619
Views
11
CrossRef citations to date
0
Altmetric
Review

Managing plant-environment-symbiont interactions to promote plant performance under low temperature stress

ORCID Icon, , ORCID Icon & ORCID Icon
Pages 2010-2027 | Received 04 Oct 2018, Accepted 11 Dec 2018, Published online: 07 Aug 2019

References

  • Abdel-Fattah, G. M., and A.-W. A. Asrar. 2012. Arbuscular mycorrhizal fungal application to improve growth and tolerance of wheat (Triticum aestivum L.) plants grown in saline soil. Acta Physiologiae Plantarum 34 (1):267–277. doi: 10.1007/s11738-011-0825-6.
  • Abdel Latef, A. A. H., and H. Chaoxing. 2011. Arbuscular mycorrhizal influence on growth, photosynthetic pigments, osmotic adjustment and oxidative stress in tomato plants subjected to low temperature stress. Acta Physiologiae Plantarum 33 (4):1217–1225. doi: 10.1007/s11738-010-0650-3.
  • Afifi, A. F. 1984. Effect of plant volatiles on rhizospheric and phyllospheric mycoflora. In Being alive on land: Proceedings of the international symposium on adaptations to the terrestrial environment held in Halkidiki., eds. N. S. Margaris, M. Arianoustou-Faraggitaki, W. C. Oechel, 257–269. Greece. 1982. Springer Netherlands, Dordrecht. doi: 10.1007/978-94-009-6578-2_27.
  • Alexandre, A., and S. Oliveira. 2013. Response to temperature stress in rhizobia. Critical Reviews in Microbiology 39 (3):219–228. doi: 10.3109/1040841X.2012.702097.
  • Alizadeh Frutan, M., H. Pirdashti, Y. Yaghoubian, and V. Babaeizad. 2016. Effect of paclobutrazol and priformospora indica inoculation on antioxidant enzymes activity and morphological characteristics of green beans (Phaseoluse vulgaris L.) in chilling stress. Journal of Plant Process and Function 5 (15):133–146.
  • Allen, M. F. 1983. Formation of vesicular-arbuscular mycorrhizae in Atriplex gardneri (Chenopodiaceae): Seasonal response in a cold desert. Mycologia 75 (5):773–776. doi: 10.2307/3792769.
  • Baltrus, D. A., Dougherty, K. K. R. Arendt, M. Huntemann, A. Clum, M. Pillay, K. Palaniappan, N. Varghese, N. Mikhailova, D. Stamatis, T. B. K., et al. 2017. Absence of genome reduction in diverse, facultative endohyphal bacteria. Microbial Genomics 3 (2):1–12. doi: 10.1099/mgen.0.000101.
  • Beltrano, J., and M. G. Ronco. 2008. Improved tolerance of wheat plants (Triticum aestivum L.) to drought stress and rewatering by the arbuscular mycorrhizal fungus Glomus claroideum: Effect on growth and cell membrane stability. Brazilian Journal of Plant Physiology 20 (1):29–37. doi: 10.1590/S1677-04202008000100004.
  • Berg, G., D. Rybakova, M. Grube, and M. Köberl. 2016. The plant microbiome explored: Implications for experimental botany. Journal of Experimental Botany 67 (4):995–1002. doi: 10.1093/jxb/erv466.
  • Bernardo, L., C. Morcia, P. Carletti, R. Ghizzoni, F. W. Badeck, F. Rizza, L. Lucini, and V. Terzi. 2017. Proteomic insight into the mitigation of wheat root drought stress by arbuscular mycorrhizae. Journal of Proteomics 169:21–32. doi: 10.1016/j.jprot.2017.03.024.
  • Berruti, A., E. Lumini, R. Balestrini, and V. Bianciotto. 2015. Arbuscular mycorrhizal fungi as natural biofertilizers: Let's benefit from past successes. Frontiers in Microbiology 6:1559, 1–13. doi: 10.3389/fmicb.2015.01559.
  • Birhane, E., F. J. Sterck, M. Fetene, F. Bongers, and T. W. Kuyper. 2012. Arbuscular mycorrhizal fungi enhance photosynthesis, water use efficiency, and growth of frankincense seedlings under pulsed water availability conditions. Oecologia 169 (4):895–904. doi: 10.1007/s00442-012-2258-3.
  • Bowman, J. P., S. A. McCammon, M. V. Brown, D. S. Nichols, and T. A. McMeekin. 1997. Diversity and association of psychrophilic bacteria in Antarctic sea ice. Applied and Environmental Microbiology 63 (8):3068–3078.
  • Campanelli, A., C. Ruta, G. De Mastro, and I. Morone-Fortunato. 2013. The role of arbuscular mycorrhizal fungi in alleviating salt stress in Medicago sativa L. var. icon. Symbiosis 59 (2):65–76. doi: 10.1007/s13199-012-0191-1.
  • Cartmill, A. D., A. Alarcón, and L. A. Valdez-Aguilar. 2007. Arbuscular mycorrhizal fungi enhance tolerance of Rosa multiflora cv. Burr to bicarbonate in irrigation water. Journal of Plant Nutrition 30 (9):1517–1540. doi: 10.1080/01904160701556802.
  • Charest, C., Y. Dalpé, and A. Brown. 1993. The effect of vesicular-arbuscular mycorrhizae and chilling on two hybrids of Zea mays L. Mycorrhiza 4 (2):89–92. doi: 10.1007/BF00204064.
  • Chen, S., W. Jin, A. Liu, S. Zhang, D. Liu, F. Wang, X. Lin, and C. He. 2013. Arbuscular mycorrhizal fungi (AMF) increase growth and secondary metabolism in cucumber subjected to low temperature stress. Scientia Horticulturae 160:222–229. doi: 10.1016/j.scienta.2013.05.039.
  • Chen, X., F. Song, F. Liu, C. Tian, S. Liu, H. Xu, and X. Zhu. 2014. Effect of different arbuscular mycorrhizal fungi on growth and physiology of maize at ambient and low temperature regimes. The Scientific World Journal 2014:1–7. doi: 10.1155/2014/956141.
  • Chu, X.T., J.J. Fu, Y.F. Sun, Y.M. Xu, Y.J. Miao, Y.F. Xu, and T.M. Hu. 2016. Effect of arbuscular mycorrhizal fungi inoculation on cold stress-induced oxidative damage in leaves of Elymus nutans Griseb. South African Journal of Botany 104:21–29. doi: 10.1016/j.sajb.2015.10.001.
  • Classen, A. T., M. K. Sundqvist, J. A. Henning, G. S. Newman, J. A. M. Moore, M. A. Cregger, L. C. Moorhead, and C. M. Patterson. 2015. Direct and indirect effects of climate change on soil microbial and soil microbial-plant interactions: What lies ahead? Ecosphere 6 (8):130–21. doi: 10.1890/ES15-00217.1.
  • da-Silva, J. R., A. Alexandre, C. Brígido, and S. Oliveira. 2017. Can stress response genes be used to improve the symbiotic performance of rhizobia? AIMS Microbiology 3 (3):365–382. doi: 10.3934/microbiol.2017.3.365.
  • Drouin, P., D. Prévost, and H. Antoun. 2000. Physiological adaptation to low temperatures of strains of Rhizobium leguminosarum bv. viciae associated with Lathyrus spp.1. FEMS Microbiology Ecology 32 (2):111–120. doi: 10.1111/j.1574-6941.2000.tb00705.x.
  • Dsouza, M., M. W. Taylor, S. J. Turner, and J. Aislabie. 2014. Genome-based comparative analyses of antarctic and temperate species of Paenibacillus. Plos ONE 9 (10):e108009, 1–12. doi: 10.1371/journal.pone.0108009.
  • Duperron, S. 2017. The concept of symbiosis, from past to present. Microbial symbioses. Amsterdam: Elsevier, 1–17. doi: 10.1016/B978-1-78548-220-5.50001-5.
  • Eisenhauer, N., A. Lanoue, T. Strecker, S. Scheu, K. Steinauer, M. P. Thakur, and L. Mommer. 2017. Root biomass and exudates link plant diversity with soil bacterial and fungal biomass. Scientific Reports 7:44641, 1–8. doi: 10.1038/srep44641.
  • Estrada, B., R. Aroca, F. J. M. Maathuis, J. M. Barea, and J. M. Ruiz-Lozano. 2013. Arbuscular mycorrhizal fungi native from a Mediterranean saline area enhance maize tolerance to salinity through improved ion homeostasis. Plant, Cell & Environment 36 (10):1771–1782. doi: 10.1111/pce.12082.
  • Evelin, H., and R. Kapoor. 2014. Arbuscular mycorrhizal symbiosis modulates antioxidant response in salt-stressed Trigonella foenum-graecum plants. Mycorrhiza 24 (3):197–208. doi: 10.1007/s00572-013-0529-4.
  • Evelin, H., R. Kapoor, and B. Giri. 2009. Arbuscular mycorrhizal fungi in alleviation of salt stress: A review. Annals of Botany 104 (7):1263–1280. doi: 10.1093/aob/mcp251.
  • Fan, Q.-J., and J.-H. Liu. 2011. Colonization with arbuscular mycorrhizal fungus affects growth, drought tolerance and expression of stress-responsive genes in Poncirus trifoliata. Acta Physiologiae Plantarum 33 (4):1533–1542. doi: 10.1007/s11738-011-0789-6.
  • Fernandez, O., A. Theocharis, S. Bordiec, R. Feil, L. Jacquens, C. Clément, F. Fontaine, and E. A. Barka. 2012. Burkholderia phytofirmans PsJN acclimates grapevine to cold by modulating carbohydrate metabolism. Molecular Plant-Microbe Interactions 25 (4):496–504. doi: 10.1094/MPMI-09-11-0245.
  • Fu, Y., H. Gao, H. Li, Y. Qin, W. Tang, J. Lu, M. Li, L. Shao, and H. Liu. 2017. Change of growth promotion and disease resistant of wheat seedling by application of biocontrol bacterium Pseudochrobactrum kiredjianiae A4 under simulated microgravity. Acta Astronautica 139 (Supplement C):222–227. doi: 10.1016/j.actaastro.2017.06.022.
  • Gavito, M. E., and C. Azcón–Aguilar. 2012. Temperature stress in arbuscular mycorrhizal fungi: A test for adaptation to soil temperature in three isolates of Funneliformis mosseae from different climates. Agricultural and Food Science 21 (1):2–11. doi: 10.23986/afsci.4994.
  • Ghobakhlou, A., S. Laberge, H. Antoun, D. S. Wishart, J. Xia, R. Krishnamurthy, and R. Mandal. 2013. Metabolomic analysis of cold acclimation of arctic Mesorhizobium sp. Strain N33. PLoS ONE 8 (12):e84801, 1–15. doi: 10.1371/journal.pone.0084801.
  • González, M. B. R., and J. Gonzalez-López. 2013. Beneficial plant-microbial interactions: Ecology and applications. Boca Raton, FL: CRC Press. doi: 10.1201/b15251.
  • Gougoulias, C., J. M. Clark, and L. J. Shaw. 2014. The role of soil microbes in the global carbon cycle: Tracking the below-ground microbial processing of plant-derived carbon for manipulating carbon dynamics in agricultural systems. Journal of the Science of Food and Agriculture 94 (12):2362–2371. doi: 10.1002/jsfa.6577.
  • Gpey, W. E. 1991. Influence of temperature on colonization of spring barleys by vesicular arbuscular mycorrhizal fungi. Plant and Soil 137 (2):181–190. doi: 10.1007/BF00011196.
  • Graham, P. H. 1992. Stress tolerance in Rhizobium and Bradyrhizobium, and nodulation under adverse soil conditions. Canadian Journal of Microbiology 38 (6):475–484. doi: 10.1139/m92-079.
  • Gupta, V. 2011. Microbes and Soil Structure. In Encyclopedia of agrophysics., eds J. Gliński, J. Horabik, J. Lipiec, 470–472. Dordrecht: Springer Netherlands. doi: 10.1007/978-90-481-3585-1_91.
  • Hart, M. M., and J. N. Klironomos. 2003. Diversity of arbuscular mycorrhizal fungi and ecosystem functioning. In Mycorrhizal ecology., M. G. A. Van Der Heijden, I. R. Sanders, 225–242. Berlin, Heidelberg: Springer Berlin Heidelberg. doi: 10.1007/978-3-540-38364-2_9.
  • Hayat, W., H. Aman, U. Irshad, M. Azeem, A. Iqbal, and R. Nazir. 2017. Analysis of ecological attributes of bacterial phosphorus solubilizers, native to pine forests of Lower Himalaya. Applied Soil Ecology 112:51–59. doi: 10.1016/j.apsoil.2016.11.004.
  • Howieson, J., and R. Ballard. 2004. Optimising the legume symbiosis in stressful and competitive environments within southern Australia—some contemporary thoughts. Soil Biology and Biochemistry 36 (8):1261–1273. doi: 10.1016/j.soilbio.2004.04.008.
  • Hu, W., H. Zhang, H. Chen, and M. Tang. 2017. Arbuscular mycorrhizas influence Lycium barbarum tolerance of water stress in a hot environment. Mycorrhiza 27 (5):451–463. doi: 10.1007/s00572-017-0765-0.
  • Janczarek, M., K. Rachwał, and A. Turska-Szewczuk. 2017. A mutation in pssE affects exopolysaccharide synthesis by Rhizobium leguminosarum bv. trifolii, its surface properties, and symbiosis with clover. Plant and Soil 417 (1–2):331–347. doi: 10.1007/s11104-017-3262-5.
  • Johnson, N. C., J. H. Graham, and F. A. Smith. 1997. Functioning of mycorrhizal associations along the mutualism–parasitism continuum. New Phytologist 135 (4):575–585. doi: 10.1046/j.1469-8137.1997.00729.x.
  • Junge, K., B. Christner, and J. T. Staley. 2011. Diversity of psychrophilic bacteria from sea ice - and glacial ice communities. In Extremophiles handbook. ed. K. Horikoshi, 793–815. Tokyo: Springer Japan. doi: 10.1007/978-4-431-53898-1_39.
  • Kang, S. W., B. Y. Jeon, T. S. Hwang, and D. H. Park. 2009. Symbiotic relationship between Microbacterium sp. SK0812 and Candida tropicalis SK090404. The Journal of Microbiology 47 (6):721–727. doi: 10.1007/s12275-009-0146-2.
  • Keto-Timonen, R., N. Hietala, E. Palonen, A. Hakakorpi, M. Lindström, and H. Korkeala. 2016. Cold shock proteins: A minireview with special emphasis on csp-family of enteropathogenic Yersinia. Frontiers in Microbiology 7:1151, 1–7. doi: 10.3389/fmicb.2016.01151.
  • Kim, K. Y., Y. S. Cho, B. K. Sohn, R. D. Park, J. H. Shim, S. J. Jung, Y. W. Kim, and K. Y. Seong. 2002. Cold-storage of mixed inoculum of Glomus intraradices enhances root colonization, phosphorus status and growth of hot pepper. Plant and Soil 238 (2):267–272. doi: 10.1023/A:1014474617170.
  • Kishitani, S., K. Watanabe, S. Yasuda, K. Arakawa, and T. Takabe. 1994. Accumulation of glycinebetaine during cold acclimation and freezing tolerance in leaves of winter and spring barley plants. Plant, Cell and Environment 17 (1):89–95. doi: 10.1111/j.1365-3040.1994.tb00269.x.
  • Kwon, S. J., S. I. Kwon, M. S. Bae, E. J. Cho, and O. K. Park. 2007. Role of the methionine sulfoxide reductase MsrB3 in cold acclimation in Arabidopsis. Plant and Cell Physiology 48 (12):1713–1723. doi: 10.1093/pcp/pcm143.
  • Kytöviita, M.-M. 2005. Asymmetric symbiont adaptation to Arctic conditions could explain why high Arctic plants are non-mycorrhizal. FEMS Microbiology Ecology 53 (1):27–32. doi: 10.1016/j.femsec.2004.09.014.
  • Laforest-Lapointe, I., A. Paquette, C. Messier, and S. W. Kembel. 2017. Leaf bacterial diversity mediates plant diversity and ecosystem function relationships. Nature 546 (7656):145–147. doi: 10.1038/nature22399.
  • Laguerre, G., P. van Berkum, N. Amarger, and D. Prévost. 1997. Genetic diversity of rhizobial symbionts isolated from legume species within the genera Astragalus, Oxytropis, and Onobrychis. Applied and Environmental Microbiology 63 (12):4748–4758.
  • Laranjo, M., and S. Oliveira. 2011. Tolerance of Mesorhizobium type strains to different environmental stresses. Antonie Van Leeuwenhoek 99 (3):651–662. doi: 10.1007/s10482-010-9539-9.
  • Larrainzar, E., and S. Wienkoop. 2017. A proteomic view on the role of legume symbiotic interactions. Frontiers in Plant Science 8:1267, 1–13. doi: 10.3389/fpls.2017.01267.
  • Lekberg, Y., and R. T. Koide. 2008. Effect of soil moisture and temperature during fallow on survival of contrasting isolates of arbuscular mycorrhizal fungi. Botany 86 (10):1117–1124. doi: 10.1139/B08-077.
  • Li, H.-Y., M. Shen, Z.-P. Zhou, T. Li, Y.-I. Wei, and L.-b Lin. 2012. Diversity and cold adaptation of endophytic fungi from five dominant plant species collected from the Baima Snow Mountain, Southwest China. Fungal Diversity 54 (1):79–86. doi: 10.1007/s13225-012-0153-1.
  • Lipson, D. A., R. F. Wilson, and W. C. Oechel. 2005. Effects of elevated atmospheric CO2 on soil microbial biomass, activity, and diversity in a chaparral ecosystem. Applied and Environmental Microbiology 71 (12):8573–8580. doi: 10.1128/AEM.71.12.8573-8580.2005.
  • Liu, A., S. Chen, R. Chang, D. Liu, H. Chen, G. J. Ahammed, X. Lin, and C. He. 2014. Arbuscular mycorrhizae improve low temperature tolerance in cucumber via alterations in H2O2 accumulation and ATPase activity. Journal of Plant Research 127 (6):775–785. doi: 10.1007/s10265-014-0657-8.
  • Liu, M.-Z., and C. P. Osborne. 2008. Leaf cold acclimation and freezing injury in C3 and C4 grasses of the Mongolian Plateau. Journal of Experimental Botany 59 (15):4161–4170. doi: 10.1093/jxb/ern257.
  • Mageswari, A., P. Subramanian, R. Srinivasan, S. Karthikeyan, and K. M. Gothandam. 2015. Astaxanthin from psychrotrophic Sphingomonas faeni exhibits antagonism against food-spoilage bacteria at low temperatures. Microbiological Research 179:38–44. doi: 10.1016/j.micres.2015.06.010.
  • Maggi, O., Tosi, S. M. Angelova, E. Lagostina, A. A. Fabbri, L. Pecoraro, E. Altobelli, A. M. Picco, E. Savino, E. Branda, B., et al. 2013. Adaptation of fungi, including yeasts, to cold environments. Plant Biosystems - An International Journal Dealing with All Aspects of Plant Biology 147 (1):247–258. doi: 10.1080/11263504.2012.753135.
  • Maksimov, E. G., Mironov, K. S. M. S. Trofimova, N. L. Nechaeva, D. A. Todorenko, K. E. Klementiev, G. V. Tsoraev, E. V. Tyutyaev, A. A. Zorina, P. V. Feduraev, S. I., et al. 2017. Membrane fluidity controls redox-regulated cold stress responses in cyanobacteria. Photosynthesis Research 133 (1):215–223. doi: 10.1007/s11120-017-0337-3.
  • Margesin, R., V. Fauster, and P. A. Fonteyne. 2005. Characterization of cold-active pectate lyases from psychrophilic Mrakia frigida. Letters in Applied Microbiology 40 (6):453–459. doi: 10.1111/j.1472-765X.2005.01704.x.
  • Medina, A., and R. Azcón. 2010. Effectiveness of the application of arbuscular mycorrhiza fungi and organic amendments to improve soil quality and plant performance under stress conditions. Journal of Soil Science and Plant Nutrition 10 (3):354–372. doi: 10.4067/S0718-95162010000100009.
  • Mei, Y.-Z., P.-W. Huang, Y. Liu, W. He, and W.-W. Fang. 2016. Cold stress promoting a psychrotolerant bacterium Pseudomonas fragi P121 producing trehaloase. World Journal of Microbiology and Biotechnology 32 (8):1–9. doi: 10.1007/s11274-016-2097-1.
  • Michaux, C., E. Holmqvist, E. Vasicek, M. Sharan, L. Barquist, A. J. Westermann, J. S. Gunn, and J. Vogel. 2017. RNA target profiles direct the discovery of virulence functions for the cold-shock proteins CspC and CspE. Proceedings of the National Academy of Sciences 114 (26):6824–6829. doi: 10.1073/pnas.1620772114.
  • Millar, N. S., and A. E. Bennett. 2016. Stressed out symbiotes: Hypotheses for the influence of abiotic stress on arbuscular mycorrhizal fungi. Oecologia 182 (3):625–641. doi: 10.1007/s00442-016-3673-7.
  • Miltner, A., H.-H. Richnow, F.-D. Kopinke, and M. Kästner. 2004. Assimilation of CO2 by soil microorganisms and transformation into soil organic matter. Organic Geochemistry 35 (9):1015–1024. doi: 10.1016/j.orggeochem.2004.05.001.
  • Mishra, Pankaj K., Shekhar C. Bisht, Pooja Ruwari, Gopal K. Joshi, G. Singh, Jaideep K. Bisht, and J.C. Bhatt. 2011. Bioassociative effect of cold tolerant Pseudomonas spp. and Rhizobium leguminosarum-PR1 on iron acquisition, nutrient uptake and growth of lentil (Lens culinaris L.). European Journal of Soil Biology 47 (1):35–43. doi: 10.1016/j.ejsobi.2010.11.005.
  • Mishra, P. K., S. C. Bisht, J. K. Bisht, and J. C. Bhatt. 2012. Cold-tolerant PGPRs as bioinoculants for stress management. In Bacteria in Agrobiology: Stress Management., ed. D. K. Maheshwari, 95–118. Berlin, Heidelberg: Springer Berlin Heidelberg. doi: 10.1007/978-3-642-23465-1_6.
  • Mishra, P. K., S. C. Bisht, P. Ruwari, G. Selvakumar, G. K. Joshi, J. K. Bisht, J. C. Bhatt, and H. S. Gupta. 2011. Alleviation of cold stress in inoculated wheat (Triticum aestivum L.) seedlings with psychrotolerant Pseudomonads from NW Himalayas. Archives of Microbiology 193 (7):497–513. doi: 10.1007/s00203-011-0693-x.
  • Morita, R. Y. 1975. Psychrophilic bacteria. Bacteriological Reviews 39 (2):144–167.
  • Ouellet, F., and J.-B. Charron. 2013. Cold acclimation and freezing tolerance in plants, eLS. Chichester, UK: John Wiley & Sons, Ltd. doi: 10.1002/9780470015902.a0020093.pub2
  • Paço, A., C. Brígido, A. Alexandre, P. F. Mateos, and S. Oliveira. 2016. The symbiotic performance of chickpea rhizobia can be improved by additional copies of the clpB chaperone gene. Plos ONE 11 (2):e0148221, 1–18. doi: 10.1371/journal.pone.0148221.
  • Padbhushan, R., and D. Kumar. 2015. Yield and nutrient uptake of green gram (Vigna radiata L.) as influenced by boron application in boron-deficient calcareous soils of Punjab. Communications in Soil Science and Plant Analysis 46 (7):908–923. doi: 10.1080/00103624.2015.1018520.
  • Panadero, J., C. Pallotti, S. Rodríguez-Vargas, F. Randez-Gil, and J. A. Prieto. 2006. A downshift in temperature activates the high osmolarity glycerol (HOG) pathway, which determines freeze tolerance in Saccharomyces cerevisiae. Journal of Biological Chemistry 281 (8):4638–4645. doi: 10.1074/jbc.M512736200.
  • Pistelli, L., V. Ulivieri, S. Giovanelli, L. Avio, M. Giovannetti, and L. Pistelli. 2017. Arbuscular mycorrhizal fungi alter the content and composition of secondary metabolites in Bituminaria bituminosa L. Plant Biology 19 (6):926–933. doi: 10.1111/plb.12608.
  • Poltronieri, P., V. Mezzolla, and O. F. D’Urso. 2014. Bacterial small RNAs and their role in stress tolerance and adaptation to environment. Research in Cell Biology 2 (1):8–16. doi: 10.5923/j.cellbiology.20140201.02.
  • Prévost, D., P. Drouin, S. Laberge, A. Bertrand, J. Cloutier, and G. Lévesque. 2003. Cold-adapted rhizobia for nitrogen fixation in temperate regions. Canadian Journal of Botany 81 (12):1153–1161. doi: 10.1139/b03-113.
  • Qin, Y., Y. Fu, W. Kang, H. Li, H. Gao, K. S. Vitalievitch, and H. Liu. 2017. Isolation and identification of a cold-adapted bacterium and its characterization for biocontrol and plant growth-promoting activity. Ecological Engineering 105 (Supplement C):362–369. doi: 10.1016/j.ecoleng.2017.04.045.
  • Quiroga, G., G. Erice, R. Aroca, F. Chaumont, and J. M. Ruiz-Lozano. 2017. Enhanced drought stress tolerance by the arbuscular mycorrhizal symbiosis in a drought-sensitive maize cultivar is related to a broader and differential regulation of host plant aquaporins than in a drought-tolerant cultivar. Frontiers in Plant Science 8:1056, 1–15. doi: 10.3389/fpls.2017.01056.
  • Rahimzadeh, S., and A. R. Pirzad. 2017. Microorganisms (AMF and PSB) interaction on linseed productivity under water-deficit condition. International Journal of Plant Production 11 (2):259–274. doi: 10.22069/ijpp.2017.3423.
  • Rayirath, P., B. Benkel, D. Mark Hodges, P. Allan-Wojtas, S. MacKinnon, A. T. Critchley, and B. Prithiviraj. 2009. Lipophilic components of the brown seaweed, Ascophyllum nodosum, enhance freezing tolerance in Arabidopsis thaliana. Planta 230 (1):135–147. doi: 10.1007/s00425-009-0920-8.
  • Rinu, K., and A. Pandey. 2010. Temperature-dependent phosphate solubilization by cold- and pH-tolerant species of Aspergillus isolated from Himalayan soil. Mycoscience 51 (4):263–271. doi: 10.1007/S10267-010-0036-9.
  • Robledo, M., A. Peregrina, V. Millán, N. I. García-Tomsig, O. Torres-Quesada, P. F. Mateos, A. Becker, and J. I. Jiménez-Zurdo. 2017. A conserved α-proteobacterial small RNA contributes to osmoadaptation and symbiotic efficiency of rhizobia on legume roots. Environmental Microbiology 19 (7):2661–2680. doi: 10.1111/1462-2920.13757.
  • Sardesai, N., and C. R. Babu. 2001. Poly-β-hydroxybutyrate metabolism is affected by changes in respiratory enzymatic activities due to cold stress in two psychrotrophic strains of Rhizobium. Current Microbiology 42 (1):53–58. doi: 10.1007/s002840010178.
  • Schreiner, R. P., J. M. Tarara, and R. P. Smithyman. 2007. Deficit irrigation promotes arbuscular colonization of fine roots by mycorrhizal fungi in grapevines (Vitis vinifera L.) in an arid climate. Mycorrhiza 17 (7):551–562. doi: 10.1007/s00572-007-0128-3.
  • Schüβler, A., D. Schwarzott, and C. Walker. 2001. A new fungal phylum, the Glomeromycota: Phylogeny and evolution. Mycological Research 105 (12):1413–1421. doi: 10.1017/S0953756201005196.
  • Selvakumar, G., K. Kim, C. C. Shagol, M. M. Joe, and T. Sa. 2017. Spore associated bacteria of arbuscular mycorrhizal fungi improve maize tolerance to salinity by reducing ethylene stress level. Plant Growth Regulation 81 (1):159–165. doi: 10.1007/s10725-016-0184-9.
  • Selvakumar, G., S. Kundu, P. Joshi, S. Nazim, A. D. Gupta, P. K. Mishra, and H. S. Gupta. 2008. 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 Journal of Microbiology and Biotechnology 24 (7):955–960. doi: 10.1007/s11274-007-9558-5.
  • Sessitsch, A., A. Weilharter, M. H. Gerzabek, H. Kirchmann, and E. Kandeler. 2001. Microbial population structures in soil particle size fractions of a long-term fertilizer field experiment. Applied and Environmental Microbiology 67 (9):4215–4224. doi: 10.1128/aem.67.9.4215-4224.2001.
  • Shahzad, R., A. L. Khan, S. Bilal, M. Waqas, S.-M. Kang, and I.-J. Lee. 2017. Inoculation of abscisic acid-producing endophytic bacteria enhances salinity stress tolerance in Oryza sativa. Environmental and Experimental Botany 136:68–77. doi: 10.1016/j.envexpbot.2017.01.010.
  • Sharma, C., R. K. Gupta, R. K. Pathak, and K. K. Choudhary. 2013. Seasonal colonization of arbuscular mycorrhiza fungi in the roots of Camellia sinensis (tea) in different tea gardens of India. ISRN Biodiversity 2013:1–6. doi: 10.1155/2013/593087.
  • Shi, S.-M., K. Chen, Y. Gao, B. Liu, X.-H. Yang, X.-Z. Huang, G.-X. Liu, L.-Q. Zhu, and X.-H. He. 2016. Arbuscular mycorrhizal fungus species dependency governs better plant physiological characteristics and leaf quality of mulberry (Morus alba L.) seedlings. Frontiers in Microbiology 7:1030, 1–11. doi: 10.3389/fmicb.2016.01030.
  • Shires, K., and L. Steyn. 2001. The cold-shock stress response in Mycobacterium smegmatis induces the expression of a histone-like protein. Molecular Microbiology 39 (4):994–1009. doi: 10.1046/j.1365-2958.2001.02291.x.
  • Shtark, O. Y., A. Y. Borisov, V. A. Zhukov, T. A. Nemankin, and I. A. Tikhonovich. 2012. Multicomponent symbiosis of legumes with beneficial soil microorganisms: Genetic and evolutionary bases of application in sustainable crop production. Russian Journal of Genetics: Applied Research 2 (2):177–189. doi: 10.1134/S2079059712020116.
  • Shtark, O. Y., V. A. Zhukov, A. S. Sulima, R. Singh, T. S. Naumkina, G. A. Akhtemova, and A. Y. Borisov. 2015. Prospects for the use of multi-component symbiotic systems of the Legumes. Ecological Genetics 13 (1):33–46. doi: 10.17816/ecogen13133-46.
  • Srinivasan, R., A. Mageswari, P. Subramanian, V. K. Maurya, C. Sugnathi, C. Amballa, T. Sa, and K. Gothandam. 2017. Exogenous expression of ACC deaminase gene in psychrotolerant bacteria alleviates chilling stress and promotes plant growth in millets under chilling conditions. Indian Journal of Experimental Biology 55 (7):463–468.
  • Strimbeck, G. R., P. G. Schaberg, C. G. Fossdal, W. P. Schröder, and T. D. Kjellsen. 2015. Extreme low temperature tolerance in woody plants. Frontiers in Plant Science 6:884, 1–15. doi: 10.3389/fpls.2015.00884.
  • Su, F., C. Jacquard, S. Villaume, J. Michel, F. Rabenoelina, C. Clément, E. A. Barka, S. Dhondt-Cordelier, and N. Vaillant-Gaveau. 2015. Burkholderia phytofirmans PsJN reduces impact of freezing temperatures on photosynthesis in Arabidopsis thaliana. Frontiers in Plant Science 6:810, 1–13. doi: 10.3389/fpls.2015.00810.
  • Subramanian, P., K. Kim, R. Krishnamoorthy, A. Mageswari, G. Selvakumar, and T. Sa. 2016. Cold stress tolerance in psychrotolerant soil bacteria and their conferred chilling resistance in tomato (Solanum lycopersicum Mill.) under low temperatures. Plos ONE 11 (8):e0161592, 1–17. doi: 10.1371/journal.pone.0161592.
  • Subramanian, P., R. Krishnamoorthy, M. Chanratana, K. Kim, and T. Sa. 2015. Expression of an exogenous 1-aminocyclopropane-1-carboxylate deaminase gene in psychrotolerant bacteria modulates ethylene metabolism and cold-induced genes in tomato under chilling stress. Plant Physiology and Biochemistry 89:18–23. doi: 10.1016/j.plaphy.2015.02.003.
  • Sun, H., M. Santalahti, J. Pumpanen, K. Koster, F. Berninger, T. Raffaello, A. Jumpponen, F. O. Asiegbu, and J. Heinonsalo. 2015. Fungal community shifts in structure and function across a boreal forest fire chronosequence. Applied and Environmental Microbiology 81 (22):7869–7880. doi: 10.1128/AEM.02063-15.
  • Suyal, D. C., S. Kumar, A. Yadav, Y. Shouche, and R. Goel. 2017. Cold stress and nitrogen deficiency affected protein expression of psychrotrophic dyadobacter psychrophilus B2 and Pseudomonas jessenii MP1. Frontiers in Microbiology 8:430, 1–6. doi: 10.3389/fmicb.2017.00430.
  • Tardy, V., O. Mathieu, J. Leveque, S. Terrat, A. Chabbi, P. Lemanceau, L. Ranjard, and P. A. Maron. 2014. Stability of soil microbial structure and activity depends on microbial diversity. Environmental Microbiology Reports 6 (2):173–183. doi: 10.1111/1758-2229.12126.
  • Theocharis, A., S. Bordiec, O. Fernandez, S. Paquis, S. Dhondt-Cordelier, F. Baillieul, C. Clément, and E. A. Barka. 2012. Burkholderia phytofirmans PsJN primes Vitis vinifera L. and confers a better tolerance to low nonfreezing temperatures. Molecular Plant-Microbe Interactions 25 (2):241–249. doi: 10.1094/MPMI-05-11-0124.
  • Thomas-Hall, S. R., B. Turchetti, P. Buzzini, E. Branda, T. Boekhout, B. Theelen, and K. Watson. 2010. Cold-adapted yeasts from Antarctica and the Italian Alps—description of three novel species: Mrakia robertii sp. nov., Mrakia blollopis sp. nov. and Mrakiella niccombsii sp. nov. Extremophiles 14 (1):47–59. doi: 10.1007/s00792-009-0286-7.
  • Thomashow, M. F. 1999. Plant cold acclimation: Freezing tolerance genes and regulatory mechanisms. Annual Review of Plant Physiology and Plant Molecular Biology 50 (1):571–599. doi: 10.1146/annurev.arplant.50.1.571.
  • Tiwari, S., V. Prasad, P. S. Chauhan, and C. Lata. 2017. Bacillus amyloliquefaciens confers tolerance to various abiotic stresses and modulates plant response to phytohormones through osmoprotection and gene expression regulation in rice. Frontiers in Plant Science 8:1510, 1–13. doi: 10.3389/fpls.2017.01510.
  • Tsuji, M. 2016. Cold-stress responses in the Antarctic basidiomycetous yeast Mrakia blollopis. Royal Society Open Science 3 (7):160106, 1–13. doi: 10.1098/rsos.160106.
  • Urcelay, C., and S. Díaz. 2003. The mycorrhizal dependence of subordinates determines the effect of arbuscular mycorrhizal fungi on plant diversity. Ecology Letters 6 (5):388–391. doi: 10.1046/j.1461-0248.2003.00444.x.
  • Van Der Heijden, M. G., S. De Bruin, L. Luckerhoff, R. S. Van Logtestijn, and K. Schlaeppi. 2016. A widespread plant-fungal-bacterial symbiosis promotes plant biodiversity, plant nutrition and seedling recruitment. The ISME Journal 10 (2):389–399. doi: 10.1038/ismej.2015.120.
  • van der Heijden, Marcel G. A., John N. Klironomos, Margot Ursic, Peter Moutoglis, Ruth Streitwolf-Engel, Thomas Boller, Andres Wiemken, and Ian R. Sanders. 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396 (6706):69–72. doi: 10.1038/23932.
  • Van Der Heijden, M. G. A., R. D. Bardgett, and N. M. Van Straalen. 2008. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecology Letters 11 (3):296–310. doi: 10.1111/j.1461-0248.2007.01139.x.
  • Varga, S., and M.-M. Kytöviita. 2016. Faster acquisition of symbiotic partner by common mycorrhizal networks in early plant life stage. Ecosphere 7 (1):e01222, 1–13. doi: 10.1002/ecs2.1222.
  • Verma, P., A. N. Yadav, S. Kazy, B. Sing, V. S. Chauhan, and A. Suman. 2015. Plant growth promotion and mitigation of cold stress in inoculated wheat (Triticum aestivum L.) by K-solubilizing psychrotolerant Methylobacterium phyllosphaerae strain IARI-HHS2-67. International Conference on “Low Temperature Science and Biotechnological Advances”, National Bureau of Plant Genetic Resources (NBPGR-ICAR) Pusa Campus, New Delhi-110012. doi: 10.13140/RG.2.1.4885.1362.
  • Wachowska, U., W. Irzykowski, M. Jędryczka, A. D. Stasiulewicz-Paluch, and K. Głowacka. 2013. Biological control of winter wheat pathogens with the use of antagonistic Sphingomonas bacteria under greenhouse conditions. Biocontrol Science and Technology 23 (10):1110–1122. doi: 10.1080/09583157.2013.812185.
  • Wang, B., D. Funakoshi, Y. Dalpé, and C. Hamel. 2002. Phosphorus-32 absorption and translocation to host plants by arbuscular mycorrhizal fungi at low root-zone temperature. Mycorrhiza 12 (2):93–96. doi: 10.1007/s00572-001-0150-9.
  • Warren, G. J. 1998. Cold stress: Manipulating freezing tolerance in plants. Current Biology 8 (15):R514–516. doi: 10.1016/S0960-9822(07)00335-1.
  • Witter, L. D. 1961. Psychrophilic bacteria—a review. Journal of Dairy Science 44 (6):983–1015. doi: 10.3168/jds.S0022-0302(61)89851-2.
  • Wright, S. F., J. L. Starr, and I. C. Paltineanu. 1999. Changes in aggregate stability and concentration of glomalin during tillage management transition. Soil Science Society of America Journal 63 (6):1825–1829. doi: 10.2136/sssaj1999.6361825x.
  • Xiaochuang, C., Z. Chu, Z. Lianfeng, Z. Junhua, S. Hussain, W. Lianghuan, and J. Qianyu. 2017. Glycine increases cold tolerance in rice via the regulation of N uptake, physiological characteristics, and photosynthesis. Plant Physiology and Biochemistry 112:251–260. doi: 10.1016/j.plaphy.2017.01.008.
  • Yadav, A. N., P. Verma, V. Kumar, S. G. Sachan, and A. K. Saxena. 2017. Extreme cold environments: A suitable niche for selection of novel psychrotrophic microbes for biotechnological applications. Advances in Biotechnology and Microbiology 2 (2):555584, 1–4. doi: 10.19080/AIBM.2017.02.555584.
  • Yu, T.-F., Z.-S. Xu, J.-K. Guo, Y.-X. Wang, B. Abernathy, J.-D. Fu, X. Chen, Y.-B. Zhou, M. Chen, X.-G. Ye., et al. 2017. Improved drought tolerance in wheat plants overexpressing a synthetic bacterial cold shock protein gene. SeCspA 7:44050, 1–14. doi: 10.1038/srep44050.
  • Zaidi, A., and S. Khan. 2005. Interactive effect of rhizotrophic microorganisms on growth, yield, and nutrient uptake of wheat. Journal of Plant Nutrition 28 (12):2079–2092. doi: 10.1080/01904160500320897.
  • Zhang, W., H. Zhang, L. Ning, B. Li, and M. Bao. 2016. Quantitative proteomic analysis provides novel insights into cold stress responses in petunia seedlings. Frontiers in Plant Science 7:136, 1–13. doi: 10.3389/fpls.2016.00136.
  • Zhang, Y., S. Dong, Q. Gao, S. Liu, H. Ganjurjav, X. Wang, X. Su, and X. Wu. 2017. Soil bacterial and fungal diversity differently correlated with soil biochemistry in alpine grassland ecosystems in response to environmental changes. Scientific Reports 7:43077, 1–10. doi: 10.1038/srep43077.
  • Zhang, Z., J. Zhang, and Y. Huang. 2014. Effects of arbuscular mycorrhizal fungi on the drought tolerance of Cyclobalanopsis glauca seedlings under greenhouse conditions. New Forests 45 (4):545–556. doi: 10.1007/s11056-014-9417-9.
  • Zhou, Z., H. Ma, K. Liang, G. Huang, and K. Pinyopusarerk. 2012. Improved tolerance of teak (Tectona grandis L.f.) seedlings to low-temperature stress by the combined effect of arbuscular mycorrhiza and paclobutrazol. Journal of Plant Growth Regulation 31 (3):427–435. doi: 10.1007/s00344-011-9252-6.
  • Zhu, X.-C., F.-B. Song, and H.-W. Xu. 2010a. Arbuscular mycorrhizae improves low temperature stress in maize via alterations in host water status and photosynthesis. Plant and Soil 331 (1-2):129–137. doi: 10.1007/s11104-009-0239-z.
  • Zhu, X. C., F. B. Song, T. D. Liu, and S. Q. Liu. 2010b. Arbuscular mycorrhizae reducing water loss in maize plants under low temperature stress. Plant Signaling & Behavior 5 (5):591–593. doi: 10.4161/psb.11498.
  • Zhu, X., F. Song, and F. Liu. 2016. Altered amino acid profile of arbuscular mycorrhizal maize plants under low temperature stress. Journal of Plant Nutrition and Soil Science 179 (2):186–189. doi: 10.1002/jpln.201400165.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.