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Stress Signalling in the Phytomicrobiome: Breadth and Potential

  • Sahana Basu
  • Gautam KumarEmail author
Chapter
  • 47 Downloads
Part of the Environmental and Microbial Biotechnology book series (EMB)

Abstract

Higher plants continually compete with microbes to conserve their predominance within the particular niche. Plants have evolved constant relationships with a suite of microbes, known as the phytomicrobiome. The associates of phytomicrobiome exhibit symbiotic relationship. Plant-microbe and microbe-microbe interactions within the phytomicrobiome are carried out through the release of signalling compounds. Bacterial community within the phytomicrobiome communicates among themselves through quorum-sensing mechanism. Diversity, stability and resilience of microbial community in phytomicrobiome are the major determinants of plant health and productivity. Therefore, phytomicrobiome is under intensive investigation to improve our understanding of its strong effects on plant development, health and resistance to parasites. Exploration of the plant-microbe interactions within the phytomicrobiome is a promising avenue to improve crop productivity and agricultural sustainability. Understanding the regulation and relatedness of plant and microbial community may aid in engineering plants with improved pathogen resistance and novel symbiotic interactions. Comprehensive study of phytomicrobiome, especially the molecular signalling pathway, may provide new insights into the mechanism of plant disease management, successively inspiring new plant breeding strategies.

Keywords

Crop Molecular signal Phytomicrobiome Symbiosis Quorum sensing 

References

  1. Alexandre A, Oliveira S (2011) Most heat-tolerant rhizobia show high induction of major chaperone genes upon stress. FEMS Microbiol Ecol 75:28–36CrossRefPubMedPubMedCentralGoogle Scholar
  2. Auge RM (2001) Water relations, drought and vesicular arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42CrossRefGoogle Scholar
  3. Baldwin IT, Halitschke R, Paschold A, von Dahl CC, Presto CA (2006) Volatile signaling in plant-plant interactions: “Talking Trees” in the genomics era. Science 311:812–815CrossRefPubMedPubMedCentralGoogle Scholar
  4. Balestrini R, Lumini E, Borriello R, Bianciotto V (2015) Plant-soil biota interactions. In: Paul EA (ed) Soil microbiology, ecology and biochemistry. Academic Press; Elsevier, London, pp 311–338CrossRefGoogle Scholar
  5. Barra L, Pica N, Gouffi K, Walker GC, Blanco C, Trautwetter A (2003) Glucose 6-phosphate dehydrogenase is required for sucrose and trehalose to be efficient osmoprotectants in Sinorhizobium meliloti. FEMS Microbiol Lett 229:183–188CrossRefPubMedPubMedCentralGoogle Scholar
  6. Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 8:478–486CrossRefGoogle Scholar
  7. Berg G, Zachow C, Müller H, Philipps J, Tilcher R (2013) Next-generation bio-products sowing the seeds of success for sustainable agriculture. Agronomy 3:648–656CrossRefGoogle Scholar
  8. Berg G, Grube M, Schloter M, Smalla K (2014) Unraveling the plant microbe: looking back and future perspectives. Front Microbiol 5:148PubMedPubMedCentralGoogle Scholar
  9. Berreck M, Haselwandter K (2001) Effect of the arbuscular mycorrhizal symbiosis upon uptake of cesium and other cations by plants. Mycorrhiza 10:275–280CrossRefGoogle Scholar
  10. Bloemberg GV, Lugtenberg BJJ (2001) Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr Opin Plant Biol 4:343–350CrossRefGoogle Scholar
  11. Boddey RM, Urquiaga S, Reis V, Dobereiner J (1991) Biological nitrogen fixation associated with sugar cane. Plant Soil 137:111–117CrossRefGoogle Scholar
  12. Bonfante P, Genre A (2008) Plants and arbuscular mycorrhizal fungi: an evolutionary developmental perspective. Trends Plant Sci 9:402–498Google Scholar
  13. Boscari A, Mandon K, Poggi MC, Le Rudulier D (2004) Functional expression of Sinorhizobium meliloti BetS, a high-affinity betaine transporter, in Bradyrhizobium japonicum USDA110. Appl Environ Microbiol 70:5916–5922CrossRefPubMedPubMedCentralGoogle Scholar
  14. Bragina A, Berg C, Müller H, Moser D, Berg G (2013) Insights into functional bacterial diversity and its effects on Alpine bog ecosystem functioning. Sci Rep 3:1955CrossRefPubMedPubMedCentralGoogle Scholar
  15. Brem D, Leuchtmann A (2002) Intraspecific competition of endophyte infected vs uninfected plants of two woodland grass species. Oikos 96:281–290CrossRefGoogle Scholar
  16. Bunn R, Lekberg Y, Zabinski C (2009) Arbuscular mycorrhizal fungi ameliorate temperature stress in thermophilic plants. Ecology 90(5):1378–1388CrossRefPubMedPubMedCentralGoogle Scholar
  17. Calcagno C, Novero M, Genre A, Bonfante P, Lanfranco L (2012) The exudate from an arbuscular mycorrhizal fungus induces nitricoxide accumulation in Medicago truncatula roots. Mycorrhiza 22:259–269CrossRefPubMedPubMedCentralGoogle Scholar
  18. Capoen W, Sun J, Wysham D, Otegui MS, Venkateshwaran M, Hirsch S, Miwa H, Downie JA, Morris RJ, Ane JM, Oldroyd GE (2011) Nuclear membranes control symbiotic calcium signaling of legumes. Proc Natl Acad Sci U S A 108:14348–14353CrossRefPubMedPubMedCentralGoogle Scholar
  19. Chabaud M, Gherbi H, Pirolles E, Vaissayre V, Fournier J, Moukouanga D, Franche C, Bogusz D, Tisa LS, Barker DG, Svistoonoff S (2016) Chitinase-resistant hydrophilic symbiotic factors secreted by Frankia activate both Ca2+ spiking and NIN gene expression in the actinorhizal plant Casuarina glauca. New Phytol 209:86–93CrossRefPubMedPubMedCentralGoogle Scholar
  20. Chamberlain CJ (1935) Gymnosperms, structure and function. University of Chicago Press, ChicagoGoogle Scholar
  21. Charpentier M, Myriam Charpentier A, Bredemeier R, Wanner G, Takeda N, Schleiff E, Parniske M (2008) Lotus japonicus CASTOR and POLLUX are ion channels essential for perinuclear calcium spiking in legume root endosymbiosis. Plant Cell 20:3467–3479CrossRefPubMedPubMedCentralGoogle Scholar
  22. Chein CT, Maundu J, Cavaness J, Daudurand LM, Orser CS (1992) Characterization of salt-tolerant and salt-sensitive mutants of Rhizobium leguminosarum biovar viciae strain C1204b. FEMS Microbiol Lett 90:135–140CrossRefGoogle Scholar
  23. Chen P (2011) Symbiotic effectiveness, competitiveness and salt tolerance of lucerne rhizobia. RMIT University, AustraliaGoogle Scholar
  24. Chernin L, Ismailov Z, Haran S, Chet I (1995) Chitinolytic Enterobacter agglomerans antagonistic to fungal plant pathogens. App Env Microbiol 61:1720–1726CrossRefGoogle Scholar
  25. Choudhary DK, Prakash A, Johri BN (2007) Induced systemic resistance (ISR) in plants: mechanism of action. Indian J Microbiol 47:289–297CrossRefGoogle Scholar
  26. Costa JL, Paulsrud P, Lindblad P (1999) Cyanobiont diversity within coralloid roots of selected cycad species. FEMS Microbiol Ecol 28:85–91CrossRefGoogle Scholar
  27. Daei G, Ardekani M, Rejali F, Teimuri S, Miransari M (2009) Alleviation of salinity stress on wheat yield, yield components, and nutrient uptake using arbuscular mycorrhizal fungi under field conditions. J Plant Physiol. 166:217–225CrossRefGoogle Scholar
  28. Dang JL, Horvath DM, Staskawicz BJ (2013) Pivoting the plant immune system from dissection to deployment. Science 341:746–751CrossRefGoogle Scholar
  29. De Meyer G, Capieau K, Audenaert K, Buchala A, Metraux JP, Hofte M (1999) Nanogram amounts of salicylic acid produced by the rhizobacterium Pseudomonas aeruginosa 7NSK2 activate the systemic acquired resistance pathway in Bean. Mol Plant-Microbe Interact 12:450–458CrossRefPubMedPubMedCentralGoogle Scholar
  30. de Souza JT, de Boer M, de Waard P, van Beek TA, Raaijmakers JM (2003) Biochemical, genetic, and zoosporicidal properties of cyclic lipopeptide surfactants produced by Pseudomonas fluorescens. Appl Environ Microbiol. 69:7161–7172CrossRefPubMedPubMedCentralGoogle Scholar
  31. Duffy BK, Defago G (1997) Zinc improves biocontrol of Fusarium crown and root rot of tomato by Pseudomonas fluorescens and represses the production of pathogen metabolites inhibitory to bacterial antibiotic biosynthesis. Phytopathology 87:1250–1257CrossRefGoogle Scholar
  32. Duffy BK, Defago G (1999) Environmental factors modulating antibiotic and siderophore biosynthesis by Pseudomonas fluorescens biocontrol strains. Appl Environ Microbiol 65:2429–2438CrossRefPubMedPubMedCentralGoogle Scholar
  33. Dunne C, Crowley JJ, Moenne-Loccoz Y, Dowling DN, de Bruijn FJ, O’Gara F (1997) Biological control of Pythium ultimum by Stenotrophomonas maltophilia W81 is mediated by an extracellular proteolytic activity. Microbiology 143:3921–3931CrossRefGoogle Scholar
  34. East R (2013) Soil science comes to life: Plants may be getting a little help with their tolerance of drought and heat. Nature 501:18–19CrossRefGoogle Scholar
  35. El-Tarabily KA, Sykes ML, Kurtboke ID, Hardy GE, St J, Barbosa AM, Dekker RFH (1996) Synergistic effects of a cellulase-producing Micromonospora carbonacea and an antibiotic-producing Streptomyces violascens on the suppression of Phytophthora cinnamomi root rot of Banksia grandis. Can J Bot 74:618–624CrossRefGoogle Scholar
  36. Farrar K, Bryant D, Cope-Selby N (2014) Understanding and engineering beneficial plant-microbe interactions: plant growth promotion in energy crops. Plant Biotechnol J 12:1193–1206CrossRefPubMedPubMedCentralGoogle Scholar
  37. Fasim F, Ahmed N, Parsons R, Gadd GM (2002) Solubilization of zinc salts by a bacterium isolated from the air environment of a tannery. FEMS Microbiol Lett 213:1–6CrossRefGoogle Scholar
  38. Feng G, Zhang FS, Li XL, Tian CY, Tang C, Rengel Z (2002) Improved tolerance of maize plants to salt stress by arbuscular mycorrhiza is related to higher accumulation of soluble sugars in roots. Mycorrhiza 12:185–190CrossRefGoogle Scholar
  39. Ferluga S, Venturi V (2009) OryR is a LuxR-Family protein involved in interkingdom signalling between pathogenic Xanthomonas oryzae pv. oryzae and Rice. J Bacteriol 191:890–897CrossRefGoogle Scholar
  40. Fridlender M, Inbar J, Chet I (1993) Biological control of soilborne plant pathogens by a b-1,3-glucanase-producing Pseudomonas cepacia. Soil Biol Biochem 25:1211–1221CrossRefGoogle Scholar
  41. Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S, Ward E, Kessmann H, Ryals J (1993) Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261:754–756CrossRefPubMedPubMedCentralGoogle Scholar
  42. Gianfreda L, Rao MA (2004) Potential of extra cellular enzymes in remediation of polluted soils: a review. Enzyme Microb Technol 35:339–354CrossRefGoogle Scholar
  43. Giri B, Kapoor R, Mukerji KG (2003) Influence of arbuscular mycorrhizal fungi and salinity on growth, biomass, and mineral nutrition of Acacia auriculiformis. Biol Fertil Soils 38:170–175CrossRefGoogle Scholar
  44. Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 251:1–7CrossRefPubMedPubMedCentralGoogle Scholar
  45. Graham PH, Draeger KJ, Ferrey ML, Conroy MJ, Hammer BE, Martínez E, Aarons SR, Quinto C (1994) Acid pH tolerance in strains of Rhizobium and Bradyrhizobium, and initial studies on the basis for acid tolerance of Rhizobium tropici UMR1899. Can J Microbiol 40:198–207CrossRefGoogle Scholar
  46. Groth M, Takeda N, Perry J, Uchida H, Draxl S, Brachmann A, Sato S, Tabata S, Kawaguchi M, Wang TL, Parniske M (2010) NENA, a Lotus japonicus homolog of Sec13, is required for rhizodermal infection by arbuscular mycorrhiza fungi and rhizobia but dispensable for cortical endosymbiotic development. Plant Cell 22:2509–2526CrossRefPubMedPubMedCentralGoogle Scholar
  47. Grover M, Ali SZ, Sandhya V, Rasul A, Venkateswarlu B (2010) Role of microorganisms in adaptation of agriculture crops to abiotic stresses. World J Microbiol Biotechnol 27:1231–1240CrossRefGoogle Scholar
  48. Harrier LA, Watson CA (2003) The role of arbuscular mycorrhizal fungi in sustainable cropping systems. Adv Agron 79:185–225CrossRefGoogle Scholar
  49. Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59:19–42CrossRefGoogle Scholar
  50. Hartel PG, Alexander M (1984) Temperature and desiccation tolerance of cowpea rhizobia. Can J Microbiol 30:820–823CrossRefGoogle Scholar
  51. Hartl FU, Hayer-Hartl M (2009) Converging concepts of protein folding in vitro and in vivo. Nat Struct Mol Biol 16:574–581CrossRefPubMedPubMedCentralGoogle Scholar
  52. Hartmann A, Schikora A (2012) Quorum sensing of bacteria and trans-kingdom interactions of N-acylhomoserine lactones with eukaryotes. J Chem Ecol 38:70–713CrossRefGoogle Scholar
  53. Hartmann A, Schmid M, Tuinen D, Berg G (2009) Plant-driven selection of microbes. Plant Soil 321:235–257CrossRefGoogle Scholar
  54. Hartmann A, Rothballer M, Hense BA, Schroder P (2014) Bacterial quorum sensing compounds are important modulators of microbe-plant interactions. Front Plant Sci 5:131CrossRefPubMedPubMedCentralGoogle Scholar
  55. Hayman DS, Tavares M (1985) Plant growth responses to vesicular arbuscular mycorrhiza. New Phytol 100:367–377CrossRefGoogle Scholar
  56. Haynes RJ (1990) Active ion uptake and maintenance of cation-anion balance: a critical examination of their role in regulating rhizosphere pH. Plant Soil 126:247–264CrossRefGoogle Scholar
  57. Hildebrandt U, Regvar M, Bothe H (2007) Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry 68:139–146CrossRefPubMedPubMedCentralGoogle Scholar
  58. Huang HL, Zhang SZ, Wu NY, Luo L, Christie P (2009) Influence of Glomus etunicatum/Zea mays mycorrhiza on atrazine degradation, soil phosphatase and dehydrogenase activities, and soil microbial community structure. Soil Biol Biochem 41:726–734CrossRefGoogle Scholar
  59. Hungria M, Franco AA (1993) Effects of high temperature on nodulation and nitrogen fixation by Phaseolus vulgaris L. Plant Soil 149:95–102CrossRefGoogle Scholar
  60. Jack WE, Tagg JR, Ray B (1995) Bacteriocins of Gram-positive bacteria. Microbiol Rev 59:171–200CrossRefPubMedPubMedCentralGoogle Scholar
  61. Jiang JQ, Wei W, Du BH, Li XH, Wang L, Yang SS (2004) Salt tolerance genes involved in cation efflux and osmoregulation of Sinorhizobium fredii RT19 detected by isolation and characterization of Tn5 mutants. FEMS Microbiol Lett 239:139–146CrossRefPubMedPubMedCentralGoogle Scholar
  62. Jin Y, Liu H, Luo D, Yu N, Dong W, Wang C, Zhang X, Dai H, Yang J, Wang E (2016) DELLA proteins are common components of symbiotic rhizobial and mycorrhizal signalling pathways. Nat Commun 7:12433–12446CrossRefPubMedPubMedCentralGoogle Scholar
  63. Joner EJ, Johansen A, Loibner AP, de la Cruz MA, Szolar OH, Portal JM, Leyval C (2001) Rhizosphere effects on microbial community structure and dissipation and toxicity of polycyclic aromatic hydrocarbons (PAHs) in spiked soil. Environ Sci Technol 35(13):2773–2777CrossRefPubMedPubMedCentralGoogle Scholar
  64. Jung WJ, An KN, Jin YL, Park RD, Lim KT, Kim KY, Kim TH (2003) Biological control of damping-off caused by Rhizoctonia solani using chitinase producing Paenibacillus illinoisensis KJA-424. Soil Biol Biochem 35:1261–1264CrossRefGoogle Scholar
  65. Jung WJ, Jin YL, Kim KY, Park RD, Kim TH (2005) Changes in pathogenesis-related proteins in pepper plants with regard to biological control of phytopthora blight with Paenibacillus illinoisensis. Biocontrol 50:165–178CrossRefGoogle Scholar
  66. Jung WJ, Mabood F, Souleimanov A, Smith DL (2011) Induction of defense-related enzymes in soybean leaves by class IId bacteriocins (thuricin 17and bacthuricin F4) purified from Bacillus strains. Microbiol Res 167:14–19CrossRefPubMedPubMedCentralGoogle Scholar
  67. Karadeniz A, Topeuoglu SF, Inan S (2006) Auxins, gibberellin, cytokinin and abscisic acid production in some bacteria. World J Microbiol Biotechnol 22:1061–1064CrossRefGoogle Scholar
  68. Kembel SW, O’Connor TK, Arnold HK, Hubbell SP, Wright SJ, Green JL (2014) Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest. Proc Natl Acad Sci U S A 38:13715–13720CrossRefGoogle Scholar
  69. Kevei Z, Lougnon G, Mergaert P, Horvath GV, Kereszt A, Jayaraman D, Zaman N, Marcel F, Regulski K, Kiss GB, Kondorosi A, Endre G, Kondorosi E, Ane JM (2007) 3-hydroxy-3-methylglutaryl coenzyme A reductase1 interacts with NORK and is crucial for nodulation in Medicago truncatula. Plant Cell 19:3974–3989CrossRefPubMedPubMedCentralGoogle Scholar
  70. Kim KY, Jordan D, McDonald GA (1998) Effect of phosphate solubilizing bacteria and vesicular-arbuscular-mycorrhizae on tomato growth and soil microbial activity. Biol Fertil Soil 26:79–87CrossRefGoogle Scholar
  71. Kim BS, Moon SS, Hwang BK (1999) Isolation, identification and antifungal activity of a macrolide antibiotic, oligomycin A, produced by Streptomyces libani. Can J Bot 77:850–858Google Scholar
  72. Knack JJ, Wilcox LW, Delaux PM, Ane JM, Piotrowski MJ, Cook ME, Graham JM, Graham LE (2015) Microbiomes of streptophyte algae and bryophytes suggest that a functional suite of microbiota fostered plant colonization of land. Int J Plant Sci 176:405–420CrossRefGoogle Scholar
  73. Koide RT, Kabir Z (2000) Extraradical hyphae of the mycorrhizal fungus Glomus intraradices can hydrolyse organic phosphate. New Phytol. 148:511–517CrossRefGoogle Scholar
  74. Krasova-Wade T, Diouf O, Ndoye I, Sall CE, Braconnier S, Neyra M (2006) Water condition effects on rhizobia competition for cowpea nodule occupancy. African J Biotech 5:1457–1463Google Scholar
  75. Kumar S, Mukerji KG, Lai R (1996) Molecular aspects of pesticide degradation by microorganisms. Crit Rev Microbiol 22:1–26CrossRefPubMedPubMedCentralGoogle Scholar
  76. Kumar G, Purty RS, Sharma MP, Singla-Pareek SL, Pareek A (2009) Physiological responses among Brassica species under salinity stress show strong correlation with transcript abundance for SOS pathway-related genes. J Plant Physiol 166:507–520CrossRefPubMedPubMedCentralGoogle Scholar
  77. Lambais MR (2006) Unraveling the signalling and signal transduction mechanisms controlling arbuscular mycorrhiza development. Sci Agric 63(4):405–413CrossRefGoogle Scholar
  78. Lefebvre B, Timmers T, Mbengue M, Moreau S, Herve C, Toth K, Bittencourt-Silvestre J, Klaus D, Deslandes L, Godiard L, Murray JD, Udvardi MK, Raffaele S, Mongrand S, Cullimore J, Gamas P, Niebel A, Ott T (2010) A remorin protein interacts with symbiotic receptors and regulates bacterial infection. Proc Natl Acad Sci U S A 107:2343–2348CrossRefPubMedPubMedCentralGoogle Scholar
  79. Leyval C, Joner EJ, del Val C, Haselwandter K (2002) Potential of arbuscular mycorrhizal fungi for bioremediation. In: Gianinazzi S, Schuepp JM, Barea JM, Haselwandter K (eds) Mycorrhizal technology in agriculture, from genes to bioproducts. Birkhauser Verlag, Basel, Switzerland, pp 175–186CrossRefGoogle Scholar
  80. Lindblad P (2009) Cyanobacteria in symbiosis with Cycads in prokaryotic symbionts in plants. Microbiol Monogr 8:225–233. Pawlowski KCrossRefGoogle Scholar
  81. Liu Y, Lam MC, HHP F (2001) Adsorption of heavy metals by EPS of activated sludge. Water Sci Technol 43:59–66CrossRefPubMedPubMedCentralGoogle Scholar
  82. Liu H, Chen W, Wu M, Wu R, Zhou Y, Gao Y, Ren A (2017) Arbuscular mycorrhizal fungus inoculation reduces the drought-resistance advantage of endophyte-infected versus endophyte-free Leymus chinensis. Mycorrhiza 27(8):791–799CrossRefPubMedPubMedCentralGoogle Scholar
  83. Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, del Rio TG, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL (2012) Defining the core Arabidopsis thaliana root. Nature 488:86–90CrossRefPubMedPubMedCentralGoogle Scholar
  84. Ma Y, Prasad MNV, Rajkumar M, Freitas H (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnology Adv 29(2):248–258Google Scholar
  85. Mabood F, Zhou X, Smith DL (2014) Microbial signaling and plant growth promotion. Can J Plant Sci 94:1051–1063CrossRefGoogle Scholar
  86. Madsen EB, Madsen LH, Radutoiu S, Olbryt M, Rakwalska M, Szczyglowski K, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J (2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425:637–640CrossRefPubMedPubMedCentralGoogle Scholar
  87. Marin M, Ybarra M, Fe A, Garcia-Ferriz L (2002) Effect of arbuscular mycorrhizal fungi and pesticides on Cynara cardunculus growth. Agric Food Sci Finland. 11:245–251CrossRefGoogle Scholar
  88. Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press Ltd, LondonGoogle Scholar
  89. Martinez-Toledo MV, Salmeron V, Rodelas B, Pozo C, Gonzalez-Lopez J (1996) Studies on the effects of the herbicide simazine on microflora of four agricultural soils. Environ Toxicol Chem 15:1115–1118Google Scholar
  90. Mathur SC (1999) Future of Indian pesticides industry in next millennium. Pestic Inf 24:9–23Google Scholar
  91. Michiels J, Verreth C, Vanderleyden J (1994) Effects of temperature stress on bean nodulating Rhizobium strains. Appl Environ Microbiol 60:1206–1212CrossRefPubMedPubMedCentralGoogle Scholar
  92. Milner JL, Raffel SJ, Lethbridge BJ, Handelsman J (1995) Culture conditions that influence accumulation of zwittermicin A by Bacillus cereus UW85. Appl Microbiol Biotechnol 43:685–691CrossRefGoogle Scholar
  93. Milner JL, Silo-Suh L, Lee JC, He H, Clardy J, Handelsman J (1996) Production of kanosamine by Bacillus cereus UW85. Appl Environ Microbiol 62:3061–3065CrossRefPubMedPubMedCentralGoogle Scholar
  94. Miransari M (2009) Contribution of arbuscular mycorrhizal symbiosis to plant growth under different types of soil stress. Plant Biol 12:563–569Google Scholar
  95. Miransari M (2010) Contribution of arbuscular mycorrhizal symbiosis to plant growth under different types of soil stress. Plant Biol 12:563–569PubMedPubMedCentralGoogle Scholar
  96. Munchbach M, Nocker A, Narberhaus F (1999) Multiple small heat shock proteins in Rhizobia. J Bacteriol 181:83–90CrossRefPubMedPubMedCentralGoogle Scholar
  97. Nakayama T, Homma Y, Hashidoko Y, Mizutani J, Tahara S (1999) Possible role of xanthobaccins produced by Stenotrophomonas sp. strain SB-K88 in suppression of sugar beet damping-off disease. Appl Environ Microbiol 65:4334–4339CrossRefPubMedPubMedCentralGoogle Scholar
  98. Nandal K, Sehrawat AR, Yadav AS, Vashishat RK, Boora KS (2005) High temperature-induced changes in exo-polysaccharides, lipopolysaccharides and protein profile of heat-resistant mutants of Rhizobium sp. (Cajanus). Microbiol Res 160:367–373CrossRefGoogle Scholar
  99. Newman EI, Reddell P (1987) The distribution of mycorrhizas among families of vascular plants. New Phytol 106:745–751CrossRefGoogle Scholar
  100. Nielsen TH, Sorensen J (2003) Production of cyclic lipopeptides by Pseudomonas fluorescens strains in bulk soil and in the sugar beet rhizosphere. Appl Environ Microbiol 69:861–868CrossRefPubMedPubMedCentralGoogle Scholar
  101. Noel TC, Sheng C, Yost CK, Pharis RP, Hynes MF (1996) Rhizobium leguminosarum as a plant growth-promoting rhizobacterium: direct growth promotion of canola and lettuce. Can J Microbiol 42:279–283CrossRefGoogle Scholar
  102. Oldroyd GED (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11:252–263CrossRefGoogle Scholar
  103. Ortiz-Castro R, Martinez-Trujillo M, Lopez-Bucio J (2008) N-acyl-L-homoserine lactones: a class of bacterial quorum-sensing signals alter post-embryonic root development in Arabidopsis thaliana. Plant Cell Environ 31:1497–1509CrossRefPubMedPubMedCentralGoogle Scholar
  104. Ownley BH, Weller DM, Thomashow LS (1992) Influence of in situ and in vitro pH on suppression of Gaeumannomyces graminis var. tritici by Pseudomonas fluorescens. 2–79. Phytopathology 82:178–184CrossRefGoogle Scholar
  105. Picard C, Di Cello F, Ventura M, Fani R, Guckert A (2000) Frequency and biodiversity of 2,4-diacetylphloroglucinol-producing bacteria isolated from the maize rhizosphere at different stages of plant growth. Appl Environ Microbiol 66:948–955CrossRefPubMedPubMedCentralGoogle Scholar
  106. Pieterse CMJ, Van Wees SCM, Van Pelt JA, Knoester M, Laan R, Gerrits H, Weisbeek PJ, van Loon LC (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571–1580CrossRefPubMedPubMedCentralGoogle Scholar
  107. Ping L, Boland W (2004) Signals from the underground: bacterial volatiles promote growth in Arabidopsis. Trends Plant Sci 9:263–266CrossRefGoogle Scholar
  108. Pleban S, Chernin L, Chet I (1997) Chitinolytic activity of an endophytic strain of Bacillus cereus. Lett Appl Microbiol 25:284–288CrossRefGoogle Scholar
  109. Poovaiah BW, Du L, Wang H, Yang T (2013) Recent advances in calcium/calmodulin-mediated signaling with an emphasis on plant: microbe interactions. Plant Physiol 163:531–542CrossRefPubMedPubMedCentralGoogle Scholar
  110. Press CM, Wilson M, Tuzun S, Kloepper JW (1997) Salicylic acid produced by Serratia marcescens 90-166 is not the primary determinant of induced systemic resistance in cucumber or tobacco. Mol Plant-Microbe Interact 10:761–768CrossRefGoogle Scholar
  111. Quiza L, St-Arnaud M, Yergeau E (2015) Harnessing phytomicrobiome signalling for rhizosphere microbiome engineering. Front Plant Sci 6:507CrossRefPubMedPubMedCentralGoogle Scholar
  112. Raaijmakers JM, Vlami M, de Souza JT (2002) Antibiotic production by bacterial biocontrol agents. A Van Leeuw J Microb 81:537–547CrossRefGoogle Scholar
  113. Redeker D, Kodner R, Graham L (2000) Glomalean fungi from the Ordovician. Science 289:1920–1921CrossRefGoogle Scholar
  114. Richardson AE, Henderson AP, James GS, Simpson RJ (1988) Consequences of soil acidity and the effect of lime on the nodulation of Trifolium subterraneum L. growing in an acid soil. Soil Biol Biochem 20:439–445CrossRefGoogle Scholar
  115. Riely BK, Mun JH, Ane JM (2006) Unravelling the molecular basis for symbiotic signal transduction in legumes. Mol Plant Pathol 7:197–207CrossRefPubMedPubMedCentralGoogle Scholar
  116. Rillig MC, Maestre FT, Lamit LJ (2003) Microsite differences in fungal hyphal length, glomalin, and soil aggregate stability in semiarid Mediterranean steppes. Soil Biol Biochem 35:1257–1260CrossRefGoogle Scholar
  117. Rillig MC, Aguilar-Trigueros CA, Bergmann J, Verbruggen E, Veresoglou SD, Lehmann A (2015) Plant root and mycorrhizal fungal traits for understanding soil aggregation. New Phytol 205:1385–1388CrossRefPubMedPubMedCentralGoogle Scholar
  118. Rivera-Becerril F, van Tuinen D, Martin-Laurent F, Metwally A, Dietz KJ, Gianinazzi S, Gianinazzi-Pearson V (2005) Molecular changes in Pisum sativum L. roots during arbuscular mycorrhiza buffering of cadmium stress. Mycorrhiza 16:51–60CrossRefPubMedPubMedCentralGoogle Scholar
  119. Rodriguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339CrossRefPubMedPubMedCentralGoogle Scholar
  120. Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza 13:309–317CrossRefPubMedPubMedCentralGoogle Scholar
  121. Ruiz-Lozano JM, Porcel R, Aroca R (2006) Does the enhanced tolerance of arbuscular mycorrhizal plants to water deficit involve modulation of drought-induced plant genes? New Phytol 171:693–698CrossRefPubMedPubMedCentralGoogle Scholar
  122. Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner HY, Hunt MD (1996) Systemic acquired resistance. Plant Cell 8:1809–1819CrossRefPubMedPubMedCentralGoogle Scholar
  123. Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Pare PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci USA 100:4927–4932CrossRefPubMedPubMedCentralGoogle Scholar
  124. Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Pare PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026CrossRefPubMedPubMedCentralGoogle Scholar
  125. Saito K, Yoshikawa M, Yano K, Miwa H, Uchida H, Asamizu E, Sato S, Tabata S, Imaizumi-Anraku H, Umehara Y, Kouchi H, Murooka Y, Szczyglowski K, Downie JA, Parniske M, Hayashi M, Kawaguchi M (2007) NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus. Plant Cell 19:610–624CrossRefPubMedPubMedCentralGoogle Scholar
  126. Schmidt R, Koberl M, Mostafa A, Ramadan EM, Monschein M, Jensen KB, Bauer R, Berg G (2014) Effects of bacterial inoculants on the indigenous microbiome and secondary metabolites of chamomile plants. Front Microbiol 64:111Google Scholar
  127. Seguel A, Cumming JR, Klugh-Stewart K, Cornejo P, Borie F (2013) The role of arbuscular mycorrhizas in decreasing aluminium phytotoxicity in acidic soils: a review. Mycorrhiza 23(3):167–183CrossRefPubMedPubMedCentralGoogle Scholar
  128. Serdyuk OP, Smolygina LD, Muzafarov EN, Adanin VM, Arinbasarov MU (1995) 4-Hydroxyphenethyl alcohol, a new cytokinin-like substance from the phototrophic purple bacterium Rhodospirillum rubrum 1R. FEBS Lett 365:10–12CrossRefPubMedPubMedCentralGoogle Scholar
  129. Shimoda Y, Han L, Yamazaki T, Suzuki R, Hayashi M, Imaizumi-Anraku H (2012) Rhizobial and fungal symbioses show different requirements for calmodulin binding to calcium calmodulin-dependent proteinkinase in Lotus japonicus. Plant Cell 24:304–321CrossRefPubMedPubMedCentralGoogle Scholar
  130. Sieberer BJ, Chabaud M, Fournier J, Timmers AC, Barker DG (2012) A switch in Ca2+ spiking signature is concomitant with endosymbiotic microbe entry into cortical root cells of Medicago truncatula. Plant J 69:822–830CrossRefPubMedPubMedCentralGoogle Scholar
  131. Singh PP, Shin YC, Park CS, Chung YR (1999) Biological control of Fusarium wilt of cucumber by chitinolytic bacteria. Phytopathology 89:92–99CrossRefPubMedPubMedCentralGoogle Scholar
  132. Singh S, Katzer K, Lambert J, Cerri M, Parniske M (2014) CYCLOPS, a DNA-binding transcriptional activator, orchestrates symbiotic root nodule development. Cell Host Microbe 15:139–152CrossRefPubMedPubMedCentralGoogle Scholar
  133. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, CambridgeGoogle Scholar
  134. Smith DL, Zhou X (2014) An effective integrated research approach to study climate change in Canada. Can J Plant Sci 94:995–1008CrossRefGoogle Scholar
  135. Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16–20CrossRefPubMedPubMedCentralGoogle Scholar
  136. Smith DL, Subramanian S, Lamont JR, Bywater-Ekegärd M (2015) Signaling in the phytomicrobiome: breadth and potential. Front. PlantSci 6:709–717Google Scholar
  137. Stan V, Gament E, Cornea CP, Voaides C, Dusa M, Plopeanu G (2011) Effects of heavy metal from polluted soils on the Rhizobium diversity. Not Bot Hort Agrobot Cluj 39:88–95CrossRefGoogle Scholar
  138. Steenhoudt O, Vanderleyden J (2000) Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol Rev 24:487–506CrossRefPubMedPubMedCentralGoogle Scholar
  139. Straight PD, Kolter R (2009) Inter species chemical communication in bacterial development. Annu Rev Microbiol 63:99–118CrossRefPubMedPubMedCentralGoogle Scholar
  140. Streeter JG (2003) Effect of trehalose on survival of Bradyrhizobium japonicum during desiccation. J Appl Microbiol 95:484–491CrossRefPubMedPubMedCentralGoogle Scholar
  141. Subramanian K, Santhanakrishnan P, Balasubramanian P (2006) Responses of field grown tomato plants to arbuscular mycorrhizal fungal colonization under varying intensities of drought stress. Sci Horticult 107:245–253CrossRefGoogle Scholar
  142. Sugawara M, Cytryn EJ, Sadowsky MJ (2010) Functional role of Bradyrhizobium japonicum trehalose biosynthesis and metabolism genes during physiological stress and nodulation. Appl Environ Microbiol 76:1071–1081CrossRefPubMedPubMedCentralGoogle Scholar
  143. Takeda N, Maekawa T, Hayashi M (2012) Nuclear-localized and deregulated calcium- and calmodulin-dependent protein kinase activates rhizobial and mycorrhizal responses in Lotus japonicus. Plant Cell 24:810–822CrossRefPubMedPubMedCentralGoogle Scholar
  144. Tian CY, Feng G, Li XL, Zhang FS (2004) Different effects of arbuscular mycorrhizal fungal isolates from saline or non-saline soil on salinity tolerance of plants. Appl Soil Ecol 26:143–148CrossRefGoogle Scholar
  145. Tirichine L, Imaizumi-Anraku H, Yoshida S, Murakami Y, Madsen LH, Miwa H, Nakagawa T, Sandal N, Albrektsen AS, Kawaguchi M, Downie A, Sato S, Tabata S, Kouchi H, Parniske M, Kawasaki S, Stougaard J (2006) Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development. Nature 441:1153–1156CrossRefPubMedPubMedCentralGoogle Scholar
  146. Turner NC, Wright GC, Siddique KHM (2000) Adaptation of grain legumes (pulses) to water-limited environments. Adv Agron 71:193–231CrossRefGoogle Scholar
  147. Valois D, Fayad K, Barbasubiye T, Garon M, Dery C, Brzezinski R, Beaulieu C (1996) Glucanolytic actinomycetes antagonistic to Phytophthora fragariae var. rubi, the causal agent of raspberry root rot. Appl Environ Microbiol 62:1630–1635CrossRefPubMedPubMedCentralGoogle Scholar
  148. van Aarle IM, Olsson PA, Soderstrom B (2002) Arbuscular mycorrhizal fungi respond to the substrate pH of their extraradical mycelium by altered growth and root colonization. New Phytol 155:173–182CrossRefGoogle Scholar
  149. van Loon LC (1997) Induced resistance in plants and the role of pathogenesis-related proteins. Eur J Plant Pathol 103:753–765CrossRefGoogle Scholar
  150. Vanderlinde EM, Harrison JJ, Muszynski A, Carlson RW, Turner RJ, Yost CK (2010) Identification of a novel ABC transporter required for desicattion tolerance, and biofilm formation in Rhizobium leguminosarum bv. viciae 3841. FEMS Microbiol Ecol 71:327–340CrossRefPubMedPubMedCentralGoogle Scholar
  151. Venkateshwaran M, Cosme A, Han L, Banba M, Satyshur KA, Schleiff E, Parniske M, Imaizumi-Anraku H, An JM (2012) The recent evolution of a symbiotic ion channel in the legume family altered ion conductance and improved functionality in calcium signaling. Plant Cell 24:2528–2545CrossRefPubMedPubMedCentralGoogle Scholar
  152. Venkateshwaran M, Jayaraman D, Chabaud M, Genre A, Balloon AJ, Maeda J, Forshey K, den Os D, Kwiecien NW, Coon JJ, Barker DG, An JM (2015) A role for the mevalonate pathway in early plant symbiotic signaling. Proc Natl Acad Sci U S A 112:9781–9786CrossRefPubMedPubMedCentralGoogle Scholar
  153. Vessey JK (2003) Plant gowth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586CrossRefGoogle Scholar
  154. Vivas A, Azcon R, Biro B, Barea JM, Ruiz-Lozano JM (2003) Influence of bacterial strains isolated from lead-polluted soil and their interactions with arbuscular mycorrhizae on the growth of Trifolium pratense L. under lead toxicity. Can J Microbiol 49:577–588CrossRefGoogle Scholar
  155. Wang FY, Tong RJ, Shi ZY, Xu XF, He XH (2011) Inoculations with arbuscular mycorrhizal fungi increase vegetable yields and decrease phoxim concentrations in carrot and green onion and their soils. PLoS One 6(2):e16949CrossRefPubMedPubMedCentralGoogle Scholar
  156. Watkin ELJ, O’Hara GW, Glenn AR (2003) Physiological responses to acid stress of an acid-soil tolerant and an acid-soil sensitive strain of Rhizobium leguminosarum biovar trifolii. Soil Biol Biochem 35:621–624CrossRefGoogle Scholar
  157. Wei G, Kloepper JW, Tuzun S (1991) Induction of systemic resistance of cucumber to Colletotrichum orbiculare by select strains of plant growth promoting rhizobacteria. Phytopathology 81:1508–1512CrossRefGoogle Scholar
  158. Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487–511CrossRefGoogle Scholar
  159. White JC, Ross DW, Gent MPN, Eitzer BD, Mattina MJI (2006) Effect of mycorrhizal fungi on the phytoextraction of weathered p,p-DDE by Cucurbita pepo. J Hazard Mater 137:1750–1757CrossRefGoogle Scholar
  160. Wu N, Zhang S, Huang H, Shan X, Christie P, Wang Y (2008) DDT uptake by arbuscular mycorrhizal alfalfa and depletion in soil as influenced by soil application of a non-ionic surfactant. Environ Pollut 151(3):569–575CrossRefGoogle Scholar
  161. Wulf A, Manthey K, Doll J, Perlick A, Franken P, Linke B, Meyer F, Kuster H, Krajinski F (2003) Transcriptional changes in response to arbuscular mycorrhiza development in the model plant Medicago truncatula. Mol Plant Microbe 16:306–314CrossRefGoogle Scholar
  162. Xu J, Xiao-Lin L, Luo L (2012) Effects of engineered Sinorhizobium meliloti on cytokinin synthesis and tolerance of alfalfa to extreme drought stress. Appl Environ Microbiol 78:8056CrossRefPubMedPubMedCentralGoogle Scholar
  163. Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14(1):1–4CrossRefPubMedPubMedCentralGoogle Scholar
  164. Yano K, Yoshida S, Muller J, Singh S, Banba M, Vickers K, Markmann K, White C, Schuller B, Sato S, Asamizu E, Tabatae S, Murooka Y, Perry J, Wang TL, Kawaguchi M, Imaizumi-Anraku H, Hayashi M, Parniske M (2008) CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc Natl Acad Sci U S A 105:20540–20545CrossRefPubMedPubMedCentralGoogle Scholar
  165. Yelton MM, Yang SS, Edie SA, Lim ST (1983) Characterization of an effective salt-tolerant fast-growing strain of Rhizobium japonicum. J Gen Microbiol 129:1537–1547Google Scholar
  166. Zamioudis C, Mastranesti P, Dhonukshe P, Blilou I, Pieterse CMJ (2013) Unraveling root developmental programs initiated by beneficial Pseudomonas spp. Bacteria. Plant Physiol 162:304–318CrossRefPubMedPubMedCentralGoogle Scholar
  167. Zhan HJ, Lee CC, Leigh JA (1991) Induction of the second exopolysaccharide (EPS) in Rhizobium meliloti SU47 by low phosphate concentrations. J Bacteriol 173:7391–7394CrossRefPubMedPubMedCentralGoogle Scholar
  168. Zhang XP, Karsisto M, Harper R, LindstroEm K (1991) Diversity of Rhizobium bacteria isolated from the root nodules of leguminous trees. Int J Syst Evol Bacteriol 41:104–113CrossRefGoogle Scholar
  169. Zhang RQ, Zhu HH, Zhao HQ, Yao Q (2013) Arbuscular mycorrhizal fungal inoculation increases phenolic synthesis in clover roots via hydrogen peroxide, salicylic acid and nitric oxide signaling pathways. J Plant Physiol 170:74–79CrossRefPubMedPubMedCentralGoogle Scholar
  170. Zhu J, Winans SC (2001) The quorum-sensing transcriptional regulator TraR requires its cognate signaling ligand for protein folding, protease resistance, and dimerization. Proc Natl Acad Sci U S A 98:1507–1512CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer Nature Singapore Pte Ltd. 2020

Authors and Affiliations

  1. 1.Department of BiotechnologyAssam UniversitySilcharIndia
  2. 2.Department of Life ScienceCentral University of South BiharGayaIndia

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