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Mycorrhiza

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Holobiont chronobiology: mycorrhiza may be a key to linking aboveground and underground rhythms

  • Soon-Jae Lee
  • David Morse
  • Mohamed HijriEmail author
Review

Abstract

Circadian clocks are nearly ubiquitous timing mechanisms that can orchestrate rhythmic behavior and gene expression in a wide range of organisms. Clock mechanisms are becoming well understood in fungal, animal, and plant model systems, yet many of these organisms are surrounded by a complex and diverse microbiota which should be taken into account when examining their biology. Of particular interest are the symbiotic relationships between organisms that have coevolved over time, forming a unit called a holobiont. Several studies have now shown linkages between the circadian rhythms of symbiotic partners. Interrelated regulation of holobiont circadian rhythms seems thus important to coordinate shifts in activity over the day for all the partners. Therefore, we suggest that the classical view of “chronobiological individuals” should include “a holobiont” rather than an organism. Unfortunately, mechanisms that may regulate interspecies temporal acclimation and the evolution of the circadian clock in holobionts are far from being understood. For the plant holobiont, our understanding is particularly limited. In this case, the holobiont encompasses two different ecosystems, one above and the other below the ground, with the two potentially receiving timing information from different synchronizing signals (Zeitgebers). The arbuscular mycorrhizal (AM) symbiosis, formed by plant roots and fungi, is one of the oldest and most widespread associations between organisms. By mediating the nutritional flux between the plant and the many microbes in the soil, AM symbiosis constitutes the backbone of the plant holobiont. Even though the importance of the AM symbiosis has been well recognized in agricultural and environmental sciences, its circadian chronobiology remains almost completely unknown. We have begun to study the circadian clock of arbuscular mycorrhizal fungi, and we compile and here discuss the available information on the subject. We propose that analyzing the interrelated temporal organization of the AM symbiosis and determining its underlying mechanisms will advance our understanding of the role and coordination of circadian clocks in holobionts in general.

Keywords

Arbuscular mycorrhizal fungi (AMF) Symbiosis Diurnal rhythm Feedback regulation Circadian clock Coevolution 

Notes

Acknowledgments

We thank Miss Jinwon Kim for assistance in preparing the figure and Dr. Marc St-Arnaud and Dr. Ian Sanders for their helpful comments on the manuscript. We also thank Dr. Dave Janos and two anonymous reviewers of their helpful comments on the manuscript. This work was supported by an NSERC Discovery grant to MH which is gratefully acknowledged.

References

  1. Ahmadjian V (1994) The lichen symbiosis. Nord J Bot 14(5):588.  https://doi.org/10.1111/j.1756-1051.1994.tb00653.x CrossRefGoogle Scholar
  2. Alarcon A, Davies FT Jr, Egilla JN, Fox TC, Estrada-Luna AA, Ferrera-Cerrato R (2002) Short term effects of Glomus claroideum and Azospirillum brasilense on growth and root acid phosphatase activity of Carica papaya L. under phosphorus stress. Rev Latinoam Microbiol 44(1):31–37PubMedGoogle Scholar
  3. Beans C (2017) Core concept: probing the phytobiome to advance agriculture. Proc Natl Acad Sci U S A 114(34):8900–8902CrossRefPubMedPubMedCentralGoogle Scholar
  4. Beneduzi A, Ambrosini A, Passaglia LMP (2012) Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genet Mol Biol 35:1044–1051CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bever JD (1994) Feeback between plants and their soil communities in an old field community. Ecology 75(7):1965–1977.  https://doi.org/10.2307/1941601 CrossRefGoogle Scholar
  6. Blackall LL, Wilson B, van Oppen MJH (2015) Coral-the world’s most diverse symbiotic ecosystem. Mol Ecol 24(21):5330–5347CrossRefPubMedGoogle Scholar
  7. Blanke V, Renker C, Wagner M, Fullner K, Held M, Kuhn AJ, Buscot F (2005) Nitrogen supply affects arbuscular mycorrhizal colonization of Artemisia vulgaris in a phosphate-polluted field site. New Phytol 166(3):981–992CrossRefPubMedGoogle Scholar
  8. Bordenstein SR, Theis KR (2015) Host biology in light of the microbiome: ten principles of holobionts and hologenomes. PLoS Biol 13(8):e1002226CrossRefPubMedPubMedCentralGoogle Scholar
  9. Boxall SF, Dever LV, Kneřová J, Gould PD, Hartwell J (2017) Phosphorylation of Phosphoenolpyruvate Carboxylase Is Essential for Maximal and Sustained Dark CO2 Fixation and Core Circadian Clock Operation in the Obligate Crassulacean Acid Metabolism Species Kalanchoë fedtschenkoi. Plant Cell 29(10):2519–2536Google Scholar
  10. Challet E, Caldelas I, Graff C, Pevet P (2003) Synchronization of the molecular clockwork by light- and food-related cues in mammals. Biol Chem 384(5):711–719CrossRefPubMedGoogle Scholar
  11. Chen BD, Zhu YG, Duan J, Xiao XY, Smith SE (2007) Effects of the arbuscular mycorrhizal fungus Glomus mosseae on growth and metal uptake by four plant species in copper mine tailings. Environ Pollut 147(2):374–380CrossRefPubMedGoogle Scholar
  12. Chen AH, Lubkowicz D, Yeong V, Chang RL, Silver PA (2015) Transplantability of a circadian clock to a noncircadian organism. Sci Adv 1(5):e1500358CrossRefPubMedPubMedCentralGoogle Scholar
  13. Ciani A, Goss KU, Schwarzenbach RP (2005) Light penetration in soil and particulate minerals. Eur J Soil Sci 56(5):561–574.  https://doi.org/10.1111/j.1365-2389.2005.00688.x CrossRefGoogle Scholar
  14. Collett MA, Garceau N, Dunlap JC, Loros JJ (2002) Light and clock expression of the Neurospora clock gene frequency is differentially driven by but dependent on WHITE COLLAR-2. Genetics 160(1):149–158PubMedPubMedCentralGoogle Scholar
  15. Cruz AF, Ishii T (2012) Arbuscular mycorrhizal fungal spores host bacteria that affect nutrient biodynamics and biocontrol of soil-borne plant pathogens. Biol Open 1(1):52–57CrossRefPubMedGoogle Scholar
  16. Czeisler CA, Gooley JJ (2007) Sleep and circadian rhythms in humans. Cold Spring Harb Symp Quant Biol 72:579–597CrossRefPubMedGoogle Scholar
  17. D'Alessandro M, Beesley S, Kim JK, Chen R, Abich E, Cheng W, Yi P, Takahashi JS, Lee C (2015) A tunable artificial circadian clock in clock-defective mice. Nat Commun 6:8587CrossRefPubMedPubMedCentralGoogle Scholar
  18. Del Campo EM, Catala S, Gimeno J, del Hoyo A, Martinez-Alberola F, Casano LM, Grube M, Barreno E (2013) The genetic structure of the cosmopolitan three-partner lichen Ramalina farinacea evidences the concerted diversification of symbionts. FEMS Microbiol Ecol 83(2):310–323CrossRefPubMedGoogle Scholar
  19. Dibner C, Schibler U, Albrecht U (2010) The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu Rev Physiol 72:517–549CrossRefPubMedPubMedCentralGoogle Scholar
  20. Dodd IC, Ruiz-Lozano JM (2012) Microbial enhancement of crop resource use efficiency. Curr Opin Biotechnol 23(2):236–242CrossRefPubMedGoogle Scholar
  21. Dodd IC, Puertolas J, Huber K, Perez-Perez JG, Wright HR, Blackwell MSA (2015) The importance of soil drying and re-wetting in crop phytohormonal and nutritional responses to deficit irrigation. J Exp Bot 66(8):2239–2252CrossRefPubMedPubMedCentralGoogle Scholar
  22. Dunlap JC, Loros JJ (2005) Analysis of circadian rhythms in Neurospora: overview of assays and genetic and molecular biological manipulation. Methods Enzymol 393:3–22CrossRefPubMedGoogle Scholar
  23. Durand M, Mainson D, Porcheron B, Maurousset L, Lemoine R, Pourtau N (2018) Carbon source-sink relationship in Arabidopsis thaliana: the role of sucrose transporters. Planta 247(3):587–611CrossRefPubMedGoogle Scholar
  24. Eymann C, Lassek C, Wegner U, Bernhardt J, Fritsch OA, Fuchs S, Otto A, Albrecht D, Schiefelbein U, Cernava T, Aschenbrenner I, Berg G, Grube M, Riedel K (2017) Symbiotic interplay of fungi, algae, and bacteria within the lung lichen Lobaria pulmonaria L. Hoffm. as assessed by state-of-the-art metaproteomics. J Proteome Res 16(6):2160–2173CrossRefPubMedGoogle Scholar
  25. Gallego M, Virshup DM (2007) Post-translational modifications regulate the ticking of the circadian clock. Nat Rev Mol Cell Biol 8(2):139–148CrossRefPubMedGoogle Scholar
  26. Gilbert SF, Sapp J, Tauber AI (2012) A symbiotic view of life: we have never been individuals. Q Rev Biol 87(4):325–341CrossRefPubMedGoogle Scholar
  27. Gopalakrishnan S, Sathya A, Vijayabharathi R, Varshney RK, Gowda CLL, Krishnamurthy L (2015) Plant growth promoting rhizobia: challenges and opportunities. 3 Biotech 5(4):355–377CrossRefPubMedGoogle Scholar
  28. Greenham K, McClung CR (2015) Integrating circadian dynamics with physiological processes in plants. Nat Rev Genet 16(10):598–610CrossRefPubMedGoogle Scholar
  29. Greer R, Dong X, Morgun A, Shulzhenko N (2016) Investigating a holobiont: microbiota perturbations and transkingdom networks. Gut Microbes 7(2):126–135CrossRefPubMedPubMedCentralGoogle Scholar
  30. Gutierrez RA, Stokes TL, Thum K, Xu X, Obertello M, Katari MS, Tanurdzic M, Dean A, Nero DC, McClung CR, Coruzzi GM (2008) Systems approach identifies an organic nitrogen-responsive gene network that is regulated by the master clock control gene CCA1. Proc Natl Acad Sci U S A 105(12):4939–4944CrossRefPubMedPubMedCentralGoogle Scholar
  31. Haag KL (2018) Holobionts and their hologenomes: evolution with mixed modes of inheritance. Genet Mol Biol 41:189–197Google Scholar
  32. Halaban R (1968) The circadian rhythm of leaf movement of Coleus blumei x C. frederici, a short day plant. II. The effects of light and temperature signals. Plant Physiol 43(12):1887–1893CrossRefPubMedPubMedCentralGoogle Scholar
  33. Halberg F, Cornelissen G, Katinas G, Syutkina EV, Sothern RB, Zaslavskaya R, Halberg F, Watanabe Y, Schwartzkopff O, Otsuka K, Tarquini R, Frederico P, Siggelova J (2003) Transdisciplinary unifying implications of circadian findings in the 1950s. J Circadian Rhythms 1(1):2CrossRefPubMedPubMedCentralGoogle Scholar
  34. Halberg F, Cornelissen G, Faraone P, Poeggeler B, Hardeland R, Katinas G, Schwartzkopff O, Otsuka K, Bakken EE (2005) Prokaryotic and eukaryotic unicellular chronomics. Biomed Pharmacother 59(Suppl 1):S192–S202CrossRefPubMedPubMedCentralGoogle Scholar
  35. Hansel CM, Fendorf S, Jardine PM, Francis CA (2008) Changes in bacterial and archaeal community structure and functional diversity along a geochemically variable soil profile. Appl Environ Microbiol 74(5):1620–1633CrossRefPubMedPubMedCentralGoogle Scholar
  36. Harmer SL, Panda S, Kay SA (2001) Molecular bases of circadian rhythms. Annu Rev Cell Dev Biol 17:215–253CrossRefPubMedGoogle Scholar
  37. Haydon MJ, Román Á, Arshad W (2015) Nutrient homeostasis within the plant circadian network. Front Plant Sci 6:299CrossRefPubMedPubMedCentralGoogle Scholar
  38. Heath-Heckman EA, Peyer SM, Whistler CA, Apicella MA, Goldman WE, McFall-Ngai MJ (2013) Bacterial bioluminescence regulates expression of a host cryptochrome gene in the squid-Vibrio symbiosis. MBio 4(2):e00167-13Google Scholar
  39. Hernandez RR, Allen MF (2013) Diurnal patterns of productivity of arbuscular mycorrhizal fungi revealed with the soil ecosystem observatory. New Phytol 200(2):547–557CrossRefPubMedPubMedCentralGoogle Scholar
  40. Hill EM, Robinson LA, Abdul-Sada A, Vanbergen AJ, Hodge A, Hartley SE (2018) Arbuscular mycorrhizal fungi and plant chemical defence: effects of colonisation on aboveground and belowground metabolomes. J Chem Ecol 44(2):198–208CrossRefPubMedPubMedCentralGoogle Scholar
  41. Honegger R, Edwards D, Axe L (2013) The earliest records of internally stratified cyanobacterial and algal lichens from the Lower Devonian of the Welsh Borderland. New Phytol 197(1):264–275CrossRefPubMedGoogle Scholar
  42. Hurley JM, Loros JJ, Dunlap JC (2016) The circadian system as an organizer of metabolism. Fungal Genet Biol 90:39–43CrossRefPubMedGoogle Scholar
  43. Ito H, Mutsuda M, Murayama Y, Tomita J, Hosokawa N, Terauchi K, Sugita C, Sugita M, Kondo T, Iwasaki H (2009) Cyanobacterial daily life with Kai-based circadian and diurnal genome-wide transcriptional control in Synechococcus elongatus. Proc Natl Acad Sci U S A 106(33):14168–14173CrossRefPubMedPubMedCentralGoogle Scholar
  44. James AB, Monreal JA, Nimmo GA, Kelly CL, Herzyk P, Jenkins GI, Nimmo HG (2008) The circadian clock in Arabidopsis roots is a simplified slave version of the clock in shoots. Science 322(5909):1832–1835CrossRefPubMedGoogle Scholar
  45. Jansa J, Bukovska P, Gryndler M (2013) Mycorrhizal hyphae as ecological niche for highly specialized hypersymbionts - or just soil free-riders? Front Plant Sci 4:134CrossRefPubMedPubMedCentralGoogle Scholar
  46. Jefferson RA (2019) Hormones and the Holobiont: origins and some implications of hologenome theory. In: The second international conference on holobionts, Montreal, pp 8–10Google Scholar
  47. Johnson CH, Golden SS, Kondo T (1998) Adaptive significance of circadian programs in cyanobacteria. Trends Microbiol 6(10):407–410CrossRefPubMedGoogle Scholar
  48. Johnston JD, Ordovas JM, Scheer FA, Turek FW (2016) Circadian rhythms, metabolism, and chrononutrition in rodents and humans. Adv Nutr 7(2):399–406CrossRefPubMedPubMedCentralGoogle Scholar
  49. Kaiser C, Kilburn MR, Clode PL, Fuchslueger L, Koranda M, Cliff JB, Solaiman ZM, Murphy DV (2015) Exploring the transfer of recent plant photosynthates to soil microbes: mycorrhizal pathway vs direct root exudation. New Phytol 205(4):1537–1551CrossRefPubMedGoogle Scholar
  50. Kolling K, Thalmann M, Muller A, Jenny C, Zeeman SC (2015) Carbon partitioning in Arabidopsis thaliana is a dynamic process controlled by the plants metabolic status and its circadian clock. Plant Cell Environ 38(10):1965–1979CrossRefPubMedPubMedCentralGoogle Scholar
  51. Kondo T, Ishiura M (2000) The circadian clock of cyanobacteria. Bioessays 22(1):10–15CrossRefPubMedGoogle Scholar
  52. Larcher W (2003) Physiological plant ecology. Springer-Verlag Berlin Heidelberg, BerlinCrossRefGoogle Scholar
  53. Lee S-J, Kong M, Morse D, Hijri M (2018) Expression of putative circadian clock components in the arbuscular mycorrhizal fungus Rhizoglomus irregulare. Mycorrhiza 28:523–534CrossRefPubMedGoogle Scholar
  54. Lemanceau P, Blouin M, Muller D, Moenne-Loccoz Y (2017) Let the core microbiota be functional. Trends Plant Sci 22(7):583–595CrossRefPubMedGoogle Scholar
  55. Leone V, Gibbons SM, Martinez K, Hutchison AL, Huang EY, Cham CM, Pierre JF, Heneghan AF, Nadimpalli A, Hubert N et al (2015) Effects of diurnal variation of gut microbes and high-fat feeding on host circadian clock function and metabolism. Cell Host Microbe 17(5):681–689CrossRefPubMedPubMedCentralGoogle Scholar
  56. Levy O, Kaniewska P, Alon S, Eisenberg E, Karako-Lampert S, Bay LK, Reef R, Rodriguez-Lanetty M, Miller DJ, Hoegh-Guldberg O (2011) Complex diel cycles of gene expression in coral-algal symbiosis. Science 331(6014):175CrossRefPubMedGoogle Scholar
  57. Lewis MT, Feldman JF (1996) Evolution of the frequency (frq) clock locus in ascomycete fungi. Mol Biol Evol 13(9):1233–1241CrossRefPubMedGoogle Scholar
  58. Liang X, Bushman FD, FitzGerald GA (2015) Rhythmicity of the intestinal microbiota is regulated by gender and the host circadian clock. Proc Natl Acad Sci U S A 112(33):10479–10484CrossRefPubMedPubMedCentralGoogle Scholar
  59. Loros JJ, Dunlap JC (2001) Genetic and molecular analysis of circadian rhythms in Neurospora. Annu Rev Physiol 63:757–794CrossRefPubMedGoogle Scholar
  60. Loza-Correa M, Gomez-Valero L, Buchrieser C (2010) Circadian clock proteins in prokaryotes: hidden rhythms? Front Microbiol 1:130CrossRefPubMedPubMedCentralGoogle Scholar
  61. Maeght J-L, Rewald B, Pierret A (2013) How to study deep roots-and why it matters. Front Plant Sci 4:299CrossRefPubMedPubMedCentralGoogle Scholar
  62. Margulis L, Fester R (1991) Symbiosis as a source of evolutionary innovation. MIT Press,Google Scholar
  63. Mas P, Yanovsky MJ (2009) Time for circadian rhythms: plants get synchronized. Curr Opin Plant Biol 12(5):574–579CrossRefPubMedGoogle Scholar
  64. McClung CR (2006) Plant circadian rhythms. Plant Cell 18(4):792–803CrossRefPubMedPubMedCentralGoogle Scholar
  65. McDonald MJ, Rosbash M (2001) Microarray analysis and organization of circadian gene expression in Drosophila. Cell 107(5):567–578CrossRefPubMedGoogle Scholar
  66. Meglouli H, Lounes-Hadj Sahraoui A, Magnin-Robert M, Tisserant B, Hijri M, Fontaine J (2018) Arbuscular mycorrhizal inoculum sources influence bacterial, archaeal, and fungal communities' structures of historically dioxin/furan-contaminated soil but not the pollutant dissipation rate. Mycorrhiza 28:635–650CrossRefPubMedGoogle Scholar
  67. Mendoza J, Graff C, Dardente H, Pevet P, Challet E (2005) Feeding cues alter clock gene oscillations and photic responses in the suprachiasmatic nuclei of mice exposed to a light/dark cycle. J Neurosci 25(6):1514–1522CrossRefPubMedGoogle Scholar
  68. Michael TP, Salome PA, McClung CR (2003) Two Arabidopsis circadian oscillators can be distinguished by differential temperature sensitivity. Proc Natl Acad Sci U S A 100(11):6878–6883CrossRefPubMedPubMedCentralGoogle Scholar
  69. Mindell DP (1992) Phylogenetic consequences of symbioses: Eukarya and Eubacteria are not monophyletic taxa. Bio Systems 27(1):53–62CrossRefPubMedGoogle Scholar
  70. Mittag M (2001) Circadian rhythms in microalgae. Int Rev Cytol 206:213–247CrossRefPubMedGoogle Scholar
  71. Mohammad MJ, Pan WL, Kennedy AC (2005) Chemical alteration of the rhizosphere of the mycorrhizal-colonized wheat root. Mycorrhiza 15(4):259–266CrossRefPubMedGoogle Scholar
  72. Mori T, Johnson CH (2000) Circadian control of cell division in unicellular organisms. Prog Cell Cycle Res 4:185–192CrossRefPubMedGoogle Scholar
  73. Mukherji A, Kobiita A, Ye T, Chambon P (2013) Homeostasis in intestinal epithelium is orchestrated by the circadian clock and microbiota cues transduced by TLRs. Cell 153(4):812–827CrossRefPubMedGoogle Scholar
  74. Muller LM, von Korff M, Davis SJ (2014) Connections between circadian clocks and carbon metabolism reveal species-specific effects on growth control. J Exp Bot 65(11):2915–2923CrossRefPubMedGoogle Scholar
  75. Nagel DH, Kay SA (2012) Complexity in the wiring and regulation of plant circadian networks. Curr Biol 22(16):R648–R657CrossRefPubMedPubMedCentralGoogle Scholar
  76. Ohtomo R, Saito M (2005) Polyphosphate dynamics in mycorrhizal roots during colonization of an arbuscular mycorrhizal fungus. New Phytol 167(2):571–578CrossRefPubMedGoogle Scholar
  77. Oosterhuis DM (1990) Growth and development of a cotton plant. In: Miley WN, Oosterhuis DM (Eds.) Nitrogen nutrition in cotton: Practical Issues, Proceedings, Southern Branch Workshop for Practicing Agronomists. American Society of Agronomy, Madison, WI, pp.1-24Google Scholar
  78. Ouyang Y, Andersson CR, Kondo T, Golden SS, Johnson CH (1998) Resonating circadian clocks enhance fitness in cyanobacteria. Proc Natl Acad Sci U S A 95(15):8660–8664CrossRefPubMedPubMedCentralGoogle Scholar
  79. Pallas JE, Samish JYB, Willmer CM (1974) Endogenous rhythmic activity of photosynthesis, transpiration, dark respiration, and carbon dioxide compensation point of peanut leaves. Plant Physiol 53(6):907–911CrossRefPubMedPubMedCentralGoogle Scholar
  80. Pando MP, Morse D, Cermakian N, Sassone-Corsi P (2002) Phenotypic rescue of a peripheral clock genetic defect via SCN hierarchical dominance. Cell 110(1):107–117CrossRefPubMedGoogle Scholar
  81. Pankova H, Lepinay C, Rydlova J, Voriskova A, Janouskova M, Dostalek T, Munzbergova Z (2018) Arbuscular mycorrhizal fungi and associated microbial communities from dry grassland do not improve plant growth on abandoned field soil. Oecologia 186(3):677–689CrossRefPubMedGoogle Scholar
  82. Piggins HD (2002) Human clock genes. Ann Med 34(5):394–400CrossRefPubMedGoogle Scholar
  83. Rivero J, Alvarez D, Flors V, Azcon-Aguilar C, Pozo MJ (2018) Root metabolic plasticity underlies functional diversity in mycorrhiza-enhanced stress tolerance in tomato. New Phytol 220(4):1322–1336CrossRefPubMedGoogle Scholar
  84. Roenneberg T, Morse D (1993) Two circadian oscillators in one cell. Nature 362(6418):362–364.  https://doi.org/10.1038/362362a0 CrossRefPubMedGoogle Scholar
  85. Rosenberg E, Sharon G, Atad I, Zilber-Rosenberg I (2010) The evolution of animals and plants via symbiosis with microorganisms. Environ Microbiol Rep 2(4):500–506CrossRefPubMedGoogle Scholar
  86. Sancar G, Sancar C, Brunner M (2012) Metabolic compensation of the Neurospora clock by a glucose-dependent feedback of the circadian repressor CSP1 on the core oscillator. Genes Dev 26:2435–2442.  https://doi.org/10.1101/gad.199547.112 CrossRefPubMedPubMedCentralGoogle Scholar
  87. Sanchez SE, Kay SA (2016) The plant circadian clock: from a simple timekeeper to a complex developmental manager. Cold Spring Harb Perspect Biol 16(8):a027748CrossRefGoogle Scholar
  88. Schüβler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105(12):1413–1421.  https://doi.org/10.1017/S0953756201005196 CrossRefGoogle Scholar
  89. Schwarz JA, Brokstein PB, Voolstra C, Terry AY, Manohar CF, Miller DJ, Szmant AM, Coffroth MA, Medina M (2008) Coral life history and symbiosis: functional genomic resources for two reef building Caribbean corals, Acropora palmata and Montastraea faveolata. BMC Genomics 9:97CrossRefPubMedPubMedCentralGoogle Scholar
  90. Sender R, Fuchs S, Milo R (2016) Revised estimates for the number of human and bacteria cells in the body. PLoS Biol 14(8):e1002533CrossRefPubMedPubMedCentralGoogle Scholar
  91. Shukla A, Vyas D, Anuradha J (2013) Soil depth: an overriding factor for distribution of arbuscular mycorrhizal fungi. J Soil Sci Plant Nutr 13:23–33.  https://doi.org/10.4067/S0718-95162013005000003 CrossRefGoogle Scholar
  92. Simon L, Bousquet J, Levesque CR, Lalonde M (1993) Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Nature 363:67–69CrossRefGoogle Scholar
  93. Smith A (1932) Seasonal subsoil temperature variations. J Agric Res 44(5):421–428Google Scholar
  94. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, Third edn. Academic Press, New YorkGoogle Scholar
  95. Solis-Dominguez FA, Valentin-Vargas A, Chorover J, Maier RM (2011) Effect of arbuscular mycorrhizal fungi on plant biomass and the rhizosphere microbial community structure of mesquite grown in acidic lead/zinc mine tailings. Sci Total Environ 409(6):1009–1016CrossRefPubMedPubMedCentralGoogle Scholar
  96. Sorek M, Yacobi YZ, Roopin M, Berman-Frank I, Levy O (2013) Photosynthetic circadian rhythmicity patterns of Symbiodinium, [corrected] the coral endosymbiotic algae. Proc Biol Sci 280(1759):20122942CrossRefPubMedPubMedCentralGoogle Scholar
  97. Sorek M, Diaz-Almeyda EM, Medina M, Levy O (2014) Circadian clocks in symbiotic corals: the duet between Symbiodinium algae and their coral host. Mar Genomics 14:47–57CrossRefPubMedGoogle Scholar
  98. Soriano MI, Roibas B, Garcia AB, Espinosa-Urgel M (2010) Evidence of circadian rhythms in non-photosynthetic bacteria? J Circadian Rhythms 8:8CrossRefPubMedPubMedCentralGoogle Scholar
  99. Stone E, Kalisz P (1991a) On the maximum extent of tree roots. For Ecol Manag 46:59–102CrossRefGoogle Scholar
  100. Stone EL, Kalisz PJ (1991b) On the maximum extent of tree roots. For Ecol Manag 46(1–2):59–102.  https://doi.org/10.1016/0378-1127(91)90245-Q CrossRefGoogle Scholar
  101. Storch K-F, Lipan O, Leykin I, Viswanathan N, Davis FC, Wong WH, Weitz CJ (2002) Extensive and divergent circadian gene expression in liver and heart. Nature 417(6884):78–83CrossRefPubMedGoogle Scholar
  102. Subramanian P, Balamurugan E, Suthakar G (2003) Circadian clock genes in Drosophila: recent developments. Indian J Exp Biol 41(8):797–804PubMedGoogle Scholar
  103. Thaiss CA, Zeevi D, Levy M, Zilberman-Schapira G, Suez J, Tengeler AC, Abramson L, Katz MN, Korem T, Zmora N, Kuperman Y, Biton I, Gilad S, Harmelin A, Shapiro H, Halpern Z, Segal E, Elinav E (2014) Transkingdom control of microbiota diurnal oscillations promotes metabolic homeostasis. Cell 159(3):514–529CrossRefPubMedGoogle Scholar
  104. Thirkell TJ, Cameron DD, Hodge A (2016) Resolving the ‘nitrogen paradox’ of arbuscular mycorrhizas: fertilization with organic matter brings considerable benefits for plant nutrition and growth. Plant Cell Environ 39(8):1683–1690CrossRefPubMedPubMedCentralGoogle Scholar
  105. Turner S, Mikutta R, Meyer-Stuve S, Guggenberger G, Schaarschmidt F, Lazar CS, Dohrmann R, Schippers A (2017) Microbial community dynamics in soil depth profiles over 120,000 years of ecosystem development. Front Microbiol 8:874CrossRefPubMedPubMedCentralGoogle Scholar
  106. Vančurová L, Muggia L, Peksa O, Řídká T, Škaloud P (2018) The complexity of symbiotic interactions influences the ecological amplitude of the host: A case study in Stereocaulon (lichenized Ascomycota).Molecular Ecology 27(14):3016–3033Google Scholar
  107. Vijayan V, Zuzow R, O’Shea EK (2009) Oscillations in supercoiling drive circadian gene expression in cyanobacteria. Proc Natl Acad Sci U S A 106(52):22564–22568CrossRefPubMedPubMedCentralGoogle Scholar
  108. Walter J, Martinez I, Rose DJ (2013) Holobiont nutrition: considering the role of the gastrointestinal microbiota in the health benefits of whole grains. Gut Microbes 4(4):340–346CrossRefPubMedPubMedCentralGoogle Scholar
  109. Wang G-Y, Shi J-L, Ng G, Battle SL, Zhang C, Lu H (2011) Circadian clock-regulated phosphate transporter PHT4;1 plays an important role in Arabidopsis defense. Mol Plant 4(3):516–526CrossRefPubMedPubMedCentralGoogle Scholar
  110. Wang X-X, Wang X, Sun Y, Cheng Y, Liu S, Chen X, Feng G, Kuyper TW (2018) Arbuscular mycorrhizal fungi negatively affect nitrogen acquisition and grain yield of maize in a N deficient soil. Front Microbiol 9:418CrossRefPubMedPubMedCentralGoogle Scholar
  111. Wier AM, Nyholm SV, Mandel MJ, Massengo-Tiasse RP, Schaefer AL, Koroleva I, Splinter-Bondurant S, Brown B, Manzella L, Snir E, Almabrazi H, Scheetz TE, Bonaldo MF, Casavant TL, Soares MB, Cronan JE, Reed JL, Ruby EG, McFall-Ngai MJ (2010) Transcriptional patterns in both host and bacterium underlie a daily rhythm of anatomical and metabolic change in a beneficial symbiosis. Proc Natl Acad Sci U S A 107(5):2259–2264CrossRefPubMedPubMedCentralGoogle Scholar
  112. Yazdanbakhsh N, Sulpice R, Graf A, Stitt M, Fisahn J (2011) Circadian control of root elongation and C partitioning in Arabidopsis thaliana. Plant Cell Environ 34(6):877–894CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Institut de Recherche en Biologie Végétale (IRBV)Université de MontréalMontréalCanada
  2. 2.Department of Ecology and EvolutionUniversity of LausanneLausanneSwitzerland

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