Advertisement

Applied Microbiology and Biotechnology

, Volume 103, Issue 2, pp 643–657 | Cite as

Bioprospecting cold-adapted plant growth promoting microorganisms from mountain environments

  • Anita PandeyEmail author
  • Luis Andrés Yarzábal
Mini-Review

Abstract

Mountain soils are challenging environments for all kinds of living things, including plants and microorganisms. Many cold-adapted microorganisms colonizing these extreme soils play important roles as promoters of plant growth and development; for that reason, they are called collectively plant growth-promoting microorganisms (PGPM). Even though there is seldom doubt concerning the usefulness of PGPM to develop eco-friendly bioinoculants, including biofertilizers and biocontrollers, a series of aspects need to be addressed in order to make this technology field-applicable. Among these aspects, the ecological and rhizosphere competences of PGPM are of paramount importance, particularly when considering the development of bioinoculants, well suited for the intensification of mountainous agricultural production. Studies on native, cold-adapted PGPM conducted in the Indian Himalayan region (IHR) and the Tropical Andes (TA) lead nowadays the research in this field. Noticeably, some common themes are emerging. For instance, soils in these mountain environments are colonized by many cold-adapted PGPM able to mobilize soil nutrients and to inhibit growth of plant pathogens. Studies aimed at deeply characterizing the abilities of such PGPM is likely to substantially contribute towards a better crop productivity in mountainous environments. The present review focuses on the importance of this microbial resource to improve crop productivity in IHR and TA. We also present a number of successful examples, which emphasize the effectiveness of some bioinoculants—developed from naturally occurring PGPM—when applied in the field.

Keywords

Plant growth-promoting microorganisms Mountain environments Indian Himalayan region Tropical Andes Cold-adapted microorganisms 

Notes

Acknowledgments

This review emerged on the basis of the case studies conducted by the authors in various mountain locations at GB Pant National Institute of Himalayan Environment & Sustainable Development (India), and at Universidad de Los Andes (Venezuela) and Universidad de Cuenca (Ecuador). Present and former directors of GBPNIHESD (India) and Universidad de Los Andes (Venezuela), are gratefully acknowledged for their support. Dr. DS Rawat is thanked for verifying the IHR map. LAY acknowledges Proyecto Prometeo of the National Secretary of Science, Technology, and Innovation of Ecuador (SENESCYT).

Funding

AP acknowledges the Ministry of Environment, Forest & Climate Change, Department of Biotechnology, and Council of Scientific & Industrial Research, Govt. of India and Uttarakhand State Council for Science and Technology, Govt. of Uttarakhand for financial support.

Compliance with ethical standards

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare that they have no competing interests.

References

  1. Adesemoye A, Kloepper J (2009) Plant–microbes interactions in enhanced fertilizer-use efficiency. Appl Microbiol Biotechnol 85:1–12Google Scholar
  2. Adhikari P, Pandey A (2018) Phosphate solubilization potential of endophytic fungi isolated from Taxus wallichiana Zucc. roots. Rhizosphere (in press)Google Scholar
  3. Adl S (2016) Rhizosphere, food security, and climate change: a critical role for plant-soil research. Rhizosphere 1:1–3Google Scholar
  4. Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ Sci 26:1–20Google Scholar
  5. Alori ET, Dare MO, Babalola OO (2017) Microbial inoculants for soil quality and plant health. In: Lichtfouse E (ed) Sustainable Agriculture Reviews, vol 22. Springer, Cham, pp 281–307Google Scholar
  6. Aly AH, Debbab A, Proksch P (2011) Fungal endophytes: unique plant inhabitants with great promises. Appl Microbiol Biotechnol 90:1829–1845Google Scholar
  7. Andrade-Linares DR, Grosch R, Restrepo S, Krumbein A, Franken P (2011) Effects of dark septate endophytes on tomato plant performance. Mycorrhiza 21:413–422Google Scholar
  8. Arcos J, Zúñiga D (2015) Efecto de rizobacterias en el control de Rhizoctonia solani en el cultivo de papa. Ecol Apl 14:95–101Google Scholar
  9. Arcos J, Zúñiga D (2016) Rizobacterias promotoras de crecimiento de plantas con capacidad para mejorar la productividad en papa. Rev Latinoam Papa 20:18–31Google Scholar
  10. Artursson V, Finlay RD, Jansson JK (2006) Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ Microbiol 8:1–10Google Scholar
  11. Bafana A (2013) Diversity and metabolic potential of culturable root-associated bacteria from Origanum vulgare in sub-Himalayan region. World J Microbiol Biotechnol 29:63–74Google Scholar
  12. Bakker PAHM, Berendsen RL, Doornbos RF, Wintermans PCA, Pieterse CMJ (2013) The rhizosphere revisited: root microbiomics. Front Plant Sci 4:165.  https://doi.org/10.3389/fpls.2013.00165 Google Scholar
  13. Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486Google Scholar
  14. 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 68:1–13Google Scholar
  15. Berg G, Rybakova D, Grube M, Köberl M (2016) The plant microbiome explored: implications for experimental botany. J Exp Bot 67:995–1002Google Scholar
  16. Berríos G, Cabrera G, Gidekel M, Gutiérrez-Moraga A (2013) Characterization of a novel Antarctic plant growth-promoting bacterial strain and its interaction with Antarctic hair grass (Deschampsia antarctica Desv). Polar Biol 36:349–362Google Scholar
  17. Berruti A, Lumini E, Balestrini R, Bianciotto V (2016) Arbuscular mycorrhizal fungi as natural biofertilizers: let’s benefit from past successes. Front Microbiol 6:1559.  https://doi.org/10.3389/fmicb.2015.01559 Google Scholar
  18. Bhardwaj DP, Lundquist P, Alstrom S (2008) Arbuscular mycorrhizal fungal spore-associated bacteria affect mycorrhizal colonization, plant growth and potato pathogens. Soil Biol Biochem 40:2494–2501Google Scholar
  19. Borsdorf A, Stadel C (2015) The cultural development of the Andes. In: Borsdorf A, Stadel C (eds) The Andes: a geographical portrait. Springer International Publishing, Basel, pp 99–132Google Scholar
  20. Bradley JA, Singarayer JS, Anesio AM (2014) Microbial community dynamics in the forefield of glaciers. Proc R Soc B 281:20140882Google Scholar
  21. Bryant JA, Lamanna C, Morlon H, Kerkhoff AJ, Enquist BJ, Green JL (2008) Microbes on mountainsides: contrasting elevational patterns of bacterial and plant diversity. PNAS 105:1505–11511Google Scholar
  22. Busby PE, Soman C, Wagner MR, Friesen ML, Kremer J, Bennett A, Morsy M, Eisen JA, Leach JE, Dangl JL (2017) Research priorities for harnessing plant microbiomes in sustainable agriculture. PLoS Biol 15(3):e2001793.  https://doi.org/10.1371/journal.pbio.2001793 Google Scholar
  23. Calvo Vélez P, Meneses LR, Zúñiga Dávila D (2008) Estudio de las poblaciones microbianas de la rizósfera del cultivo de papa (Solanum tuberosum) en zonas altoandinas. Ecol Appl 7:141–148Google Scholar
  24. Calvo P, Zúñiga D (2010) Caracterización fisiológica de cepas de Bacillus spp. aisladas de la rizósfera de papa (Solanum tuberosum). Ecol Appl 9:31–39Google Scholar
  25. Calvo P, Ormeño-Orrillo E, Martínez-Romero E, Zúniga D (2010) Characterization of Bacillus isolates of potato rhizosphere from Andean soils of Peru and their potential PGPR characteristics. Braz J Microbiol 41:899–906Google Scholar
  26. Castellano-Hinojosa A, Pérez-Tapia V, Bedmar E, Santillana N (2018) Purple corn-associated rhizobacteria with potential for plant growth promotion. J Appl Microbiol 124:1254–1264Google Scholar
  27. Celis-Zambrano C, Moreno Durán G, Sequeda-Castañeda LG, García Caicedo A, Albarracín DM, Charry B, Claudia L (2014) Determining the effectiveness of Candida guilliermondii in the biological control of Rhizopus stolonifer in postharvest tomatoes. Univ Sci 19:51–62Google Scholar
  28. Chakraborty U, Chakraborty BN, Basnet M, Chakraborty AP (2009) Evaluation of Ochrobactrum anthropi TRS-2 and its talc based formulation for enhancement of growth of tea plants and management of brown root rot disease. J Appl Microbiol 107:625–634Google Scholar
  29. Chaurasia B, Pandey A, Palni LMS, Trivedi P, Kumar B, Colvin N (2005) Diffusible and volatile compounds produced by an antagonistic Bacillus subtilis strain cause structural deformations in pathogenic fungi in vitro. Microbiol Res 160:75–81Google Scholar
  30. Chettri N, Sharma E (2016) Reconciling the mountain biodiversity conservation and human wellbeing: drivers of biodiversity loss and new approaches in the Hindu-Kush Himalayas. Proc Indian Natl Sci Acad 82:1–21Google Scholar
  31. Ciccazzo S, Esposito A, Borruso L, Brusetti L (2016) Microbial communities and primary succession in high altitude mountain environments. Ann Microbiol 66:43–60Google Scholar
  32. Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678Google Scholar
  33. Contreras-Liza SE, Sánchez LL, Zúñiga Dávila DE (2017) Agronomical performance of potato (Solanum tuberosum L.) cv. ‘Unica’ under inoculation with native rhizobacteria and application of acetyl salicylic acid. Rev Ciên Agrovet, Lages 16:456–462Google Scholar
  34. Correa-Galeote D, Bedmar EJ, Fernández-González AJ, Fernández-López M, Arone GJ (2016) Bacterial communities in the rhizosphere of amilaceous maize (Zea mays L.) as assessed by pyrosequencing. Front Plant Sci 7:1016.  https://doi.org/10.3389/fpls.2016.01016 Google Scholar
  35. D’Amico S, Collins T, Marx J-C, Feller G, Gerday C (2006) Psychrophilic microorganisms: challenges for life. EMBO Rep 7:385–389Google Scholar
  36. Davies TFJ, Calderón MC, Huaman Z (2005a) Influence of arbuscular mycorrhizae indigenous to Peru and a flavonoid on growth, yield, and leaf elemental concentration of “Yungay” potatoes. Hortic Sci 40:381–385Google Scholar
  37. Davies TFJ, Calderón CM, Huaman Z, Gómez R (2005b) Influence of a flavonoid (Formononetin) on mycorrhizal activity and potato crop productivity in the highlands of Peru. Sci Hortic 106:318–329Google Scholar
  38. Devi LS, Polashree Khaund P, Fenella MW, Nongkhlaw FMW, Joshi SR (2012) Diversity of culturable soil micro-fungi along altitudinal gradients of eastern Himalayas. Mycobiology 40:151–158Google Scholar
  39. Dillehay TD, Rossen J, Andres TC, Williams DE (2007) Preceramic adoption of peanut, squash, and cotton in northern Peru. Science 316:1890–1893Google Scholar
  40. Dion P (2008) The microbiological promises of extreme soils. In: Dion P, Nautiyal CS (eds) Microbiology of extreme soils. Soil biology, vol 13. Springer-Verlag, Berlin, Heidelberg, pp 3–13Google Scholar
  41. Duc L, Noll M, Meier BE, Bürgmann H, Zeyer J (2009) High diversity of diazotrophs in the forefield of a receding alpine glacier. Microb Ecol 57:179–190Google Scholar
  42. Forster J (1887) Über eihnigh Eigenschafter leuchtender Bakterien. Centr Bakteriol Rev Parasitenk 2:337–340Google Scholar
  43. Francis I, Holsters M, Vereecke D (2010) The gram-positive side of plant–microbe interactions. Environ Microbiol 12:1–12Google Scholar
  44. Franco J, Main G, Navia O, Ortuño N, Herbas J (2011) Improving productivity of traditional Andean small farmers by bio-rational soil management: I. the potato case. Rev Lat Papa 16:270–290Google Scholar
  45. Franco J, Main G, Urquieta E (2015) Valorización de la diversidad microbiológica andina a través de la intensificación sostenible de sistemas agrícolas basados en el cultivo de papa (VALORAM), pp 52–57. In: Fundación PROINPA. Informe Compendio 2011–2014. Cochabamba – Bolivia. Available at: http://www.proinpa.org/publico/Informe_compendio_2011_2014/valorizacion%20de%20la%20diversidad%20microbiologica.pdf
  46. Frey-Klett P, Garbaye J, Tarkka M (2007) The mycorrhiza helper bacteria revisited. New Phytol 176:22–36Google Scholar
  47. Georlette D, Blaise V, Collins T, D’Amico S, Gratia E, Hoyoux A, Marx JC, Sonan G, Feller G, Gerday C (2004) Some like it cold: biocatalysis at low temperatures. FEMS Microbiol Rev 28:25–42Google Scholar
  48. Ghildiyal A, Pandey A (2008) Isolation of cold tolerant antifungal strains of Trichoderma spp. from glacial sites of Indian Himalayan region. Res J Microbiol 3:559–564Google Scholar
  49. Ghyselinck J, Velivelli SLS, Heylen K, O’Herlihy E, Franco J, Rojas M, De Vos P, Doyle Prestwich B (2013) Bioprospecting in potato fields in the central Andean highlands: screening of rhizobacteria for plant growth-promoting properties. Syst Appl Microbiol 36:116–127Google Scholar
  50. Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39Google Scholar
  51. Gulati A, Vyas P, Rahi P, Kasana RC (2009) Plant growth-promoting and rhizosphere-competent Acinetobacter rhizosphaerae strain BIHB 723 from the cold deserts of the Himalayas. Curr Microbiol 58:371–377Google Scholar
  52. Gulati A, Sharma N, Vyas P, Sood S, Rahi P, Pathania V, Prasad R (2010) Organic acid production and plant growth promotion as a function of phosphate solubilization by Acinetobacter rhizosphaerae strain BIHB 723 isolated from the cold deserts of the trans-Himalayas. Arch Microbiol 192:975–983Google Scholar
  53. Gulati A, Sood S, Rahi P, Thakur R, Chauhan S, Chadha IC (2011) Diversity analysis of diazotrophic bacteria associated with the roots of tea (Camellia sinensis (L.) OKuntze). J Microbiol Biotechnol 21:545–555Google Scholar
  54. Hamilton LS (2002) Why mountain matters? World conservation: the IUCN bulletin1/2002Google Scholar
  55. Harman GE, Herrera-Estrella AH, Horwitz BA, Lorito M (2012) Trichoderma—from basic biology to biotechnology. Microbiology 158:1–2Google Scholar
  56. Hiltner L (1904) Uber neuere Erfahrungen and Probleme auf dem Gebiet der Bodenbakteriologie und unter besonderer Berucksichtigung der Grundungung und Brache. Arb Dtsch Landwirtsch Ges 98:59–78Google Scholar
  57. Hussein KA, Joo JH (2017) Stimulation, purification, and chemical characterization of siderophores produced by the rhizospheric bacterial strain Pseudomonas putida. Rhizosphere 4:16–21Google Scholar
  58. Jain R, Pandey A (2016) A phenazine-1-carboxylic acid producing polyextremophilic Pseudomonas chlororaphis (MCC2693) strain, isolated from mountain ecosystem, possesses biocontrol and plant growth promotion abilities. Microbiol Res 190:63–71Google Scholar
  59. Kaira GS, Dhakar K, Pandey A (2015) A psychrotolerant strain of Serratia marcescens (MTCC 4822) produces laccase at wide temperature and pH range. AMB Express 5(1):92.  https://doi.org/10.1186/s13568-014-0092-1 Google Scholar
  60. Keller NP, Turner G, Bennett JW (2005) Fungal secondary metabolism—from biochemistry to genomics. Nat Rev Microbiol 3:937–947Google Scholar
  61. Kobayashi DY, Palumbo JD (2000) Bacterial endophytes and their effects on plants and uses in agriculture. In: Bacon CW, White JF (eds) Microbial endophytes. Marcel Dekker Inc, New York, pp 199–233Google Scholar
  62. Korner C (2004) Mountain biodiversity, its causes and function. Ambio Suppl 13:11–17Google Scholar
  63. Kshetri L, Nevita T, Pandey P (2015) Plant growth promoting rhizobacteria (PGPR) and their application for sustainable agriculture in north eastern region of India. ENVIS Bull Himal Ecol 23:41–47Google Scholar
  64. Kumar A, Verma JP (2018) Does plant—microbe interaction confer stress tolerance in plants: a review? Microbiol Res 207:41–52Google Scholar
  65. Kumar B, Trivedi P, Pandey A (2007) Pseudomonas corrugata: a suitable bacterial inoculant for maize grown under rainfed conditions of Himalayan region. Soil Biol Biochem 39:3093–3100Google Scholar
  66. Kumar A, Singh S, Pandey A (2009) General microflora, arbuscular mycorrhizal colonization and occurrence of endophytes in rhizosphere of two age groups of Ginkgo biloba L. of Indian central Himalaya. Ind J Microbiol 49:134–141Google Scholar
  67. Kusari S, Hertweck C, Spiteller M (2012) Chemical ecology of endophytic fungi: origins of secondary metabolites. Chem Biol 19:792–798Google Scholar
  68. Lugtenberg BJJ, Kamilova F (2009) Plant growth promoting rhizobacteria. Annu Rev Microbiol 63:363–383Google Scholar
  69. Lyngwi NA, Joshi SR (2014) Economically important Bacillus and related genera: a mini review. In: Sen A (ed) Biology of useful plants and microbes. Narosa Publishing House, New Delhi, pp 33–43Google Scholar
  70. Lyngwi NA, Koijam K, Sharma D, Joshi SR (2013) Cultivable bacterial diversity along the altitudinal zonation and vegetation range of tropical eastern Himalaya. Int J Trop Biol 61:467–490Google Scholar
  71. Malviya MK, Sharma A, Pandey A, Rinu K, Sati P, Palni LMS (2012) Bacillus subtilis NRRL B-30408: a potential inoculant for crops grown under rainfed conditions in the mountains. J Soil Sci Plant Nutr 12:811–824Google Scholar
  72. Massaccesi L, Benucci GMN, Gigliotti G, Cocco S, Corti G, Agnelli A (2015) Rhizosphere effect of three plant species of environment under periglacial conditions (Majella massif, Central Italy). Soil Biol Biochem 89:184–195Google Scholar
  73. Mauchline TH, Malone JG (2017) Life in earth—the root microbiome to the rescue? Curr Opin Microbiol 37:23–28Google Scholar
  74. Meyer AF, Lipson DA, Martin AP, Schadt CD, Schmidt SK (2004) Molecular and metabolic characterization of cold-tolerant alpine soil Pseudomonas sensu stricto. Appl Environ Microbiol 70:483–489Google Scholar
  75. Mishra J, Arora NK (2017) Secondary metabolites of fluorescent pseudomonads in biocontrol of phytopathogens for sustainable agriculture. Appl Soil Ecol 125:35–45Google Scholar
  76. Mishra PK, Mishra S, Selvakumar G, Bisht SC, Bisht JK, Kundu S, Gupta HS (2008) Characterisation of a psychrotolerant plant growth promoting Pseudomonas sp. strain PGERs17 (MTCC 9000) isolated from North Western Indian Himalayas. Ann Microbiol 58:561–568Google Scholar
  77. Mishra PK, Bisht SC, Ruwari P, Selvakumar G, Joshi GK, Bisht JK, Bhatt JC, Gupta HS (2011) Alleviation of cold stress in inoculated wheat (Triticum aestivum L.) seedlings with psychrotolerant pseudomonads from NW Himalayas. Arch Microbiol 193:497–513Google Scholar
  78. Moreno R, Rojo F (2014) Features of pseudomonads growing at low temperatures: another facet of their versatility. Environ Microbiol Rep 6:417–426Google Scholar
  79. Nadeem SM, Ahmad M, Zahir ZA, Javaid A, Ashraf M (2014) The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnol Adv 32:429–448Google Scholar
  80. Negi YK, Prabha D, Garg SK, Kumar J (2011) Genetic diversity among cold-tolerant fluorescent Pseudomonas isolates from Indian Himalayas and their characterization for biocontrol and plant growth-promoting activities. J Plant Growth Regul 30:128–143Google Scholar
  81. Ogata-Gutiérrez K, Alvarado D, Chumpitaz-Segovia C, Zúñiga-Dávila D (2016) Characterization of plant growth promoting rhizobacteria isolated from the rhizosphere of Peruvian highlands native crops. Int J Plant Soil Sci 11:1–8Google Scholar
  82. Ogata-Gutiérrez K, Chumpitaz-Segovia C, Lirio-Paredes J, Finetti-Sialer MM, Zúñiga-Dávila D (2017) Characterization and potential of plant growth promoting rhizobacteria isolated from native Andean crops. World J Microbiol Biotechnol 33:203–215Google Scholar
  83. Ortiz-Ojeda P, Ogata-Gutiérrez K, Zúñiga-Dávila D (2017) Evaluation of plant growth promoting activity and heavy metal tolerance of psychrotrophic bacteria associated with maca (Lepidium meyenii Walp.) rhizosphere. AIMS Microbiol 3:279–292Google Scholar
  84. Ortuño N, Castillo JA, Claros M, Navia O, Angulo M, Barja D, Gutiérrez C, Angulo V (2013) Enhancing the sustainability of quinoa production and soil resilience by using bioproducts made with native microorganisms. Agronomy 3:732–746Google Scholar
  85. Ortuño N, Claros M, Gutiérrez C, Angulo M, Castillo J (2014) Bacteria associated with the cultivation of quinoa in the Bolivian Altiplano and their biotechnological potential. Rev Agric 53:53–61Google Scholar
  86. Ortuño N, Castillo J, Miranda C, Claros M, Soto X (2017) The use of secondary metabolites extracted from Trichoderma for plant growth promotion in the Andean highlands. Renew Agric Food Syst 32:366–375Google Scholar
  87. Oswald A, Calvo Vélez P, Zúñiga Dávila D, Arcos Pineda J (2010) Evaluating soil rhizobacteria for their ability to enhance plant growth and tuber yield in potato. Ann Appl Biol 157:259–271Google Scholar
  88. Pandey A, Kumar S (1989) Potential of azotobacters and azospirilla as biofertilizers for upland agriculture: a review. J Sci Indus Res 48:134–144Google Scholar
  89. Pandey A, Palni LMS (1998a) Microbes in Himalayan soils: biodiversity and potential applications. J Sci Indus Res 57:668–673Google Scholar
  90. Pandey A, Palni LMS (1998b) Isolation of Pseudomonas corrugata from Sikkim Himalaya. World J Microbiol Biotechnol 14:411–413Google Scholar
  91. Pandey A, Palni LMS (2007) The rhizosphere effect in trees of the Indian central Himalaya with special reference to altitude. Appl Ecol Environ Res 5:93–102Google Scholar
  92. Pandey A, Sharma E, Palni LMS (1998) Influence of bacterial inoculation on maize in upland farming systems of the Sikkim Himalaya. Soil Biol Biochem 30:379–384Google Scholar
  93. Pandey A, Durgapal A, Joshi M, Palni LMS (1999) Influence of Pseudomonas corrugata inoculation on root colonization and growth promotion of two important hill crops. Microbiol Res 154:259–266Google Scholar
  94. Pandey A, Trivedi P, Kumar B, Palni LMS (2006) Characterization of a phosphate solubilizing and antagonistic strain of Pseudomonas putida (B0) isolated from a sub-alpine location in the Indian central Himalaya. Curr Microbiol 53:102–107Google Scholar
  95. Pandey A, Das N, Kumar B, Rinu K, Trivedi P (2008) Phosphate solubilization by Penicillium spp. isolated from soil samples of Indian Himalayan region. World J Microbiol Biotechnol 24:97–102Google Scholar
  96. Pandey A, Singh S, Kumar A, Malviya MK, Rinu K (2009) Isolation of an endophytic plant growth promoting bacterium Pseudomonas sp. strain gb3 (MTCC 9476) from Ginkgo biloba L., growing in temperate Himalaya. Nat Acad Sci Lett 32:83–88Google Scholar
  97. Pandey A, Singh S, Palni LMS (2013) Microbial inoculants to support tea industry in India. Ind J Biotechnol 12:13–19Google Scholar
  98. Pandey A, Sati P, Malviya MK, Singh S, Kumar A (2014) Use of endophytic bacterium (Pseudomonas sp., MTCC9476) in propagation and conservation of Ginkgo biloba L.: a living fossil. Curr Sci 106:1066–1067Google Scholar
  99. Pandey A, Dhakar K, Jain R, Pandey N, Gupta VK, Kooliyottil R, Dhyani A, Malviya MK, Adhikari P (2018) Cold adapted fungi from Indian Himalaya: untapped source for bioprospecting. Proc Natl Acad Sci India Sect B Biol Sci 1–8.  https://doi.org/10.1007/s40011-018-1002-0
  100. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6(10):763–775Google Scholar
  101. Pérez B, Gabriel J, Angulo A, Gonzáles R, Magne J, Ortuño N, Cadima X (2015) Efecto de los bioinsumos sobre la capacidad de respuesta de cultivares nativos de papa (Solanum tuberosum L.) a sequía. Rev Lat Papa 19:40–58Google Scholar
  102. Pestalozzi H (2000) Sectoral fallow systems and the management of soil fertility: the rationality of indigenous knowledge in the high Andes of Bolivia. Mt Res Dev 20:64–71Google Scholar
  103. Pfeiffer S, Mitter B, Oswald A, Schloter-Hai B, Schloter M, Declerck S, Sessitsch A (2017) Rhizosphere microbiomes of potato cultivated in the high Andes show stable and dynamic core microbiomes with different responses to plant development. FEMS Microbiol Ecol 93(2).  https://doi.org/10.1093/femsec/fiw242
  104. Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799Google Scholar
  105. Pieterse CM, Zamioudis C, Berendsen RL, Weller DM, Van Wees SC, Bakker PA (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375Google Scholar
  106. Piperno DR (2011) The origins of plant cultivation and domestication in the new world tropics: patterns, processes, and new developments. Curr Anthropo l52:S453–S470Google Scholar
  107. Porras-Alfaro A, Bayman P (2011) Hidden fungi, emergent properties: endophytes and microbiomes. Annu Rev Phytopathol 49:291–315Google Scholar
  108. Qadri M, Johri S, Shah BA, Khajuria A, Sidiq T, Lattoo SK, Abdin MZ, Riyaz-Ul-Hassan S (2013) Identification and bioactive potential of endophytic fungi isolated from selected plants of the Western Himalayas. Springer Plus 2–8. http://www.springerplus.com/content/2/1/8
  109. Raaijmakers JM, Vlami M, de Souza JT (2002) Antibiotic production by bacterial biocontrol agents. Antonie Van Leeuwenhoek 81:537–547Google Scholar
  110. Rahi P, Vyas P (2015) Microorganisms associated with tea rhizosphere in the Indian Himalayan region. ENVIS Bull Himal Ecol 23:48–54Google Scholar
  111. Rai M, Rathod D, Agarkar G, Dar M, Brestic M, Pastore GM, Junior MRM (2014) Fungal growth promotor endophytes: a pragmatic approach towards sustainable food and agriculture. Symbiosis 62:63–79Google Scholar
  112. Rajkumar M, Benedict Bruno L, Rajesh Banu J (2017) Alleviation of environmental stress in plants: the role of beneficial Pseudomonas spp. Crit Rev Environ Sci Technol 47:372–407Google Scholar
  113. Reinhold-Hurek B, Hurek T (2011) Living in side plants: bacterial endophytes. Curr Opin Plant Biol 14:435–443Google Scholar
  114. Rinu K, Pandey A (2009) Bacillus subtilis NRRL B-30408 inoculation enhances the symbiotic efficiency of Lens esculenta Moench at a Himalayan location. J Plant Nutr Soil Sci 172:134–139Google Scholar
  115. Rinu K, Pandey A (2010) Temperature dependent phosphate solubilization by cold and pH tolerant species of Aspergillus isolated from Himalayan soil. Mycoscience 51:263–271Google Scholar
  116. Rinu K, Pandey A (2011) Slow and steady phosphate solubilization by a psychrotolerant strain of Paecilomyces hepiali (MTCC 9621). World J Microbiol Biotechnol 27:1055–1062Google Scholar
  117. Rinu K, Pandey A, Palni LMS (2012) Utilization of psychrotolerant phosphate solubilizing fungi under low temperature conditions of the mountain ecosystem. In: Satyanarayana T, Johri BN, Prakash A (eds) Microorganisms in sustainable agriculture and biotechnology. SpringerScience + Buisiness Media, Dordrecht, pp 77–90Google Scholar
  118. Rinu K, Malviya MK, Sati P, Tiwari SC, Pandey A (2013) Response of cold tolerant Aspergillus spp to solubilization of Fe and Al phosphate in presence of different nutritional sources. ISRN Soil Sci Article ID 59854, 10 pages.  https://doi.org/10.1155/2013/598541
  119. Rinu K, Sati P, Pandey A (2014) Trichoderma gamsii (NFCCI 2177): a newly isolated endophytic, psychrotolerant, plant growth promoting, and antagonistic fungal strain. J Basic Microbiol 54:408–417Google Scholar
  120. Rodríguez R, Redman R (2008) 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 59:1109–1114Google Scholar
  121. Rodríguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim Y, Redman RS (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2:404–416Google Scholar
  122. Rudrappa T, Czymmek KJ, Paré PW, Bais HP (2008) Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148:1547–1556Google Scholar
  123. Saharan BS, Nehra V (2011) Plant growth promoting rhizobacteria: a critical review. Life Sci Med Res 21:1–30Google Scholar
  124. Saleem M, Law AD, Sahib MR, Pervaiz ZH, Zhang Q (2018) Impact of root system architecture on rhizosphere and root microbiome. Rhizosphere 6:47–51Google Scholar
  125. Santoyo G, Moreno-Hagelsieb G, Orozco-Mosqueda MC, Glick BR (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99Google Scholar
  126. Schloter M, Nannipieri P, Sorensen SJ, van Elsas JD (2018) Microbial indicators for soil quality. Biol Fertil Soils 54:1–10Google Scholar
  127. Selvakumar G, Kundu S, Joshi P, Nazim S, Gupta AD, Mishra PK, Gupta HS (2008a) Characterization of a cold-tolerant plant growth-promoting bacterium Pantoea dispersa 1A isolated from a sub-alpine soil in the North Western Indian Himalayas. World J Microbiol Biotechnol 24:955–960Google Scholar
  128. Selvakumar G, Mohan M, Kudu S, Gupta AD, Joshi P, Nazim S, Gupta HS (2008b) Cold tolerance and plant growth promotion potential of Serratia marcescens strain SRM (MTCC 8708) isolated from flowers of summer squash (Cucurbita pepo). Lett Appl Microbiol 46:171–175Google Scholar
  129. Selvakumar G, Joshi P, Mishra PK, Bisht JK, Gupta HS (2009a) Mountain aspect influences the genetic clustering of psychrotolerant phosphate solubilizing pseudomonads in the Uttarakhand Himalayas. Curr Microbiol 59:432–438Google Scholar
  130. Selvakumar G, Joshi P, Nazim S, Mishra PK, Bisht JK, Gupta HS (2009b) Phosphate solubilization and growth promotion by Pseudomonas fragi CS11RH1 (MTCC 8984), a psychrotolerant bacterium isolated from a high altitude Himalayan rhizosphere. Biologia 64:239–245Google Scholar
  131. Selvakumar G, Kundu S, Joshi P, Nazim S, Gupta AD, Gupta HS (2010) Growth promotion of wheat seedlings by Exiguobacterium acetylicum 1P (MTCC 8707) a cold tolerant bacterial strain from the Uttarakhand Himalayas. Ind J Microbiol 50:50–56Google Scholar
  132. Senés-Guerrero C, Schüssler A (2016) A conserved arbuscular mycorrhizal fungal core-species community colonizes potato roots in the Andes. Fungal Divers 77:317–333Google Scholar
  133. Shafi J, Tian H, Ji M (2017) Bacillus species as versatile weapons for plant pathogens: a review. Biotechnol Biotechnol Equip 31:446–459Google Scholar
  134. Shanmugam V, Sharma V, Ananthapadmanaban (2008) Genetic relatedness of Trichoderma isolates antagonistic against Fusarium oxysporum f.sp. dianthi inflicting carnation wilt. Folia Microbiol 53:130–138Google Scholar
  135. Singh S, Pandey A (2017) Plant-associated microbial endophytes: promising source for bioprospecting. In: Kalia VC, Shouche Y, Purohit HJ, Rahi P (eds) Mining of microbial wealth and metagenomics, Springer Nature Singapore Pte Ltd.  https://doi.org/10.1007/978-981-10-5708-3_15
  136. Singh B, Trivedi P (2017) Microbiome and the future for food and nutrient security. Microbial Biotechnol 10:50–53Google Scholar
  137. Singh B, Kaur P, Gopichand SRD, Ahuja PS (2008a) Biology and chemistry of Ginkgo biloba. Fitoterapia 79:401–418Google Scholar
  138. Singh S, Pandey A, Palni LMS (2008b) Screening of arbuscular mycorrhizal fungal consortia developed from the rhizospheres of natural and cultivated tea plants for growth promotion in tea [Camellia sinensis (L.)O. Kuntze]. Pedobiologia 52:119–125Google Scholar
  139. Singh S, Pandey A, Kumar B, Palni LMS (2010) Enhancement in growth and quality parameters of tea [Camellia sinensis (L.) O. Kuntze] through inoculation with arbuscular mycorrhizal fungi in an acid soil. Biol Fertil Soils 46:427–433Google Scholar
  140. Singh LP, Gill SG, Tuteja N (2011) Unraveling the role of fungal symbionts in plant abiotic stress tolerance. Plant Signal Behav 6:175–191Google Scholar
  141. Sood A, Sharma S, Kumar V, Thakur RL (2008) Established and abandoned tea (Camillia sinensis L.) rhizosphere: dominant bacteria and their antagonism. Pol J Microbiol 57:71–76Google Scholar
  142. Stefan M, Mihasan M, Dunca S (2008) Plant growth promoting rhizobacteria can inhibit the in vitro germination of Glycine max L. seeds. Scientific annals of university “Alexandru Ioan Cuza” Iasi. Sect. Genet Mol Biol 3:105–110Google Scholar
  143. Suryanarayanan TS, Thirunavukkarasu N, Govindarajulu MB, Sasse F, Jansen R, Murali TS (2009) Fungal endophytes and bioprospecting. Fungal Biol Rev 23:9–19Google Scholar
  144. Tewari S, Arora NK (2013) Plant growth promoting rhizobacteria for ameliorating abiotic stresses triggered due to climatic variability. Clim Chang Environ Sustain 1:95–103Google Scholar
  145. Tewari VP, Verma RK, von Gadow K (2017) Climate change effects in the Western Himalayan ecosystems of India: evidence and strategies. For Ecosyst 4:13Google Scholar
  146. Trivedi P, Pandey A (2008) Recovery of plant growth promoting rhizobacteria from sodium alginate beads after three years following storage at 4°C. J Indus Microbiol Biotechnol 35:205–209Google Scholar
  147. Trivedi P, Pandey A, Palni LMS (2005) Carrier based formulations of plant growth promoting bacteria suitable for use in the colder regions. World J Microbiol Biotechnol 21:941–945Google Scholar
  148. Trivedi P, Pandey A, Palni LMS (2008) In vitro evaluation of antagonistic properties of Pseudomonas corrugata. Microbiol Res 163:329–336Google Scholar
  149. Trivedi P, Pandey A, Palni LMS (2012) Bacterial inoculants for field applications under mountain ecosystem: present initiatives and future prospects. In: Maheshwari DK (ed) Bacteria in agrobiology: plant probiotics. Springer, Berlin, pp 15–44Google Scholar
  150. Velázquez E, Silva LR, Ramírez-Bahena MH, Peix A (2016) Diversity of potassium-solubilizing microorganisms and their interactions with plants. In: Meena VS, Maurya BR, Verma JP, Meena RS (eds) Potassium solubilizing microorganisms for sustainable agriculture. Springer, New Delhi, pp 99–110.  https://doi.org/10.1007/978-81-322-2776-2_7 Google Scholar
  151. Velivelli SLS, Kromann P, Lojan P, Rojas M, Franco J, Suarez JP, Prestwich BD (2015) Identification of mVOCs from Andean rhizobacteria and field evaluation of bacterial and mycorrhizal inoculants on growth of potato in its center of origin. Microb Ecol 69:652–667Google Scholar
  152. Verma JP, Yadav J, Tiwari KN, Kumar A (2013) Effect of indigenous Mesorhizobium spp. and plant growth promoting rhizobacteria on yields and nutrients uptake of chickpea (Cicer arietinum L.) under sustainable agriculture. Ecol Eng 51:282–286Google Scholar
  153. Vyas P, Joshi R, Sharma KC, Rahi P, Gulati A, Gulati A (2010) Cold-adapted and rhizosphere-competent strain of Rahnella sp. with broad-spectrum plant growth-promotion potential. J Microbiol Biotechnol 20:1724–1734Google Scholar
  154. Wallenstein MD (2017) Managing and manipulating the rhizosphere microbiome for plant health: a systems approach. Rhizosphere 3:230–232Google Scholar
  155. Wani ZA, Ashraf N, Mohiuddin T, Riyaz-Ul-Hassan S (2015) Plant-endophyte symbiosis, an ecological perspective. Appl Microbiol Biotechnol 99:2955–2965Google Scholar
  156. Yarzábal LA, Chica EJ (2017) Potential for developing low-input sustainable agriculture in the tropical Andes by making use of native microbial resources. In: Singh D, Singh H, Prabha R (eds) Plant-microbe interactions in agro-ecological perspectives. Springer, Singapore, pp 29–54Google Scholar
  157. Yarzábal LA, Chica EJ, Quichimbo P (2017) Microbial diversity of tropical Andean soils and low-input sustainable agriculture development. In: Meena V, Mishra P, Bisht J, Pattanayak A (eds) Agriculturally important microbes for sustainable agriculture. Springer, Singapore, pp 207–234Google Scholar
  158. Yarzábal LA, Monserrate L, Buela L, Chica E (2018) Antarctic Pseudomonas spp. promote wheat germination and growth at low temperatures. Polar Biol 41:2343–2354.  https://doi.org/10.1007/s00300-018-2374-6 Google Scholar
  159. Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32:723–735Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Centre for Environmental Assessment and Climate ChangeG.B. Pant National Institute of Himalayan Environment and Sustainable DevelopmentAlmoraIndia
  2. 2.Unidad de Salud y BienestarUniversidad Católica de CuencaCuencaEcuador
  3. 3.Departamento de Biología, Facultad de CienciasUniversidad de Los AndesMéridaVenezuela

Personalised recommendations