Seed Endophytes and Their Potential Applications

  • Haiyan Li
  • Shobhika Parmar
  • Vijay K. Sharma
  • James Francis WhiteJr


With growing interest in the role of endophyte to the host plant ecology, health, and productivity, this chapter discusses seed-inhabiting endophytes. These endophytes were less recognized when compared with those found in the other parts of the plant. However, they cannot be ignored as they are the first one colonizing young seedlings and further determining the fate of the plant. These endophytes often have potential to improve seed germination and seedling growth. Recent advances in seed endophytes have proved that they can confer stress tolerance to the host plants, especially the heavy metal resistance. Microbial dynamic equilibrium with plant systems is vital for the germination, growth, and reproductive phases of plant life cycle. The colonization and transmission of seed endophytes suggests that host plants select an endophytic community having beneficial traits that can be passed to successive generations. Seed endophytes can facilitate the improvement of seed quality and plant growth of agriculturally important crops via different biotechnological applications; they have prospects in endophyte-mediated phytoremediation applications.


Seed endophytes Plant-microbe interaction Plant growth promotion Stress tolerance Heavy metal toxicity 


  1. Abdelatey LM, Khalil WK, Ali TH et al (2011) Heavy metal resistance and gene expression analysis of metal resistance genes in gram-positive and gram-negative bacteria present in Egyptian soils. J Appl Sci Environ Sanitation 6(2):201–212Google Scholar
  2. Alibrandi P, Cardinale M, Rahman MM et al (2018) The seed endosphere of Anadenanthera colubrina is inhabited by a complex microbiota, including Methylobacterium spp. and Staphylococcus spp. with potential plant-growth promoting activities. Plant Soil 422(1–2):81–99CrossRefGoogle Scholar
  3. Al-Khashman OA, Shawabkeh RA (2006) Metals distribution in soils around the cement factory in southern Jordan. Environ Pollut 140(3):387–394PubMedCrossRefPubMedCentralGoogle Scholar
  4. Andrews GK (2000) Regulation of metallothionein gene expression by oxidative stress and metal ions. Biochem Pharmacol 59(1):95–104PubMedCrossRefPubMedCentralGoogle Scholar
  5. Bacilio-Jiménez M, Aguilar-Flores S, del Valle MV et al (2001) Endophytic bacteria in rice seeds inhibit early colonization of roots by Azospirillum brasilense. Soil Biol Biochem 33(2):167–172CrossRefGoogle Scholar
  6. Bacon CW, Hill NS (1996) Symptomless grass endophytes: products of coevolutionary symbioses and their role in the ecological adaptations of grasses. In: Redlin SC, Carris LM (eds) Endophytic fungi in grasses and woody plants: systematics, ecology, and evolution. APS Press, St Paul, MN, pp 155–178Google Scholar
  7. Bacon CW, Hinton DM (2006) Bacterial endophytes: the endophytic niche, its occupants and its utility. In: Gnanamanickam SS (ed) Plant-associated bacteria. Springer, Amsterdam, pp 15–194Google Scholar
  8. Bacon CW, White JF (2000) Microbial endophytes. Marcel Dekker, New YorkGoogle Scholar
  9. Bacon CW, Porter JK, Robbins JD et al (1977) Epichloe typhina from toxic tall fescue grasses. Appl Environ Microbiol 34(5):576–581PubMedPubMedCentralGoogle Scholar
  10. Baker KF, Smith SH (1966) Dynamics of seed transmission of plant pathogens. Annu Rev Phytopathol 4(1):311–332CrossRefGoogle Scholar
  11. Ball OJ, Prestidge RA, Sprosen JM (1995) Interrelationships between Acremonium lolii, peramine, and lolitrem B in perennial ryegrass. Appl Environ Microbiol 61(4):1527–1533PubMedPubMedCentralGoogle Scholar
  12. Barret M, Briand M, Bonneau S et al (2014) Emergence shapes the structure of the seed-microbiota. Appl Environ Microbiol 81(4):1257–1266CrossRefGoogle Scholar
  13. Bonnet M, Camares O, Veisseire P (2000) Effects of zinc and influence of Acremonium lolii on growth parameters, chlorophyll a fluorescence and antioxidant enzyme activities of ryegrass (Lolium perenne L. cv Apollo). J Exp Bot 51(346):945–953PubMedPubMedCentralGoogle Scholar
  14. Boursnell JG (1950) The symbiotic seed-borne fungus in the Cistaceae: I. Distribution and function of the fungus in the seeding and in the tissues of the mature plant. Ann Bot 14(54):217–243CrossRefGoogle Scholar
  15. Briggs L, Crush J, Ouyang L et al (2013) Neotyphodium endophyte strain and superoxide dismutase activity in perennial ryegrass plants under water deficit. Acta Physiol Plant 35(5):1513–1520CrossRefGoogle Scholar
  16. Cabral D, Stone JK, Carroll GC (1993) The internal mycobiota of Juncus spp.: microscopic and cultural observations of infection patterns. Mycol Res 97(3):367–376CrossRefGoogle Scholar
  17. Carroll G (1988) Fungal endophytes in stems and leaves: from latent pathogen to mutualistic symbiont. Ecology 69(1):2–9CrossRefGoogle Scholar
  18. Chaudhry V, Sharma S, Bansa K et al (2017) Glimpse into the genomes of rice endophytic bacteria: diversity and distribution of firmicutes. Front Microbiol 7:2115PubMedPubMedCentralCrossRefGoogle Scholar
  19. Chong TM, Yin WF, Chen JW et al (2016) Comprehensive genomic and phenotypic metal resistance profile of Pseudomonas putida strain S13.1.2 isolated from a vineyard soil. AMB Exp 6(1):95CrossRefGoogle Scholar
  20. Chu L, Li W, Li XY et al (2017) Diversity and heavy metal resistance of endophytic fungi from seeds of hyperaccumulators. Jiangsu J Agric Sci 1:008Google Scholar
  21. Cope-Selby N, Cookson A, Squance M et al (2017) Endophytic bacteria in Miscanthus seed: implications for germination, vertical inheritance of endophytes, plant evolution and breeding. GCB Bioenergy 9(1):57–77CrossRefGoogle Scholar
  22. Czarna M, Kolodziejczak M, Janska H (2016) Mitochondrial proteome studies in seeds during germination. Proteomes 4(2):19PubMedCentralCrossRefGoogle Scholar
  23. De Bary A (1866) Morphologic und physiologie der plize, Flechten, und Myxomyceten. In: Hofmeister’s hand book of physiological botany, vol 2. LeipzigGoogle Scholar
  24. Di Vietro L, Daghino S, Abbà S et al (2014) Gene expression and role in cadmium tolerance of two PLAC8-containing proteins identified in the ericoid mycorrhizal fungus Oidiodendron maius. Fungal Biol 118(8):695–703PubMedCrossRefPubMedCentralGoogle Scholar
  25. Donnarumma F, Capuana M, Vettori C et al (2011) Isolation and characterisation of bacterial colonies from seeds and in vitro cultures of Fraxinus spp. from Italian sites. Plant Biol 13(1):169–176PubMedCrossRefPubMedCentralGoogle Scholar
  26. Ernst M, Mendgen KW, Wirsel SG (2003) Endophytic fungal mutualists: seed-borne Stagonospora spp. enhance reed biomass production in axenic microcosms. Mol Plant Microbe Interact 16(7):580–587PubMedCrossRefPubMedCentralGoogle Scholar
  27. Ewald PW (1987) Transmission modes and evolution of the parasitism-mutualism continuum. Ann N Y Acad Sci 503(1):295–306PubMedCrossRefPubMedCentralGoogle Scholar
  28. Ezzouhri L, Castro E, Moya M et al (2009) Heavy metal tolerance of filamentous fungi isolated from polluted sites in Tangier, Morocco. Afr J Microbiol Res 3(2):35–48Google Scholar
  29. Facchinelli A, Sacchi E, Mallen L (2001) Multivariate statistical and GIS-based approach to identify heavy metal sources in soils. Environ Pollut 114(3):313–324PubMedCrossRefPubMedCentralGoogle Scholar
  30. Ferreira A, Quecine MC, Lacava PT et al (2008) Diversity of endophytic bacteria from Eucalyptus species seeds and colonization of seedlings by Pantoea agglomerans. FEMS Microbiol Lett 287(1):8–14PubMedCrossRefPubMedCentralGoogle Scholar
  31. Finch SC, Pennell CGL, Kerby JWF et al (2016) Mice find endophyte-infected seed of tall fescue unpalatable–implications for the aviation industry. Grass Forage Sci 71(4):659–666CrossRefGoogle Scholar
  32. Freeman EM (1903) The seed-fungus of Lolium temulentum, L, the Darnel. Proc R Soc Lond 71(467–476):27–30Google Scholar
  33. Gagne-Bourgue F, Aliferis KA, Seguin P et al (2013) Isolation and characterization of indigenous endophytic bacteria associated with leaves of switchgrass (Panicum virgatum L.) cultivars. J Appl Microbiol 114(3):836–853PubMedCrossRefPubMedCentralGoogle Scholar
  34. Ganley RJ, Newcombe G (2006) Fungal endophytes in seeds and needles of Pinus monticola. Mycol Res 110(3):318–327PubMedCrossRefPubMedCentralGoogle Scholar
  35. Gao T, Shi X (2018) Preparation of a synthetic seed for the common reed harboring an endophytic bacterium promoting seedling growth under cadmium stress. Environ Sci Pollut Res 25(9):8871–8879CrossRefGoogle Scholar
  36. González-Fernández M, García-Barrera T, Arias-Borrego A et al (2009) Metallomics integrated with proteomics in deciphering metal-related environmental issues. Biochimie 91(10):1311–1317PubMedCrossRefGoogle Scholar
  37. Hameed A, Yeh MW, Hsieh YT et al (2015) Diversity and functional characterization of bacterial endophytes dwelling in various rice (Oryza sativa L.) tissues, and their seed-borne dissemination into rhizosphere under gnotobiotic P-stress. Plant Soil 394(1–2):177–197CrossRefGoogle Scholar
  38. Hardoim PR, Van Overbeek LS, Van Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16(10):463–471PubMedCrossRefGoogle Scholar
  39. Hardoim PR, Hardoim CC, Van Overbeek LS et al (2012) Dynamics of seed-borne rice endophytes on early plant growth stages. PLoS One 7(2):e30438.
  40. Herrera SD, Grossi C, Zawoznik M et al (2016) Wheat seeds harbour bacterial endophytes with potential as plant growth promoters and biocontrol agents of Fusarium graminearum. Microbiol Res 186:37–43CrossRefGoogle Scholar
  41. Hložková K, Matěnová M, Žáčková P et al (2016) Characterization of three distinct metallothionein genes of the Ag-hyperaccumulating ectomycorrhizal fungus Amanita strobiliformis. Fungal Biol 120(3):358–369PubMedCrossRefGoogle Scholar
  42. Hodgson S, Cates C, Hodgson J et al (2014) Vertical transmission of fungal endophytes is widespread in forbs. Ecol Evol 4(8):1199–1208PubMedPubMedCentralCrossRefGoogle Scholar
  43. Hu N, Zhao B (2006) Key genes involved in heavy-metal resistance in Pseudomonas putida CD2. FEMS Microbiol Lett 267(1):17–22PubMedCrossRefGoogle Scholar
  44. Hubbard M, Germida J, Vujanovic V (2012) Fungal endophytes improve wheat seed germination under heat and drought stress. Botany 90(2):137–149CrossRefGoogle Scholar
  45. Hubbard M, Germida JJ, Vujanovic V (2014) Fungal endophytes enhance wheat heat and drought tolerance in terms of grain yield and second-generation seed viability. J Appl Microbiol 116(1):109–122PubMedCrossRefPubMedCentralGoogle Scholar
  46. Ikeda S, Fuji SI, Sato T et al (2006) Community analysis of seed-associated microbes in forage crops using culture-independent methods. Microb Environ 21(2):112–121CrossRefGoogle Scholar
  47. James D, Mathew S (2015) Antagonistic activity of endophytic microorganisms against bacterial wilt disease of tomato. Int J Curr Adv Res 4:399–404Google Scholar
  48. Job C, Rajjou L, Lovigny Y et al (2005) Patterns of protein oxidation in Arabidopsis seeds and during germination. Plant Physiol 138(2):790–802PubMedPubMedCentralCrossRefGoogle Scholar
  49. 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(6):e20396.
  50. Kaga H, Mano H, Tanaka F et al (2009) Rice seeds as sources of endophytic bacteria. Microb Environ 24(2):154–162CrossRefGoogle Scholar
  51. Kaul S, Sharma T, Dhar MK (2016) “Omics” tools for better understanding the plant–endophyte interactions. Front Plant Sci 7(955).
  52. Khalaf EM, Raizada MN (2016) Taxonomic and functional diversity of cultured seed associated microbes of the cucurbit family. BMC Microbiol 16(1):131PubMedPubMedCentralCrossRefGoogle Scholar
  53. Khalaf EM, Raizada MN (2018) Bacterial seed endophytes of domesticated cucurbits antagonize fungal and oomycete pathogens including powdery mildew. Front Microbiol 9:42PubMedPubMedCentralCrossRefGoogle Scholar
  54. Khan Z, Rehman A, Nisar MA et al (2017) Molecular basis of Cd+ 2 stress response in Candida tropicalis. Appl Microbiol Biotechnol 101(20):7715–7728PubMedCrossRefPubMedCentralGoogle Scholar
  55. Kharwar RN, Mishra A, Gond SK et al (2011) Anticancer compounds derived from fungal endophytes: their importance and future challenges. Nat Prod Rep 28(7):1208–1228PubMedCrossRefPubMedCentralGoogle Scholar
  56. Kharwar RN, Mishra A, Sharma VK et al (2014) Diversity and biopotential of endophytic fungal flora isolated from eight medicinal plants of Uttar Pradesh, India. In: Kharwar R, Upadhyay R, Dubey N, Raghuwanshi R (eds) Microbial diversity and biotechnology in food security. Springer, New Delhi, pp 23–39Google Scholar
  57. Krings M, Taylor TN, Hass H et al (2007) Fungal endophytes in a 400-million-yr-old land plant: infection pathways, spatial distribution, and host responses. New Phytol 174(3):648–657PubMedCrossRefPubMedCentralGoogle Scholar
  58. Leveille JH (1846) Considérations mycologiques, suivies d’une nouvelle classification des champignons. Imprimerie de I Martinet, ParisCrossRefGoogle Scholar
  59. Loebus J, Leitenmaier B, Meissner D et al (2013) The major function of a metallothionein from the aquatic fungus Heliscus lugdunensis is cadmium detoxification. J Inorg Biochem 127:253–260PubMedCrossRefGoogle Scholar
  60. Lopez BR, Tinoco-Ojanguren C, Bacilio M et al (2012) Endophytic bacteria of the rock-dwelling cactus Mammillaria fraileana affect plant growth and mobilization of elements from rocks. Environ Exp Bot 81:26–36CrossRefGoogle Scholar
  61. López JL, Alvarez F, Príncipe A et al (2017) Isolation, taxonomic analysis, and phenotypic characterization of bacterial endophytes present in alfalfa (Medicago sativa) seeds. J Biotechnol 267:55–62PubMedCrossRefGoogle Scholar
  62. Margaryan AA, Panosyan HH, Birkeland NK et al (2013) Heavy metal accumulation and the expression of the copA and nikA genes in Bacillus subtilis AG4 isolated from the Sotk Gold Mine in Armenia. Biol J Armenia 65(3):51–57Google Scholar
  63. Mastretta C, Taghavi S, Van Der Lelie D et al (2009) Endophytic bacteria from seeds of Nicotiana tabacum can reduce cadmium phytotoxicity. Int J Phytoremed 11(3):251–267CrossRefGoogle Scholar
  64. Maude RB (1996) Seed-borne diseases and their control: principles and practice. CAB International, WallingfordGoogle Scholar
  65. Maynaud G, Brunel B, Mornico D et al (2013) Genome-wide transcriptional responses of two metal-tolerant symbiotic Mesorhizobium isolates to zinc and cadmium exposure. BMC Genom 14(1):292CrossRefGoogle Scholar
  66. Mendarte-Alquisira C, Gutiérrez-Rojas M, González-Márquez H et al (2017) Improved growth and control of oxidative stress in plants of Festuca arundinacea exposed to hydrocarbons by the endophytic fungus Lewia sp. Plant Soil 411(1–2):347–358CrossRefGoogle Scholar
  67. Moffat AS (1999) Engineering plants to cope with metals. Science 285:369–370PubMedCrossRefPubMedCentralGoogle Scholar
  68. Monnet F, Vaillant N, Hitmi A et al (2001) Endophytic Neotyphodium lolii induced tolerance to Zn stress in Lolium perenne. Physiol Plantarum 113(4):557–563CrossRefGoogle Scholar
  69. Mundt JO, Hinkle NF (1976) Bacteria within ovules and seeds. Appl Environ Microbiol 32(5):694–698PubMedPubMedCentralGoogle Scholar
  70. Naveed M, Mitter B, Reichenauer TG et al (2014) Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17. Environ Exp Bot 97:30–39CrossRefGoogle Scholar
  71. Nelson EB (2004) Microbial dynamics and interactions in the spermosphere. Annu Rev Phytopathol 42:271–309PubMedCrossRefPubMedCentralGoogle Scholar
  72. Nelson EB (2018) The seed microbiome: origins, interactions, and impacts. Plant Soil 422(1–2):7–34CrossRefGoogle Scholar
  73. Ngugi HK, Scherm H (2006) Biology of flower-infecting fungi. Annu Rev Phytopathol 44:261–282PubMedCrossRefPubMedCentralGoogle Scholar
  74. Nies DH (1999) Microbial heavy-metal resistance. Appl Microbiol Biotechnol 51(6):730–750PubMedCrossRefPubMedCentralGoogle Scholar
  75. Parmar S, Singh V (2015) Phytoremediation approaches for heavy metal pollution: a review. J Plant Sci Res 2(2):135Google Scholar
  76. Petrini O (1991) Fungal endophytes of tree leaves. In: Andrews J, Hirano S (eds) Microbial ecology of leaves. Springer, New York, pp 179–197CrossRefGoogle Scholar
  77. Pitzschke A (2016) Developmental peculiarities and seed-borne endophytes in quinoa: omnipresent, robust bacilli contribute to plant fitness. Front Microbiol 7:2PubMedPubMedCentralCrossRefGoogle Scholar
  78. Pitzschke A (2018) Molecular dynamics in germinating, endophyte-colonized quinoa seeds. Plant Soil 422(1–2):135–154PubMedCrossRefPubMedCentralGoogle Scholar
  79. Puente ME, Li CY, Bashan Y (2009) Endophytic bacteria in cacti seeds can improve the development of cactus seedlings. Environ Exp Bot 66(3):402–408CrossRefGoogle Scholar
  80. Qin Y, Pan X, Yuan Z (2016) Seed endophytic microbiota in a coastal plant and phytobeneficial properties of the fungus Cladosporium cladosporioides. Fungal Ecol 24:53–60CrossRefGoogle Scholar
  81. Radhakrishnan R, Khan AL, Lee IJ (2013) Endophytic fungal pre-treatments of seeds alleviates salinity stress effects in soybean plants. J Microbiol 51(6):850–857PubMedCrossRefGoogle Scholar
  82. Roane TM, Pepper IL, Gentry TJ (2015) Microorganisms and metal pollutants. In: Pepper IL, Gerba CP, Gentry TJ (eds) Environmental Microbiology. Academic Press, Amsterdam, pp 415–439CrossRefGoogle Scholar
  83. Rudgers JA, Afkhami ME, Rúa MA et al (2009) A fungus among us: broad patterns of endophyte distribution in the grasses. Ecology 90(6):1531–1539PubMedCrossRefGoogle Scholar
  84. Sánchez-López AS, Thijs S, Beckers B et al (2018) Community structure and diversity of endophytic bacteria in seeds of three consecutive generations of Crotalaria pumila growing on metal mine residues. Plant Soil 422(1–2):51–66CrossRefGoogle Scholar
  85. Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109(6):661–686PubMedCrossRefPubMedCentralGoogle Scholar
  86. Selim KA, El-Beih AA, AbdEl-Rahman TM et al (2012) Biology of endophytic fungi. Curr Res Environ Appl Mycol 2(1):31–82CrossRefGoogle Scholar
  87. Shade A, Jacques MA, Barret M (2017) Ecological patterns of seed microbiome diversity, transmission, and assembly. Curr Opin Microbiol 37:15–22PubMedCrossRefPubMedCentralGoogle Scholar
  88. Shahzad R, Waqas M, Khan AL et al (2016) Seed-borne endophytic Bacillus amyloliquefaciens RWL-1 produces gibberellins and regulates endogenous phytohormones of Oryza sativa. Plant Physiol Biochem 106:236–243PubMedCrossRefPubMedCentralGoogle Scholar
  89. Shahzad R, Khan AL, Lee IJ (2018) What is there in seeds? Vertically transmitted endophytic resources for sustainable improvement in plant growth. Front Plant Sci 9:24PubMedPubMedCentralCrossRefGoogle Scholar
  90. Shearin ZR, Filipek M, Desai R et al (2018) Fungal endophytes from seeds of invasive, non-native Phragmites australis and their potential role in germination and seedling growth. Plant Soil 422(1–2):183–194CrossRefGoogle Scholar
  91. Sheibani-Tezerji R, Naveed M, Jehl MA et al (2015) The genomes of closely related Pantoea ananatis maize seed endophytes having different effects on the host plant differ in secretion system genes and mobile genetic elements. Front Microbiol 6:440PubMedPubMedCentralCrossRefGoogle Scholar
  92. Shen XY, Cheng YL, Cai CJ et al (2014) Diversity and antimicrobial activity of culturable endophytic fungi isolated from Moso bamboo seeds. PLoS One 9(4):e95838. Scholar
  93. Shen M, Zhao DK, Qiao Q et al (2015) Identification of glutathione S-transferase (GST) genes from a dark septate endophytic fungus (Exophiala pisciphila) and their expression patterns under varied metals stress. PLoS One 10(4):e0123418. Scholar
  94. Shine AM, Shakya VP, Idnurm A (2015) Phytochelatin synthase is required for tolerating metal toxicity in a basidiomycete yeast and is a conserved factor involved in metal homeostasis in fungi. Fungal Biol Biotechnol 2(1):3PubMedPubMedCentralCrossRefGoogle Scholar
  95. Siegel MR, Latch GC (1991) Expression of antifungal activity in agar culture by isolates of grass endophytes. Mycologia 83:529–537CrossRefGoogle Scholar
  96. Siegel MR, Johnson MC, Varney DR et al (1984) A fungal endophyte in tall fescue: incidence and dissemination. Phytopathology 74(8):932–937CrossRefGoogle Scholar
  97. Singh D, Geat N, Rajawat MVS et al (2018) Deciphering the mechanisms of endophyte-mediated biofortification of Fe and Zn in wheat. J Plant Growth Regul 37(1):174–182CrossRefGoogle Scholar
  98. Smith SA, Tank DC, Boulanger LA et al (2008) Bioactive endophytes warrant intensified exploration and conservation. PLoS One 3(8):e3052. Scholar
  99. Soleimani M, Hajabbasi MA, Afyuni M et al (2010) Effect of endophytic fungi on cadmium tolerance and bioaccumulation by Festuca arundinacea and Festuca pratensis. Int J Phytoremed 12(6):535–549CrossRefGoogle Scholar
  100. Strobel GA (2003) Endophytes as sources of bioactive products. Microbes Infect 5(6):535–544PubMedCrossRefPubMedCentralGoogle Scholar
  101. Strobel G, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67(4):491–502PubMedPubMedCentralCrossRefGoogle Scholar
  102. Su C, Jiang L, Zhang W (2014) A review on heavy metal contamination in the soil worldwide: situation, impact and remediation techniques. Environ Skeptics Critics 3(2):24–38Google Scholar
  103. Sun Y, Wang Q, Lu X et al (2012) Endophytic fungal community in stems and leaves of plants from desert areas in China. Mycol Prog 11(3):781–790CrossRefGoogle Scholar
  104. Sundaramoorthy S, Balabaskar P (2013) Evaluation of combined efficacy of Pseudomonas fluorescens and Bacillus subtilis in managing tomato wilt caused by Fusarium oxysporum f. sp. lycopersici (Fol). Plant Pathol J 12(4):154–161CrossRefGoogle Scholar
  105. Tan RX, Zou WX (2001) Endophytes: a rich source of functional metabolites. Nat Prod Rep 18(4):448–459PubMedCrossRefPubMedCentralGoogle Scholar
  106. Tiller KG (1992) Urban soil contamination in Australia. Soil Res 30(6):937–957CrossRefGoogle Scholar
  107. Timmusk S, Paalme V, Pavlicek T et al (2011) Bacterial distribution in the rhizosphere of wild barley under contrasting microclimates. PLoS One 6(3):e17968. Scholar
  108. Topalidis V, Harris A, Hardaway CJ et al (2017) Investigation of selected metals in soil samples exposed to agricultural and automobile activities in Macedonia, Greece using inductively coupled plasma-optical emission spectrometry. Microchem J 130:213–220CrossRefGoogle Scholar
  109. Truyens S, Weyens N, Cuypers A et al (2013) Changes in the population of seed bacteria of transgenerationally Cd-exposed Arabidopsis thaliana. Plant Biol 15(6):971–981PubMedCrossRefPubMedCentralGoogle Scholar
  110. Truyens S, Jambon I, Croes S et al (2014) The effect of long-term Cd and Ni exposure on seed endophytes of Agrostis capillaris and their potential application in phytoremediation of metal-contaminated soils. Int J Phytoremed 16(7–8):643–659CrossRefGoogle Scholar
  111. Truyens S, Weyens N, Cuypers A et al (2015) Bacterial seed endophytes: genera, vertical transmission and interaction with plants. Environ Microbiol Rep 7(1):40–50CrossRefGoogle Scholar
  112. Truyens S, Beckers B, Thijs S et al (2016) Cadmium-induced and trans-generational changes in the cultivable and total seed endophytic community of Arabidopsis thaliana. Plant Biol 18(3):376–381PubMedCrossRefPubMedCentralGoogle Scholar
  113. Unger F (1833) Die Exantheme der Pflanzen und einige mit diesen verwandte Krankheiten der Gewächse. Carl Gerold, Wien, p 421Google Scholar
  114. Vandenkoornhuyse P, Quaiser A, Duhamel M et al (2015) The importance of the microbiome of the plant holobiont. New Phytol 206(4):1196–1206CrossRefGoogle Scholar
  115. Vega FE, Simpkins A, Aime MC et al (2010) Fungal endophyte diversity in coffee plants from Colombia, Hawai’i, Mexico and Puerto Rico. Fungal Ecol 3(3):122–138CrossRefGoogle Scholar
  116. Verma VC, Kharwar RN, Strobel GA (2009) Chemical and functional diversity of natural products from plant associated endophytic fungi. Nat Prod Commun 4(11):1511–1532PubMedPubMedCentralGoogle Scholar
  117. Vujanovic V, Germida JJ (2017) Seed endosymbiosis: a vital relationship in providing prenatal care to plants. Can J Plant Sci 97(6):972–981Google Scholar
  118. Vujanovic V, St-Arnaud M, Barabé D et al (2000) Viability testing of orchid seed and the promotion of colouration and germination. Ann Bot 86(1):79–86CrossRefGoogle Scholar
  119. Walitang DI, Kim K, Madhaiyan M et al (2017) Characterizing endophytic competence and plant growth promotion of bacterial endophytes inhabiting the seed endosphere of Rice. BMC Microbiol 17(1):209PubMedPubMedCentralCrossRefGoogle Scholar
  120. Walitang DI, Kim CG, Jeon S et al (2018) Conservation and transmission of seed bacterial endophytes across generations following crossbreeding and repeated inbreeding of rice at different geographic locations. Microbiol Open.
  121. Welty RE, Craig AM, Azevedo MD (1994) Variability of ergovaline in seeds and straw and endophyte infection in seeds among endophyte-infected genotypes of tall fescue. Plant Dis 78(9):845–849CrossRefGoogle Scholar
  122. West CP (1994) Physiology and drought tolerance of endophyte-infected grasses. In: Bacon CW, White JF Jr (eds) Biotechnology of endophytic fungi of grasses. CRC, Boca Raton, FL, pp 87–99Google Scholar
  123. Wiewióra B, Żurek G, Żurek M (2015) Endophyte-mediated disease resistance in wild populations of perennial ryegrass (Lolium perenne). Fungal Ecol 15:1–8CrossRefGoogle Scholar
  124. Wilkinson HH, Siegel MR, Blankenship JD et al (2000) Contribution of fungal loline alkaloids to protection from aphids in a grass-endophyte mutualism. Mol Plant Microbe Interact 13(10):1027–1033PubMedCrossRefGoogle Scholar
  125. Wu W, Huang H, Ling Z et al (2016) Genome sequencing reveals mechanisms for heavy metal resistance and polycyclic aromatic hydrocarbon degradation in Delftia lacustris strain LZ-C. Ecotoxicology 25(1):234–247PubMedCrossRefGoogle Scholar
  126. Xie P, Hao X, Herzberg M et al (2015) Genomic analyses of metal resistance genes in three plant growth promoting bacteria of legume plants in Northwest mine tailings, China. J Environ Sci 27:179–187CrossRefGoogle Scholar
  127. Zhang J, Huang W (2000) Advances on physiological and ecological effects of cadmium on plants. Acta Ecol Sin 20(3):514–523Google Scholar
  128. Zhang X, Fan X, Li C et al (2010) Effects of cadmium stress on seed germination, seedling growth and antioxidative enzymes in Achnatherum inebrians plants infected with a Neotyphodium endophyte. Plant Growth Regul 60(2):91–97CrossRefGoogle Scholar
  129. Zhang X, Lin L, Chen M et al (2012a) A nonpathogenic Fusarium oxysporum strain enhances phytoextraction of heavy metals by the hyperaccumulator Sedum alfredii Hance. J Hazard Mater 229:361–370PubMedCrossRefPubMedCentralGoogle Scholar
  130. Zhang X, Li C, Nan Z (2012b) Effects of cadmium stress on seed germination and seedling growth of Elymus dahuricus infected with the Neotyphodium endophyte. Sci China Life Sci 55(9):793–799PubMedCrossRefPubMedCentralGoogle Scholar
  131. Zhang X, Wei W, Tan R (2015) Symbionts, a promising source of bioactive natural products. Sci China Chem 58(7):1097–1109CrossRefGoogle Scholar
  132. Zhang J, Zhang C, Yang J et al (2018) Insights into endophytic bacterial community structures of seeds among various Oryza sativa L. rice genotypes. J Plant Growth Regul.

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Haiyan Li
    • 1
  • Shobhika Parmar
    • 1
  • Vijay K. Sharma
    • 1
  • James Francis WhiteJr
    • 2
  1. 1.Medical School of Kunming University of Science and TechnologyKunmingChina
  2. 2.Department of Plant BiologyRutgers UniversityNew BrunswickUSA

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