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Thinking About PPFM Bacteria as a Model of Seed Endophytes: Who Are They? Where Did They Come from? What Are They Doing for the Plant? What Can They Do for Us?

  • Mark A. HollandEmail author
Chapter

Abstract

Bacteria in the genus Methylobacterium (PPFM bacteria) are distributed globally and are associated with algae, mosses, ferns, liverworts, gymnosperms and angiosperms as co-evolved symbionts. As such, they share significantly in plant metabolism, stimulating plant growth and development through the production of plant hormones and vitamins. This chapter discusses the PPFMs as model plant symbionts and considers how their symbiotic relationship with plants and be exploited to our benefit.

Keywords

Methylobacterium spp. PPFM bacteria Plant/microbe symbiosis 

References

  1. American Society for Microbiology (2014) Plants prepackage beneficial microbes in their seeds. Science Daily. www.sciencedaily.com/releases/2014/09/140929180055.htm
  2. Barret M, Briand M, Bonneau S, Preveaux A, Valiere S, Bouchez O, Hunault G, Simoneau P, Jacques M-A (2015) Emergence shapes the structure of the seed microbiota. Appl Environ Microbiol 81(4):1257–1266CrossRefGoogle Scholar
  3. Barret M, Guimbaud JF, Darrasse A, Jaques MA (2016) Plant microbiota affects seed transmission of phytopathogenic microorganisms. Mol Plant Pathol 17(6):791–795.  https://doi.org/10.1111/mpp.12382CrossRefPubMedGoogle Scholar
  4. Barrow JR, Lucero ME, Reyes-Vera I, Havstad KM (2008) Do symbiotic microbes have a role in plant evolution, performance and response to stress? Commun Integr Biol 1(1):69–73CrossRefGoogle Scholar
  5. Basile DV, Slade LL, Corpe WA (1969) A association between a bacterium and a liverwort, Scapania nemorosa. Bull Torrey Bot Club 96(6):711–714CrossRefGoogle Scholar
  6. Basile DV, Basile MR, Li QY, Corpe WA (1985) Vitamin B12-stimulated growth and development of Jungermannia leiantha Grolle and Gymnocolea inflata (Huds.) Dum. (Hepaticae). Bryologist 88(2):77–81CrossRefGoogle Scholar
  7. Bokulich NA, Lewis ZT, Boundy-Mills K, Mills DA (2016) A new perspective on microbial landscapes within food production. Curr Opin Biotechnol 37:182–189.  https://doi.org/10.1016/j.copbio.2015.12.008CrossRefPubMedPubMedCentralGoogle Scholar
  8. Briand CH, Holland MA (1999) Microbial symbionts and the evolution of fruit. In: Presented at the annual meeting of the American Society of Plant Physiologists, Baltimore, MD, 24–28 July 1999Google Scholar
  9. Butler HSK (2001) Contribution of PPFM (Methylobacterium mesophilicum), a bacterial symbiont, to cytokinin content and biomass accumulation in soybean [Glycine max (L.) Merr.] seedlings. Masters Thesis. University of Maryland Eastern Shore, Princess Anne, MDGoogle Scholar
  10. Compant S, Sessitsch A, Mathieu F (2012) The 125th anniversary of the first postulation of the soil origin of endophytic bacteria – a tribute to MLV Galippe. Plant Soil.  https://doi.org/10.1007/s11104-012-1204-9
  11. Corpe WA (1985) A method for detecting methylotrophic bacteria on solid surfaces. J Microbiol Methods 3:215–321CrossRefGoogle Scholar
  12. Corpe WA, Basile DV (1982) Methanol utilizing bacteria associated with green plants. Dev Ind Microbiol 23:483–493Google Scholar
  13. Corpe WA, Rheem S (1989) Ecology of the methylotrophic bacteria living on leaf surfaces. FEMS Micobiol Ecol 62:243–250CrossRefGoogle Scholar
  14. Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG (2005) Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438(7064):90–93CrossRefGoogle Scholar
  15. Cruz RS, Yanez-Ocampo G, Wong-Villareal A (2014) Effect of nodulating bacteria on the seed germination of Capsicum spp. Afr J Microbiol Res 8(7):659–663.  https://doi.org/10.5897/AJMR2013.6494CrossRefGoogle Scholar
  16. Delshadi S, Ebrahimi M, Shirmohammadi E (2017) Influence of plant-growth-promoting bacteria on germination, growth and nutrients’ uptake of Onobrychis sativa L. under drought stress. J Plant Interact 12(1):200–208.  https://doi.org/10.1080/17429145.2017.1316527CrossRefGoogle Scholar
  17. Doroninqa NV, Ivanova EG, Trotsenko I (2002) New evidence for the ability of methylobacteria and methanotrophs to synthesize auxins. Microbiology 71:116–118CrossRefGoogle Scholar
  18. Dunleavy JM (1988) In vitro expression of the cellulose gene in Methylobacterium mesophilicum, a seed-transmitted bacterium ubiquitous in soybean. In: Presented at 2nd biennial conference on the molecular and cellular biology of the soybean, Ames, IA, 25–27 July 1988Google Scholar
  19. Fernbach MA (1888) De l’absence des microbes dans les tissus vegetaux. Ann Inst Past 2(10):567Google Scholar
  20. Frank AC, Guzmain JPS, Shay JE (2017) Transmission of bacterial endophytes. Microorganisms 5:70.  https://doi.org/10.3390/microorganisms5040070CrossRefPubMedCentralGoogle Scholar
  21. Freyermuth SK, Long RL, Mathur S, Holland MA, Holtsford TP, Stebbins NE, Morris RO, Polacco JC (1996) Metabolic aspects of plant interaction with commensal methylotrophs. In: Lidstrom M, Tabita R (eds) Microbial growth on C1 compounds. Kluwer Academic, pp 277–284Google Scholar
  22. Gopal M, Gupta A (2016) Microbiome selection could spur next-generation plant breeding strategies. Front Microbiol 7:1971.  https://doi.org/10.3389/micb.2016.01971CrossRefPubMedPubMedCentralGoogle Scholar
  23. Grossman A (2017) Nutrient acquisition: the generation of bioactive vitamin B12 by microalgae. Curr Biol 26:R319–R337.  https://doi.org/10.1016/j.cub.2016.02.047CrossRefGoogle Scholar
  24. Gunfel PE, Landesmann JB, Martinez-Ghersa MA, Ghersa CM (2007) Effects of Neotyphoduim endophyte infection on seeds viability and germination vigor in Lolium multiflorum under accelerated aging conditions. New Zealand Grassland Association: Endophyte symposium. https://www.grassland.org.nz/publications/nzgrassland_publication_2363.pdf
  25. Hassani MA, Duran P, Hacquardo S (2018) Microbial interactions within the plant holobiont. Microbiome 6:58.  https://doi.org/10.1186/s40168-018-0445-0
  26. Helliwell KE, Wheeler GL, Leptos KC, Goldstein RE, Smith AG (2011) Insights into the evolution of vitamin B12 auxotrophy from sequenced algal genomes. Mol Biol Evol 28(10):2921–2933.  https://doi.org/10.1093/molbev/msr124CrossRefPubMedGoogle Scholar
  27. Helliwell KE, Collins S, Kazamia E, Purton S, Wheeler GL, Smith A (2015) Fundamental shift in vitamin B12 eco-physiology of a model alga demonstrated by experimental evolution. ISME J 9:1446–1455. https://www.nature.com/articles/ismej2014230CrossRefGoogle Scholar
  28. Herrera SD, Grossi C, Zawoznik M, Groppa MD (2016) Wheat seeds harbor bacterial endophytes with potential as plant growth promoters and biocontrol agents of Fusarium graminearum. Microbiol Res 186–187:37–43CrossRefGoogle Scholar
  29. Holland MA (1997) Methylobacterium and plants. Rec Res Dev Plant Phys 1:207–213Google Scholar
  30. Holland MA (2011) Nitrogen: give and take from phylloplane microbes. In: Polacco JC, Todd CD (eds) Ecological aspects of nitrogen metabolism in plants. Wiley-Blackwell, London, pp 217–230. ISBN 978-0-8138-1649-4Google Scholar
  31. Holland MA (2016) Probiotics for plants? What the PPFMs told us and some ideas about how to use them. J Wash Acad Sci 102(1):31–42Google Scholar
  32. Holland MA, Polacco JC (1992) Urease-null and hydrogenase-null phenotypes of a phylloplane bacterium reveal altered nickel metabolism in two soybean mutants. Plant Physiol 98:942–948CrossRefGoogle Scholar
  33. Holland MA, Polacco JC (1994) PPFMs and other covert contaminants: is there more to plant physiology than just plant? Annu Rev Plant Physiol Plant Mol Biol 45:197–209CrossRefGoogle Scholar
  34. Holland MA, Polacco JC (1996) Seeds, coated or impregnated with a pink pigmented facultative methylotroph, having improved germinability. U.S. Patent # 5,512,069Google Scholar
  35. Holland MA, Polacco JC (2006) A method for altering the metabolism of a plant. U.S. Patent # 8,153,118Google Scholar
  36. Holland MA, Davis R, Moffitt S, O’Laughlin K, Peach D, Sussan S, Wimbrow L, Tayman B (2000) Using “leaf prints” to investigate a common bacterium. Am Biol Teach 62(2):128–131CrossRefGoogle Scholar
  37. Holland MA, Long RLG, Polacco JC (2002) Methylobacterium spp.: Phylloplane bacteria involved in cross-talk with the plant host? In: Lindow SE, Hecht-Poinar EI, Elliot VJ (eds) Phyllosphere microbiology. APS Press, St. Paul, MN, pp 125–135Google Scholar
  38. Jalilian J, Modarres-Sanavy SAM, Saberali SF, Sadat-Asilan K (2012) Effects of the combination of beneficial microbes and nitrogen on sunflower seed yields and seed quality traits under different irrigation regimes. Field Crop Res 127:26–34.  https://doi.org/10.1016/j.fcr.2011.11.001CrossRefGoogle Scholar
  39. Jimenez-Gomez A, Celador-Lera L, Fradejas-Bayon M, Rivas R (2017) Plant probiotic bacteria enhance the quality of fruit and horticultural crops. AIMS Microbiol 3(3):483–501.  https://doi.org/10.3934/miocrobiol.2017.3.483CrossRefGoogle Scholar
  40. Johnston-Monje D, Raizada M (2011) Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology. PLoS One 6(6):e20396CrossRefGoogle Scholar
  41. Joshi JM, Holland MA (1999) Method for treating plants. U.S. Patent # 5,961,687Google Scholar
  42. Joshi JM, Holland MA (2001a) Method for treating plants. US Patent # 6,174,837Google Scholar
  43. Joshi JM, Holland MA (2001b) Method for treating plants. U.S. Patent # 6,329,320Google Scholar
  44. Kelly SM (2015) Altering growth rates and nutritional qualities of microalgal feedstocks with symbiotic bacteria. Masters Thesis. Salisbury University, Salisbury, MDGoogle Scholar
  45. Khalaf EM, Raizada MN (2018) Bacterial seed endophytes of domesticated cucurbits antagonize fungal and oomycete pathogens including powdery mildew. Front Microbiol 9:42.  https://doi.org/10.3389/micb.2018.00042CrossRefPubMedPubMedCentralGoogle Scholar
  46. Koenig RL, Morris RO, Polacco JC (2002) tRNA is the source of low-level trans-zeatin production in Methylobacterium spp. J Bacteriol 184:1832–1842CrossRefGoogle Scholar
  47. Lawrence AD, Nemoto-Smith E, Deery E, Boshoff HI, Barry CE III, Warren MJ (2018) Construction of fluorescent analogs to follow the uptake and distribution of cobalamin (Vitamin B12) in bacteria, worms, and plants. Cell Chem Biol.  https://doi.org/10.1016/j.chembiol.2018.04.012
  48. Madhaiyan M, Poonguzhali S, Ryu J, Sa T (2006) Regulation of ethylene levels in canola (Brassica campestris) by 1-aminocyclopropane-1-carboxylate deaminase-containing Methylobacterium fujisawaense. Planta 224(2):268–278CrossRefGoogle Scholar
  49. Mitter B, Sessitsch A, Naveed M (2012) Method for producing plant seed containing endophytic micro-organisms. Patent Application EP267536A1Google Scholar
  50. Mitter B, Pfaffenbichler N, Flavell R, Compant S, Antonielli L, Petric A, Berninger T, Naveed M, Sheibani-Tezerji R, vonMaltzahn G, Sessitsch A (2017) A new approach to modify plant microbiomes and traits by introducing beneficial bacterial at flowering into progeny seeds. Front Microbiol 8:11.  https://doi.org/10.3389/fmicb.2017.00011CrossRefPubMedPubMedCentralGoogle Scholar
  51. Morsy M (2015) Microbial symbionts: a potential bio-boom. J Investig Genom 2(1):00015Google Scholar
  52. Mundt JO, Hinkle NF (1976) Bacteria within ovules and seeds. Appl Environ Microbiol 32(5):694–698PubMedPubMedCentralGoogle Scholar
  53. Munsanje EM (1999) Potential of a cytokinin-excreting Methylobacterium as a biofertilizer in soybean production. PhD Dissertation. University of Maryland Eastern Shore, Princess Anne, MDGoogle Scholar
  54. Munsanje EM, Holland MA, Joshi JM (1998) The significance of PPFM foliar spray on soybean yield. In: Dadson RB, Noureldin RA (eds) Soybeans in Egypt: research, production, economics, nutrition and health. University of Maryland Press, Bethesda, MD, pp 69–78Google Scholar
  55. O’Callaghan M (2016) Microbial inoculation of seed for improved crop performance: issues and opportunities. Appl Microbiol Biotechnol 100:5729–5746.  https://doi.org/10.1007/s00253-016-7590-9CrossRefPubMedPubMedCentralGoogle Scholar
  56. Omer ZS, Tombolini R, Gerhardson B (2004) Plant colonization by pink-pigmented facultative methylotrophic bacteria (PPFMs). FEMS Microbiol Ecol 47:319–326CrossRefGoogle Scholar
  57. Pitzschke A (2016) Developmental peculiarities and seed-borne endophytes in quinoa: omnipresent, robust bacilli contribute to plant fitness. Front Micro 7:article 2.  https://doi.org/10.3389/fmicb.2016.00002CrossRefGoogle Scholar
  58. Pohjanen J, Koskimaki JJ, Pirttila AM (2014) Interactions of meristem-associated endophytic bacteria. In: Verma VJ, Gange AC (eds) Advances in endophytic research. Springer.  https://doi.org/10.1007/978-81-322-1575-2
  59. Polacco JC, Holland MA (1993) A method for altering the metabolism of a plant. U.S. Patent # 5,268,171Google Scholar
  60. Rahman M, As Sabir A, Mukta JA, Khan MMA, Mohi-Ud-Din M, Miah MG, Rahman M, Islam MT (2018) Plant probiotic bacteria Bacillus and Paraburkholderia improve growth, yield and content of antioxidants in strawberry fruit. Sci Rep 8:2504.  https://doi.org/10.1038/s41598-018-20235-1CrossRefPubMedPubMedCentralGoogle Scholar
  61. Rodrigues Pereira AS, Houwen PWJ, Deurenberg-Vos HWJ, Pey EBF (1972) Cytokinins and the bacterial symbiosis os Ardisia species. Z Pflanzenphysiol 68:170–177CrossRefGoogle Scholar
  62. Romine MF, Rodionov DA, Maezato Y, Andersona LN, Nandhikonda P, Rodionova IA, Carred A, Li X, Xu C, Clauss TRW, Kim YM, Metz TO, Wright AT (2017) Elucidation of roles for vitamin B12 in regulation of folate, ubiquinone, and methionine metabolism. Proc Natl Acad Sci USA. doi: https://doi.org/10.1073/pnas.1612360114
  63. Samova LA, Pechurkin NS, Sarangove AB, Pisman TI (2001) Effect of bacterial population density on germination wheat seeds and dynamics of simple artificial ecosystems. Adv Space Res 27(9):1611–1615CrossRefGoogle Scholar
  64. Sanchez-Lopez AS, Pintelon I, Stevens V, Imperato V, Timmermans JP, Gonzalez-Chavez C, Carillo-Gonzalez R, Van Hamme J, Vangronsveld J, Thijs S (2018) Seed endophyte microbiome of Crotalaria pumila unpeeled: identification of plant-beneficial methylobacteria. Int J Mol Sci 19:291.  https://doi.org/10.3390/jims19010291CrossRefPubMedCentralGoogle Scholar
  65. Sato K, Kudo Y, Muramatsu K (2004) Incorporation of a high level of vitamin B12 into a vegetable, kaiware daikon (Japanese radish sprout), by the absorption from its seeds. Biochim Biophys Acta 1672:135–137CrossRefGoogle Scholar
  66. Shahzad R, Khan AL, Bilal S, Asaf S, Lee I (2018) What is there in seeds? Vertically transmitted endophytic resources for sustainable improvement in plant growth. Front Plant Sci 9:24.  https://doi.org/10.3389/fpls.2018.00024CrossRefPubMedPubMedCentralGoogle Scholar
  67. Shuang S, Zhenfang G, Xiaolei G (2015) The effect of bacteria on seed germination in sorghum and rape under cadmium and petroleum conditions. Int J Biotechnol Wellness Indus 4:123–127CrossRefGoogle Scholar
  68. Siddikee A, Hamayun M, Han G-H, Sa T-m (2010) Optimization of gibberellic acid production by Methylobacterium oryzae CBMB20 Md. Korean J Soil Sci Fert 43(4):522–527Google Scholar
  69. Sudre C, Akiba F (2015) Influence of effective microorganisms on seed germination and plantlet vigor of selected crops. https://www.researchgate.net/publication/265524659Google Scholar
  70. Sy A, Giraud E, Jourand P, Garcia N, Willems A, De L Prin Y, Neyra M, Gillis M, Boivin M, Dreyfus B (2001) Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. J Bacteriol 183:214–220CrossRefGoogle Scholar
  71. Taga ME, Walker GC (2010) Sinorhizobium meliloti requires a cobalamin-dependent ribonucleotide reductase for symbiosis with its plant host. MPMI 23(12):1643–1654.  https://doi.org/10.1094/MPMI-07-10-0151CrossRefPubMedGoogle Scholar
  72. Taylor GT, Sullivan CW (2008) Vitamin B12 and cobalt cycling among diatoms and bacteria in Antarctic sea ice microbial communities. Limnol Oceanogr 53(5):1862–1877CrossRefGoogle Scholar
  73. Truyens S, Weyens N, Cuypers A, Vangronsveld J (2015) Bacterial seed endophytes: genera, vertical transmission and interaction with plants. Environ Microbiol Rep 7(1):40–50CrossRefGoogle Scholar
  74. Vaughan MJ, Mitchell T, Mc Spadden Gardener BB (2015) What’s inside the bean we brew? A new approach to mining the coffee microbiome. Appl Environ Microbiol 81(19):6518–6527.  https://doi.org/10.1128/AEM.01933-15CrossRefPubMedPubMedCentralGoogle Scholar
  75. Walitang DI, Kim K, Madhaiyan M, Kim YK, Kang Y, Sa T (2017) Characterizing endophytic competence and plant growth promotion of bacterial endophytes inhabiting the seed endosphere of rice. BMC Microbiol 17:209.  https://doi.org/10.1186/s12866-1117-0CrossRefPubMedPubMedCentralGoogle Scholar
  76. White JF Jr, Johnson H, Torres MS Irizarry I (2012) Nutritional endosymbiotic systems in plants: bacteria function like “quasi-organelles” to convert atmospheric nitrogen into plant nutrients. J Plant Pathol Microb 3:7.  https://doi.org/10.4172/2157-7471.1000e104CrossRefGoogle Scholar
  77. Witzig SB, Holland MA (1998) A microbial symbiont used to alter the nutritional quality of plants. Presented at the annual meeting of the American Society of Plant Physiologists, Madison, WI, 27 June–2 JulyGoogle Scholar
  78. Wu CH, Bernard SM, Andersen GL, Chen W (2009) Developing microbe-plant interactions for applications in plant-growth promotion and disease control, production of useful compounds, remediation and carbon sequestration. Microb Biotechnol 2(4):428–440CrossRefGoogle Scholar
  79. Yarzabal LA, Monserrate L, Buela L, Chica E (2018) Antarctic Pseudomonas spp. promote wheat growth at low temperature. Polar Biol.  https://doi.org/10.1007/s00300-018-2374-6
  80. Yousaf A, Qadir A, Anjum T, Ahmad A (2015) Identification of microbial metabolites elevating vitamin contents in barley seeds. J Agric Food Chem 63:7301–7310CrossRefGoogle Scholar
  81. Yousaf A, Qadir A, Anjum T, Khan Dr RI, Naughton D, Yousaf A (2017) Evaluation of bacterial strains for the induction of plant biochemicals, nutritional contents and isozymes in barley. J Nutr Food Sci 7(5):1000623.  https://doi.org/10.4172/2155-9600.1000623CrossRefGoogle Scholar
  82. Zhu YL, She XP, Wang JS, Lv HY (2017) Endophytic bacterial effects on seed germination and mobilization of reserves in Ammodendron biofolium. Pak J Bot 49(5):2029–2035Google Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of BiologySalisbury UniversitySalisburyUSA

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