Sel’skokhozyaistvennaya Biologiya [Agricultural Biology], 2017, Vol. 52, № 5, p. 917-927
(how to cite this article).

doi: 10.15389/agrobiology.2017.5.917eng

UDC 633/635:57.086.83:579

 

ENDOPHYTES, AS PROMOTORS OF in vitro PLANT GROWTH
(review)

L.S. Samarina, V.I. Malyarovskaya, E.V. Rogozhina, L.S. Malyukova

All-Russian Research Institute of Floriculture and Subtropical Crops, Federal Agency of Scientific Organizations, 2/28, ul. Yana Fabritsiusa, Sochi, 354002 Russia,
e-mail bfbr@vniisubtrop.ru, MalukovaLS@mail.ru, samarinalidia@gmail.com (corresponding author)

ORCID:
Malyukova L.S. orcid.org/0000-0002-0500-1198

Received June 29, 2017

 

In vitro plant propagation is a developed biotechnology, however until now there are no effective protocols for many perennials, especially for trees. High contamination of mature explants during tissue culture initiation, low multiplication and rooting during following passages are the main challenges. Aseptic culture of explants is associated with stress due to tissue damage and exposition to aggressive disinfectants and antibiotics during initiation. These could be the reasons of virulence of endophytes in following propagation. Plant-associated microorganisms were until recently seen as a problem for micropropagation, leading to contamination of in vitro explants. However recent studies showed that colonization of endophytes often play crucial role for increasing viability of in vitro and ex vitro plants. Most endophytes affect positively plant growth, providing nutrients and exhibiting antagonism to pathogens, as well as decreasing stress effects on plants. Beneficial effects were obtained in using Beauveria bassiana (J. Akello et al., 2007), Piriformospora indica and other members of family Sebacinales (P. Sharma et al., 2014), Fusarium oxysporum (A.S.Y. Ting et al., 2008), Ophistoma-like fungi(M. Mucciarelli et al., 2003), Phialocephala fortinii (M. Vohnik et al., 2003), Trichoderma harzianum and other Trichoderma species (P. Franken et al., 2012). Of bacteria, Acetobacter diazotrophicus (C.O. Azlin et al., 2007), Achromobacter xylosoxidans (A. Benson et al., 2014), Azospirillum brasilense (E.E. Larraburu et al., 2015), Azotobacter chroococcum (E.E. Larraburu et al., 2007), Bacillus subtilis (M. Vestberg et al., 2004), B. megaterium (P. Trivedi et al., 2007), Burkholderia phytofirmans (E.A. Ait Barka et al., 2000), B. vietnamiensis (M. Govindarajan et al., 2006), Enterobacter sp. (M.S. Mirza et al., 2001), Klebsiella variicola (C.-Y. Wei et al., 2014), Microbacterium sp. (M. Quambusch et al., 2014), Pseudomonas fluorescens (J. Thomas et al., 2010) и P. putida (R. Lifshitz et al., 1987) also can beneficially influence plants. But until now it is unclear which factor is a trigger switched endophytes from mutualism to virulence. The only way to control such a change is to develop optimal conditions (time of obtaining explants, culture media composition and pH, temperature, etc.) in view to save in vitro mutualism with benefit for both host plant and the endophyte. Studies of many perennials showed the in vitro biotization to be helpful in microclonal propagation and plant rooting. Particularly, arbuscular micorhyza, ectomicorhyzal fungi, ericoid micorhyzal fungi, and wide range of bacteria influence positively plant micropropagation. Bacterial and fungal endophytes could stimulate plant growth due to activation of plant protection mechanisms, induction of systemic resistance to pathogens, phytohormone synthesis and better transport of water and nutrients. In this, the difficulties of classification and obtaining pure cultures of microorganisms are the main problems faced with.

Keywords: micropropagation, endophyte, plant culture media, growth regulators, phytohormones.

 

 

Full article (Rus)

Full text (Eng)

 

REFERENCES

  1. Prakash J. Micropropagation of ornamental perennials: progress and problems. Acta Horticulturae (ISHS), 2009, 812: 289-294 CrossRef
  2. Tailor J., Harrier L. Beneficial influences of arbuscular micorrhizal fungi on the micropropagation of woody and fruit trees. In: Micropropagation of woody trees and fruits. Forestry sciences. V. 75. S.M. Jain, K. Ishii (eds.). Springer, Dordrecht, 2003: 129-150 CrossRef
  3. Kloepper J.W., McInroy J.A., Hu C.-H. Association of plant damage with increased populations of deleterious endophytes following use of Benlate systemic fungicide. Proc. 5th Int. Symp. «Endophytes for plant protection: the state of the art» (Humboldt University, Berlin, 26-29 May, 2013). C. Schneider, C. Leifert, F. Feldmann (eds.). Berlin-Dahlem, 2013: 56-69
  4. Cassels A.C. Doyle-Prestwich B. Detection and elimination of microbial endophytes and prevention of contamination in plant tissue culture. In: Plant tissue culture, development, and biotechnology. Boca Raton, 2011: 223-238 CrossRef
  5. Dunaeva S.E., Osledkin Yu.S. Bacterial microorganisms associated with the plant tissue culture: identification and possible role (review). Sel’skokhozyaistvennaya biologiya [Agricultural Biology], 2015, 50(1): 3-15 CrossRef
  6. Kolomiets T.M., Malyarovskaya V.I., Gubaz S.L. Plodovodstvo i yagodovodstvo Rossii, 2015, 43: 99-103 (in Russ.).
  7. Malyarovskaya V.I. Subtropicheskoe i dekorativnoe sadovodstvo, 2012, 47(2): 161-167 (in Russ.).
  8. Samarina L.S. Optimizatsiya priemov mikrorazmnozheniya i sokhraneniya limona in vitro. Kandidatskaya dissertatsiya. Moskva, 2013 (in Russ.).
  9. Friesen M.L., Porter S.S., Stark S.C., von Wetteberg E.J., Sachs J.L., Martinez-Romero E. Microbially mediated plant functional traits. Annual Review of Ecology, Evolution, and Systematics, 2011, 42: 23-46 CrossRef
  10. Bulgarelli D., Schlaeppi K., Spaeten S., Ver Loren van Themaat E., Schulze-Lefert P. Structure and functions of the bacterial microbiota of plants. Annu. Rev. Plant Biol., 2013, 64: 807-838 CrossRef
  11. Jacobs S., Zechmann B., Molitor A., Trujillo M., Petutschnig E., Lipka V., Kogel K.-H., Schäfer P. Broad-spectrum suppression of innate immunity is required for colonization of Arabidopsis roots by the fungus Piriformospora indica. Plant Physiol., 2011, 156: 726-740 CrossRef
  12. Partida-Martínez L.P., Heil M. The microbe-free plant: fact or artifact? Front. Plant Sci., 2011, 2: 100 CrossRef
  13. Provorov N.A., Vorob'ev N.I. Ekologicheskaya genetika, 2013, 11(1): 12-22 (in Russ.).
  14. Brinkmann N., Marheine M., Heine-Dobbernack E., Verbarg S., Frühling A. Spröer C., Mohr K.I., Schumacher H.M. Investigation of latent bacterial infections in callus cultures reveal new Paenibacillus species. In: Endophytes for plant protection: the state of the art. Proc. 5th Int. Symp. «Endophytes for plant protection: the state of the art» (Humboldt University, Berlin, 26-29 May, 2013). C. Schneider, C. Leifert, F. Feldmann (eds.). Berlin-Dahlem, 2013: 10-11.
  15. Kolomiets T.M., Malyarovskaya V.I., Gvasaliya M.V., Samarina L.S., Sokolov R.N. Propagation in vitro of subtropical, ornamental crops and endemic species of western caucasus: developed and improved protocols. Sel’skokhozyaistvennaya biologiya [Agricultural Biology], 2014, 3: 49-58 CrossRef
  16. Qin S., Xing K., Jiang J.H., Xu L.H., Li W.J. Biodiversity, bioactive natural products and biotechnological potential of plant-associated endophytic actinobacteria. Appl. Microbiol. Biotechnol., 2011, 89(3): 457-473 CrossRef
  17. Nowak J. Benefits of in vitro «biotization» of plant tissue cultures with microbial inoculants. In Vitro Cell. Dev. Biol. — Plant, 1998, 34: 122-130 CrossRef
  18. Rai M.K. Current advances in mycorrhization in micropropagation. In Vitro Cell. Dev. Biol. — Plant, 2001, 37:158-167 CrossRef
  19. Kapoor R., Sharma D., Bhatnagar A.K. Arbuscular mycorrhizae in micropropagation systems and their potential applications. Science Horticulturae, 2008, 116: 227-239 CrossRef
  20. Jansa J., Vosatka M. In vitro and post vitro inoculation of micropropagated Rhododendrons with ericoid mycorrhizaln fungi. Appl. Soil Ecol., 2000, 15: 125-136 CrossRef
  21. Akello J., Dubois T., Gold C.S., Coyne D., Nakavuma J., Paparu P. Beauveria bassiana (Balsamo) Vuillemin as an endophyte in tissue culture banana (Musa spp.). J. Invertebr. Pathol., 2007, 96: 34-42 CrossRef
  22. Sharma P., Kharkwal A.C., Abdin M.Z., Varma A. Piriformospora indica improves micropropagation, growth and phytochemical content of Aloe vera L. plants. Symbiosis, 2014, 64: 11-23 CrossRef
  23. Ting A.S.Y., Meon S., Kadir J., Radu S., Singh G. Endophytic microorganisms as potential growth promoters of banana. BioControl, 2008, 53: 541-553 CrossRef
  24. Mucciarelli M., Scannerini S., Bertea C., Maffei M. In vitro and in vivo pepper-mint (Mentha piperita) growth promotion by nonmycorrhizal fungal colonization. New Phytologist, 2003, 158: 579-591 CrossRef
  25. Vohnik M., Lukancic S., Bahor E., Regvar M., Vosatka M., Vodnik D. Inoculation of Rhododendron cv. Belle-Heller with two strains of Phialocephala fortinii in two different substrates. Folia Geobotanica, 2003, 38: 191-200 CrossRef
  26. Franken P. The plant strengthening root endophyte Piriformospora indica: potential application and the biology behind. Appl. Microbiol. Biot., 2012, 96: 1455-1464 CrossRef
  27. Mayerhofer M.S., Kernaghan G., Harper K.A. The effects of fungal root endophytes on plant growth: a meta-analysis. Mycorrhiza, 2012, 23: 119-128 CrossRef
  28. Azlin C.O., Amir H.G., ChanLai K., Zamzuri I. Effect of plant growth-promoting rhizobacteria on root formation and growth of tissue cultured oil palm (Elaeis guineensis Jacq.). Biotechnology, 2007, 6: 549-554 CrossRef
  29. Benson A., Joe M.M., Karthikeyan B., Sa T., Rajasekaran C. Role of Achromobacter xylosoxidans AUM54 in micropropagation of endangered medicinal plant Naravelia zeylanica (L.) DC. J. Plant Growth Regul., 2014, 33: 202-213 CrossRef
  30. Larraburu E.E., Llorente B.E. Anatomical changes induced by Azospirillum brasilense in in vitro rooting of pink lapacho. Plant Cell Tiss. Organ Cult., 2015, 122: 175-184 CrossRef
  31. Larraburu E.E., Carletti S.M., Rodriguez Caceres E.A., Llorente B.E. Micropropagation of photinia employing rhizobacteria to promote root development. Plant Cell Rep., 2007, 26: 711-717 CrossRef
  32. Vestberg M., Kukkonen S., Saari K., Parikka P., Huttunen J., Tainio L., Devos N., Weekers F., Kevers C., Thonart P., Lemoine M.C., Cordier C., Alabouvette C., Gianinazzi S. Microbial inoculation for improving the growth and health of micropropagated strawberry. Appl. Soil Ecol., 2004, 27: 243-258 CrossRef
  33. Trivedi P., Pandey A. Biological hardening of micropropagated Picrorhiza kurrooa Royel ex Benth., an endangered species of medical importance. World Journal of Microbiology and Biotechnology, 2007, 23: 877-878 CrossRef
  34. Ait Barka E.A., Belarbi A., Hachet C., Nowak J., Audran J.C. Enhancement of in vitro growth and resistance to gray mould of Vitis vinifera co-cultured with plant growth-promoting rhizobacteria. FEMS Microbiol. Lett., 2000, 186: 91-95 CrossRef
  35. Govindarajan M., Balandreau J., Muthukumarasamy R., Revathi G., Lakshmina-Rasimhan C. Improved yield of micropropagated sugarcane following inoculation by endophytic Burkholderia vietnamiensis. Plant Soil, 2006, 280: 239-252 CrossRef
  36. Mirza M.S., Ahmad W., Latif F., Haurat J., Bally R., Normand P., Malik K.A. Isolation, partial characterization and the effect of plant growth-promoting bacteria (PGPB) on micropropagated sugarcane in vitro. Plant Soil, 2001, 237: 47-54 CrossRef
  37. Wei C.-Y., Lin L., Luo L.-J., Xing Y.-X., Hu C.-J., Yang L.-T., Li Y.-R., An Q. Endophytic nitrogen-fixing Klebsiella variicola strain DX120E promotes sugarcane growth. Biol. Fertil. Soils, 2014, 50: 657-666 CrossRef
  38. Quambusch M., Pirttila A.M., Tejesvi M.V., Winkelmann T., Bartsch M. Endophytic bacteria in plant tissue culture: differences between easy- and difficult-to-propagate Prunus avium genotypes. Tree Physiology, 2014, 34(5): 524-533 CrossRef
  39. Thomas J., Ajay D., Raj Kumar R., Mandal A.K.A. Influence of beneficial microorganisms during in vivo acclimatization of in vitro-derived tea (Camellia sinensis) plants. Plant Cell Tiss. Organ Cult., 2010, 101: 365-370 CrossRef
  40. Lifshitz R., Kloepper J.W., Kozlowski M., Simonson C., Carlson J., Tipping E.M., Zaleska I. Growth promotion of canola (rapeseed) seedlings by a strain of Pseudomonas putida under gnotobiotic conditions. Can. J. Microbiol., 1987, 33: 390-395 CrossRef
  41. Ovando-Medina I., Adriano-Anaya L., Chávez-Aguilar A., Oliva-Lla-ve A., Ayora-Talavera T., Dendooven L., Gutierrez-Miceli F., Salvador-Figueroa M. Ex vitro survival and early growth of Alpinia purpurata plantlets inoculated with Azotobacter and Azospirillum. Pakistan Journal of Biological Sciences, 2007, 10: 3454-3457 CrossRef
  42. Nowak J., Shulaev V. Priming for transplant stress resistance in in vitro propagation. In Vitro Cell. Dev. Biol. — Plant, 2003, 39: 107-124 CrossRef
  43. Harish S., Kavino M., Kumar N., Saravanakumar D., Soorianathasun-daram K., Samiyappan R. Biohardening with plant growth promoting rhizosphere and endophytic bacteria induces systemic resistance against Banana bunchy top virus. Appl. Soil Ecol., 2008, 39: 187-200 CrossRef
  44. Zabetakis I. Enhancement of flavour biosynthesis from strawberry (Fragaria x ananassa) callus cultures by Methylobacterium species. Plant Cell Tiss. Organ Cult., 1997, 50: 179-183 CrossRef
  45. Ortiz-Castro R., Contreras-Cornejo H., Macias-Rodriguez L., Lopez-Bucio J. The role of microbial signals in plant growth and development. Plant Signaling & Behavior, 2009, 4: 701-712 CrossRef
  46. Compant D., Duffy B., Nowak J., Clément C., Barka E.A. Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl. Environ. Microbiol., 2005, 71: 4951-4959 CrossRef
  47. Sziderics A.H., Rasche F., Trognitz F., Sessitsch A., Wilhelm E. Bacterial endophytes contribute to abiotic stress adaptation in pepper plants (Capsicum annuum L.). Can. J. Microbiol., 2007, 53: 1195-1202 CrossRef
  48. Lin L, Xu X.D. Indole-3-acetic acid production by endophytic Streptomyces sp. En-1 isolated from medicinal plants. Curr. Microbiol., 2013, 67(2): 209-217 CrossRef
  49. Igarashi Y. Screening of novel bioactive compounds from plant-associated actinomycetes. Actinomycetologica, 2004, 18: 63-66 CrossRef
  50. Rashad F.M., Fathy H.M., El-Zayat A.S., Elghonaimy A.M. Isolation and characterization of multifunctional Streptomyces species with antimicrobial, nematicidal and phytohormone activeiekhties from marine environments in Egypt. Microbiol. Res., 2015, 175: 34-47 CrossRef
  51. Sousa J., Olivares F.L. Plant growth promotion by streptomycetes: ecophysiology, mechanisms and applications. Chemical and Biological Technologies in Agriculture, 2016, 3: 24 CrossRef
  52. Normand L., Bärtschi H., Debaud J.C., Gay G. Rooting and acclimatization of  micropropagated  cuttings  of Pinus  pinaster and Pinus sylvestris are enhanced by the ectomycorrhizal fungus Hebeloma cylindrosporum. Physiologia Plantarum, 1996, 98: 759-766 CrossRef
  53. Oliveira P., Barriga J., Cavaleiro C., Peixe A., Potes A.Z. Sustained in vitro root development obtained in Pinus pinea L. inoculated with ectomycorrhizal fungi. Forestry, 2003, 76(5): 579-587 CrossRef
  54. Blaha D., Prigent-Combaret C., Mirza M.S., Moenne-Loccoz Y. Phylogeny of the 1-aminocyclopropane-1-carboxylic acid deaminase-encoding gene acdS in phytobeneficial and pathogenic Proteobacteria and relation with strain biogeography. FEMS Microbiol. Ecol., 2005, 56: 455-470 CrossRef
  55. Zawadzka M., Trzcinski P., Nowak K., Orlikowska T. The impact of three bacteria isolated from contaminated plant cultures on in vitro multiplication and rooting of microshoots of four ornamental plants. Journal of Horticultural Research, 2013, 21(2): 41-51 CrossRef
  56. Grotkass C., Hutter I., Feldmann F. Use of arbuscular mycorrhizal fungi to reduce weaning stress of micropropagated Baptisia tinctoria (L.) R. BR. Acta Hort. (ISHS), 2000, 530: 305-312.
  57. Barka E.A., Gognies S., Nowak J., Audran J.-C., Belarbi A. Inhibitory effect of endophytic bacteria on Botrytis cinerea and its influence to promote the grapevine growth. Biol.  Control, 2002, 24: 135-142 CrossRef
  58. Khaosaad T., García-Garrido J.M., Steinkellner S., Vierheilig H. Take-all disease is systemically reduced in roots of mycorrhizal barley plants. Soil Biol. Biochem., 2007, 39: 727-734 CrossRef
  59. Istifadah N., McGee P.A. Endophytic Chaetomium globosum reduces development of tan spot in wheat caused by Pyrenophora triticirepentis. Australasian Plant Pathology, 2006, 35: 411-418 CrossRef
  60. Koczwara K., Panka D., Jeske M, Musial N. Effect of Neotyphodium lolii on production of β-1,3-glucanases and chitinases in perennial ryegrass (Lolium perenne L.) infected by Fusarium poae. In: Endophytes for plant protection: the state of the art. Proc. 5th Int. Symp. «Endophytes for plant protection: the state of the art» (Humboldt University, Berlin, 26-29 May, 2013). C. Schneider, C. Leifert, F. Feldmann (eds.). Berlin-Dahlem, 2013: 123-124.
  61. Singh L.P., Gill S.S., Tuteja N. Unraveling the role of fungal symbionts in plant abiotic stress tolerance. Plant Signaling & Behavior, 2011, 6(2): 175-191 CrossRef
  62. Mohammad M.J., Malkawi H.I., Shibli R. Effects of arbuscular mycorrhizal fungi and phosphorus fertilization on growth and nutrient uptake of barley grown on soils with different levels of salts. J. Plant Nutr., 2011, 26: 125-137 CrossRef
  63. Evelin H., Kapoor R., Giri B. Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Annals of Botany, 2009, 104(7): 1263-1280 CrossRef
  64. Hardoim P.R., van Overbeek L.S., Berg G., Pirttilä A.M., Compant S., Campisano A., Döring M., Sessitsch A. The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol. Mol. Biol. Rev., 2015, 79: 293-320 CrossRef
  65. Abbamondi G.R., Tommonaro G., Weyens N., Thijs S., Sillen W., Gkorezis P., Iodice C., Rangel W.M., Nicolaus B., Vangronsveld J. Plant growth-promoting effects of rhizospheric and endophytic bacteria associated with different tomato cultivars andnew tomato hybrids. Chemical and Biological Technologies in Agriculture, 2016, 3(1): 1-10 CrossRef
  66. Bonaldi M., Chen X., Kunova A., Pizzatti C., Saracchi M., Cortesi P. Colonization of lettuce rhizosphere and roots by tagged Streptomyces. Front. Microbiol., 2015, 6: 25 CrossRef
  67. Francis I., Holsters M., Vereecke D. The Gram-positive side of plantmicrobe interactions. Environ. Microbiol., 2010, 12(1): 1-12 CrossRef
  68. Nebbioso A., De Martino A., Eltlbany N., Smalla K., Piccolo A. Phytochemical profiling of tomato roots following treatments with different microbial inoculants as revealed by IT-TOF mass spectrometry. Chemical and Biological Technologies in Agriculture, 2016, 3(1): 1-8 CrossRef
  69. Sessitsch A.1., Hardoim P., Döring J., Weilharter A., Krause A., Woyke T., Mitter B., Hauberg-Lotte L., Friedrich F., Rahalkar M., Hurek T., Sarkar A., Bodrossy L., van Overbeek L., Brar D., van Elsas J.D., Reinhold-Hurek B. Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol. Plant-Microbe Interact., 2012, 25: 28-36 CrossRef
  70. Bulgari D., Casati P., Crepaldi P., Daffonchio D., Quaglino F, Brusetti L., Bianco P.A.. Restructuring of endophytic bacterial communities in grapevine yellows-diseased and recovered Vitis vinifera L. plants. Appl. Environ. Microbiol., 2011, 77: 5018-5022 CrossRef
  71. Campisano A., Antonielli L., Pancher M., Yousaf S., Pindo M., Pertot I. Bacterial endophytic communities in the grapevine depend on pest management. PLoS ONE, 2014: 9(11): e112763 CrossRef
  72. Klocke E., Weinzierl K., Abel S. Occurrence of endophytes during Pelargonium protoplast culture. In: Endophytes for plant protection: the state of the art. Proc. 5th Int. Symp. «Endophytes for plant protection: the state of the art» (Humboldt University, Berlin, 26-29 May, 2013). C. Schneider, C. Leifert, F. Feldmann (eds.). Berlin-Dahlem, 2013: 94-99.

 

back