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The Hologenome Hypothesis and Its Application to Plant-Microbe Interactions on an Evolutionary Scale

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Microbes: The Foundation Stone of the Biosphere

Part of the book series: Advances in Environmental Microbiology ((AEM,volume 8))

Abstract

When roots are pulled from the ground, one cannot ignore the soil particles with their rhizosphere microbes still attached to the root surface and root hairs. The rhizosphere is home to a vast variety of microorganisms that associate with plants and either positively or negatively influences plant growth, while the rhizosheath is defined as the weight of soil strongly attached to the plant root surfaces. Root hairs, epidermal extensions that increase surface area, are a critical component of rhizosheaths. Within the root and in continuation with the aerial portion of the plant is the endosphere, providing both intra- and extracellular locations for microbial habitation. Endophytic microbes often enter plant roots through cracks in the epidermis or in areas where lateral roots emerge, or through stomata, openings for gas exchange, in the aerial parts of the plant. Microbial pathogens as well as symbionts and commensals enter into roots, stems, or leaves employing these “doorways” to enter plant tissues—sources of nutrients and carbon for microbes.

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References

  • Alori ET, Glick BR, Babalola OO (2017) Microbial phosphorus solubilization and its potential for use in sustainable agriculture. Front Microbiol 8:971

    Article  Google Scholar 

  • Backer R, Rokem JS, Ilangumaran G, Lamont J, Praslickova D, Ricci E, Subramanian S, Smith DL (2018) Plant growth-promoting rhizobacteria: context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Front Plant Sci 9:1473

    Article  Google Scholar 

  • Bashan Y, Holguin G (1998) Proposal for the division of plant growth-promoting bacteria into two classifications: biocontrol-PGPB (plant growth promoting Bacteria) and PGPB. Soil Biol Biochem 30:1225–1228

    Article  CAS  Google Scholar 

  • Beilsmith K, Thoen MPM, Brachi B, Gloss AD, Khan MH, Bergelson J (2019) Genome-wide association studies on the phyllosphere microbiome: embracing complexity in host-microbe interactions. Plant J 97:164–181. https://doi.org/10.1111/tpj.14170

    Article  CAS  PubMed  Google Scholar 

  • Brown LK, Georg TS, Neugebauer K, White PJ (2017) The rhizosheath—a potential trait for future agricultural sustainability occurs in orders throughout the angiosperms. Plant Soil 418:115–128

    Article  CAS  Google Scholar 

  • Camacho M, Camacho M, Santamaría C, Temprano F, Rodriguez-Navarro DN, Daza A (2001) Co-inoculation with Bacillus sp. CECT 450 improves nodulation in Phaseolus vulgaris L. Can J Microbiol 47(11):1058–1062. https://doi.org/10.1139/w01-107

    Article  CAS  PubMed  Google Scholar 

  • Cavicchioli R, Ripple WJ, Timmis KN, Azam F, Bakken LR, Baylis M, Behrenfeld MJ, Boetius A, Boyd PW, Classen AT, Crowther TW, Danovaro R, Foreman CM, Huisman J, Hutchins DA, Jansson JK, Karl DM, Koskella B, Mark Welch DB, Martiny JBH, Moran MA, Orphan VJ, Reay DS, Remais JV, Rich VI, Singh BK, Stein LY, Stewart FJ, Sullivan MB, van Oppen MJH, Weaver SC, Webb EA, Webster NS (2019) Scientists’ warning to humanity: microorganisms and climate change. Nature reviews. Microbiology 17(9):569–586. https://doi.org/10.1038/s41579-019-0222-5.

    Article  CAS  PubMed  Google Scholar 

  • Compant S, Samad A, Faist H, Sessitch A (2019) A review on the plant microbiome: ecology, functions, and emerging trends in microbial application. J Adv Res 19:29–37

    Article  CAS  Google Scholar 

  • de Vries FT, Griffiths RI, Knight CG, Nicolitch O, Williams A (2020) Harnessing rhizosphere microbiomes for drought-resilient crop production. Science 368:270–274

    Article  Google Scholar 

  • Edwards DS (1986) Algaophyton major, a non-vascular land-plant from the Devonian Rhynie chert. Bot J Linn Soc 93:173–204

    Article  Google Scholar 

  • Elkoca E, Kantar F, Fe S (2007) Influence of nitrogen fixing and phosphorus solubilizing bacteria on the nodulation, plant growth, and yield of chickpea. J Plant Nutr 31(1):157–171

    Article  Google Scholar 

  • Estrada-de los Santos P, Palmer M, Chávez-Ramírez B, Beukes C, Steenkamp ET, Briscoe L, Khan N, Maluk M, Lafos M, Humm E, Arabit M, Crook M, Gross E, Simon MF, Bueno dos Reis Junior F, Whitman WB, Shapiro N, Poole PS, Hirsch AM, Venter SN, James EK (2018) Whole genome analyses suggest that Burkholderia sensu lato contains two further novel genera in the “rhizoxinica-symbiotica group” (Mycetohabitans gen. Nov., and Trinickia gen. Nov.): implications for the evolution of diazotrophy and nodulation in the Burkholderiaceae. Genes 9:389. https://doi.org/10.3390/genes9080389

    Article  CAS  PubMed Central  Google Scholar 

  • Ferreira CMH, Soares HMVM, Soares EV (2019) Promising bacterial genera for agricultural practices: an insight on plant growth-promoting properties and microbial safety aspects. Sci Total Environ 682:779–799

    Article  CAS  Google Scholar 

  • Frank AB (1877) Über die biologischen Verkältnisse des Thallus einiger Krustflechten. Beiträge zur Biologie der Pflanzen 2:123–200

    Google Scholar 

  • Gilbert JA, Neufeld JD (2014) Life in a world with microbes. PLoS Biol 12:e10002020

    Article  Google Scholar 

  • Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Publishing Corporation, Scientica. Article ID 963401 2012:15. https://doi.org/10.6064/2012/963401

    Article  Google Scholar 

  • Goswami D, Thakker JN, Dhandhukia PC (2016) Portraying mechanics of plant growth promoting rhizobacteria (PGPR): a review. Cogent Food Agric 2:1127500. https://doi.org/10.1080/23311932.2015.1127500

    Article  CAS  Google Scholar 

  • Honegger R, Axe L, Edwards E (2013a) Bacterial epibionts and endolichenic actinobacteria and fungi in the lower Devonian lichen Chlorochenomycites salopensis. Fungal Biol 117:512–518

    Article  CAS  Google Scholar 

  • Honegger R, Edwards E, Axe L (2013b) The earliest records of internally stratified and algal lichens from the lower Devonian of the welsh borderland. New Phytol 197:264–273

    Article  Google Scholar 

  • Janzen DH (1985) The natural history of mutualisms. In: Bouche DH (ed) The biology of mutualism. Oxford University Press, Oxford, pp 40–97

    Google Scholar 

  • Kalayu G (2019) Phosphate solubilizing microorganisms: promising approach as biofertilizers. Int J Agron 2019. Article ID 4917256:7. https://doi.org/10.1155/2019/4917256

    Article  CAS  Google Scholar 

  • Korir H, Mungai NW, Thuita M, Hamba Y, Masso C (2017) Co-inoculation effect of rhizobia and plant growth promoting rhizobacteria on common bean growth in low phosphorus soil. Front Plant Sci 8:141. https://doi.org/10.3389/fpls.2017.00141

    Article  PubMed  PubMed Central  Google Scholar 

  • Kotyk ME, Basinger JF (2000) The early Devonian (Pragian) zosterophyll—Bathhurstia denticulata Hueber. Can J Bot 78:193–207

    Google Scholar 

  • Lebeis SL, Paredes SH, Lundberg DS et al (2015) Plant microbiome. Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 349:860–864. https://doi.org/10.1126/science.aaa8764.

    Article  CAS  PubMed  Google Scholar 

  • Margulis L (1993) Origin of species: acquired genomes and individuality. Biosystems 31(2–3):121–125

    Article  CAS  Google Scholar 

  • Martínez-Hidalgo P, Hirsch AM (2017) The nodule microbiome: N2-fixing rhizobia do not live alone. Phytobiomes 1:70–82

    Article  Google Scholar 

  • Martínez-Hidalgo P, Maymon M, Pule-Meulenberg F, Hirsch AM (2018) Engineering root microbiomes for healthier crops and soils using beneficial, environmentally safe bacteria. Can J Microbiol 65:91–104. https://doi.org/10.1139/cjm-2018-0315

    Article  CAS  PubMed  Google Scholar 

  • Mishra PK, Mishra S, Selvakumar G, Bisht JK, Kundu S, Gupta HS (2009) Coinoculation of Bacillus thuringeinsis-KR1 with Rhizobium leguminosarum enhances plant growth and nodulation of pea (Pisum sativum L.) and lentil (Lens culinaris L.). World J Microbiol Biotechnol 25:753–761

    Article  Google Scholar 

  • Nelson EB (2018) The seed microbiome: origins, interactions, and impacts. Plant Soil 422:7–34

    Article  CAS  Google Scholar 

  • Pasteur L (1885) Observation relative à la note précédente de M. Duclaux. Compte Rendus Ge. Acad Sci 100:68

    Google Scholar 

  • Pirozynski KA, Malloch DW (1975) The origin of land plants: a matter of mycotrophism. Biosystems 6:153–164

    Article  CAS  Google Scholar 

  • Redecker D, Kodner E, Graham LE (2000) Glomalean fungi from the Ordovician. Science 289:1920–1921

    Article  CAS  Google Scholar 

  • Remy W et al (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci U S A 91:11841–11843

    Article  CAS  Google Scholar 

  • Rodriguez R, Durán P (2020) Natural holobiome engineering by using native extreme microbiome to counteract the climate change effects. Front Bioeng Biotechnol 8:568. https://doi.org/10.3389/fbioe.2020.00568

    Article  PubMed  PubMed Central  Google Scholar 

  • Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral associated bacteria. Mar Ecol Prog Ser 243:1–10

    Article  Google Scholar 

  • Rosenberg E, Zilber-Rosenberg I (2018) The hologenome concept of evolution after 10 years. Microbiome 6:78. https://doi.org/10.1186/s40168-018-0457-9

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355

    Article  CAS  Google Scholar 

  • Rubenstein CV, Gerrienne P, de la Puente GS, Astíni RA, Steemans P (2010) Early middle Ordovician evidence for land plants in Argentina (eastern Gondwana). New Phytol 188:365–369

    Article  Google Scholar 

  • Ruzzi M, Aroca R (2015) Plant growth-promoting rhizobactertia act as biostimulants in horticultures. Sci Hortic 196:124–134

    Google Scholar 

  • Sattar A, Naveed M, Ali M, Zahir ZA, Nadeem SM, Yaseen M (2019) Perspectives of potassium solubilizing microbes in sustainable food production system: a review. Appl Soil Ecol 133:146–159

    Article  Google Scholar 

  • Schwartz AR, Ortiz I, Maymon M, Herbold CW, Fujishige NA, Vijanderan JA, Villella W, Hanamoto K, Diener A, Sanders ER, DeMason DA, Hirsch AM (2013) Bacillus simplex—a little known PGPB with anti-fungal activity—alters pea legume root architecture and nodule morphology when coinoculated with Rhizobium leguminosarum bv. viciae. Agronomy 3:595–620. https://doi.org/10.3390/agronomy3040595

    Article  Google Scholar 

  • Smercina DN, Evans SE, Friesen ML, Tiemann LK (2019) To fix or not to fix: controls on free-living nitrogen fixation in the rhizosphere. Appl Environ Microbiol 85:e02546–e02518

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stein WE, Berrry CM, Morris JL, Hernick LV, Mannonlini F, Ver Straeten C, Landing E, Marshall JEA, Wellman CH, Beerling DJ, Leake JR (2019) Mid-Devonian Archaeopteris roots signal revolutionary changes in earliest fossil forests. Curr Biol 30:421. https://doi.org/10.1016/j.cub.2019.11.067

    Article  CAS  PubMed  Google Scholar 

  • Strother PK, Al-Hajri S, Traverse A (1996) New evidence for land plants from the lower middle Ordovician of Saudi Arabia. Geology 24:55–58

    Article  Google Scholar 

  • Suárez Díaz J (2019) The Hologenome concept of evolution: a philosophical and biological study. PhD thesis, University of Exeter, Exeter, The United Kingdom

    Google Scholar 

  • Tomescu AMF, Honegger R, Rothwell GW (2008) Earliest fossil record of bacterial-cyanobacterial mat consortia: the early Silurian Passage Creek biota (440 ma, Virginia, USA). Geobiology 6:120–124

    Article  CAS  Google Scholar 

  • Uroz S, Calvaruso C, Turpault MP, Frey-Klett P (2009) Mineral weathering by bacteria: ecology, actors and mechanisms. Trends Microbiol 17:378–387

    Article  CAS  Google Scholar 

  • Watanabe Y, Martini JEJ, Ohmoto H (2000) Geochemical evidence for terrestrial ecosystems 2.6 billion years ago. Nature 408:574–578. https://doi.org/10.1038/35046052

    Article  CAS  PubMed  Google Scholar 

  • Xue J, Deng Z, Huang P, Huang K, Benton MJ, Cui Y, Wang D, Liu J, Shen B, Basinger JF, Hao S (2016) Belowground rhizomes in paleosols: the hidden half of an early Devonian vascular plant. Proc Natl Acad Sci 113:9451–9456

    Article  CAS  Google Scholar 

  • Zeffa DM, Fantin LH, Koltun A, Oliveira ALM, Nunes MPBA, Canteri MG, Goncalves LSA (2020) Effects of plant growth-promoting rhizobacteria on co-inoculation with Bradyrhizobium in soybean crop: a meta-analysis of studies from 1987 to 2018. Peer J 8:e7905. https://doi.org/10.7717/peerj.7905

    Article  PubMed  Google Scholar 

  • Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Ecol 32:723–735

    Article  CAS  Google Scholar 

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Acknowledgements

We thank the Fulbright Foundation for supporting S. Kouas’ stay in the Hirsch lab, and also acknowledge the long-term grant support from the Shanbrom Foundation to study arid soils and their microbes. Thanks to S.J. Kirchanski for his helpful comments on the manuscript, and we also extend our gratitude to J.W. Schopf, J.F. Basinger, W.E. Stein, T. Algeo, D. Murphy, and J. Shen-Miller for their helpful comments, suggestions of papers, and answers to various questions sent by email. Allan Chong (UCLA) did the artwork for Fig. 21.2. We also thank Christon J. Hurst for his support and helpful comments.

Finally, we appreciate P. G. Gensel and D. Edwards for writing the book “Plant Invade the Land. Evolutionary and Environmental Perspectives”, which was an important reference for this chapter.

figure c

Saber Kouas

figure b

Noor Khan

figure a

Ann M. Hirsch

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Authors and Affiliations

  1. Department of Molecular, Cell and Developmental Biology, Los Angeles, CA, USA

    S. Kouas, N. Khan & A. M. Hirsch

  2. Faculty of Sciences of Gabes, Gabes, Tunisia

    S. Kouas

  3. Plant Physiology and Functional Genomics Research Unit, Institute of Biotechnology/University of Sfax, BP, Sfax, Tunisia

    S. Kouas

  4. Molecular Biology Institute, University of California-Los Angeles, Los Angeles, CA, USA

    A. M. Hirsch

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  1. S. Kouas
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Correspondence to A. M. Hirsch .

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  1. Cincinnati, OH, USA

    Christon J. Hurst

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Kouas, S., Khan, N., Hirsch, A.M. (2021). The Hologenome Hypothesis and Its Application to Plant-Microbe Interactions on an Evolutionary Scale. In: Hurst, C.J. (eds) Microbes: The Foundation Stone of the Biosphere. Advances in Environmental Microbiology, vol 8. Springer, Cham. https://doi.org/10.1007/978-3-030-63512-1_21

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