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The Symbiogenic Tango: Achieving Climate-Resilient Crops Via Mutualistic Plant-Fungal Relationships

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Functional Importance of the Plant Microbiome

Abstract

Symbiogenics (symbio = symbiosis; genic = gene influence) embraces a fundamental aspect of biology that all complex life on this planet is symbiotic with microorganisms. Spanning the gamut from humans harboring gut microflora that aid in digestion and health to plants employing microbes to face a myriad of biotic and abiotic stresses, symbioses allow plants and animals a level of physiological and ecological performance they cannot achieve alone. In fact, symbiotic relationships are required for optimal health and survival of plants and animals. Here, we explore how some symbiotic fungal endophytes that adapt plants to high-stress habitats can be used to mitigate climate impacts in agriculture by enhancing temperature, drought, and salt tolerance of crop plants. In addition, application of symbiogenic technology to enhance agricultural sustainability and alter the trajectory of poverty in poor rural communities around the world is discussed.

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References

  1. Bartels D, Sunkar R. Drought and salt tolerance in plants. Crit Rev Plant Sci. 2005;24:23–58.

    Article  CAS  Google Scholar 

  2. Bray EA, et al. Trends Plant Sci. 1997;2(2):48–54. PubMed PMID: ISI:A1997WG90200004

    Article  Google Scholar 

  3. Leone A, Perrotta C, Maresca B. Plant tolerance to heat stress: current strategies and new emergent insight. In: di Toppi LS, Pawlik-Skowronska B, editors. Abiotic stresses in plants. London: Kluwer Academic Pub; 2003. p. 1–22.

    Google Scholar 

  4. Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM. Thermotolerance conferred to plant host and fungal endophyte during mutualistic symbiosis. Science. 2002;298:1581.

    Article  CAS  PubMed  Google Scholar 

  5. Rodriguez RJ, Redman RS, Henson JM. The role of fungal symbioses in the adaptation of plants to high stress environments. Mitig Adapt Strateg Glob Chang. 2004;9:261–72.

    Article  Google Scholar 

  6. Smallwood MF, Calvert CM, Bowles DJ. Plant responses to environmental stress. Oxford: BIOS Scientific Publishers Limited; 1999. 224p

    Google Scholar 

  7. Wang W, Vincur B, Altman A. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta. 2003;218:1–14.

    Article  CAS  PubMed  Google Scholar 

  8. Schwaegerle KE. Quantitative genetic analysis of plant growth: biases arising from vegetative propagation. Evol Ecol. 2005;59:1259–67.

    Google Scholar 

  9. Yin X, Struik PC, Kropff MJ. Role of crop physiology in predicting gene-to-phenotype relationships. Trends Plant Sci. 2004;9:426–32.

    Article  CAS  PubMed  Google Scholar 

  10. Zhou L, Wang JK, Yi Q, Wang YZ, Zhu YG, Zhang ZH. Quantitative trait loci for seedling vigor in rice under field conditions. Field Crops Res. 2007;100:294–301.

    Article  Google Scholar 

  11. Devarajan PT, Suryanarayanan TS, Geetha V. Endophytic fungi associated with the tropical seagrass Halophila ovalis (Hydrocharitaceae). Indian J Mar Sci. 2002;31(1):73–4. PubMed PMID: ISI:000179482500012

    Google Scholar 

  12. Márquez LM, Redman RS, Rodriguez RJ, Roossinck MJ. A virus in a fungus in a plant – three way symbiosis required for thermal tolerance. Science. 2007;315:513–5.

    Article  PubMed  Google Scholar 

  13. Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, et al. Stress tolerance in plants via habitat-adapted symbiosis. ISME J. 2008;2:404–16.

    Article  PubMed  Google Scholar 

  14. Ryan F. Darwin’s blind spot: evolution beyond natural selection. Boston: Houghton Mifflin; 2002. 310p

    Google Scholar 

  15. Johri BN. Endophytes to the rescue of plants! Curr Sci. 2006;90(10):1315–6. PubMed PMID: ISI:000239381500007

    Google Scholar 

  16. Lucero ME, Barrow JR, Osuna P, Reyes I. Plant-fungal interactions in arid and semi-arid ecosystems: large-scale impacts from microscale processes. J Arid Environ. 2006;65(2):276–84. PubMed PMID: ISI:000236645400007

    Article  Google Scholar 

  17. Maggio A, Bressan RA, Ruggiero C, Xiong L, Grillo S. Salt tolerance: placing advances in molecular genetics into a physiological and agronomic context. In: di Toppi LS, Pawlik-Skowronska B, editors. Abiotic stresses in plants. London: Kluwer Academic Pub; 2003. p. 53–70.

    Chapter  Google Scholar 

  18. Tuberosa R, Grillo S, Ellis RP. Unravelling the genetic basis of drought tolerance in crops. In: di Toppi LS, Pawlik-Skowronska B, editors. Abiotic stresses in plants. London: Kluwer Academic Pub; 2003. p. 71–122.

    Chapter  Google Scholar 

  19. Bohnert HJ, Nelson DE, Jensen RG. Adaptations to environmental stresses. Plant Cell. 1995;7:1099–111.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Jackson AO, Taylor CB. Plant-microbe interactions: life and death at the interface. Plant Cell. 1996;8:1651–68.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Macia-Vicente JG, Jansson HB, Talbot NJ, Lopez-Llorca LV. Real-time PCR quantification and live-cell imaging of endophytic colonization of barley (Hordeum vulgare) roots by Fusarium equiseti and Pochonia chlamydosporia. New Phytol. 2009;182(1):213–28. doi:10.1111/j.1469-8137.2008.02743.x. Epub 2009/01/28. PubMed PMID: 19170898

    Article  CAS  PubMed  Google Scholar 

  22. Peters S, Dammeyer B, Schulz B. Endophyte-host interactions. I. Plant defense reactions to endophytic and pathogenic fungi. Symbiosis. 1998;25(1–3):193–211. PubMed PMID: ISI:000075581300013

    Google Scholar 

  23. Redman RS, Kim YO, Woodward CJ, Greer C, Espino L, Doty SL, et al. Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: a strategy for mitigating impacts of climate change. PLoS One. 2011;6(7):e14823. doi:10.1371/journal.pone.0014823. Epub 2011/07/14. PubMed PMID: 21750695; PubMed Central PMCID: PMCPMC3130040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Stout RG, Al-Niemi TS. Heat-tolerance flowering plants of active geothermal areas in Yellowstone National Park. Ann Bot. 2002;90:259–67.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Yuan Z, Druzhinina IS, Labbe J, Redman R, Qin Y, Rodriguez R, et al. Specialized microbiome of a halophyte and its role in helping non-host plants to withstand salinity. Sci Rep. 2016;6:32467. doi:10.1038/srep32467. Epub 2016/08/31. PubMed PMID: 27572178; PubMed Central PMCID: PMCPMC5004162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Rodriguez RJ, Redman RS, Henson JM. Symbiotic lifestyle expression by fungal endophytes and the adaptation of plants to stress: unraveling the complexities of intimacy. In: Dighton J, Oudemans P, White J, editors. The fungal community: its organization and role in the ecosystem. Boca Raton: Taylor & Francis/CRC Press; 2005. p. 683–96.

    Google Scholar 

  27. Rodriguez RJ, White JFJ, Arnold AE, Redman RS. Fungal endophytes: diversity and functional roles. New Phytol. 2009;182(2):314–30.

    Article  CAS  PubMed  Google Scholar 

  28. Schulz B, Boyle C. The endophytic continuum. Mycol Res. 2005;109:661–86. PubMed PMID: ISI:000230687600001

    Article  PubMed  Google Scholar 

  29. Stone JK, Bacon CW, White JF. An overview of endophytic microbes: endophytism defined. In: Bacon CW, White JF, editors. Microbial endophytes. New York: Marcel Dekker, Inc.; 2000. p. 3–30.

    Google Scholar 

  30. Bacon CW, Hill NS. Symptomless grass endophytes: products of coevolutionary symbioses and their role in the ecological adaptations of grasses. In: Redkin SC, Carris LM, editors. Endophytic fungi in grasses and woody plants. St. Paul: APS Press; 1996. p. 155–78.

    Google Scholar 

  31. Cheplick GP, Clay K. Acquired chemical defenses in grasses – the role of fungal endophytes. Oikos. 1988;52(3):309–18. PubMed PMID: ISI:A1988N893200010

    Article  Google Scholar 

  32. Clay K. Fungal endophytes of grasses – a defensive mutualism between plants and fungi. Ecology. 1988;69(1):10–6. PubMed PMID: ISI:A1988L798500003

    Article  Google Scholar 

  33. Clay K, Holah J. Fungal endophyte symbiosis and plant diversity in successional fields. Science. 1999;285:1742–5.

    Article  CAS  PubMed  Google Scholar 

  34. Schardl C, Leuchtmann A. The Epichloe endophytes of grasses and the symbiotic continuum. In: Dighton J, White JF, Oudemans P, editors. The fungal community: its organization and role in the ecosystem. Boca Raton: Taylor & Francis; 2005. p. 475–503.

    Google Scholar 

  35. Schardl SL, Leuchtmann A, Spiering MJ. Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol. 2004;55:315–40.

    Article  CAS  PubMed  Google Scholar 

  36. Maheshwari R. What is an endophytic fungus? Curr Sci. 2006;90(10):1309. PubMed PMID: ISI:000239381500005

    Google Scholar 

  37. Murali TS, Suryanarayanan TS, Geeta R. Endophytic Phomopsis species: host range and implications for diversity estimates. Can J Microbiol. 2006;52(7):673–80. PubMed PMID: ISI:000239824600010

    Article  CAS  PubMed  Google Scholar 

  38. Redman RS, Dunigan DD, Rodriguez RJ. Fungal symbiosis: from mutualism to parasitism, who controls the outcome, host or invader? New Phytol. 2001;151:705–16.

    Article  Google Scholar 

  39. Redman RS, Freeman S, Clifton DR, Morrel J, Brown G, Rodriguez RJ. Biochemical analysis of plant protection afforded by a nonpathogenic endophytic mutant of colletotrichum magna. Plant Physiol. 1999;119:795–804.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Redman RS, Rossinck MR, Maher S, Andrews QC, Schneider WL, Rodriguez RJ. Field performance of cucurbit and tomato plants infected with a nonpathogenic mutant of Colletotrichum magna (teleomorph: Glomerella magna; Jenkins and Winstead). Symbiosis. 2002;32:55–70.

    Google Scholar 

  41. Arnold AE, Henk DA, Eells RL, Lutzoni F, Vilgalys R. Diversity and phylogenetic affinities of foliar fungal endophytes in loblolly pine inferred by culturing and environmental PCR. Mycologia. 2007;99(2):185–206. m

    Article  CAS  PubMed  Google Scholar 

  42. Arnold AE, Lutzoni F. Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology. 2007;88(3):541–9. PubMed PMID: ISI:000245668500002

    Article  PubMed  Google Scholar 

  43. Arnold AE, Mejia LC, Kyllo D, Rojas EI, Maynard Z, Robbins N, et al. Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci U S A. 2003;100(26):15649–54. PubMed PMID: ISI:000187554600066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Druege U, Baltruschat H, Franken P, et al. Sci Hortic. 2007;112(4):422–6. PubMed PMID: CCC:000246430400010

    Article  Google Scholar 

  45. Mandyam K, Jumpponen A. Seeking the elusive function of the root-colonising dark septate endophytic fungi. Stud Mycol. 2005;53:173–89. PubMed PMID: ISI:000234257200011

    Article  Google Scholar 

  46. Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, et al. The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci U S A. 2005;102:13386–91.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Sahay NS, Varma A. Piriformospora indica: a new biological hardening tool for micropropagated plants. FEMS Microbiol Lett. 1999;181:297–302.

    Article  CAS  PubMed  Google Scholar 

  48. Cline GF, Muth-Spurlock AM, Voelz BE, Lemley CO, Larson JE. Evaluating blood perfusion of the corpus luteum in beef cows during fescue toxicosis. J Anim Sci. 2016;94(1):90–5. doi:10.2527/jas.2015-9554. Epub 2016/01/27. PubMed PMID: 26812315

    Article  CAS  PubMed  Google Scholar 

  49. Fayrer-Hosken RA, Hill NS, Heusner GL, Traylor-Wiggins W, Turner K. The effects of ergot alkaloids on the breeding stallion reproductive system. Equine Vet J Suppl. 2013;45:44–7. doi:10.1111/evj.12164. Epub 2013/12/01. PubMed PMID: 24304403

    Article  Google Scholar 

  50. Johnson JM, Aiken GE, Phillips TD, Barrett M, Klotz JL, Schrick FN. Steer and pasture responses for a novel endophyte tall fescue developed for the upper transition zone. J Anim Sci. 2012;90(7):2402–9. doi:10.2527/jas.2011-4493. Epub 2012/01/31. PubMed PMID: 22287669

    Article  CAS  PubMed  Google Scholar 

  51. Matthews AK, Poore MH, Huntington GB, Green JT. Intake, digestion, and N metabolism in steers fed endophyte-free, ergot alkaloid-producing endophyte-infected, or nonergot alkaloid-producing endophyte-infected fescue hay. J Anim Sci. 2005;83(5):1179–85. Epub 2005/04/14. PubMed PMID: 15827262

    Article  CAS  PubMed  Google Scholar 

  52. Schuenemann GM, Edwards JL, Hopkins FM, Rohrbach NR, Adair HS, Scenna FN, et al. Fertility aspects in yearling beef bulls grazing endophyte-infected tall fescue pastures. Reprod Fertil Dev. 2005;17(4):479–86. Epub 2005/05/19. PubMed PMID: 15899160.

    Article  CAS  PubMed  Google Scholar 

  53. Shoup LM, Miller LM, Srinivasan M, Ireland FA, Shike DW. Effects of cows grazing toxic endophyte-infected tall fescue or novel endophyte-infected tall fescue in late gestation on cow performance, reproduction, and progeny growth performance and carcass characteristics. J Anim Sci. 2016;94(12):5105–13. doi:10.2527/jas.2016-0819. Epub 2017/01/04. PubMed PMID: 28046145

    Article  CAS  PubMed  Google Scholar 

  54. Omacini M, Chaneton EJ, Ghersa CM, Muller CB. Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature. 2001;409(6816):78–81. PubMed PMID: ISI:000166175600042

    Article  CAS  PubMed  Google Scholar 

  55. Cheplick GP. Recovery from drought stress in Lolium perenne (Poaceae): are fungal endophytes detrimental? Am J Bot. 2004;91(12):1960–8. doi:10.3732/ajb.91.12.1960. Epub 2004/12/01. PubMed PMID: 21652344

    Article  PubMed  Google Scholar 

  56. Cheplick GP. Persistence of endophytic fungi in cultivars of Lolium perenne grown from seeds stored for 22 years. Am J Bot. 2017;104(4):627–31. doi:10.3732/ajb.1700030. Epub 2017/04/16. PubMed PMID: 28411211

    Article  PubMed  Google Scholar 

  57. Cheplick GP, Harrichandra AP, Liu A. Competitive outcomes depend on host genotype, but not clavicipitaceous fungal endophytes, in Lolium perenne (Poaceae). Am J Bot. 2014;101(12):2068–78. doi:10.3732/ajb.1400264. Epub 2014/12/07. PubMed PMID: 25480704

    Article  PubMed  Google Scholar 

  58. Faeth SH. Are endophytic fungi defensive plant mutualists? (vol 98, pg 25, 2002). Oikos. 2002;99(1):200. PubMed PMID: ISI:000178883100022

    Article  Google Scholar 

  59. Saari S, Faeth SH. Hybridization of Neotyphodium endophytes enhances competitive ability of the host grass. New Phytol. 2012;195(1):231–6. doi:10.1111/j.1469-8137.2012.04140.x. Epub 2012/04/12. PubMed PMID: 22489964

    Article  CAS  PubMed  Google Scholar 

  60. Saikkonen K, Helander M, Faeth SH, Schulthess F, Wilson D. Endophyte-grass-herbivore interactions: the case of Neotyphodium endophytes in Arizona fescue populations. Oecologia. 1999;121(3):411–20. doi:10.1007/s004420050946. Epub 1999/11/01. PubMed PMID: 28308331

    Article  CAS  PubMed  Google Scholar 

  61. Saikkonen K, Phillips TD, Faeth SH, McCulley RL, Saloniemi I, Helander M. Performance of endophyte infected tall fescue in Europe and North America. PLoS One. 2016;11(6):e0157382. doi:10.1371/journal.pone.0157382. Epub 2016/06/11. PubMed PMID: 27284909; PubMed Central PMCID: PMCPMC4902185

    Article  PubMed  PubMed Central  Google Scholar 

  62. Rayner MC. Obligate symbiosis in Calluna vulgaris. Ann Bot. 1915;29:97–133.

    Article  Google Scholar 

  63. Bezerra JD, Nascimento CC, Barbosa Rdo N, da Silva DC, Svedese VM, Silva-Nogueira EB, et al. Endophytic fungi from medicinal plant Bauhinia forficata: diversity and biotechnological potential. Braz J Microbiol. 2015;46(1):49–57. doi:10.1590/S1517-838246120130657. Epub 2015/07/30. PubMed PMID: 26221088; PubMed Central PMCID: PMCPMC4512079

    Article  PubMed  PubMed Central  Google Scholar 

  64. Waqas M, Khan AL, Kamran M, Hamayun M, Kang SM, Kim YH, et al. Endophytic fungi produce gibberellins and indoleacetic acid and promotes host-plant growth during stress. Molecules. 2012;17(9):10754–73. doi:10.3390/molecules170910754. Epub 2012/09/11. PubMed PMID: 22960869

    Article  CAS  PubMed  Google Scholar 

  65. Weber RW, Stenger E, Meffert A, Hahn M. Brefeldin a production by Phoma medicaginis in dead pre-colonized plant tissue: a strategy for habitat conquest? Mycol Res. 2004;108(Pt 6):662–71. Epub 2004/08/25. PubMed PMID: 15323249

    Article  CAS  PubMed  Google Scholar 

  66. Xing YM, Chen J, Cui JL, Chen XM, Guo SX. Antimicrobial activity and biodiversity of endophytic fungi in Dendrobium devonianum and Dendrobium thyrsiflorum from Vietnam. Curr Microbiol. 2011;62(4):1218–24. doi:10.1007/s00284-010-9848-2. Epub 2010/12/25. PubMed PMID: 21181405

    Article  CAS  PubMed  Google Scholar 

  67. Petrini O. Taxonomy of endophytic fungi of aerial plant tissues. In: Fokkema NJ, van den Heuvel J, editors. Microbiology of the phyllosphere. Cambridge: Cambridge University Press; 1986. p. 175–87.

    Google Scholar 

  68. Pawlowska J, Wilk M, Sliwinska-Wyrzychowska A, Metrak M, Wrzosek M. The diversity of endophytic fungi in the above-ground tissue of two Lycopodium species in Poland. Symbiosis. 2014;63(2):87–97. doi:10.1007/s13199-014-0291-1. Epub 2014/09/30. PubMed PMID: 25264398; PubMed Central PMCID: PMCPMC4174293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Redman RS, Litvintseva A, Sheehan KB, Henson JM, Rodriguez R. Fungi from geothermal soils in Yellowstone National Park. Appl Environ Microbiol. 1999;65(12):5193–7. Epub 1999/12/03. PubMed PMID: 10583964; PubMed Central PMCID: PMCPMC91704

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM. Thermotolerance generated by plant/fungal symbiosis. Science. 2002;298(5598):1581. doi:10.1126/science.1072191. Epub 2002/11/26. PubMed PMID: 12446900

    Article  CAS  PubMed  Google Scholar 

  71. Pirozynski KA, Malloch DW. The origin of land plants a matter of mycotrophism. Biosystems. 1975;6(3):153–64.

    Article  CAS  PubMed  Google Scholar 

  72. Remy W, Taylor TN, Hass H, Kerp H. Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci U S A. 1994;91(25):11841–3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Tu JC. An improved Mathur’s medium for growth, sporulation, and germination of spores of Colletotrichum lindemuthianum. Microbios. 1985;44(178):87–93.

    CAS  Google Scholar 

  74. Ricklefs RE. Evolutionary diversification and the origin of the diversity-environment relationship. Ecology. 2006;87:S3–S13.

    Article  PubMed  Google Scholar 

  75. Rodriguez R, Redman R. More than 400 million years of evolution and some plants still can't make it on their own: plant stress tolerance via fungal symbiosis. J Exp Bot. 2008;59(5):1109–14. doi:10.1093/jxb/erm342. Epub 2008/02/13. PubMed PMID: 18267941

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank our AST team both past and present: Alec Stephen Baird, Alex Marcus Batson, Sang Hyun Cho, Eliza Alston Cliff, Zachery Gray, Evan David Groover, Roman Stentz Harto, Marian Jen-Mei Hsieh, Ryan John Manglona, Malia Marie Mercer, Natalie Marie Nasman, Tatiana Ariane Nicklason, Melissa Nicole Rienstra, and Leesa Lou Wright; and Mr. Anuj Dayama and Dr. Kalyan Dayama for assistance with organizing field tests in India, interpreting, and logistical support. Funding for field testing in India was supported in part by a Securing Water for Food grant from USAID (AID-OAA-A-15-0007) and a grant from the US-India Science and Technology Endowment Fund (EC-062).

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Correspondence to Regina S. Redman .

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Redman, R.S., Rodriguez, R.J. (2017). The Symbiogenic Tango: Achieving Climate-Resilient Crops Via Mutualistic Plant-Fungal Relationships. In: Doty, S. (eds) Functional Importance of the Plant Microbiome. Springer, Cham. https://doi.org/10.1007/978-3-319-65897-1_5

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