Biopolym. Cell. 2013; 29(3):234-243.
Reviews
Crosstalk between endophytes and a plant host within information-processing networks
1Kozyrovska N. O.
  1. Institute of Molecular Biology and Genetics, NAS of Ukraine
    150, Akademika Zabolotnoho Str., Kyiv, Ukraine, 03680

Abstract

Plants are heavily populated by pro- and eukaryotic microorganisms and represent therefore the tremendous complexity as a biological system. This system exists as an information-processing entity with rather complex processes of communication, occurring throughout the individual plant. The plant cellular information-processing network constitutes the foundation for processes like growth, defense, and adaptation to the environment. Up to date, the molecular mechanisms, underlying perception, transfer, analysis, and storage of the endogenous and environmental information within the plant, remain to be fully understood. The associated microorganisms and their investment in the information conditioning are often ignored. Endophytes as plant partners are indispensable integrative part of the plant system. Diverse endophytic microorganisms comprise «normal» microbiota that plays a role in plant immunity and helps the plant system to survive in the environment (providing assistance in defense, nutrition, detoxification etc.). The role of endophytic microbiota in the processing of information may be presumed, taking into account a plant-microbial co-evolution and empirical data. Since the literature are beginning to emerge on this topic, in this article, I review key works in the field of plant-endophytes interactions in the context of information processing and represent the opinion on their putative role in plant information web under defense and the adaptation to changed conditions.
Keywords: a plant system, endophytes, information processing, plant defense, adaptation

Supplementary data

References

[1] Friesen M., Porter S. S., Stark S. C. et al Microbially mediated plant functional traits Annu. Rev. Ecol. Evol. Syst 2011 42:23–46.
[2] Lundberg D. S., Lebeis S. L., Paredes S. H. et al. Defining the core Arabidopsis thaliana root microbiome Nature 2012 488, N 7409:86–90.
[3] Bodenhausen N., Horton M. W., Bergelson J. Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana PLoS One 2013 8, N 2 e56329.
[4] Johnston-Monje D., Raizada M. N. Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology PLoS One 2011 6, N 6 e20396.
[5] Hardoim P. R., Andreote F. D., Reinhold-Hurek B. et al. Rice root-associated bacteria: insights into community structures across 10 cultivars FEMS Microbiol. Ecol 2011 77, N 1:154–164.
[6] Bulgarelli D., Rott M., Schlaeppi K. et al. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota Nature 2012 488, N 7409:91–95.
[7] Nadell C. D., Xavier J. B., Foster K. R. The sociobiology of biofilms FEMS Microbiol. Rev 2009 33, N 1:206–224.
[8] Rosenblueth M., Martinez-Romero E. Bacterial endophytes and their interactions with hosts Mol. Plant-Microbe Interact 2006 19, N 8:827–837.
[9] Porras-Alfaro A., Bayman P. Hidden fungi, emergent properties: endophytes and microbiomes Ann. Rev. Phytopathol 2011 49:291–315.
[10] Podolich O., Laschevskyy V., Ovcharenko L. et al. Methylobacterium sp. resides in unculturable state in potato tissues in vitro and becomes culturable after induction by Pseudomonas fluorescens IMGB163 J. Appl. Microbiol. –2009 106, N 3:728–737.
[11] Jumpponen A., Jones K. L. Massively parallel 454 sequencing indicates hyperdiverse fungal communities in temperate Quercus macrocarpa phyllosphere New Phytol 2009 184, N 2:438–448.
[12] Ardanov P., Sessitsch A., Haggman H. et al. Methylobacteriuminduced endophyte community changes correspond with protection of plants against pathogen attack PLoS ONE–2012 7, N 10 e46802.
[13] Kirby J., Keasling D. Biosynthesis of plant isoprenoids: Perspectives for microbial engineering Annu. Rev. Plant Biol 2009 60:335–355.
[14] Howitz K. T., Sinclair D. A. Xenohormesis: sensing the chemical cues of other species Cell 2008 133, N 3:387–391.
[15] Zhou X., Zhu H., Liu L. et al. A review: recent advances and future prospects of taxol-producing endophytic fungi Appl. Microbiol. Biotechnol 2010 86, N 6 P.1707–1717.
[16] Fouts D. E., Tyler H. L., DeBoy R. T. et al. Complete genome sequence of the N2-fixing broad host range endophyte Klebsiella pneumoniae 342 and virulence predictions verified in mice PLoS Genet–2008 4, N 7 e1000141.
[17] Han J.-I., Choi H.-K., Lee S. W. et al. Complete genome sequence of the metabolically versatile plant growth-promoting endophyte, Variovorax paradoxus S110 J. Bacteriol 2011 193, N 5:1183–1190.
[18] Reiter B., Pfeifer U., Schwab H., Sessitsch A. Response of endophytic bacterial communities in potato plants to infection with Erwinia carotovora subsp. atroseptica Appl. Environ. Microbiol 2002 68, N 5:2261–2268.
[19] Andreote F. D., Lacava P. T., Gai C. S. et al. Model plants for studying the interaction between Methylobacterium mesophilicum and Xylella fastidiosa Can. J. Microbiol 2006 52, N 5:419–426.
[20] Podolich O. V., Lytvynenko T., Voznyuk T. M. et al. Detection of endophytic bacteria communities in aseptic potato plants after inoculation with Pseudomonas sp. IMBG163 Proc. Uzhgorod State Univ 2006 N 18:165–170.
[21] Thomas P., Swarna G. K., Patil P., Rawal R. D. 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 Tiss. Org. Cult 2008 93, N 1:39–54.
[22] Andreote F. D., de Araurjo W. D., de Azevedo J. L. et al. 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 2009 75, N 11:3396–3406.
[23] Lian J., Wang Z., Zhou S. Response of endophytic bacterial communities in banana tissue culture plantlets to Fusarium wilt pathogen infection J. Gen. Appl. Microbiol 2008 54, N 2:83–92.
[24] Conn V. M., Walker A. R., Franco C. M. Endophytic actinobacteria induce defense pathways in Arabidopsis thaliana Mol. Plant-Microbe Interact 2008 21, N 2:208–218.
[25] Barlow P. W. Reflections on «plant neurobiology» BioSystems 2008 92, N 2:132–147.
[26] Oyarce P., Gurovich L. Evidence for the transmission of information through electric potentials in injured avocado trees J. Plant Physiol 2011 168, N 2:103–108.
[27] Busch W., Benfey P. N. Information processing without brains – the power of intercellular regulators in plants Development 2010 137:1215–1226.
[28] Hauser M. T., Aufsatz W., Jonak C., Luschnig C. Transgenerational epigenetic inheritance in plants Biochim. Biophys. Acta 2011 1809, N 8:459-468.
[29] Stock A. M., Robinson V. L., Goudreau P. N. Two-component signal transduction Annu. Rev. Biochem 2000 69:183–215.
[30] Antolin-Llovera M., Ried M. K., Binder A., Parniske M. Receptor kinase signaling pathways in plant-microbe interactions Annu. Rev. Phytopathol 2012 50:451–473.
[31] Belyavskaya N. O., Kozyrovskaya N. O., Kucherenko L. O., Kordyum E. L., Kordyum V. A. Interrelations of the Klebsiella genus with the plant. 1. Electron microscopic analysis of endophytic microorganisms interrelationship with rice seedlings roots Biopolym. Cell 1995 11, N 1:55–60.
[32] Thomas P., Reddy K. Microscopic elucidation of abundant endophytic bacteria colonizing the cell wall – plasma membrane peri-space in the shoot-tip tissue of banana AoB Plants 2013; 5 : plt011
[33] Wuichet K., Cantwell B. J., Zhulin I. B. Evolution and phyletic distribution of two-component signal transduction systems Curr. Opin. Microbiol 2010 13, N 2:219–225.
[34] Morey K. J., Antunes M. S., Albrecht K. D. et al. Developing a synthetic signal transduction system in plants Methods Enzymol 2011 497:581–602.
[35] Giska F., Lichocka M., Piechocki M. et al. Phosphorylation of HopQ1, a type III effector from Pseudomonas syringae, creates a binding site for host 14-3-3 proteins Plant Physiol 2013 161, N 4:2049–2061.
[36] Nissan G., Manulis-Sasson S., Weinthal D. et al. The type III effectors HsvG and HsvB of gall-forming Pantoea agglomerans determine host specificity and function as transcriptional activators Mol. Microbiol 2006 61, N 5:1118–1131.
[37] Bauer W. D., Mathesius U. Plant responses to bacterial quorum sensing signals Curr. Opin. Plant Biol 2004 7, N 4:429–433.
[38] Durot M., Bourguignon P. Y., Schachter V. Genome-scale models of bacterial metabolism: reconstruction and applications FEMS Microbiol. Rev 2009 33, N 1:164–190.
[39] Bishopp A., Mahonen A. P., Helariutta Y. Signs of change: hormone receptors that regulate plant development Development 2006 133:1857–1869.
[40] Wasson A. P., Pellerone F. I., Mathesius U. Silencing the flavonoid pathway in Medicago truncatula inhibits root nodule formation and prevents auxin transport regulation by rhizobia Plant Cell 2006 18, N 7:1617–1629.
[41] Navarro L., Dunoyer P., Jay F. et al. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling Science 2006 312, N 5772:436–439.
[42] Zhang W., Gao S., Zhou X. et al. Bacteria-responsive microRNAs regulate plant innate immunity by modulating plant hormone networks Plant Mol. Biol 2011 75, N 1–2:93–105.
[43] Hartmann A., Schikora A. Quorum sensing of bacteria and transkingdom interactions of N-acyl homoserine lactones with eukaryotes J. Chem. Ecol 2012 38, N 6:704–713.
[44] Zuciga A., Poupin M. J., Donoso R. A. et al. Quorum sensing and 3-indole acetic acid degradation play a role in colonization and plant growth promotion of Arabidopsis thaliana by Burkholderia phytofirmans PsJN Mol. Plant-Microbe Interact 2013 26, N 5:546–553.
[45] Sessitsch A., Hardoim P., During J. et al. Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis Mol. Plant-Microbe Interact 2012 25, N 1:28–36.
[46] Rezzonico F., Smits T. H., Duffy B. Detection of AI-2 receptors in genomes of Enterobacteriaceae suggests a role of type-2 quorum sensing in closed ecosystems Sensors 2012 12, N 5:6645–6665.
[47] Hauberg-Lotte L., Klingenberg H., Scharf C. et al. Environmental factors affecting the expression of pilAB as well as the proteome and transcriptome of the grass endophyte Azoarcus sp. strain BH72 PLoS ONE 2012 7, N 1 e30421.
[48] Trognitz F., Scherwinski K., Fekete A. et al. Interaction between potato and the endophyte Burkholderia phytofirmans Tagung 59 der Vereinigung der Pfl Anzenzuchter und Saatgutkaufleute Osterreichs Raumberg-Gumpenstein, 2008:63–66.
[49] Hosni T., Moretti C., Devescovi G. et al. Sharing of quorum-sensing signals and role of interspecies communities in a bacterial plant disease ISME J 2011 5, N 12:1857–1870.
[50] Garbeva P., van Overbeek L. S., van Vuurde J. W. L., van Elsas J. D. Analysis of endophytic bacterial communities of potato by plating and denaturing gradient gel electrophoresis (DGGE) of 16S rDNA based PCR fragments Microb. Ecol 2001 41, N 4:369–383.
[51] Podolich O. V., Ardanov P. E., Voznyuk T. M. et al. Endophytic bacteria from potato in vitro activated by exogenic non-pathogenic bacteria Biopolym. Cell 2007 23, N 1:21–27.
[52] Koskimaki J. J., Hankala E., Suorsa M. et al. Mycobacteria are hidden endophytes in the shoots of rock plant [Pogonatherum paniceum (Lam.) Hack.] (Poaceae) Environ. Microbiol. Rep 2010 2, N 4:619–624.
[53] Manter D. K., Delgado J. A., Holm D. G., Stong R. A. Pyrosequencing reveals a highly diverse and cultivar-specific bacterial endophyte community in potato roots Microb. Ecol 2010 60, N 1:157–166.
[54] Lucero M. E., Unc A., Cooke P. et al. Endophyte microbiome diversity in micropropagated Atriplex canescens and Atriplex torreyi var griffithsii PLoS ONE–2011 6, N 3 e17693.
[55] Stokell J. R., Steck T. R. Viable but nonculturable bacteria eLS Chichester: John Wiley & Sons, Ltd., 2012
[56] Hong S. H., Wang X., O'Connor H. F. et al. Bacterial persistence increases as environmental fitness decreases Microb. Biotechnol 2012 5, N 4:509–522.
[57] Puspita I. D., Kamagata Y., Tanaka M. et al. Are uncultivated bacteria really uncultivable? Microbes Environ 2012 27, N 4:356–366.
[58] Ravagnani A., Finan C. L., Young M. A novel firmicute protein family related to the actinobacterial resuscitation-promoting factors by non-orthologous domain displacement BMC Genomics 2005 6:39.
[59] Puspita I. D., Uehara M., Katayama T. et al. Resuscitation promoting factor (Rpf) from Tomitella biformata AHU 1821(T) promotes growth and resuscitates non-dividing cells Microbes Environ 2013 28, N 1:58–64.
[60] Egener T., Hurek T., Reinhold-Hurek B. Endophytic expression of nif genes of Azoarcus sp. strain BH72 in rice roots Mol. Plant-Microbe Interact 1999 12, N 9:813–819.
[61] Kovtunovych G., Kovalchuk M., Lar O. et al. Use of the gusAand lux-reporter genes in monitoring plant-bacteria interactions Prospects and applications for plant-associated microbe: A laboratory manual part A: Bacteria / Eds S. Sovari, A. M. Pirttila Turku, 2008:214–218.
[62] Cordeiro F. A., Tadra-Sfeir M. Z., Huergo L. F. et al. Proteomic analysis of Herbaspirillum seropedicae cultivated in the presence of sugar cane extract J. Proteome Res 2013 12, N 3:1142–1150.
[63] Muranaka L. S., Takita M. A., Olivato J. C. et al. Global expression profile of biofilm resistance to antimicrobial compounds in the plant-pathogenic bacterium Xylella fastidiosa reveals evidence of persister cells J. Bacteriol 2012 194, N 17:4561– 4569.
[64] Schuster C. F., Bertram R. Toxin-antitoxin systems are ubiquitous and versatile modulators of prokaryotic cell fate FEMS Microbiol. Lett 2013 340, N 2:73–85.
[65] Pandey D. P., Gerdes K. Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes Nucleic Acids Res 2005 33, N 3:966–976.
[66] Taghavi S., van der Lelie D., Hoffman A. et al. Genome sequence of the plant growth promoting endophytic bacterium Enterobacter sp. 638 PLoS Genet–2010 6, N 5 e1000943.
[67] Pedrosa F. O., Monteiro R. A., Wassem R. et al. Genome of Herbaspirillum seropedicae strain SmR1, a specialized diazotrophic endophyte of tropical grasses PLoS Genet 2011 7, N 5 e1002064.
[68] Mirouze M., Paszkowski J. Epigenetic contribution to stress adaptation in plants Curr. Opin. Plant Biol 2011 14, N 3:267–274.
[69] Mathieu O., Reinders J., Caikovski M. et al. Transgenerational stability of the Arabidopsis epigenome is coordinated by CG methylation Cell 2007 130, N 5:851–862.
[70] Ardanov P., Liaschenko S., Podolich O. et al. The use of endophytic bacteria for adaptation of potato plants in vitro to ex vitro conditions for the protection of planting material from pathogens Science and Innovations 2010–6, N 6:51–55.
[71] Slaughter A., Daniel X., Flors V. et al. Descendants of primed Arabidopsis plants exhibit resistance to biotic stress Plant Physiol 2012 158, N 2:835–843.
[72] Ni M., Decrulle A. L., Fontaine F. et al. Pre-disposition and epigenetics govern variation in bacterial survival upon stress PLoS Genet–2012 8, N 12 e1003148.
[73] Alvarez M. E., Nota F., Cambiagno D. A. Epigenetic control of plant immunity Mol. Plant Pathol 2010 11, N 4:563–576.
[74] Molinier J., Ries G., Zipfel C., Hohn B. Transgeneration memory of stress in plants Nature 2006 442, N 7106:1046–1049.
[75] Yu A., Lepurea G., Jayb F. et al. Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense Proc. Natl Acad. Sci. USA 2013 110, N 6:2389–2394.
[76] Dowen R. H., Pelizzola M., Schmitz R. J. et al. Widespread dynamic DNA methylation in response to biotic stress Proc. Natl Acad. Sci. USA 2012 109, N 32 E2183–E2191.
[77] Luna E., Bruce T. J., Roberts M. R.et al. Next-generation systemic acquired resistance Plant Physiol 2012 158, N 2:844–853.
[78] Migicovsky Z., Kovalchuk I. Changes to DNA methylation and homologous recombination frequency in the progeny of stressed plants Biochem. Cell Biol 2013 91, N 1:1–5.
[79] Da K., Nowak J., Flinn B. Potato cytosine methylation and gene expression changes induced by a beneficial bacterial endophyte, Burkholderia phytofirmans strain PsJN Plant Physiol. Biochem 2012 50, N 1:24–34.
[80] Cichewicz R. H. Epigenome manipulation as a pathway to new natural product scaffolds and their congeners Nat. Prod. Rep 2010 27, N 1:11–22.
[81] Nutzmann H. W., Reyes-Dominguez Y., Scherlach K. et al. Bacteria-induced natural product formation in the fungus Aspergillus nidulans requires Saga/Ada-mediated histone acetylation Proc. Natl Acad. Sci. USA 2011 108, N 34:14282–14287.
[82] Winans S. C. A new family of quorum sensing pheromones synthesized using S-adenosylmethionine and Acyl-CoAs Mol. Microbiol 2011 79, N 6:1403–1406.
[83] Blekhman I. I. Synchronization in nature and technology Moskow: Nauka, 1981 351 p.