A Hypothetical Bottleneck in the Plant Microbiome
Abstract
The plant microbiome may be bottlenecked at the level of endophytes of individual seeds. Strong defense of developing seeds is predicted by optimal defense theory, and we have experimentally demonstrated exclusionary interactions among endophytic microbes infecting individual seeds of Centaurea stoebe. Having found a single, PDA-culturable microbe per seed or none in an exploratory study with Centaurea stoebe, we completed a more extensive survey of an additional 98 plant species representing 39 families. We again found that individual, surface-sterilized seeds of all species hosted only one PDA-culturable bacterial or fungal endophyte per seed, or none. PDA- unculturables were not determined but we expect them to also be bottlenecked in individual seeds, as they too should be governed by exclusionary interactions. If the bottleneck were confirmed with high-throughput sequencing of individual seeds then it would make sense to further investigate the Primary Symbiont Hypothesis (PSH). This includes the prediction that primary symbionts (i.e., the winners of the exclusionary battles among seed endophytes) have strong effects on seedlings depending on symbiont identity.
- Authors:
- Publication Date:
- Research Org.:
- Univ. of Idaho, Moscow, ID (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1462287
- Alternate Identifier(s):
- OSTI ID: 1510447
- Grant/Contract Number:
- SC0014547
- Resource Type:
- Published Article
- Journal Name:
- Frontiers in Microbiology
- Additional Journal Information:
- Journal Name: Frontiers in Microbiology Journal Volume: 9; Journal ID: ISSN 1664-302X
- Publisher:
- Frontiers Media SA
- Country of Publication:
- Switzerland
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; seeds; maternal transmission; plant microbiome; priority effects; fungi; bacteria
Citation Formats
Newcombe, George, Harding, Abby, Ridout, Mary, and Busby, Posy E. A Hypothetical Bottleneck in the Plant Microbiome. Switzerland: N. p., 2018.
Web. doi:10.3389/fmicb.2018.01645.
Newcombe, George, Harding, Abby, Ridout, Mary, & Busby, Posy E. A Hypothetical Bottleneck in the Plant Microbiome. Switzerland. doi:https://doi.org/10.3389/fmicb.2018.01645
Newcombe, George, Harding, Abby, Ridout, Mary, and Busby, Posy E. Tue .
"A Hypothetical Bottleneck in the Plant Microbiome". Switzerland. doi:https://doi.org/10.3389/fmicb.2018.01645.
@article{osti_1462287,
title = {A Hypothetical Bottleneck in the Plant Microbiome},
author = {Newcombe, George and Harding, Abby and Ridout, Mary and Busby, Posy E.},
abstractNote = {The plant microbiome may be bottlenecked at the level of endophytes of individual seeds. Strong defense of developing seeds is predicted by optimal defense theory, and we have experimentally demonstrated exclusionary interactions among endophytic microbes infecting individual seeds of Centaurea stoebe. Having found a single, PDA-culturable microbe per seed or none in an exploratory study with Centaurea stoebe, we completed a more extensive survey of an additional 98 plant species representing 39 families. We again found that individual, surface-sterilized seeds of all species hosted only one PDA-culturable bacterial or fungal endophyte per seed, or none. PDA- unculturables were not determined but we expect them to also be bottlenecked in individual seeds, as they too should be governed by exclusionary interactions. If the bottleneck were confirmed with high-throughput sequencing of individual seeds then it would make sense to further investigate the Primary Symbiont Hypothesis (PSH). This includes the prediction that primary symbionts (i.e., the winners of the exclusionary battles among seed endophytes) have strong effects on seedlings depending on symbiont identity.},
doi = {10.3389/fmicb.2018.01645},
journal = {Frontiers in Microbiology},
number = ,
volume = 9,
place = {Switzerland},
year = {2018},
month = {7}
}
Free Publicly Available Full Text
Publisher's Version of Record
DOI: https://doi.org/10.3389/fmicb.2018.01645
DOI: https://doi.org/10.3389/fmicb.2018.01645
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 1 work
Citation information provided by
Web of Science
Web of Science
Figures / Tables:
Table 1: Proportion of seeds either without (i.e., ‘zero’) or with one or two PDA-culturable endophytes per surface-sterilized seed (70 seeds per species for 98 plant species from 39 families).
All figures and tables
(2 total)
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
EFFECTS of DIFFERENT STORAGE CONDITIONS ON PRESERVATION of COCONUT (Cocos nucifera) WATER
journal, February 1992
- Maciel, M. I.; Oliveira, S. L.; Silva, I. P.
- Journal of Food Processing and Preservation, Vol. 16, Issue 1
Optimal Defense Theory Predicts the Ontogeny of an Induced Nicotine Defense
journal, July 2000
- Ohnmeiss, Thomas E.; Baldwin, Ian T.
- Ecology, Vol. 81, Issue 7
Functional role of an endophytic Bacillus amyloliquefaciens in enhancing growth and disease protection of invasive English ivy (Hedera helix L.)
journal, August 2015
- Soares, Marcos Antônio; Li, Hai-Yan; Bergen, Marshall
- Plant and Soil, Vol. 405, Issue 1-2
Fungal endophytes in seeds and needles of Pinus monticola
journal, March 2006
- Ganley, Rebecca J.; Newcombe, George
- Mycological Research, Vol. 110, Issue 3
Bacterial populations in juvenile maize rhizospheres originate from both seed and soil
journal, March 2016
- Johnston-Monje, David; Lundberg, Derek S.; Lazarovits, George
- Plant and Soil, Vol. 405, Issue 1-2
Fungal endophyte increases the allelopathic effects of an invasive forb
journal, February 2014
- Aschehoug, Erik T.; Callaway, Ragan M.; Newcombe, George
- Oecologia, Vol. 175, Issue 1
Food consumption trends and drivers
journal, September 2010
- Kearney, John
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 365, Issue 1554
Endophytic Fungal Mutualists: Seed-Borne Stagonospora Spp. Enhance Reed Biomass Production in Axenic Microcosms
journal, July 2003
- Ernst, Michael; Mendgen, Kurt W.; Wirsel, Stefan G. R.
- Molecular Plant-Microbe Interactions, Vol. 16, Issue 7
Evolution of endophyte?plant symbioses
journal, June 2004
- Saikkonen, K.
- Trends in Plant Science, Vol. 9, Issue 6
Niches and routes of transmission of Xanthomonas citri pv. fuscans to bean seeds
journal, July 2017
- Darrasse, Armelle; Barret, Matthieu; Cesbron, Sophie
- Plant and Soil, Vol. 422, Issue 1-2
Evolution, consequences and future of plant and animal domestication
journal, August 2002
- Diamond, Jared
- Nature, Vol. 418, Issue 6898
Out Of The Quagmire Of Plant Defense Hypotheses
journal, March 2003
- Stamp, Nancy
- The Quarterly Review of Biology, Vol. 78, Issue 1
Symbiosis Lost: Imperfect Vertical Transmission of Fungal Endophytes in Grasses
journal, September 2008
- Afkhami, Michelle E.; Rudgers, Jennifer A.
- The American Naturalist, Vol. 172, Issue 3
Exclusionary interactions among diverse fungi infecting developing seeds of Centaurea stoebe
journal, December 2012
- Raghavendra, Anil Kumar H.; Newcombe, George; Shipunov, Alexey
- FEMS Microbiology Ecology, Vol. 84, Issue 1
Imperfect Vertical Transmission of the Endophyte Neotyphodium in Exotic Grasses in Grasslands of the Flooding Pampa
journal, September 2008
- Gundel, Pedro E.; Garibaldi, Lucas A.; Tognetti, Pedro M.
- Microbial Ecology, Vol. 57, Issue 4
Endophyte Microbiome Diversity in Micropropagated Atriplex canescens and Atriplex torreyi var griffithsii
journal, March 2011
- Lucero, Mary E.; Unc, Adrian; Cooke, Peter
- PLoS ONE, Vol. 6, Issue 3
Defining the core Arabidopsis thaliana root microbiome
journal, August 2012
- Lundberg, Derek S.; Lebeis, Sarah L.; Paredes, Sur Herrera
- Nature, Vol. 488, Issue 7409
Exposure to the leaf litter microbiome of healthy adults protects seedlings from pathogen damage
journal, July 2017
- Christian, Natalie; Herre, Edward Allen; Mejia, Luis C.
- Proceedings of the Royal Society B: Biological Sciences, Vol. 284, Issue 1858
Research priorities for harnessing plant microbiomes in sustainable agriculture
journal, March 2017
- Busby, Posy E.; Soman, Chinmay; Wagner, Maggie R.
- PLOS Biology, Vol. 15, Issue 3
Evolutionary ecology of pungency in wild chilies
journal, August 2008
- Tewksbury, J. J.; Reagan, K. M.; Machnicki, N. J.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 33
Zika Virus Infection in Pregnant Women in Rio de Janeiro
journal, December 2016
- Brasil, Patrícia; Pereira, José P.; Moreira, M. Elisabeth
- New England Journal of Medicine, Vol. 375, Issue 24
NRT/PTR transporters are essential for translocation of glucosinolate defence compounds to seeds
journal, August 2012
- Nour-Eldin, Hussam Hassan; Andersen, Tonni Grube; Burow, Meike
- Nature, Vol. 488, Issue 7412
Bacterial seed endophytes: genera, vertical transmission and interaction with plants: Bacterial seed endophytes
journal, June 2014
- Truyens, Sascha; Weyens, Nele; Cuypers, Ann
- Environmental Microbiology Reports, Vol. 7, Issue 1
Plant domestication and the assembly of bacterial and fungal communities associated with strains of the common sunflower, Helianthus annuus
journal, November 2016
- Leff, Jonathan W.; Lynch, Ryan C.; Kane, Nolan C.
- New Phytologist, Vol. 214, Issue 1
Fungal endophytes limit pathogen damage in a tropical tree
journal, December 2003
- Arnold, A. E.; Mejia, L. C.; Kyllo, D.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 26
Polyphenol oxidase as a biochemical seed defense mechanism
journal, December 2014
- Fuerst, E. P.; Okubara, Patricia A.; Anderson, James V.
- Frontiers in Plant Science, Vol. 5
The Effect of Imperfect Transmission on the Frequency of Mutualistic Seed-Borne Endophytes in Natural Populations of Grasses
journal, October 1997
- Ravel, Catherine; Michalakis, Yannis; Charmet, Gilles
- Oikos, Vol. 80, Issue 1
Relocation, high-latitude warming and host genetic identity shape the foliar fungal microbiome of poplars
journal, December 2014
- Bálint, Miklós; Bartha, László; O'Hara, Robert B.
- Molecular Ecology, Vol. 24, Issue 1
Fungal endophytes: modifiers of plant disease
journal, December 2015
- Busby, Posy E.; Ridout, Mary; Newcombe, George
- Plant Molecular Biology, Vol. 90, Issue 6
A pantropically introduced tree is followed by specific ectomycorrhizal symbionts due to pseudo-vertical transmission
journal, March 2018
- Séne, Seynabou; Selosse, Marc-André; Forget, Mathieu
- The ISME Journal, Vol. 12, Issue 7
Competitiveness of endophytic Phialocephala fortinii s.l. – Acephala applanata strains in Norway spruce roots
journal, May 2018
- Stroheker, Sophie; Dubach, Vivanne; Sieber, Thomas N.
- Fungal Biology, Vol. 122, Issue 5
Inheritance of Carboxin Resistance in a European Field Isolate of Ustilago nuda
journal, February 2000
- Newcombe, G.; Thomas, P. L.
- Phytopathology, Vol. 90, Issue 2
Cost Of Chemically Defending Seeds: Furanocoumarins And Pastinaca Sativa
journal, October 1997
- Zangerl, A. R.; Berenbaum, M. R.
- The American Naturalist, Vol. 150, Issue 4
Terroir is a key driver of seed-associated microbial assemblages: Terroir shapes the seed microbiota
journal, August 2015
- Klaedtke, Stephanie; Jacques, Marie-Agnès; Raggi, Lorenzo
- Environmental Microbiology, Vol. 18, Issue 6
Revisiting the Life Cycle of Dung Fungi, Including Sordaria fimicola
journal, February 2016
- Newcombe, George; Campbell, Jason; Griffith, David
- PLOS ONE, Vol. 11, Issue 2
Seeking the elusive function of the root-colonising dark septate endophytic fungi
journal, January 2005
- Mandyam, Keerthi; Jumpponen, Ari
- Studies in Mycology, Vol. 53
Aerial Warfare: A Volatile Dialogue between the Plant Pathogen Verticillium longisporum and Its Antagonist Paenibacillus polymyxa
journal, July 2017
- Rybakova, Daria; Rack-Wetzlinger, Ute; Cernava, Tomislav
- Frontiers in Plant Science, Vol. 8
Mom Knows Best: The Universality of Maternal Microbial Transmission
journal, August 2013
- Funkhouser, Lisa J.; Bordenstein, Seth R.
- PLoS Biology, Vol. 11, Issue 8
Symbioses of Grasses with Seedborne Fungal Endophytes
journal, June 2004
- Schardl, Christopher L.; Leuchtmann, Adrian; Spiering, Martin J.
- Annual Review of Plant Biology, Vol. 55, Issue 1
Influence of Certain Fungi on Seed Germination and Seedling Survival of Four Colonizing Annuals
journal, August 1979
- Kirkpatrick, B. L.; Bazzaz, F. A.
- The Journal of Applied Ecology, Vol. 16, Issue 2
Common foliar fungi of Populus trichocarpa modify Melampsora rust disease severity
journal, November 2015
- Busby, Posy E.; Peay, Kabir G.; Newcombe, George
- New Phytologist, Vol. 209, Issue 4
The seed microbiome: Origins, interactions, and impacts
journal, May 2017
- Nelson, Eric B.
- Plant and Soil, Vol. 422, Issue 1-2
Simultaneous profiling of seed-associated bacteria and fungi reveals antagonistic interactions between microorganisms within a shared epiphytic microbiome on Triticum and Brassica seeds
journal, January 2014
- Links, Matthew G.; Demeke, Tigst; Gräfenhan, Tom
- New Phytologist, Vol. 202, Issue 2
Mortality of infected and uninfected infants born to HIV-infected mothers in Africa: a pooled analysis
journal, October 2004
- Newell, Marie-Louise; Coovadia, Hoosen; Cortina-Borja, Marjo
- The Lancet, Vol. 364, Issue 9441
Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers
journal, May 2007
- Arnold, A. Elizabeth
- Fungal Biology Reviews, Vol. 21, Issue 2-3
Interactions Between the Microbiota and the Immune System
journal, June 2012
- Hooper, L. V.; Littman, D. R.; Macpherson, A. J.
- Science, Vol. 336, Issue 6086
Distribution and dispersal of Xylaria endophytes in two tree species in Puerto Rico
journal, August 1998
- Bayman, Paul; Angulo-Sandoval, Pilar; Báez-ortiz, Zoila
- Mycological Research, Vol. 102, Issue 8
Disease suppression in winter wheat from novel symbiosis with forest fungi
journal, April 2016
- Ridout, Mary; Newcombe, George
- Fungal Ecology, Vol. 20
The defensive role of foliar endophytic fungi for a South American tree
journal, January 2016
- González-Teuber, Marcia
- AoB Plants, Vol. 8
Ecological patterns of seed microbiome diversity, transmission, and assembly
journal, June 2017
- Shade, Ashley; Jacques, Marie-Agnès; Barret, Matthieu
- Current Opinion in Microbiology, Vol. 37
Content of redox-active compounds (ie, antioxidants) in foods consumed in the United States
journal, June 2006
- Halvorsen, Bente L.; Carlsen, Monica H.; Phillips, Katherine M.
- The American Journal of Clinical Nutrition, Vol. 84, Issue 1
Socially transmitted gut microbiota protect bumble bees against an intestinal parasite
journal, November 2011
- Koch, H.; Schmid-Hempel, P.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 48
The Microbe-Free Plant: Fact or Artifact?
journal, January 2011
- Partida-Martínez, Laila P.; Heil, Martin
- Frontiers in Plant Science, Vol. 2
Endophytes of Grapevine Flowers, Berries, and Seeds: Identification of Cultivable Bacteria, Comparison with Other Plant Parts, and Visualization of Niches of Colonization
journal, May 2011
- Compant, Stéphane; Mitter, Birgit; Colli-Mull, Juan Gualberto
- Microbial Ecology, Vol. 62, Issue 1
Are endophytic fungi defensive plant mutualists?
journal, July 2002
- Faeth, Stanley H.
- Oikos, Vol. 98, Issue 1
Emergence Shapes the Structure of the Seed Microbiota
journal, December 2014
- Barret, Matthieu; Briand, Martial; Bonneau, Sophie
- Applied and Environmental Microbiology, Vol. 81, Issue 4
Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi
journal, October 1998
- Jumpponen, Ari; Trappe, James M.
- New Phytologist, Vol. 140, Issue 2
Hidden diversity of endophytic fungi in an invasive plant
journal, August 2008
- Shipunov, A.; Newcombe, G.; Raghavendra, A. K. H.
- American Journal of Botany, Vol. 95, Issue 9
Infection Studies of Discula quercina, an Endophyte of Quercus garryana
journal, September 1994
- Wilson, D.; Carroll, G. C.
- Mycologia, Vol. 86, Issue 5
Diversity of fungal endophytes in leaves and stems of wild rubber trees (Hevea brasiliensis) in Peru
journal, August 2010
- Gazis, Romina; Chaverri, Priscila
- Fungal Ecology, Vol. 3, Issue 3
Do microorganisms influence seed-bank dynamics?
journal, May 2006
- Chee-Sanford, Joanne C.; Williams, Martin M.; Davis, Adam S.
- Weed Science, Vol. 54, Issue 3
Seed transmission ofPyrenophora tritici-repentis, causal fungus of tan spot of wheat
journal, January 1995
- Schilder, A. M. C.; Bergstrom, G. C.
- European Journal of Plant Pathology, Vol. 101, Issue 1
Assembly of seed-associated microbial communities within and across successive plant generations
journal, October 2017
- Rezki, Samir; Campion, Claire; Simoneau, Philippe
- Plant and Soil, Vol. 422, Issue 1-2
Seed survival in soil: interacting effects of predation, dormancy and the soil microbial community: Seed survival in soil
journal, October 2010
- Dalling, James W.; Davis, Adam S.; Schutte, Brian J.
- Journal of Ecology, Vol. 99, Issue 1
Adaptive value, entropy and survivorship curves
journal, September 1978
- Demetrius, Lloyd
- Nature, Vol. 275, Issue 5677
Fungal endophytes directly increase the competitive effects of an invasive forb
journal, January 2012
- Aschehoug, Erik T.; Metlen, Kerry L.; Callaway, Ragan M.
- Ecology, Vol. 93, Issue 1
How context dependent are species interactions?
journal, April 2014
- Chamberlain, Scott A.; Bronstein, Judith L.; Rudgers, Jennifer A.
- Ecology Letters, Vol. 17, Issue 7
Diversity of endophytic bacteria from Eucalyptus species seeds and colonization of seedlings by Pantoea agglomerans
journal, October 2008
- Ferreira, Anderson; Quecine, Maria Carolina; Lacava, Paulo Teixeira
- FEMS Microbiology Letters, Vol. 287, Issue 1
Bacteria within ovules and seeds.
journal, January 1976
- Mundt, J. O.; Hinkle, N. F.
- Applied and Environmental Microbiology, Vol. 32, Issue 5
Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.