10.1099/ijsem.0.002668 PubMedCrossRefGoogle Scholar
  110. Zhao J, Guo L, He H et al (2014) Micromonospora taraxaci sp. nov., a novel endophytic actinomycete isolated from dandelion root (Taraxacum mongolicum Hand-Mazz.). Antonie van Leeuwenhoek 106(4):667–674PubMedCrossRefGoogle Scholar
  111. Zhao S, Liu C, Zheng W et al (2017) Micromonospora parathelypteridis sp. nov., an endophytic actinomycete with antifungal activity isolated from the root of Parathelypteris beddomei (Bak.) Ching. Int J Syst Evol Microbiol 67:268–274PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.ICAAM - Instituto de Ciências Agrárias e Ambientais Mediterrânicas, Instituto de Investigação e Formação AvançadaUniversidade de ÉvoraEvoraPortugal
  2. 2.Departamento de Microbiología y GenéticaUniversidad de SalamancaSalamancaSpain

Personalised recommendations