Skip to main content
SpringerLink
Log in

Interactions between Endophytes and Plants: Beneficial Effect of Endophytes to Ameliorate Biotic and Abiotic Stresses in Plants

  • Review Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Endophytes are typically non-pathogenic microbes that at some period in their life cycles colonize the interior spaces of plant tissues. There is a growing interest in the role of the endophytes in ameliorating various stresses on plants, including biotic stress (such as pathogenic microbes) and abiotic stress (such as drought and salt stress), because endophytes can produce phytohormones, fixing nitrogen, antagonistic substances, enzymes, which plays an important role in plants respond to biotic and abiotic stress. Previously researchers have reviewed endophytes promote plant growth through direct or indirect mechanisms. In order to further clarify the interactions between endophytes and it’s host plants, we reviewed the biological properties of endophytes isolated from different parts of plant, the methods of plant inoculation with endophytes and the beneficial effects of endophytes to mitigate biotic and abiotic stress in plants.

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

Similar content being viewed by others

References

  • Adam M, Heuer H, Hallmann J (2014) Bacterial antagonists of fungal pathogens also control root-knot nematodes by induced systemic resistance of tomato plants. Plos One 9:e90402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Adesina MF, Grosch R, Lembke A, Vatchev TD, Smalla K (2009) In vitro antagonists of Rhizoctonia solani tested on lettuce:rhizosphere competence, biocontrol efficiency and rhizosphere microbial community response. Fems Microbiol Ecol 69:62–74

    Article  CAS  PubMed  Google Scholar 

  • Afzal M, Khan S, Iqbal S, Mirza MS, Khan QM (2013) Inoculation method affects colonization and activity of Burkholderia phytofirmans PsJN during phytoremediation of diesel-contaminated soil. Int Biodeter Biodegr 85:331–336

    Article  CAS  Google Scholar 

  • Afzal M, Khan QM, Sessitsch A (2014) Endophytic bacteria:prospects and applications for the phytoremediation of organic pollutants. Chemosphere 117:232–242

    Article  CAS  PubMed  Google Scholar 

  • Agrarwissenschaften DD (2007) Dissecting rhizobacteria-induced systemic resistance in tomato against Meloidogyne incognita-The first step using molecular tools

    Google Scholar 

  • Ali S, Charles TC, Glick BR (2014) Amelioration of high salinity stress damage by plant growth-promoting bacterial endophytes that contain ACC deaminase. Plant Physiol Bioch 80:160–167

    Article  CAS  Google Scholar 

  • Anuar EN, Nulit R, Idris AS (2015) Growth promoting effects of endophytic fungus Phlebia GanoEF3 on oil palm (Elaeis guineensis) seedlings. Int J Agric Biol 17:135–141

    Google Scholar 

  • Aroca R, Ruizlozano JM, Zamarreño AM, Paz JA, Garcíamina JM, Pozo MJ (2013) Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. J Plant Physiol 170:47–55

    Article  CAS  PubMed  Google Scholar 

  • Bacon CW, Jr JFW (2015) Functions, mechanisms and regulation of endophytic and epiphytic microbial communities of plants. Symbiosis 68:1–12

    Google Scholar 

  • Ban Y, Zhouying XU, Yang Y, Zhang H, Chen H, Tang M (2017) Effect of dark septate endophytic fungus Gaeumannomyces cylindrosporus on plant growth, photosynthesis and Pb tolerance of maize (Zea mays L.). Pedosphere 27:283–292

    Article  Google Scholar 

  • Bauen AW, Dunnett AJ, Richter GM, Dailey AG, Aylott M, Casella E (2010) Modelling supply and demand of bioenergy from short rotation coppice and Miscanthus in the UK. Bioresour Technol 101:8132–8143

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bibi F, Yasir M, Song GC, Lee SY, Chung YR (2012) Diversity and characterization of endophytic bacteria associated with tidal flat plants and their antagonistic effects on oomycetous plant pathogens. Plant Pathol J 28:20–31

    Article  CAS  Google Scholar 

  • Bressan W, Borges MT (2004) Delivery methods for introducing endophytic bacteria into maize. Biocontrol 49:315–322

    Article  Google Scholar 

  • Bulgarelli D, Schlaeppi K, Spaepen S, Themaat EVLV, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838

    Article  CAS  PubMed  Google Scholar 

  • Chadha N, Mishra M, Rajpal K, Bajaj R, Choudhary DK, Varma A (2015) An ecological role of fungal endophytes to ameliorate plants under biotic stress. Arch Microbiol 197:869–881

    Article  CAS  PubMed  Google Scholar 

  • Chang P, Gerhardt KE, Huang XD, Yu XM, Glick BR, Gerwing PD (2014) Plant growth-promoting bacteria facilitate the growth of barley and oats in salt-impacted soil:implications for phytoremediation of saline soils. Int J Phytoremediat 16:1133–1147

    Article  CAS  Google Scholar 

  • Cherif H, Marasco R, Rolli E, Ferjani R, Fusi M, Soussi A (2015) Oasis desert farming selects environment-specific date palm root endophytic communities and cultivable bacteria that promote resistance to drought. Env Microbiol Rep 7:668–678

    Article  CAS  Google Scholar 

  • Choudhary DK (2012) Microbial rescue to plant under habitatimposed abiotic and biotic stresses. Appl Microbiol Biot 96:1137–1155

    Article  CAS  Google Scholar 

  • Choudhury FK, Rivero RM, Blumwald E, Mittler R (2017) Reactive oxygen species, abiotic stress and stress combination. Plant J 90:856–867

    Article  CAS  PubMed  Google Scholar 

  • Clemow SR, Clairmont L, Madsen LH, Guinel FC (2011) Reproducible hairy root transformation and spot-inoculation methods to study root symbioses of pea. Plant Methods 7:1–15

    Article  Google Scholar 

  • Cohen AC, Bottini R, Pontin M, Berli FJ, Moreno D, Boccanlandro H (2015) Azospirillum brasilense ameliorates the response of Arabidopsis thaliana to drought mainly via enhancement of ABA levels. Physiol Plantarum 153:79–90

    Article  CAS  Google Scholar 

  • Das I, Panda MK, Rath CC, Tayung K (2017) Bioactivities of bacterial endophytes isolated from leaf tissues of Hyptis suaveolens against some clinically significant pathogens. J Appl Pharm Sci 7:131–136

    Google Scholar 

  • Ding S, Huang CL, Sheng HM, Song CL, Li YB, An LZ (2011) Effect of inoculation with the endophyte Clavibacter sp. strain Enf12 on chilling tolerance in Chorispora bungeana. Physiol Plantarum 141:141–151

    Article  CAS  Google Scholar 

  • Dutta D, Puzari KC, Gogoi R, Dutta P, Dutta D, Puzari KC (2014) Endophytes:exploitation as a tool in plant protection. Braz Arch Biol Techn 57:621–629

    Article  Google Scholar 

  • Egamberdieva D, Jabborova D (2015) Efficiency of phytohormoneproducing Pseudomonas to improve salt stress tolerance in Jew’s mallow (Corchorus olitorius L.). Plant-Growth-Promoting Rhizobacteria (PGPR) and Medicinal Plants 42:201–213

    Article  CAS  Google Scholar 

  • Egamberdieva D, Wirth SJ, Shurigin VV, Hashem A, Abdallah EF (2017) Endophytic bacteria improve plant growth, symbiotic performance of chickpea (Cicer arietinum L.) and induce suppression of root rot caused by Fusarium solani under salt stress. Front Microbiol 8:1887–1899

    Article  PubMed  PubMed Central  Google Scholar 

  • Fahad S, Hussain S, Bano A, Saud S, Hassan S, Shan D (2015) Potential role of phytohormones and plant growth-promoting rhizobacteria in abiotic stresses:consequences for changing environment. Environ Sci Pollut R 22:4907–4921

    Article  Google Scholar 

  • Fernandez O, Theocharis A, Bordiec S, Feil R, Jacquens L, Clément C (2012) Burkholderia phytofirmans PsJN acclimates grapevine to cold by modulating carbohydrate metabolism. Mol Plant Microbe Interact 25:496–504

    Article  CAS  PubMed  Google Scholar 

  • Fu W, Xu M, Sun K, Hu L, Cao W, Dai C (2018) Biodegradation of phenanthrene by endophytic fungus Phomopsis liquidambari in vitro and in vivo. Chemosphere 203:160–169

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Gao FK, Dai CC, Liu XZ (2010) Mechanisms of fungal endophytes in plant protection against pathogens. Afr J Microbiol Res 4:1346–1351

    Google Scholar 

  • Genre A (2005) Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17:3489–3499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Germaine KJ, Liu X, Cabellos GG, Hogan JP, Ryan D, Dowling DN (2006) Bacterial endophyte-enhanced phytoremediation of the organochlorine herbicide 2,4-dichlorophenoxyacetic acid. Fems Microbiol Ecol 57:302–310

    Article  CAS  PubMed  Google Scholar 

  • Glick BR (2012) Plant growth-promoting bacteria:mechanisms and applications. Scientifica (Cairo) 2012:963401

    Google Scholar 

  • Glick BR (2015) Beneficial plant-bacterial interactions. Springer Berlin

    Google Scholar 

  • Gond SK, Bergen MS, Torres MS (2015) Endophytic Bacillus spp. produce antifungal lipopeptides and induce host defence gene expression in maize. Microbiol Res 172:79–87

    Article  CAS  PubMed  Google Scholar 

  • Gond SK, Torres MS, Bergen MS, Helsel Z, White JF (2015) Induction of salt tolerance and up-regulation of aquaporin genes in tropical corn by rhizobacterium Pantoea agglomerans. Lett Appl Microbiol 60:392–399

    Article  CAS  PubMed  Google Scholar 

  • Govindarajan M, Balandreau J, Kwon SW, Weon HY, Lakshminarasimhan C (2008) Effects of the inoculation of Burkholderia vietnamensis and related endophytic diazotrophic bacteria on grain yield of rice. Microb Ecol 55:21–37

    Article  PubMed  Google Scholar 

  • Grunewaldt-Stöcker G, Alten HV (2003). Plant health effects of Acremonium, root endophytes compared to those of arbuscular mycorrhiza. Roots:The Dynamic Interface between Plants and the Earth 445−454

    Book  Google Scholar 

  • Gusain YS, Singh US, Sharma AK (2015) Bacterial mediated amelioration of drought stress in drought tolerant and susceptible cultivars of rice (Oryza sativa L.). Afr J Biotechnol 14:764–773

    Article  CAS  Google Scholar 

  • Hamilton CE, Gundel PE, Helander M, Saikkonen K (2012) Endophytic mediation of reactive oxygen species and antioxidant activity in plants:a review. Fungal Diversity 54:1–10

    Article  Google Scholar 

  • Hamilton CE, Bauerle TL (2012) A new currency for mutualism? fungal endophytes alter antioxidant activity in hosts responding to drought. Fungal Divers 54:39–49

    Article  Google Scholar 

  • Hameed A, Dilfuza E, Abd-Allah EF, Hashem A, Kumar A, Ahmad P (2014) Salinity stress and arbuscular mycorrhizal symbiosis in plants. Use of Microbes for the Alleviation of Soil Stresses 7:139–159

    Article  Google Scholar 

  • Hardoim PR, Overbeek LSV, Elsas JDV (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471

    Article  CAS  PubMed  Google Scholar 

  • Hardoim PR, Overbeek LSV, Berg G, Pirttilä AM, Compant S, Campisano A (2015) The hidden world within plants:ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320

    Article  PubMed  PubMed Central  Google Scholar 

  • Hashem A, Abdallah EF, Alqarawi AA, Alhuqail AA, Wirth S, Egamberdieva D (2016) The interaction between arbuscular mycorrhizal fungi and endophytic bacteria enhances plant growth of Acacia gerrardii under salt stress. Front Microbiol 7:868–882

    Article  Google Scholar 

  • Hata K, Sone K (2008) Isolation of endophytes from leaves of neolitsea sericea, in broadleaf and conifer stands. Mycoscience 49:229–232

    Article  Google Scholar 

  • Hodge A, Berta G, Doussan C, Merchan F, Crespi M (2009) Plant root growth, architecture and function. Plant Soil 321:153–187

    Article  CAS  Google Scholar 

  • Huang Z, Cai X, Shao C, She Z, Xia X, Chen Y (2008) Cheminform abstract:chemistry and weak antimicrobial activities of phomopsins produced by mangrove endophytic fungus Phomopsis sp. ZSUH76. Phytochemistry 69:1604–1608

    Article  CAS  PubMed  Google Scholar 

  • Hume DE, Ryan GD, Gibert A, Helander M, Mirlohi A, Sabzalian M. R (2016) Epichloë Fungal Endophytes for Grassland Ecosystems, E Lichtfouse ed, Sustainable Agriculture Reviews, Springer Switzland, pp233-305

    Google Scholar 

  • Jaber LR (2015) Grapevine leaf tissue colonization by the fungal entomopathogen Beauveria bassiana s.l. and its effect against downy mildew. Biocontrol 60:103–112

    Article  Google Scholar 

  • Jaber LR, Salem NM (2014) Endophytic colonisation of squash by the fungal entomopathogen Beauveria bassiana (Ascomycota:Hypocreales) for managing Zucchini yellow mosaic virus in cucurbits. Biocontrol Sci Techn 24:1096–1109

    Article  Google Scholar 

  • Jasim B, Jimtha John C, Shimil V, Jyothis M, Radhakrishnan EK (2015) Studies on the factors modulating indole-3-acetic acid production in endophytic bacterial isolates from Piper nigrum and molecular analysis of ipdc gene. J Appl Microbiol 117:786–799

    Article  CAS  Google Scholar 

  • Jha Y, Subramanian RB, Patel S (2011) Combination of endophytic and rhizospheric plant growth promoting rhizobacteria in Oryza sativa shows higher accumulation of osmoprotectant against saline stress. Acta Physiol Plant 33:797–802

    Article  Google Scholar 

  • Jian J, Ma Y, Sha C, Liu C, Song Y, Yi Q (2016) Melatonin-producing endophytic bacteria from grapevine roots promote the abiotic stress-induced production of endogenous melatonin in their hosts. Front Plant Sci 7:1387

    Google Scholar 

  • Jin HQ, Liu HB, Xie YY, Zhang YG, Xu QQ, Mao LJ (2017) Effect of the dark septate endophytic fungus Acrocalymma vagum on heavy metal content in tobacco leaves. Symbiosis 74:89–95

    Article  CAS  Google Scholar 

  • Joe MM, Islam MR, Karthikeyan B, Bradeepa K, Sa T (2012) Resistance responses of rice to rice blast fungus after seed treatment with the endophytic Achromobacter xylosoxidans AUM54 strains. Crop Prot 42:141–148

    Article  Google Scholar 

  • Jogawat A, Saha S, Bakshi M, Dayaman V, Kumar M, Dua M (2013) Piriformospora indica rescues growth diminution of rice seedlings during high salt stress. Plant Signal Behav 8:e26891

    Google Scholar 

  • Jr WJ, Torres MS, Sullivan RF, Jabbour RE, Chen Q, Tadych M (2014) Occurrence of Bacillus amyloliquefaciens as a systemic endophyte of vanilla orchids. Microsc Res Techniq 77:874–885

    Article  CAS  Google Scholar 

  • Kang JW, Khan Z, Doty SL (2012) Biodegradation of trichloroethylene by an endophyte of hybrid poplar. Appl Environ Microb 78:3504–3507

    Article  CAS  Google Scholar 

  • Katarina Cankar, Hojka Kraigher, Maja Ravnikar, Maja Rupnik. (2010) Bacterial endophytes from seeds of Norway spruce (Picea abies L. Karst). Fems Microbiol Lett 244:341–345

    Google Scholar 

  • Khan AL, Hussain J, Al-Harrasi A, Al-Rawahi A, Lee IJ (2013) Endophytic fungi:resource for gibberellins and crop abiotic stress resistance. Crit Rev Biotechnol 35:62–74

    Article  CAS  PubMed  Google Scholar 

  • Khan AL, Shinwari ZK, Kim YH, Waqas M, Hamayun M, Kamran M (2012) Role of endophyte Chaetomium globosum LK4 in growth of Capsicum annuum by producion of gibberellins and indole acetic acid. Pak J Bot 44:1601–1607

    Google Scholar 

  • Khan AL, Waqas M, Kang SM, Al-Harrasi A, Hussain J, Al-Rawahi A (2014) Bacterial endophyte Sphingomonas sp. LK11 produces gibberellins and IAA and promotes tomato plant growth. J Microbiol 52:689–695

    CAS  Google Scholar 

  • Khan Z, Rho H, Firrincieli A, Shang HH, Luna V, Masciarelli O (2016) Growth enhancement and drought tolerance of hybrid poplar upon inoculation with endophyte consortia. Curr Plant Biol 6:38–47

    Article  Google Scholar 

  • Knoth JL, Kim SH, Ettl GJ, Doty SL (2013) Effects of cross host species inoculation of nitrogen-fixing endophytes on growth and leaf physiology of maize. GCB Bioenergy 5:408–418

    Article  CAS  Google Scholar 

  • Knoth JL, Kim SH, Ettl GJ, Doty SL. (2014) Biological nitrogen fixation and biomass accumulation within poplar clones as a result of inoculations with diazotrophic endophyte consortia. New Phytol 201:599–609

    Article  CAS  PubMed  Google Scholar 

  • Köberl M, Ramadan EM, Adam M, Cardinale M, Hallmann J, Heuer H (2013) Bacillus and Streptomyces were selected as broadspectrum antagonists against soilborne pathogens from arid areas in Egypt. Fems Microbiol Lett 342:168–178

    Article  CAS  PubMed  Google Scholar 

  • Kumara PM, Shweta S, Vasanthakumari MM, Sachin N, Manjunatha BL, Jadhav SS (2014) Endophytes and plant secondary metabolite synthesis:molecular and evolutionary perspective, In VC Verma, AC Gange, eds, Advances in Endophytic Research, Springer India, pp 177-190

    Google Scholar 

  • Kusari P, Kusari S, Spiteller M, Kayser O (2013) Endophytic fungi harbored in Cannabis sativa L.:diversity and potential as biocontrol agents against host plant-specific phytopathogens. Fungal Divers 60:137–151

    Article  Google Scholar 

  • Lata R, Chowdhury S, Gond SK, White JJ (2018) Induction of abiotic stress tolerance in plants by endophytic microbes. Lett Appl Microbiol 66:268–276

    Article  CAS  PubMed  Google Scholar 

  • Lee SK, Sohn EY, Hamayun M, Yoon JY, Lee IJ. (2010) Effect of silicon on growth and salinity stress of soybean plant grown under hydroponic system. Agroforest Syst 80:333–340

    Article  Google Scholar 

  • Lei Z, Zhong J, Hao L, Xin K, Chen C, Li Q (2017) Complete genome sequence of the drought resistance-promoting endophyte Klebsiella sp. LTGPAF-6F. J Biotechnol 246:36–39

    Google Scholar 

  • Leonhardt T, Sácký J, Šimek P, Šantrůček J, Kotrba P (2014) Metallothionein-like peptides involved in sequestration of Zn in the Zn-accumulating ectomycorrhizal fungus Russula atropurpurea. Metallomics 6:1693–1701

    Article  CAS  PubMed  Google Scholar 

  • Li HY, Wei DQ, Shen M, Zhou ZP (2012) Endophytes and their role in phytoremediation. Fungal Divers 54:11–18

    Article  Google Scholar 

  • Lugtenberg BJJ, Mercado-Blanco J (2014) Biotechnological applications of bacterial endophytes. Current Biotechnology 3:60–75

    Article  CAS  Google Scholar 

  • Mapelli F, Marasco R, Rolli E, Barbato M, Cherif H, Guesmi A (2013) Potential for plant growth promotion of rhizobacteria associated with Salicornia growing in Tunisian hypersaline soils. Biomed Res Int 2013:248078

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marella S (2014) Bacterial endophytes in sustainable cropproduction:Applications, recent developments and challenges ahead. Int J Life Sci Res 2:46–56

    Google Scholar 

  • Mastouri F, Björkman T, Harman GE (2010) Seed treatment with Trichoderma harzianum alleviates biotic, abiotic, and physiological stresses in germinating seeds and seedlings. Phytopathology 100:1213–1221

    Article  CAS  PubMed  Google Scholar 

  • Matsuoka H, Akiyama M, Kobayashi K, Yamaji K (2013) Fe and P solubilization under limiting conditions by bacteria isolated from Carex kobomugi roots at the Hasaki Coast. Curr Microbiol 66:314–321

    Article  CAS  PubMed  Google Scholar 

  • Mendez MO, Maier RM (2008) Phytostabilization of mine tailings in arid and semiarid environments:an emerging remediation technology. Environ Health Persp 116:278–283

    Article  CAS  Google Scholar 

  • Meyer SED, Beuf KD, Vekeman B, Willems A (2015) A large diversity of non-rhizobial endophytes found in legume root nodules in Flanders (Belgium). Soil Biol Biochem 83:1–11

    Article  CAS  Google Scholar 

  • Miller G, Suzuki N, Ciftciyilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  CAS  PubMed  Google Scholar 

  • Miottovilanova L, Jacquard C, Courteaux B, Wortham L, Michel J, Clément C (2016) Burkholderia phytofirmans PsJN confers grapevine resistance against Botrytis cinerea via a direct antimicrobial effect combined with a better resource mobilization. Front Plant Sci 7:1236

    Google Scholar 

  • Mohanty SR, Dubey G, Kollah B (2017) Endophytes of Jatropha curcas, promote growth of maize, Rhizosphere, Vol 3, Elsevier BV, Amsterdam, pp 20-28

    Google Scholar 

  • Molinamontenegro MA, Oses R, Torresdíaz C, Atala C, Zuritasilva A, Ruizlara S (2016) Root-endophytes improve the ecophysiological performance and production of an agricultural species under drought condition. Aob Plants 8:plw062

    Google Scholar 

  • Momose A, Hiyama T, Nishimura K, Ishizaki N, Ishikawa S, Yamamoto M (2013) Characteristics of nitrogen fixation and nitrogen release from diazotrophic endophytes isolated from sugarcane (Saccharum officinarum L.) stems. Niigata University Agricultural Department Research Report (in Chinese) 66:1–9

    CAS  Google Scholar 

  • Munif A, Hallmann J, Sikora RA (2013) The influence of endophytic bacteria on Meloidogyne incognita infection and tomato plant growth. Journal of the International Society for Southeast Asian Agricultural Sciences 19:68–74

    Google Scholar 

  • Murphy BR, Doohan FM, Hodkinson TR (2014) Yield increase induced by the fungal root endophyte Piriformospora indica in barley grown at low temperature is nutrient limited. Symbiosis 62:29–39

    Article  Google Scholar 

  • Murilloamador B, Yamada S, Yamaguchi T, Ruedapuente E, ÁvilaSerrano N, Garcíahernández JL (2007) Influence of calcium silicate on growth, physiological parameters and mineral nutrition in two legume species under salt stress. J Agron Crop Sci 193:413–421

    Article  CAS  Google Scholar 

  • Müller H, Westendorf C, Leitner E, Chernin L, Riedel K, Schmidt S (2009) Quorum-sensing effects in the antagonistic rhizosphere bacterium Serratia plymuthica HRO-C48. Fems Microbiol Ecol 67:468–4678

    Article  CAS  PubMed  Google Scholar 

  • Nagata S, Yamaji K, Nomura N, Ishimoto H (2015) Root endophytes enhance stress-tolerance of Cicuta virosa L. growing in a mining pond of eastern Japan. Plant Spec Biol 30:116–125

    Article  Google Scholar 

  • Narisawa K, Kawamata H, Currah RS, Hashiba T (2002) Suppression of verticillium wilt in eggplant by some fungal root endophytes. Eur J Plant Pathol 108:103–109

    Article  Google Scholar 

  • Naveed M, Mitter B, Reichenauer TG, Wieczorek K, Sessitsch A (2014) Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17. Environ Exp Bot 97:30–39

    Article  CAS  Google Scholar 

  • Nawrotchorabik K (2013) The use of interactions in dual cultures in vitro to evaluate the pathogenicity of fungi and susceptibility of host plant genotypes. doi:10.5772/53214

    Google Scholar 

  • Nelson EB (2004) Microbial dynamics and interactions in the spermosphere. Annu Rev Phytopathol 42:271–309

    Article  CAS  PubMed  Google Scholar 

  • Nia SH, Zarea MJ, Rejali F, Varma A (2012) Yield and yield components of wheat as affected by salinity and inoculation with Azospirillum strains from saline or non-saline soil. Journal of the Saudi Society of Agricultural Sciences 11:113–121

    Article  Google Scholar 

  • Oberhofer M, Leuchtmann A (2013) Hordelymus europaeus benefits from natural hybrid and non-hybrid endophytes under drought stress. International Symposium on Fungal Endophytes of Grasses. doi:20.500.11850/57752

    Google Scholar 

  • Olivares FL, Aguiar NO, Rosa RCC, Canellas LP (2015) Substrate biofortification in combination with foliar sprays of plant growth promoting bacteria and humic substances boosts production of organic tomatoes. Sci Hortic 183:100–108

    Article  Google Scholar 

  • Padgham JL, Sikora RA (2007) Biological control potential and modes of action of Bacillus megaterium against Meloidogyne graminicola on rice. Crop Prot 26:971–977

    Article  Google Scholar 

  • Pageni B, Lupwayi N, Akter Z (2014) Plant growth-promoting and phytopathogen-antagonistic properties of bacterial endophytes from potato (Solanum tuberosum L.) cropping systems. Can J Plant Sci 94:835–844

    Article  Google Scholar 

  • Palus JA, Borneman J, Ludden PW, Triplett EW (1996) A diazotrophic bacterial endophyte isolated from stems of zea mays, l. and zea luxurians, iltis and doebley. Plant Soil 186:135–142

    Article  CAS  Google Scholar 

  • Patel D, Saraf M (2013) Influence of soil ameliorants and microflora on induction of antioxidant enzymes and growth promotion of Jatropha curcas L. under saline condition. Eur J Soil Biol 55:47–54

    Article  CAS  Google Scholar 

  • Parande S, Zamani GR, Zahan MHS, Ghaderi MG (2013) Effects of silicon application on the yield and component of yield in the common bean (Phaseolus vulgaris) under salinity stress. International Journal of Agronomy and Plant Production, Vol 4, Victor Quest Publications, London, pp 1574-1579

    Google Scholar 

  • Piccoli P, Bottini R (2013) Abiotic Stress Tolerance Induced by Endophytic PGPR, In R Aroca, eds, Symbiotic Endophytes, Soil Biology, Vol 37, Springer, Berlin, Heidelberg, pp 151-163

    Book  Google Scholar 

  • Pinheiro EA, Carvalho JM, Santos DC, Feitosa AO, Marinho PS, Guilhon GM. (2013) Chemical constituents of Aspergillus sp EJC08 isolated as endophyte from Bauhinia guianensis and their antimicrobial activity. An Acad Bras Cienc 85:1247–1252

    Article  CAS  PubMed  Google Scholar 

  • Piyasena KGNP, Wickramarachchi WART, Kumar NS, Jayasinghe L, Fujimoto Y (2015) Two phytotoxic azaphilone derivatives from Chaetomium globosum, a fungal endophyte isolated from Amaranthus viridis leaves. Mycology 6:158–160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rasche F, Trondl R, Naglreiter C, Reichenauer TG, Sessitsch A (2006) Chilling and cultivar type affect the diversity of bacterial endophytes colonizing sweet pepper (Capsicum anuum L.). Can J Microbiol 52:1036–1045

    Article  CAS  PubMed  Google Scholar 

  • Redman RS, Yong OK, Woodward CJDA, Greer C, Espino L, Doty SL (2011) Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis:a strategy for mitigating impacts of climate change. Plos One 6:e14823

    Google Scholar 

  • Reinholdhurek B, Hurek T (2011) Living inside plants:bacterial endophytes. Curr Opin Plant Biol 14:435–443

    Article  Google Scholar 

  • Rho H, Hsieh M, Kandel SL, Cantillo J, Doty SL, Kim SH (2017) Do endophytes promote growth of host plants under stress? a metaanalysis on plant stress mitigation by endophytes. Microb Ecol 75:1–12

    Google Scholar 

  • Rodriguez RJ, Jr WJ, Arnold AE, Redman RS (2009) Fungal endophytes:diversity and functional roles. New Phytol 182:314–330

    Article  CAS  PubMed  Google Scholar 

  • Rosenblueth M, MartãNez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant Microbe In 19:827–837

    Article  CAS  Google Scholar 

  • Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes:recent developments and applications. Fems Microbiol Lett 278:1–9

    Article  CAS  PubMed  Google Scholar 

  • Samina M, Tom K, Bruce R, George L (2010) Growth promoting effects of corn (Zea mays) bacterial isolates under greenhouse and field conditions. Soil Biol Biochem 42:1848–1856

    Article  CAS  Google Scholar 

  • Santiago IF, Rosa CA, Rosa LH (2016) Endophytic symbiont yeasts associated with the Antarctic angiosperms Deschampsia antarctica and Colobanthus quitensis. Polar Biol 40:1–7

    Google Scholar 

  • Santoyo G, Morenohagelsieb G, Del COM. Glick BR (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99

    Article  CAS  PubMed  Google Scholar 

  • Sandhya V, Shrivastava M, Ali SZ, Prasad VSSK (2017) Endophytes from maize with plant growth promotion and biocontrol activity under drought stress. Russian Agricultural Sciences 43:22–34

    Article  Google Scholar 

  • Saraf M, Jha CK, Patel D (2010) The role of ACC deaminase producing PGPR in Sustainable Agriculture. In D Maheshwari, eds, Plant Growth and Health Promoting Bacteria, Microbiology Monographs, Vol 18, Springer, Berlin, Heidelberg, pp 365-385

    Book  Google Scholar 

  • Sasan R, Bidochka M (2013) Antagonism of the endophytic insect pathogenic fungus Metarhizium robertsii against the bean plant pathogen Fusarium solani f. sp. phaseoli. Can J Plant Pathol 35:288–293

    Article  CAS  Google Scholar 

  • Sajid Mahmood Nadeem, Zahir Ahmad Zahir, Muhammad Naveed, Muhammad Ashraf (2010) Microbial ACC-deaminase:prospects and applications for inducing salt tolerance in plants. Crit Rev Plant Sci 29:360–393

    Article  CAS  Google Scholar 

  • Scherwinski K, Grosch R, Berg G (2008) Effect of bacterial antagonists on lettuce:active biocontrol of Rhizoctonia solani and negligible, short-term effects on nontarget microorganisms. Fems Microbiol Ecol 64:106–116

    Article  CAS  PubMed  Google Scholar 

  • Schulz B, Boyle C (2005) The endophytic continuum. Mycological Research 109:661–686

    Article  PubMed  Google Scholar 

  • Schlaeppi K, Bulgarelli D (2015) The plant microbiome at work. Mol Plant Microbe In 28:212–217

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Shah A, Dar NJ, Hassan QP, Ahmad M (2016) Endophytes and neurodegenerative diseases:a hope in desperation. CNS and Neurological Disorders-Drug Targets 15:1231–1239

    Article  CAS  PubMed  Google Scholar 

  • Shah A, Rather MA, Qazi PH, Aga MA, Mushtaq S, Shah AM (2017) Discovery of antimicrobial and antitubercular molecules from Fusarium solani:an endophyte of Glycyrrhiza glabra. J Appl Microbiol 122:1168–1176

    Article  CAS  PubMed  Google Scholar 

  • Sharma P, Khanna V, Kumari P. (2013) Efficacy of aminocyclopropane-1-carboxylic acid (ACC)-deaminase-producing rhizobacteria in ameliorating water stress in chickpea under axenic conditions. Afr J Microbiol Res 7:5749–5757

    Article  CAS  Google Scholar 

  • Sheng XF, Chen XB, He LY (2008) Characteristics of an endophytic pyrene-degrading bacterium of Enterobacter sp. 12J1 from Allium macrostemon Bunge. Int Biodeter Biodegr 62:88–95

    Article  CAS  Google Scholar 

  • Shi P, Zhu K, Zhang Y, Chai T (2016) Growth and cadmium accumulation of Solanum nigrum L. seedling were enhanced by heavy metal-tolerant strains of Pseudomonas aeruginosa. Water Air Soil Poll 227:459, doi:10.1007/s11270-016-3167-6

    Article  CAS  Google Scholar 

  • Simpson K, Gillespie WA (2012) Emerging methods for diagnostics and mitigation of crop environmental stress in a changing climate. Hortscience A Publication of the American Society for Horticultural Science 47:684–686

    Google Scholar 

  • Singh LP, Gill SS, Tuteja N (2011) Unraveling the role of fungal symbionts in plant abiotic stress tolerance. Plant Signal Behav 6:175–191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sikora RA, Schäfer K, Dababat AA (2007) Modes of action associated with microbially induced in planta, suppression of plant-parasitic nematodes. Australas Plant Path 36:124–134

    Article  Google Scholar 

  • Silva DPD, Castañedaojeda MP, Moretti C, Buonaurio R, Ramos C, Venturi V (2014) Bacterial multispecies studies and microbiome analysis of a plant disease. Microbiology 160:556–566

    Article  CAS  Google Scholar 

  • Singh V (2016) Potential of bacterial endophytes as plant growth promoting factors. J Plant Pathol 7:7–9

    Google Scholar 

  • Skirycz A, Inzé D (2010) More from less:plant growth under limited water. Curr Opin Biotech 21:197–203

    Article  CAS  PubMed  Google Scholar 

  • Song M, Chai Q, Li X, Yao X, Li C, Christensen MJ (2015) An asexual epichloë, endophyte modifies the nutrient stoichiometry of wild barley (Hordeum brevisubulatum) under salt stress. Plant Soil 387:153–165

    Article  CAS  Google Scholar 

  • Spiers DE, Wax LE, Eichen PA, Rottinghaus GE, Evans TJ, Keisler DH (2012) Use of different levels of ground endophyte-infected tall fescue seed during heat stress to separate characteristics of fescue toxicosis. J Anim Sci 90:3457–3467

    Article  CAS  PubMed  Google Scholar 

  • Stuart Card, Linda Johnson, Suliana Teasdale, John Caradus (2016) Deciphering endophyte behaviour:the link between endophyte biology and efficacious biological control agents. FEMS Microbiol Ecol 92:fiw114

    Google Scholar 

  • Suárez R, Wong A, Ramírez M, Barraza A, Orozco MC, Cevallos MA (2008) Improvement of drought tolerance and grain yield in common bean by overexpressing trehalose-6-phosphate synthase in rhizobia. Mol Plant Microbe In 21:958–966

    Article  CAS  Google Scholar 

  • Sundram S, Meon S, Seman IA, Othman R (2015) Application of arbuscular mycorrhizal fungi with Pseudomonas aeruginosa UPMP3 reduces the development of Ganoderma basal stem rot disease in oil palm seedlings. Mycorrhiza 25:387–397

    Article  CAS  PubMed  Google Scholar 

  • Thomas P, Upreti R (2014) Testing of bacterial endophytes from nonhost sources as potential antagonistic agents against tomato wilt pathogen. Adv Microbiol 4:656–666

    Article  Google Scholar 

  • Tian B, Zhang C, Ye Y, Wen J, Wu Y, Wang H (2017) Beneficial traits of bacterial endophytes belonging to the core communities of the tomato root microbiome. Agr Ecosyst Environ 247:149–156

    Article  Google Scholar 

  • Ting ASY, Mah SW, Tee CS (2012) Evaluating the feasibility of induced host resistance by endophytic isolate Penicillium citrinum BTF08 as a control mechanism for Fusarium wilt in banana plantlets. Biol Control 61:155–159

    Article  Google Scholar 

  • Toro M, Azcon R, Barea J. (1997) Improvement of arbuscular mycorrhiza development by inoculation of soil with phosphate-solubilizing rhizobacteria to improve rock phosphate bioavailability (32p) and nutrient cycling. Appl Environ Microb 63:4408–4412

    CAS  Google Scholar 

  • Truyens S, Weyens N, Cuypers A, Vangronsveld J (2015) Bacterial seed endophytes:genera, vertical transmission and interaction with plants. Env Microbiol Rep 7:40–50

    Article  Google Scholar 

  • Upreti R, Thomas P (2015) Root-associated bacterial endophytes from Ralstonia solanacearum resistant and susceptible tomato cultivars and their pathogen antagonistic effects. Front Microbiol 6:255–266

    Article  PubMed  PubMed Central  Google Scholar 

  • Valluru R, Link J, Claupein W (2012) Consequences of early chilling stress in two. Plant Biology14:641−651

    Google Scholar 

  • Vardharajula S, Skz A, Shrivastava M (2017) Plant growth promoting endophytes and their interaction with plants to alleviate abiotic stress. Curr Biotechnol 6:252–263

    Article  Google Scholar 

  • Vargas L, Brígida ABS, Filho JPM, Carvalho TGD, Rojas CA, Vaneechoutte D (2014) Drought tolerance conferred to sugarcane by association with Gluconacetobacter diazotrophicus:a transcriptomic view of hormone pathways. Plos One 9:e114744

    Google Scholar 

  • Vurukonda SSKP, Vardharajula S, Shrivastava M, Skz A (2016) Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol Res 184:13–24

    Article  PubMed  Google Scholar 

  • Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci USA 102:13386–13391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang C, Wang C, Gao YL, Wang YP, Guo JH (2016) A consortium of three plant growth-promoting rhizobacterium strains acclimates Lycopersicon esculentum and confers a better tolerance to chilling stress. J Plant Growth Regul 35:54–64

    Article  CAS  Google Scholar 

  • Wang K, Yan PS, Ding QL, Wu QX, Wang ZB, Peng J (2013) Diversity of culturable root-associated/endophytic bacteria and their chitinolytic and aflatoxin inhibition activity of peanut plant in China. World J Microb Biot 29:1–10

    Article  CAS  Google Scholar 

  • Wani ZA, Ashraf N, Mohiuddin T, Riyazulhassan S (2015) Plantendophyte symbiosis, an ecological perspective. Appl Microbiol Biot 99:2955–2965

    Article  CAS  Google Scholar 

  • Waqas M, Khan AL, Kang SM, Yoonha K, Injung L (2014) Phytohormone-producing fungal endophytes and hardwoodderived biochar interact to ameliorate heavy metal stress in soybeans. Biol Fert Soils 50:1155–1167

    Article  CAS  Google Scholar 

  • Waqas M, Khan AL, Kamran M, Hamayun M, Kang SM, Kim YH (2012) Endophytic fungi produce gibberellins and indoleacetic acid and promotes host-plant growth during stress. Molecules 17:10754–10773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weyens N, van der Lelie D, Taghavi S, Vangronsveld J. (2009) Phytoremediation:plant-endophyte partnerships take the challenge. Curr Opin Biotechnol 20:248–254

    Article  CAS  PubMed  Google Scholar 

  • White JF, Kingsley KI, Kowalski KP, Irizarry I, Micci A, Soares MA (2018) Disease protection and allelopathic interactions of seedtransmitted endophytic Pseudomonads of invasive reed grass (Phragmites australis). Plant Soil 422:1–14

    Article  CAS  Google Scholar 

  • Xia L, Geng X, Xie R, Lei F, Jiang J, Lu G (2016) The endophytic bacteria isolated from elephant grass (Pennisetum purpureum Schumach) promote plant growth and enhance salt tolerance of Hybrid Pennisetum. Biotechnol Biofuels 9:190–201

    Article  CAS  Google Scholar 

  • Xu Le, Wang Aiai, Wang Jun, Wei Qiao, Zhang Wenying (2017) Piriformospora indica confers drought tolerance on Zea mays L. through enhancement of antioxidant activity and expression of drought-related genes. Crop J 5:251–258

    Article  Google Scholar 

  • Yamaji K, Watanabe Y, Masuya H, Shigeto A, Yui H, Haruma T (2016) Root fungal endophytes enhance heavy-metal stress tolerance of clethra barbinervis growing naturally at mining sites via growth enhancement, promotion of nutrient uptake and decrease of heavy-metal concentration. Plos One 11:e0169089

    Google Scholar 

  • Yang S, Vanderbeld B, Wan J, Huang Y (2010) Narrowing down the targets:towards successful genetic engineering of droughttolerant crops. Mol Plant 3:469–490

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Li C, Nan Z (2012) Effects of cadmium stress on seed germination and seedling growth of Elymus dahuricus infected with the Neotyphodium endophyte. Science China Life Sciences 55:793–799.

    Article  CAS  PubMed  Google Scholar 

  • Zhao L, Xu Y, Lai XH, Shan C, Deng Z, Ji Y (2015) Screening and characterization of endophytic Bacillus and Paenibacillus strains from medicinal plant Lonicera japonica for use as potential plant growth promoters. Braz J Microbiol 46:977–989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao S, Zhou N, Zhao ZY, Zhang K, Wu GH, Tian CY (2016) Isolation of endophytic plant growth-promoting bacteria associated with the halophyte Salicornia europaea and evaluation of their promoting activity under salt stress. Curr Microbiol 73:574–581

    Article  CAS  PubMed  Google Scholar 

  • Zhou JY, Yuan J, Li X, Ning YF, Dai CC (2015) Endophytic bacteriumtriggered reactive oxygen species directly increase oxygenous sesquiterpenoid content and diversity in Atractylodes lancea. Appl Environ Microb 82:1577–1585.

    Article  CAS  Google Scholar 

Download references

Author information

Author notes

  1. These authors contributed equally in this work.

Authors and Affiliations

  1. College of Pharmacy, Ningxia Medical University, Yinchuan, 750004, China

    Yu zhang, Xiaxia Yu, Wenjin Zhang, Xiaojia Zhang, Gaochang Cui & Xinhui Zhang

  2. Ningxia Engineering and Technology Research Center of Hui Medicine Modernization, Ningxia Collaborative Innovation Center of Hui Medicine, Key Laboratory of Hui Ethnic Medicine Modernization, Ministry of Education, Yinchuan, 750004, China

    Xinhui Zhang

  3. Laboratory Animal Center, Ningxia Medical University, Yinchuan, 750004, China

    Duoyong Lang

Authors
  1. Yu zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaxia Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wenjin Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Duoyong Lang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiaojia Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gaochang Cui
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xinhui Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xinhui Zhang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

zhang, Y., Yu, X., Zhang, W. et al. Interactions between Endophytes and Plants: Beneficial Effect of Endophytes to Ameliorate Biotic and Abiotic Stresses in Plants. J. Plant Biol. 62, 1–13 (2019). https://doi.org/10.1007/s12374-018-0274-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-018-0274-5

Keywords

Search

Navigation