Circadian Rhythms in Plant-Microbe Interaction: For Better Performance of Bioinoculants in the Agricultural Fields

  • Raghavendra Maddur Puttaswamy
Part of the Soil Biology book series (SOILBIOL, volume 55)


Circadian rhythm (CR) is an important regulator of numerous basic functions of the living organisms such as carbon metabolism, gene expression and regulation, growth and reproduction. It is widely accepted, and several research activities prove its implication on health and disease especially in humans and plants including microbes associated with it. CR is reported to regulate circadian clock which is subjected to extensive natural variation during day and night, light intensity, availability of nutrients, stress and other factors. CR varies within and between species; this underlies the importance of understanding the phenomenon at the individual level to develop disease management strategies or production of microbial formulations used for growth promotion. In plants, rhizosphere microorganisms extensively depend on the root exudates, and its composition is reported to alter with CR in response to external stimuli including global warming and pollution. These microbes play an important role in plant growth and its environmental fitness and hence the concept of plant growth-promoting rhizobacteria (PGPR) came to existence. However, even today circadian clock regulating interaction of PGPR with plants is not extensively studied, and hence most of the time, microbes developed in the laboratory fail to perform in the field level. The world is awaiting another green revolution to feed the growing population with bitter experience of the previous revolution. It is the right time to understand the circadian clock at the species level and to develop suitable formulations to exploit the beneficial aspect of plant-microbe interaction to achieve high yield in the agricultural fields as a part of the sustainable agriculture. Understanding the CR in plant-pathogen interaction will also help to develop suitable treatment strategies to overcome the yield loss due to infection.


Plant growth-promoting rhizobacteria Sustainable agriculture Rhizosphere microflora Circadian clock 


  1. Abbott L, Murphy D (2003) Soil biology fertility: a key to sustainable land use in agriculture. Kluwer Academic, Dordrecht, pp 187–203Google Scholar
  2. Adeola AJ, Apapa AN, Adeyemo AI, Alaye SA, Ogunjobi JA (2014) Seasonal variation in plants consumption pattern by foraging Olive baboons (Papio anubis. Lesson, 1827) inside Kainji lake national park, Nigeria. J Appl Sci Environ Manage 18:481–484Google Scholar
  3. Barber DA, Martin JK (1976) The release of organic substances by cereal roots into soil. New Phytol 76:69–80CrossRefGoogle Scholar
  4. Baudoin E, Benizri E, Guckert AV (2002) Impact of growth stage on the bacterial community structure along maize roots, as determined by metabolic and genetic fingerprinting. Appl Soil Ecol 19:135–145CrossRefGoogle Scholar
  5. Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13PubMedCrossRefGoogle Scholar
  6. Blasing OE, Gibon Y, Gunther M, Hohne M, Morcuende R, Osuna D, Thimm O, Usadel B, Scheible WR, Stitt M (2005) Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell 17:3257–3281PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bressan M, Roncato MA, Bellvert F, Comte G, Haichar EZF, Achouak W, Berge O (2009) Exogenous glucosinolate produced by Arabidopsis thaliana has an impact on microbes in the rhizosphere and plant roots. Int Soc Microb Ecol J 3:1243–1257Google Scholar
  8. Bulgarelli D, Rott M, Schlaeppi K, Van Themaat EV, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E, Peplies J, Gloeckner FO, Amann R, Eickhorst T, Schulze-Lefert P (2012) Revealing structure and assembly cues for Arabidopsis root inhabiting bacterial microbiota. Nature 488:91–95PubMedCrossRefGoogle Scholar
  9. Bunning E (1931) Untersuchungen uber die autonomen tagesperiodischen Bewungen der Primarblatter von Phaseolus multiflorus. Jahrb Wiss Bot 75:439–480Google Scholar
  10. Castro HF, Classen AT, Austin EE, Norby RJ, Schadt CW (2010) Soil microbial community response to multiple experimental climate change drivers. Appl Environ Microbiol 76:999–1007PubMedCrossRefGoogle Scholar
  11. Cieslinski G, van Rees KCJ, Huang PM (1997) Low molecular weight organic acids released from roots of durum wheat and flax into sterile nutrient solutions. J Plant Nutr 20:753–764CrossRefGoogle Scholar
  12. Compant S, Reiter B, Sessitsch A, Nowak J, Clément C, Ait Barka E (2005) Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. strain PsJN. Appl Environ Microbiol 71:1685–1693PubMedPubMedCentralCrossRefGoogle Scholar
  13. Compant S, Kaplan H, Sessitsch A, Nowak J, Ait Barka E, Clément C (2008) Endophytic colonization of Vitis vinifera L. by Burkholderia phytofirmans strain PsJN: from the rhizosphere to inflorescence tissues. FEMS Microbiol Ecol 63:84–93PubMedCrossRefGoogle Scholar
  14. Compant S, Clément C, Sessitsch A (2010a) Colonization of plant growth-promoting bacteria in the rhizo- and endosphere of plants: importance, mechanisms involved and future prospects. Soil Biol Biochem 42:669–678CrossRefGoogle Scholar
  15. Compant S, Marcel GA, Heijden VD, Sessitsch A (2010b) Climate change effects on beneficial plant-microorganisms interaction. FEMS Microbiol Ecol 66:197–214Google Scholar
  16. Daniel X, Sugano S, Tobin EM (2004) CK2 phosphorylation of CCA1 is necessary for its circadian oscillator function in Arabidopsis. Proc Natl Acad Sci 101:3293–3297CrossRefGoogle Scholar
  17. Dodd AN, Salathia N, Hall A, Kevei E, Toth R, Nagy F, Hiberd JM, Millar AJ, Webb AA (2005) Plant circadian clocks increase photosynthesis, growth, survival and competitive advantage. Science 309:630–633PubMedCrossRefGoogle Scholar
  18. Dowson-Day MJ, Millar AJ (1999) Circadian dysfunction causes aberrant hypocotyl elongation patterns in Arabidopsis. Plant J 17:63–71PubMedCrossRefGoogle Scholar
  19. Drigo B, Kowalchuk GA, van Veen JA (2008) Climate change goes underground: effects of elevated atmospheric CO2 on microbial community structure and activities in the rhizosphere. Biol Fertil Soils 44:667–679CrossRefGoogle Scholar
  20. Drigo B, Kowalchuk GA, Knapp BA, Pijl AS, Boschker HT, Veen JA (2013) Impacts of 3 years of elevated atmospheric CO2 on rhizosphere carbon flow and microbial community dynamics. Glob Chang Biol 19:621–636PubMedCrossRefGoogle Scholar
  21. Dunfield KE, Germida JJ (2003) Seasonal changes in the rhizosphere microbial communities associated with field grown genetically modified Canola (Brassica napus). Appl Environ Microbiol 69:7310–7318PubMedPubMedCentralCrossRefGoogle Scholar
  22. Dunlap JC (1999) Molecular bases for circadian clocks. Cell 96:271–290PubMedCrossRefGoogle Scholar
  23. Engelmann W, Johnsson A (1998) Rhythms in organ movement. In: Lumsden PJ, Millar AJ (eds) Biological rhythms and photoperiodism in plants. BIOS Scientific, Oxford, pp 35–50Google Scholar
  24. Fejes E, Nagy F (1998) Molecular analysis of circadian clock regulated gene expression in plants: features of the ‘output’ pathways. In: Lumsden PJ, Millar AJ (eds) Biological rhythms and photoperiodism in plants. BIOS Scientific, Oxford, pp 99–118Google Scholar
  25. Finlayson SA, Lee IJ, Mullet JE, Morgan PW (1999) The mechanism of rhythmic ethylene production in sorghum. The role of phytochrome B and simulated shading. Plant Physiol 119:1083–1089PubMedPubMedCentralCrossRefGoogle Scholar
  26. Forchetti G, Masciarelli O, Alemano S, Alvarez D, Abdala G (2007) Endophytic bacteria in sunflower (Helianthus annuus L.): Isolation, characterization, and production of jasmonates and abscisic acid in culture medium. Appl Microbiol Biotechnol 76:1145–1152PubMedCrossRefGoogle Scholar
  27. Foster KR, Morgan PW (1995) Genetic regulation of development in Sorghum bicolor (IX. The ma3 R allele disrupts diurnal control of gibberellin biosynthesis). Plant Physiol 108:337–343PubMedPubMedCentralCrossRefGoogle Scholar
  28. Fowler SG, Cook D, Tomashow MF (2005) Low temperature induction of Arabidopsis CBF1, 2 and 3 is gated by the circadian clock. Plant Physiol 137:961–968PubMedPubMedCentralCrossRefGoogle Scholar
  29. Gomes NCH, Heuer H, Schonfeld J, Costa R, Hagler-Mendoca L, Smalla K (2001) Bacterial diversity of the rhizosphere of maize (Zea mays) grown in tropical soil studies by temperature gradient gel electrophoresis. Plant Soil 233:167–180CrossRefGoogle Scholar
  30. Gomez LA, Simon E (1995) Circadian rhythm of Robinia pseudoacacia leaflets movements: role of calcium and phytochrome. Photochem Photobiol 61:210–215CrossRefGoogle Scholar
  31. Graf A, Schlereth A, Stitt M, Smith AM (2010) Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. Proc Natl Acad Sci 107:9458–9463PubMedCrossRefGoogle Scholar
  32. Grayston SJ, Griffith GS, Mawdsley JL, Campbell CD, Bardgett RD (2001) Accounting for variability in soil microbial communities for temperate upland grassland ecosystems. Soil Biol Biochem 33:533–551CrossRefGoogle Scholar
  33. Green RM, Tingay S, Wang ZY, Tobin EM (2002) Circadian rhythms confer a higher level of fitness to Arabidopsis plants. Plant Physiol 129:576–584PubMedPubMedCentralCrossRefGoogle Scholar
  34. Greenham K, McClung CR (2015) Integrating circadian dynamics with physiological processes in plants. Nat Rev Genet 16:598–610PubMedCrossRefGoogle Scholar
  35. Guadagno CR, Ewers BE, Weinig C (2018) Circadian rhythms and redox state in plants. Front Plant Sci 9:247–256PubMedPubMedCentralCrossRefGoogle Scholar
  36. Gutierrez RA, Stokes TL, Thum K, Xu X, Obertello M, Katari MS, Tanurdzic M, DeanA NDC, 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 105:4939–4944PubMedCrossRefGoogle Scholar
  37. Haase S, Philippot L, Neumann G, Marhan S, Kandeler E (2008) Local response of bacterial densities and enzyme activities to elevated atmospheric CO2 and different N supply in the rhizosphere of Phaseolus vulgaris L. Soil Biol Biochem 40:1225–1234CrossRefGoogle Scholar
  38. Halberg F, Halberg E, Barnum CP, Bittner JJ (1959) Physiologic 24-hour periodicity in human beings and mice, the lighting regimen and daily routine. In: Withrow RB (ed) Photoperiodism and related phenomenon in plants and animals, vol 55. Education Publishing, Washington, DC, pp 803–878Google Scholar
  39. Halberg F, Carandente F, Cornelissen G, Katinas GS (1977) Glossary of chronobiology. For Chron 4:1–189Google Scholar
  40. Hallmann J (2001) Plant interactions with endophytic bacteria. In: Jeger MJ, Spence NJ (eds) Biotic interactions in plant–pathogen associations. CABI Publishing, Wallingford, pp 87–119CrossRefGoogle Scholar
  41. Harmer SL (2009) The circadian system in higher plants. Annu Rev Plant Biol 60:357–377PubMedCrossRefGoogle Scholar
  42. Harmer SL, Hogenesch JB, Straume M, Chang HS, Han B, Zhu T, Wang X, Kreps JA, Kay SA, Zhu T, Wang X (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290:2110–2113PubMedCrossRefGoogle Scholar
  43. Hennessey TL, Field CB (1991) Oscillations in carbon assimilation and stomatal conductance under constant condition. Plant Physiol 96:831–836PubMedPubMedCentralCrossRefGoogle Scholar
  44. Hillman WS (1956) Injury of tomato plants by continuous light and unfavorable photoperiodic cycles. Am J Bot 43:89–96CrossRefGoogle Scholar
  45. Hubbard CJ, Brock MT, Dipen LTAV, Maignien L, Ewers BE, Weining C (2017) The plant circadian clock influences rhizosphere community structure. Int Soc Microb Ecol J 12:400–410Google Scholar
  46. Igiehon NO, Babalola OO (2018) Rhizosphere microbiome modulators: contributions of nitrogen fixing bacteria towards sustainable agriculture. Int J Environ Res Public Health 15:576–610CrossRefGoogle Scholar
  47. IPCC Climate Change Reports (2007) Impacts, adaptations and vulnerability. Cambridge University Press, Cambridge, pp 79–89Google Scholar
  48. Jarillo JA, Capel J, Cashmore AR (2003) Physiological and molecular characteristics of plant circadian clocks. In: Sehgal A (ed) Molecular biology of circadian rhythms. Wiley, Hoboken, NJ, pp 185–209Google Scholar
  49. Johnsson A (2007) Oscillations in plant transpiration. In: Mancuso S, Shabala S (eds) Rhythms in plants: phenomenology, mechanisms and adaptive significance. Springer, Berlin, pp 225–230Google Scholar
  50. Jones TL, Ort DR (1997) Circadian regulation of sucrose phosphate synthase activity in tomato by protein phosphatase activity. Plant Physiol 113:1167–1175PubMedPubMedCentralCrossRefGoogle Scholar
  51. Jouve L, Greppin H, Agosti RD (1998) Arabidopsis thaliana floral stem elongation: evidence for an endogenous circadian rhythm. Plant Physiol Biochem 36:469–472CrossRefGoogle Scholar
  52. Kamilova F, Kravchenko LV, Shaposhinkov AI, Azarova T, Makarova N, Lugtenberg B (2006) Organic acids, sugars and L-tryptophan in exudates of vegetables growing on stonewool and their effects on activities of rhizosphere bacteria. Mol Plant-Microbe Interact 19:250–256PubMedCrossRefGoogle Scholar
  53. Kandeler E, Mosier AR, Morgan JA, Milchunas DG, King JY, Rudolph S, Tscherko D (2006) Response of soil microbial biomass and enzyme activities to the transient elevation of carbon dioxide in a semi-arid grassland. Soil Biol Biochem 38:2448–2460CrossRefGoogle Scholar
  54. Kellmann JW, Hoffrogge R, Piechulla B (1999) Transcriptional regulation of oscillating steady-state Lhc mRNA levels: Characterization of two Lhca promoter fragments in transgenic tobacco plants. Biol Rhythm Res 30:264–271CrossRefGoogle Scholar
  55. Kim HY, Cote GG, Crain RC (1993) Potassium channels in Samanea saman protoplasts controlled by phytochrome and the biological clock. Science 260:960–962PubMedCrossRefGoogle Scholar
  56. Kloppstech K (1985) Diurnal and circadian rhythmicity in the expression of light induced nuclear messenger RNAs. Plant 165:502–506CrossRefGoogle Scholar
  57. Knight H, Thomson AJW, McWatters HG (2008) Sensitive to freezing integrates cellular and environmental inputs to the plant circadian clock. Plant Physiol 148:293–303PubMedPubMedCentralCrossRefGoogle Scholar
  58. Kolling K, Thalmann M, Muller A, Jenny C, Zeeman SC (2015) Carbon partitioning in Arabidopsis thaliana is a dynamic process controlled by the plant metabolic status and its circadian clock. Cell Environ 38:1965–1979CrossRefGoogle Scholar
  59. Konmonth-Schultz HA, Golembeski GS, Imaizumi T (2013) Circadian clock regulated physiological outputs: dynamic responses in nature. Semin Cell Dev Biol 24:407–413CrossRefGoogle Scholar
  60. Landry LG, Chappel CCS, Last RL (1995) Arabidopsis mutants lacking phenolic sunscreens exhibit enhanced ultraviolet-B injury and oxidative damage. Plant Physiol 109:1159–1166PubMedPubMedCentralCrossRefGoogle Scholar
  61. Leone V, Gibbons SM, Martinez K, Hutchinson AL, Huang EY, Cham CM, Pierre JF, Heneghan AF, Nadimpalli HN, Zale E, Wang Y, Huang Y, Theriault B, Dinner AR, Musch MW, Kudsk KA, Prendergast BJ, Gilbert JA, Chang EB (2015) Effects of diurnal variation of gut microbes and high-fat feeding on host circadian clock function and metabolism. Cell Host Microbe 17:681–689PubMedPubMedCentralCrossRefGoogle Scholar
  62. Li J, Ou-Lee TM, Raba R, Amundson RG, Last RL (1993) Arabidopsis flavonoid mutants are hypersensitive to UV-B irradiation. Plant Cell 5:171–179PubMedPubMedCentralCrossRefGoogle Scholar
  63. 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 112:10479–10484PubMedCrossRefGoogle Scholar
  64. Linnaeus C (1770) Systema natvrae oer regna tria natvrae, secvndvm classes, ordines, genera, species cvm characteribvs, et differentiis. Tomvs III, pp 1–236Google Scholar
  65. Liu Z, Taub CC, McClung CR (1996) Identification of an Arabidopsis Rubisco Activase (RCA) minimal promoter regulated by phytochrome and the circadian clock. Plant Physiol 112:43–51PubMedPubMedCentralCrossRefGoogle Scholar
  66. Madhu M, Hatfield JL (2013) Dynamics of plant root growth under increased atmospheric carbon dioxide. Agron J 105:657–669CrossRefGoogle Scholar
  67. Mairan D (1729) Observation botanique. Hist Acad Roy Sci:35–36Google Scholar
  68. McClung CR, Kay SA (1994) Circadian rhythms in Arabidopsis thaliana. In: Meyweowitz EM, Somerville CR (eds) Arabidopsis. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 615–637Google Scholar
  69. Merbach W, Mirus E, Knof G, Remus R, Ruppel S, Russow R, Gransee A, Schulze J (1999) Release of carbon and nitrogen compounds by plant roots and their possible ecological importance. J Plant Nutr Soil Sci 162:373–383CrossRefGoogle Scholar
  70. Michael TP, McClung CR (2003) Enhancer trapping reveals widespread circadian clock transcriptional control in Arabidopsis thaliana. Plant Physiol 132:629–639PubMedPubMedCentralCrossRefGoogle Scholar
  71. Michael TP, Salome PA, Yu HJ, Spencer TR, Sharp EL, McPeek MA, Alonso JM, Ecker JR, McClung CR (2003) Enhanced fitness conferred by naturally occurring variation in the circadian clock. Science 302:1049–1053PubMedCrossRefGoogle Scholar
  72. Miethling R, Wieland G, Backhaus H, Tebbe CC (2000) Variation of microbial rhizosphere communities in response to crop species, soil origin and inoculation with Sinorhizobium meliloti L33. Microb Ecol 40:43–56PubMedCrossRefGoogle Scholar
  73. Millar AJ, Kay SA (1991) Circadian control of cab gene transcription and mRNA accumulation in Arabidopsis. Plant Cell 3:541–550PubMedPubMedCentralCrossRefGoogle Scholar
  74. Millar AJ, Short SR, Chua NH, Kay SA (1992) A novel circadian phenotype based on firefly luciferase expression in transgenic plants. Plant Cell 4:1075–1087PubMedPubMedCentralGoogle Scholar
  75. Muller LM, Korff MV, Davis SJ (2014) Connections between circadian clocks and carbon metabolism reveal species-specific effects on growth control. J Exp Bot 65:2915–2923PubMedCrossRefGoogle Scholar
  76. Nagy F, Kay SA, Chua N-H (1988) A circadian clock regulates transcription of the wheat Cab-1 gene. Genes Dev 2:376–382CrossRefGoogle Scholar
  77. Nimmo HG (2000) The regulation of phosphoenolpyruvate carboxylase in CAM plants. Trends Plant Sci 5:75–80PubMedCrossRefGoogle Scholar
  78. Piechulla B (1999) Circadian expression of the light harvesting complex protein genes in plants. Chronobiol Int 16:115–128PubMedCrossRefGoogle Scholar
  79. Pilgrim ML, Caspar T, Quail PH, McClung CR (1993) Circadian and light regulated expression of nitrate reductase in Arabidopsis. Plant Mol Biol 23:349–364PubMedCrossRefGoogle Scholar
  80. Pillay VK, Nowak J (1997) Inoculum density, temperature, and genotype effects on in vitro growth promotion and epiphytic and endophytic colonization of tomato (Lycopersicon esculentum L.) seedlings inoculated with a pseudomonad bacterium. Can J Microbiol 43:54–361CrossRefGoogle Scholar
  81. Raja P, Uma S, Gopal H, Govindarajan K (2006) Impact of bioinoculants consortium on rice root exudates, biological nitrogen fixation and plant growth. J Biol Sci 6(5):815–823CrossRefGoogle Scholar
  82. Rangaswami G (1988) Soil plant microbe interrelationships. Indian Phytopathol 41:165–172Google Scholar
  83. Raschke K (1979) Movements of stomata. In: Haupt W, Feinleib ME (eds) Physiology of movements, encyclopedia of plant physiology, vol 7. Springer, Berlin, pp 383–441Google Scholar
  84. Roden LC, Ingle RA (2009) Lights, rhythms, infection: the role of light and the circadian clock in determining the outcome of plant pathogen interactions. Plant Cell 21:2546–2552PubMedPubMedCentralCrossRefGoogle Scholar
  85. Samach A, Coupland G (2000) Time measurement and the control of flowering in plants. Bioassays 22:38–47CrossRefGoogle Scholar
  86. Schaffer R, Landgraf J, Accerbi M, Simon V, Larson M, Wisman E (2001) Microarray analysis of diurnal and circadian regulated genes in Arabidopsis. Plant Cell 13:113–123PubMedPubMedCentralCrossRefGoogle Scholar
  87. Schilling G, Gransee A, Deubel A, Lezovic G, Ruppel S (1998) Phosphorus availability, root exudates and microbial activity in the rhizosphere. Ucits Pflanzenernahrung Boden 161:465–478CrossRefGoogle Scholar
  88. Seo PJ, Mas P (2015) Stressing the role of the plant circadian clock. Trends Plant Sci 20:230–237PubMedCrossRefGoogle Scholar
  89. Sharma AK, Bhattacharyya PN, Rajkhowa DJ, Jha DK (2014) Impact of global climate change on beneficial plant-microbe association. Annals Biol Res 5:36–37Google Scholar
  90. Sheik CS, Beasley WH, Elshahed MS, Zhou X, Luo Y, Krumholz LR (2011) Effect of warming and drought on grassland microbial communities. Int Soc Microb Ecol J 5:1692–1700Google Scholar
  91. Singh BK, Bardgett RD, Smith P, Reay DS (2010) Microorganisms and climate change: terrestrial feedbacks and mitigation options. Nat Rev Microbiol 8:779–790PubMedCrossRefGoogle Scholar
  92. Song YH, Ito S, Imaizumi T (2010) Similarities in the circadian clock and photoperiodism in plants. Curr Opin Plant Biol 13:594–603PubMedPubMedCentralCrossRefGoogle Scholar
  93. Staiger D, Apel K (1999) Circadian clock-regulated expression of an RNA binding protein in Arabidopsis: characterization of a minimal promoter element. Mol Gen Genet 261:811–819PubMedCrossRefGoogle Scholar
  94. Staiger D, Apel K, Trepp G (1999) The Atger3 promoter confers circadian clock-regulated transcription with peak expression at the beginning of night. Plant Mol Biol 40:873–882PubMedCrossRefGoogle Scholar
  95. Staley C, Ferrieri AP, Tfaily MM, Cui Y, Chu RK, Wang P, Shaw JB, Ansong CK, Brewer H, Norbeck AD, Markillie M, Amaral FD, Tuleski T, Pellizzaro T, Agtuca B, Ferrieri R, Tringe SG, Pasa-Tolic L, Stacey G, Sadowsky MJ (2017) Diurnal cycling of rhizosphere bacterial communities is associated with shifts in carbon metabolism. Microbiome 5:65–78PubMedPubMedCentralCrossRefGoogle Scholar
  96. Stevbak K, Scherber C, Gladbach DJ, Beier C, Mikkelsen TN, Christensen S (2012) Interactions between above and below ground organisms modified in climate change experiments. Nat Clim Chang 2:805–888CrossRefGoogle Scholar
  97. Strayer C, Oyama T, Schultz TF, Raman R, Somers DE, Mas P, Panda S, Kreps JA, Kay SA (2000) Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science 289:768–771PubMedCrossRefGoogle Scholar
  98. Sulpice R, Flis A, Ivakov AA, Apelt F, Krohan N, Encke B et al (2014) Arabidopsis coordinates the diurnal regulation of carbon allocation and growth across a wide range of photoperiods. Mol Plant 7:137–155PubMedCrossRefGoogle Scholar
  99. Taiz L, Zeiger E (1998) Plant physiology. Sinauer Associates, Sunderland, MA, pp 543–590Google Scholar
  100. Thaiss CA, Zeevi D, Levy M, Zilberman-Schapira G, Suez J, Tengeler AC, Abrmson L, Katz MN, Korem T, Zmora N, Kuperman Y, Biton I, Gilad S, Harmelin A, Shapiro H, Halpern Z, Seqal E, Elinay E (2014) Transkingdom control of microbiota diurnal oscillations promotes metabolic homeostasis. Cell 159:517–529CrossRefGoogle Scholar
  101. Vancura V (1964) Root exudates of plants. Analysis of root exudates of barley and wheat in their initial phases of growth. Plant Soil 21:231–234CrossRefGoogle Scholar
  102. Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51PubMedPubMedCentralCrossRefGoogle Scholar
  103. Yanovsky MJ, Kay SA (2001) Signaling networks in the plant circadian system. Curr Opin Plant Biol 4:429–435PubMedCrossRefGoogle Scholar
  104. Yerushalmi S, Yakir E, Green RM (2011) Circadian clocks and adaptation in Arabidopsis. Mol Ecol 20:1155–1165PubMedCrossRefGoogle Scholar
  105. Zarrinpar A, Chaix A, Yooseph S, Panda S (2014) Diet and feeding pattern affect the diurnal dynamics of the gut microbiome. Cell Metab 20:1006–1017PubMedPubMedCentralCrossRefGoogle Scholar
  106. Zhong HH, McClung CR (1996) The circadian clock gates expression of two Arabidopsis catalase genes to distinct and opposite circadian phases. Mol Gen Genet 251:196–203PubMedGoogle Scholar
  107. Zolla G, Badri DV, Bakker MG, Manter DK, Vivanco JM (2013) Soil microbiomes vary in their ability to confer drought tolerance to Arabidopsis. Appl Soil Ecol 68:1–9CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Raghavendra Maddur Puttaswamy
    • 1
  1. 1.Maharani’s Science College for Women (Affiliated to University of Mysore)MysuruIndia

Personalised recommendations