Abstract
Background
From the point of view of systems biology, the plant is considered a super organism that consists of the plant per se and numerous populations of pro- and eukaryotic microbial organisms. Each plant species hosts a genotype-specific core microbiome, dynamically responding to environmental cues, such as soil quality. In the plant endosphere, microbial organisms are an indispensable part of the information processing system, and the plant-endophyte interrelationships result in mutual adjustments through this system. Within the plant tissue, part of the microbiota resides in state called “viable but nonculturable”. Pathogen attack or environmental stress can provoke the dormant forms. The link between reviving of endophytic bacterial populations and plant disease resistance in the endosphere is discussed in this paper.
Scope and conclusions
The innate endophytic communities possess resistance-competent members, which can be in a latent state. The latent populations can be revived by an incoming microbial organism (e.g. a biocontrol agent or a pathogen), or other environmental factors. Reviving endophytic bacterial populations can be a putative mechanism of the endophyte-mediated plant resistance. Based on the published results, we suggest that the endophyte-mediated stress tolerance or disease resistance can develop, if the plant hosts a sufficient diversity of ‘protective’ endophytes. Alternatively, the plant can become susceptible upon loss of strategic members from endophytic microbial cohorts. Resident endophytes can be envisaged as a hidden reserve of plant protection to be used in green plant biotechnology. Selection of plant genotypes and soil type hosting beneficial microbiomes should become a common practice for improving plant resistance to complement advanced genetic technologies applied in plant biotechnology.
Similar content being viewed by others
References
Andreote FD, Gullo MJM, Lima AOS, Maccheroni JW, Azevedo JL, Araújo WL (2004) Impact of genetically modified Enterobacter cloacae on indigenous endophytic community of Citrus sinensis seedlings. J Microbiol 42:169–173
Andreote FD, de Araújo WL, de Azevedo JL, van Elsas JD, Da Rocha UN, van Overbeek LS (2009) Endophytic colonization of potato (Solanum tuberosum L.) by a novel competent bacterial endophyte, Pseudomonas putida strain P9, and its effect on associated bacterial communities. Appl Environ Microbiol 75:3396–3406
Andreote FD, Da Rocha UN, Araújo WL, Azevedo JL, van Overbeek LS (2010) Effect of bacterial inoculation, plant genotype and developmental stage on root-associated and endophytic bacterial communities in potato (Solanum tuberosum). Antonie Van Leeuwenhoek 97:389–399
Araújo WL, Marcon J, Maccheroni JW, van Elsas JD, van Vuurde JWL, Azevedo JL (2002) Diversity of endophytic bacterial populations and their interaction with Xylella fastidiosa in citrus plants. Appl Environ Microbiol 68:4906–4914
Ardanov Р, Lyastchenko S, Podolich O, Ryazantsev V, Zaets І, Kozyrovska N (2010) Use of endophytic bacteria for adaptation of in vitro-grown potato plants to ex vitro conditions and protection of planting material from phytopathogens. Science and Innovation 6:51–55
Ardanov P, Ovcharenko L, Zaets I, Kozyrovska N, Pirttilä AM (2011) Endophytic bacteria enhancing growth and disease resistance of potato (Solanum tuberosum L.). Biol Control 56:43–49
Ardanov P, Sessitsch A, Häggman H, Kozyrovska N, Pirttilä AM (2012) Methylobacterium-induced endophyte community changes correspond with protection of plants against pathogen attack. PLoS One 7:e46802
Balaban NQ, Merrin J, Chait R, Leibler S (2004) Bacterial persistence as a phenotypic switch. Science 305:1622–1625
Barber DA, Martin JK (1976) The release of organic substances by cereal roots into soil. New Phytol 76:69–80
Berg G, Krechel A, Ditz M, Sikora RA, Ulrich A, Hallmann J (2005) Endophytic and ectophytic potato‐associated bacterial communities differ in structure and antagonistic function against plant pathogenic fungi. FEMS Microbiol Ecol 51:215–229
Bodenhausen N, Horton MW, Bergelson J (2013) Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLoS One 8:e56329
Brader G, Compant S, Mitter B, Trognitz F, Sessitsch A (2014) Metabolic potential of endophytic bacteria. Curr Opin Biotechnol 27:30–37
Bulgarelli D, Rott M, Schlaeppi K, Ver Loren E, van Themaat N, Ahmadinejad FA, Rauf P, Huettel B, Reinhardt R, Schmelzer E, Peplies J, Gloeckner FO, Amann R, Eickhorst T, Schulze-Lefert P (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 487:91–95
Busch W, Benfey PN (2010) Information processing without brains - the power of intercellular regulators in plants. Development 137:1215–1226
Choudhary DK, Johri BN (2009) Interactions of Bacillus spp. and plants - with special reference to induced systemic resistance (ISR). Microbiol Res 164:493–513
Cichewicz RH (2010) Epigenome manipulation as a pathway to new natural product scaffolds and their congeners. Nat Prod Rep 27:11–22
Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678
Conn VM, Franco CMM (2004) Effect of microbial inoculants on the indigenous actinobacterial endophyte population in the roots of wheat as determined by terminal restriction fragment length polymorphism. Appl Environ Microbiol 70:6407–6413
Conn VM, Walker AR, Franco CMM (2008) Endophytic actinobacteria induce defense pathways in Arabidopsis thaliana. Mol Plant Microbe Interact 21:208–218
Da K, Nowak J, Flinn B (2012) Potato cytosine methylation and gene expression changes induced by a beneficial bacterial endophyte, Burkholderia phytofirmans strain PsJN. Plant Physiol Biochem 50:24–34
de Oliveira Costa LE, de Queiroz MV, Borges AC, de Moraes CA, de Araújo EF (2012) Isolation and characterization of endophytic bacteria isolated from the leaves of the common bean (Phaseolus vulgaris). Braz J Microbiol 43:1562–1575
Deng Y, Zhu Y, Wang P, Zhu L, Zheng J, Li R, Ruan L, Peng D, Sun M (2011) Complete genome sequence of Bacillus subtilis BSn5, an endophytic bacterium of Amorphophallus konjac with antimicrobial activity for the plant pathogen Erwinia carotovora subsp. carotovora. J Bacteriol 193:2070–2071. doi:10.1128/JB.00129-11
Ding S, Huang CL, Sheng HM, Song CL, Li YB (2011) An effect of inoculation with the endophyte Clavibacter sp. strain Enf12 on chilling tolerance in Chorispora bungeana. Physiol Plant 141:141–151
Fouts DE, Tyler HL, DeBoy RT, Daugherty S, Ren Q, Badger JH, Durkin AS, Huot H, Shrivastava S, Kothari S, Dodson RJ, Mohamoud Y, Khouri H, Roesch LF, Krogfelt KA, Struve C, Triplett EW, Methe BA (2008) Complete genome sequence of the N2-fixing broad host range endophyte Klebsiella pneumoniae 342 and virulence predictions verified in mice. PLoS Genet 4:e1000141
Friesen M (2011) Microbially mediated plant functional traits. Annu Rev Ecol Evol Syst 42:23–46
Gaca AC, JK Kajfasz, JH Miller, K Liu, JD Wang, J Abranches, JA Lemos (2013) Basal levels of (p) ppGpp in Enterococcus faecalis: the magic beyond the stringent response. mBio 4:e00646-13
Gaiero JR, McCall CA, Thompson KA, Day NJ, Best AS, Dunfield KE (2013) Inside the root microbiome: bacterial root endophytes and plant growth promotion. Am J Bot 100:1738–1750
Garbeva P, van Overbeek LS, van Vuurde JWL, van Elsas JD (2001) Analysis of endophytic bacterial communities of potato by plating and denaturing gradient gel electrophoresis (DGGE) of 16S rDNA based PCR fragments. Microb Ecol 41:369–383
Goh C-H, Veliz Vallejos DF, Nicotra AB, Mathesius U (2013) The impact of beneficial plant-associated microbes on plant phenotypic plasticity. J Chem Ecol 39:826–839
Han JI, Choi HK, Lee SW, Orwin PM, Kim J, Laroe SL, Kim TG, O’Neil J, Leadbetter JR, Lee SY, Hur CG, Spain JC, Ovchinnikova G, Goodwin L, Han C (2011) Complete genome sequence of the metabolically versatile plant growth-promoting endophyte, Variovorax paradoxus S110. J Bacteriol 193:1183–1190
Hardoim PR, Andreote FD, Reinhold-Hurek B, Sessitsch A, van Overbeek LS, van Elsas JD (2011) Rice root‐associated bacteria: insights into community structures across 10 cultivars. FEMS Microbiol Ecol 77:154–164
Hardoim P, R Nissinen, JD van Elsas (2012) Ecology of bacterial endophytes in sustainable agriculture. Pages 97–126 in. Bacteria in Agrobiology: Plant Probiotics (Maheshwari, D.K., ed.), Springer Berlin Heidelberg
Högberg P, Högberg MN, Göttlicher SG, Betson NR, Keel SG, Metcalfe DB, Campbell C, Schindlbacher A, Hurry V, Lundmark T, Linder S, Näsholm T (2008) High temporal resolution tracing of photosynthate carbon from the tree canopy to forest soil microorganisms. New Phytol 177:220–228
Hosni T, Moretti C, Devescovi G, Suarez-Moreno ZR, Fatmi MB, Guarnaccia C, Pongor S, Onofri A, Buonaurio R, Venturi V (2011) Sharing of quorum-sensing signals and role of interspecies communities in a bacterial plant disease. ISME J 5:1857–1870
Howitz KT, Sinclair DA (2008) Xenohormesis: sensing the chemical cues of other species. Cell 133:387–391
Jayaraman R (2008) Bacterial persistence: some new insights into an old phenomenon. J Biosci 307:795–805
Johnston-Monje D, Raizada MN (2011) Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology. PLoS One 6:e20396
Kehr J, Buhtz A (2008) Long distance transport and movement of RNA through the phloem. J Exp Bot 59:85–92
Kirby J, Keasling D (2009) Biosynthesis of plant isoprenoids: perspectives for microbial engineering. Annu Rev Plant Biol 60:335–355
Koskimäki JJ, Hankala E, Suorsa M, Nylund S, Pirttilä AM (2010) Mycobacteria are hidden endophytes in the shoots of rock plant [Pogonatherum paniceum (Lam.) Hack.] (Poaceae). Env Microbiol Rep 2:619–624
Kozyrovska NO (2013) Crosstalk between endophytes and a plant host within information-processing networks. Biopolym Cell 29:234–243
Krings M, Taylor TN, Hass H, Kerp H, Dotzler N, Hermsen EJ (2007) Fungal endophytes in a 400-million-yr-old land plant: infection pathways, spatial distribution, and host responses. New Phytol 174:648–657
Kusari S, Hertweck C, Spiteller M (2012) Chemical ecology of endophytic fungi: origins of secondary metabolites. Chem Biol 19:792–798
Lacava PT, Araújo WL, Marcon J, WJr M, Azevedo JL (2004) Interaction between endophytic bacteria from citrus plants and the phytopathogenic bacteria Xylella fastidiosa, causal agent of citrus-variegated chlorosis. Lett Appl Microbiol 39:55–59
Lewis K (2010) Persister cells. Annu Rev Microbiol 64:357–372
Lian J, Wang Z, Zhou S (2008) Response of endophytic bacterial communities in banana tissue culture plantlets to Fusarium wilt pathogen infection. J Gen Appl Microbiol 54:83–92
Likar M (2011) Dark Septate Endophytes and Mycorrhizal Fungi of Trees Affected by Pollution. In: AM Pirttila and AC Frank (eds.), Endophytes of Forest Trees: Biology and Applications, Forestry Sciences 80, pp 189–201
Liu WY, Chung KM, Wong CF, Jiang JW, Hui RK, Leung FC (2012) Complete genome sequence of the endophytic Enterobacter cloacae subsp. cloacae strain ENHKU01. J Bacteriol 194:5965–5965. doi:10.1128/JB.01394-12
Liu W, Yuan JS, Stewart CN Jr (2013) Advanced genetic tools for plant biotechnology. Nature Rev Genet 4:781–793
López-López A, Rogel MA, Ormeño-Orrillo E, Martínez-Romero J, Martínez-Romero E (2010) Phaseolus vulgaris seed-borne endophytic community with novel bacterial species such as Rhizobium endophyticum sp. nov. Syst Appl Microbiol 33:322–327
Lucero ME, Unc A, Cooke P, Dowd S, Sun S (2011) Endophyte microbiome diversity in micropropagated Atriplex canescens and Atriplex torreyi var griffithsii. PLoS One 6:e17693
Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, Rio TGD, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 487:86–90
Madhaiyan M, Suresh Reddy BV, Anandham R, Senthilkumar M, Poonguzhali S, Sundaram SP, Sa T (2006) Plant growth-promoting Methylobacterium induces defence responses in groundnut (Arachis hypogeea L.) compared with rot pathogens. Curr Genet 53:270–276
Malfanova N, Kamilova F, Validov S, Chebotar V, Lugtenberg B (2013) Is L-arabinose important for the endophytic lifestyle of Pseudomonas spp.? Arch Microbiol 195:9–17
Manter DK, Delgado JA, Holm DG, Stong RA (2010) Pyrosequencing reveals a highly diverse and cultivar-specific bacterial endophyte community in potato roots. Microb Ecol 60:157–166
Muñoz Bodnar A, Bernal A, Szurek B, López CE (2012) Tell me a tale of TALEs. Mol Biotechnol 53:228–235
Muranaka LS, Takita MA, Olivato JC, Kishi LT, de Souza AA (2012) Global expression profile of biofilm resistance to antimicrobial compounds in the plant-pathogenic bacterium Xylella fastidiosa reveals evidence of persister cells. J Bacteriol 194:4561–4569
Nielsen ME, Feechan A, Böhlenius H, Ueda T, Thordal-Christensen H (2012) Arabidopsis ARF-GTP exchange factor, GNOM, mediates transport required for innate immunity and focal accumulation of syntaxin PEN1. Proc Natl Acad Sci U S A 109:11443–11448
Nützmann HW, Reyes-Dominguez Y, Scherlach K, Schroeckh V, Horn F, Gacek A, Schümann J, Hertweck C, Strauss J, Brakhage AA (2011) Bacteria-induced natural product formation in the fungus Aspergillus nidulans requires Saga/Ada-mediated histone acetylation. Proc Natl Acad Sci U S A 108:14282–14287
Oliver JD (2005) The viable but nonculturable state in bacteria. J Microbiol 43:93–100
Oliver JD (2010) Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS Microbiol Rev 34:415–425
Pedrosa FO, Monteiro RA, Wassem R, Cruz LM, Ayub RA, Colauto NB, Fernandez MA, Fungaro MHP, Grisard EC (2011) Genome of Herbaspirillum seropedicae strain SmR1, a specialized diazotrophic endophyte of tropical grasses. PLoS Genet 7:e1002064
Peng A, Liu J, Gao Y, Chen Z (2013) Distribution of endophytic bacteria in Alopecurus aequalis Sobol and Oxalis corniculata L. from soils contaminated by polycyclic aromatic hydrocarbons. PLoS One 8:e83054
Pirttilä AM, Laukkanen H, Hohtola A (2002) Chitinase production in callus of pine (Pinus sylvestris L.): a defense reaction against endophytes? Planta 214:848–852
Pirttilä AM, Joensuu P, Pospiech H, Jalonen J, Hohtola A (2004) Bud endophytes of Scots pine produce adenine derivatives and other compounds that affect morphology and mitigate browning of callus cultures. Physiol Plant 121:305–312
Pirttilä AM, Pospiech H, Laukkanen H, Myllylä R, Hohtola A (2005) Seasonal variations in location and population structure of endophytes in buds of Scots pine. Tree Physiol 25:289–297
Podolich O, Ardanov P, Voznyuk T, Kovalchuk M, Danylchenko O, Laschevskyi V, Lyastchenko S, Kozyrovska N (2007) Endophytic bacteria from potato in vitro activated by exogenic non-pathogenic bacteria. Biopolym Cell 23:21–27
Podolich O, Laschevskyy V, Ovcharenko L, Kozyrovska N, Pirttilä AM (2009) Methylobacterium sp. resides in unculturable state in potato tissues in vitro and becomes culturable after induction by Pseudomonas fluorescens IMGB163. J Appl Microbiol 106:728–737
Potrykus K, Cashel M (2008) (p) ppGpp: still magical? Annu Rev Microbiol 62:35–51
Procópio REL, Araújo WL, JrW M, Azevedo JL (2009) Characterization of an endophytic bacterial community associated with Eucalyptus spp. Genet Mol Res 8:1408–1422
Puspita ID, Kamagata Y, Tanaka M, Asano K, Nakatsu CH (2012) Are uncultivated bacteria really uncultivable? Microbes Environ 27:356–366
Reiter B, Pfeifer U, Schwab H, Sessitsch A (2002) Response of endophytic bacterial communities in potato plants to infection with Erwinia carotovora subsp. atroseptica. Appl Environ Microbiol 68:2261–2268
Rodriguez RJ, White JF, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330
Rosenblueth M, Martinez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant Microbe Interact 19:827–837
Seghers D, Wittebolle L, Top EM, Verstraete W, Siciliano SD (2004) Impact of agricultural practices on the Zea mays L. endophytic community. Appl Environ Microbiol 70:1475–1482
Sessitsch A, Reiter B, Pfeifer U, Wilhelm E (2002) Cultivation-independent population analysis of bacterial endophytes in three potato varieties based on eubacterial and Actinomycetes-specific PCR of 16S rRNA genes. FEMS Microbiol Ecol 39:23–32
Sessitsch A, Reiter B, Berg G (2004) Endophytic bacterial communities of field-grown potato plants and their plant-growth-promoting and antagonistic abilities. Can J Microbiol 50:239–249
Sessitsch A, 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 JD, Reinhold-Hurek B (2012) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant Microbe Interact 25:28–36
Shapiro JA (2010) Mobile DNA and evolution in the 21st century. Mob DNA 1:4–18
Shi J, Liu A, Li X, Feng S, Chen W (2011) Inhibitory mechanisms induced by the endophytic bacterium MGY2 in controlling anthracnose of papaya. Biol Control 56:2–8
Taghavi S, van der Lelie D, Hoffman A, Zhang YB, Walla MD, Vangronsveld J, Newman L, Monchy S (2010) Genome sequence of the plant growth promoting endophytic bacterium Enterobacter sp. 638. PLoS Genet 6:e1000943
Taghavi S, Weyens N, Vangronsveld J, van der Lelie D (2011) Improved phytoremediation of organic contaminants through egineering of bacterial endophytes of trees. Endophytes of Forest Trees Forestry Sciences 80:205–216
Tejesvi MV, Ruotsalainen AL, Markkola AM, Pirttilä AM (2010) Root endophytes along a primary succession gradient in northern Finland. Fungal Divers 41:125–134
Thomas P, Swarna GK, Patil P, Rawal RD (2008) Ubiquitous presence of normally non-culturable endophytic bacteria in field shoot-tips of banana and their gradual activation to quiescent cultivable form in tissue cultures. Plant Cell Tissue Organ Cult 93:39–54
Thomas T, Gilbert J, Meyer F (2012) Metagenomics - a guide from sampling to data analysis. Microbial Informat Experiment 2:3
Viñas M, Sabaté J, José M, Solanas AM (2005) Bacterial community dynamics and polycyclic aromatic hydrocarbon degradation during bioremediation of heavily creosote-contaminated soil. Appl Environ Microbiol 71:7008–7018
Wilson D (1995) Endophyte — the evolution of a term, and clarification of its use and definition. Oikos 73:274–276
Wood TK, SJ Knabel, TK Kwan (2013) Bacterial persister cell formation and dormancy. Appl Environ Microbiol, published online ahead of print, doi:10.1128/AEM.02636-13
Zaets I, Kozyrovska N (2012) Heavy metal resistance in plants: a putative role of endophytic bacteria. In: Zaidi A et al (eds) Toxicity of heavy metals to legumes and bioremediation. Springer-Verlag, Wien, pp 203–217
Zaets I, Kramarev S, Kozyrovska N (2010) Inoculation with a bacterial consortium alleviates the effect of cadmium overdose in soybean plants. Centr Eur J Biol 5:481–490
Zamioudis C, Pieterse CMJ (2012) Modulation of host immunity by beneficial microbes. Mol Plant Microbe Interact 25:139–150
Zhang H, Xie X, Kim MS, Kornyeyev DA, Holaday S, Paré PW (2008) Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. Plant J 56:264–273
Acknowledgments
We thank Mr. O. Burlak for cooperation in research on persisters, Dr. Pious Thomas (Indian Institute of Horticultural Research) and anonymous reviewers for a critical reading of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Choong-Min Ryu..
Rights and permissions
About this article
Cite this article
Podolich, O., Ardanov, P., Zaets, I. et al. Reviving of the endophytic bacterial community as a putative mechanism of plant resistance. Plant Soil 388, 367–377 (2015). https://doi.org/10.1007/s11104-014-2235-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-014-2235-1