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Disease protection and allelopathic interactions of seed-transmitted endophytic pseudomonads of invasive reed grass (Phragmites australis)

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Abstract

Background and aims

Non-native Phragmites australis (haplotype M) is an invasive grass that decreases biodiversity and produces dense stands. We hypothesized that seeds of Phragmites carry microbes that improve seedling growth, defend against pathogens and maximize capacity of seedlings to compete with other plants.

Methods

We isolated bacteria from seeds of Phragmites, then evaluated representatives for their capacities to become intracellular in root cells, and their effects on: 1.) germination rates and seedling growth, 2.) susceptibility to damping-off disease, and 3.) mortality and growth of competitor plant seedlings (dandelion (Taraxacum officionale F. H. Wigg) and curly dock (Rumex crispus L.)).

Results

Ten strains (of 23 total) were identified and characterized; seven were identified as Pseudomonas spp. Strains Sandy LB4 (Pseudomonas fluorescens) and West 9 (Pseudomonas sp.) entered root meristems and became intracellular. These bacteria improved seed germination in Phragmites and increased seedling root branching in Poa annua. They increased plant growth and protected plants from damping off disease. Sandy LB4 increased mortality and reduced growth rates in seedlings of dandelion and curly dock.

Conclusions

Phragmites plants associate with endophytes to increase growth and disease resistance, and release bacteria into the soil to create an environment that is favorable to their seedlings and less favorable to competitor plants.

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References

  • Aloysius SKD, Paton AM (1984) Artificially induced symbiotic associations of L-form bacteria and plants. J Appl Bacteriol 56:465–477

    Article  Google Scholar 

  • Arnold AE, Lutzoni F (2007) Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88:541–549. doi:10.1890/05-1459

    Article  PubMed  Google Scholar 

  • Beltran-Garcia M, White JF, Prado FM, Prieto KR, Yamaguchi LF, Torres MS, Kato MJ, Madeiros HG, Di Mascio P (2014) Nitrogen acquisition in Agave tequilana from degradation of endophytic bacteria. Sci Report 4:6938. doi:10.1038/srep06938

    Article  CAS  Google Scholar 

  • Clay K (1988) Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 69:10–16

    Article  Google Scholar 

  • Clay K, Shearin ZRC, Bourke KA, Bickford WA, Kowalski KP (2016) Diversity of fungal endophytes in non-native Phragmites australis in the Great Lakes. Biol Invasions. doi:10.1007/s10530-016-1137y

    Google Scholar 

  • Compant S, Duffy B, Nowak J, Clément C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Ernst M, Mendgen KW, Wirsel SG (2003) Endophytic fungal mutualists: seedborne Stagonospora spp enhance reed biomass production in axenic microcosms. Mol Plant-Microbe Interact 16:580–587

    Article  CAS  PubMed  Google Scholar 

  • Fischer MS, Rodriguez RJ (2013) Fungal endophytes of invasive Phragmites australis populations vary in species composition and fungicide susceptibility. Symbiosis 61:55–62

    Article  CAS  Google Scholar 

  • Gond SK, Bergen MS, Torres MS, White JF (2015) Effect of bacterial endophyte on expression of defense genes in Indian popcorn against Fusarium moniliforme. Symbiosis 66:133–140. doi:10.1007/s13199-015-0348-9

    Article  CAS  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 

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

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hurek T, Handley L, Reinhold-Hurek B, Piché Y (2002) Azoarcus grass endophytes contribute fixed nitrogen to the plant in an unculturable state. Mol Plant-Microbe Interact 15:233–242

    Article  CAS  PubMed  Google Scholar 

  • Johnston-Monje D, Lundberg DS, Lazarovits G, Reis VM, Raizada MN (2016) Bacterial populations in juvenile maize rhizospheres originate from both seed and soil. Plant Soil 405(1):337–355

    Article  CAS  Google Scholar 

  • Kloepper JW, Ryu CM, Zhang S (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259–1266

    Article  CAS  PubMed  Google Scholar 

  • Kowalski KP, Bacon C, Bickford W, Braun H, Clay K et al (2015) Advancing the science of microbial symbiosis to support invasive species management: a case study on Phragmites in the great lakes. Front Microbiol 6:1–14

    Article  Google Scholar 

  • Lamb TG, Tonkyn DW, Kluepfel DA (1996) Movement of Pseudomonas aureofaciens from the rhizosphere to aerial plant tissue. Can J Microbiol 42:1112–1120

    Article  CAS  Google Scholar 

  • Lane DJ (1991) 16S/23S rRNA sequencing. In: Goodfellow M, Stackebrandt E (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 115–175

    Google Scholar 

  • Li HY, Zhu JN, Zhai ZH, Zhang Q (2010) Endophytic bacterial diversity in roots of Phragmites australis in constructed Beijing Cuihu wetland (China). FEMS Microbiol Lett 309:84–93

    CAS  PubMed  Google Scholar 

  • Li HY, Li DW, He CM, Zhou ZP, Mei T, Xu HM (2012) Diversity and heavy metal tolerance of endophytic fungi from six dominant plant species in a Pb–Zn mine wasteland. China Fungal Ecology 5:309–315

    Article  Google Scholar 

  • Ligon JM, Hill DS, Hammer PE, Torkewitz NR, Hoffman D, Kempf H-J, van Pee K-H (2000) Natural products with antifungal activity from Pseudomonas biocontrol bacteria. Pest Manag Sci 56:688–695

    Article  CAS  Google Scholar 

  • Paungfoo-Lonhienne C, Rentsch D, Robatzek S, Webb R, Sagulenko E, Nasholm T, Schmidt S, Lonhienne T (2010) Turning the table: plants consume microbes as a source of nutrients. PLoS One 5(7):e11915

    Article  PubMed  PubMed Central  Google Scholar 

  • Paungfoo-Lonhienne C, Schmidt S, Webb R, Lonhienne T (2014) Rhizophagy—A New Dimension of Plant–Microbe Interactions. In: de Briujn FJ (ed) Molecular Microbial Ecology of the Rhizosphere. doi:10.1002/9781118297674.ch115

    Google Scholar 

  • Petti CA (2007) Detection and identification of microorganisms by gene amplification and sequencing. Medical Microbiology 44:1108–1114

    CAS  Google Scholar 

  • Puente ME, Li C, Bashan Y (2009) Rock-degrading endophytic bacteria in cacti. Environ Exp Bot 66:389–401

    Article  CAS  Google Scholar 

  • Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM (2002) Thermotolerance generated by plant/fungal symbiosis. Science 298:1581

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez RK, Henson J, van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim Y-O, Redman RS (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2(4):404–416

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Rout ME, Chrzanowski TH (2009) The invasive Sorghum halepense harbors endophytic N2-fixing bacteria and alters soil biogeochemistry. Plant Soil 315:163. doi:10.1007/s11104-008-9740-z

    Article  CAS  Google Scholar 

  • Rudrappa T, Bonsall J, Gallagher JL, Seliskar DM, Bais HP (2007) Root-secreted allelochemical in the noxious weed Phragmites australis deploys a reactive oxygen species response and microtubule assembly disruption to execute rhizo-toxicity. J Chem Ecol 33:1898–1918

    Article  CAS  PubMed  Google Scholar 

  • Rudrappa T, Choi YS, Levia DF, Legates DR, Lee KH, Bais HP (2009) Phragmites australis root secreted phytotoxin undergoes photo-degredation to execute severe phototoxicity. Plant Signal Behav 4(6):506–513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schulz B, Boyle C (2006) What are endophytes? In: Scultz B, Boyle C, Sieber T (eds) Microbial root endophytes. Springer-Verlag, Berlin, pp 1–10

    Chapter  Google Scholar 

  • Sharma SB, Sayyed RZ, Trivedi MH, Gobi TA (2013) Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. SpringerPlus 2:587

    Article  PubMed  PubMed Central  Google Scholar 

  • Soares MA, Li HY, Bergen M, da Silva JM, Kowalski K, White JF (2015) Functional role of an endophytic Bacillus amyloliquefaciens in enhancing growth and disease protection of invasive English ivy (Hedera helix L.). Plant Soil. doi:10.1007/s11104-015-2638-7

    Google Scholar 

  • Soares MA, Li HY, Kowalski KP, Bergen M, Torres MS, White JF (2016a) Functional role of bacteria from invasive Phragmites australis in promotion of host growth. Microb Ecol. doi:10.1007/s00248-016-0793-x

    PubMed Central  Google Scholar 

  • Soares MA, Li HY, Kowalski KP, Bergen M, Torres MS, White JF (2016b) Evaluation of the functional roles of fungal endophytes of Phragmites australis from high and low saline sites. Biol Invasions. doi:10.1007/s10530-016-1160-z

    Google Scholar 

  • Stone JK, Bacon CW, White JW (2000) An overview of endophytic microbes: endophytism defined. In: Bacon CW, White JF (eds) Microbial endophytes. Marcel-Dekker, New York, pp 3–30

    Google Scholar 

  • Uddin MN, Robinson RW, Caridi D, Harun AY (2014) Is phytotoxity of Phragmites australis residue influenced by decomposition condition, time and density? Mar Freshw Res 65:505–516

    Article  CAS  Google Scholar 

  • Visca P, Imperi F, Lamont IL (2006) Pyoverdine siderophores: from biogenesis to biosignificance. Trends Microbiol 15:22–30

    Article  PubMed  Google Scholar 

  • Weidenhamer JD, Li M, Allman J, Bergosh RG, Posner M (2013) Evidence does not support a role for gallic acid in Phragmites australis invasion success. J Chem Ecol 39:323–332

    Article  CAS  PubMed  Google Scholar 

  • White JF, Torres MS (2009) Is plant endophyte-mediated defensive mutualism the result of oxidative stress protection? Physiol Plant 138(4):440–446. doi:10.1111/j.1399-3054.2009.01332

    Article  PubMed  Google Scholar 

  • White JF, Crawford H, Torres MS, Mattera R, Irizarry I, Bergen MS (2012) A proposed mechanism for nitrogen acquisition by grass seedlings through oxidation of symbiotic bacteria. Symbiosis 57:61–171. doi:10.1007/s13199-012-01

    Article  Google Scholar 

  • White JF, Torres MS, Somu MP, Johnson H, Irizarry I, Chen Q, Zhang N, Walsh E, Tadych M, Bergen M (2014) Hydrogen peroxide staining to visualize intracellular bacterial infections of seedling root cells. Microsc Res Tech. doi:10.1002/jemt.22375

    Google Scholar 

  • White JF, Chen Q, Torres MS, Mattera R, Irizarry I, Tadych M, Bergen M (2015) Collaboration between grass seedlings and rhizobacteria to scavenge organic nitrogen in soils. AoB Plants. doi:10.1093/aobpla/plu093

    PubMed  PubMed Central  Google Scholar 

  • Zeller S, Brandl H, Schmid B (2007) Host-plant selectivity of rhizobacteria in crop/weed model system. PLoS One 2(9):e846. doi:10.1371/journal.pone.0000846

    Article  PubMed  PubMed Central  Google Scholar 

  • Zolg W, Ottow JCG (1975) Pseudomonas glathei sp. nov. a new nitrogen scavenging rod isolated from acid lateritic relicts in Germany. Z Allg Mikrobiol 15:287–299

    Article  Google Scholar 

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Acknowledgements

The authors are grateful for support from the John E. and Christina C. Craighead Foundation, USDA-NIFA Multistate Project W3147, the New Jersey Agricultural Experiment Station, the United States Geological Survey Cooperative Ecosystems Study Unit Agreement G13 AC00291, the Federal University of Mato Grosso (UFMT), The Brazilian National Council for Scientific and Technological Development (CNPq) for Post-doctoral Fellowship and the International Institute of Science and Technology in Wetlands (INAU). Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

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Correspondence to James F. White.

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White, J.F., Kingsley, K.I., Kowalski, K.P. et al. Disease protection and allelopathic interactions of seed-transmitted endophytic pseudomonads of invasive reed grass (Phragmites australis). Plant Soil 422, 195–208 (2018). https://doi.org/10.1007/s11104-016-3169-6

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