Evaluation of Ice Nucleation Activity (INA) and INA Gene Detection in the Bacteria Isolated from Pistachio Trees in Kerman Province, Iran

Document Type: Research Article

Authors

1 Department of Plant Protection, Faculty of Agricultural Sciences and Food Industries, Science and Research Branch, Islamic Azad University, Tehran, Iran

2 Plant protection Department, Faculty of Agriculture, Vali- E- Asr University of Rafsanjan, Iran

3 Biotechnology Department, Institute of Science and High Technology and Environmental Sciences, Graduate University of Advanced Technology, Kerman, Iran

Abstract

IIce nucleation active (INA) bacteria are common epiphytic inhabitants that cause frost damage in many plants in the near-zero temperatures. Yet, no studies were found in ice nucleation bacteria associated with pistachio trees. In our earlier study some INA strains were identified and reported. These were assigned as Pseudomonas fragi, P. putida, P. moraviensis and Pantoea agglomerans. In current work, two new strains namely P. viridiflava and Entrobacter cloacea were identified. Their ice nucleation frequency were evaluated and compared with above-mentioned ice positive strains isolated from pistachio trees. Pseudomonas fragi raf3 was considered as the most ice nucleation active bacteria. This was followed by P. putida raf6, P. moraviensis raf1, P. moraviensis raf5, Pantoea agglomeranse raf7, P. viridiflava raf2, Entrobacter cloacea raf8 and Pseudomonas sp. raf4, respectively. To detect INA genes, two sets of degenerate primers were used and partial INA gene sequences were amplified. INA gene sequence) 425bp) for Pseudomonas putida raf6,  Pantoea agglomerans raf7 and P. fragi raf3 were amplified with primer pair of 3308/3463. Whereas, a fragment of 194bp was detected in Pseudomonas sp. raf4P. moraviensis raf5 and  P. moraviensis raf1using forward and reverse primer pair of 3076/3463. Entrobacter cloacea raf8 has reported for the first time as epiphytic ice plus strain. The capability of the latter as a bacterial biocontrol agent against insect pests was reported.

Keywords


Block W (2002) Interactions of water, ice nucleators and desiccation in invertebrate cold survival. European Journal of Entomology. 99(2), 259-266‏.

Burke MJ, Gusta LV, Quamme HA, Weiser CJ, Li PH (1976) Freezing and injury in plants. Annual Review of Plant Physiology. 27, 507-528.

Buttner MP, Amy PS (1989) Survival of ice nucleation-active and genetically engineered non-ice-nucleating Pseudomonas syringae strains after freezing. Applied and Environmental Microbiology. 55(7), 1690-1694.‏

Deininger CA, Mueller GM, Wolber PK (1987) Immunological characterization of ice nucleation proteins from Pseudomonas syringae, Pseudomonas fluorescens, and Erwinia herbicola. Journal of Bacteriology. 170(2), 669- 675.

Edwards AR, Van Den Bussche RA, Wichman HA, Orser CS (1994) Unusual pattern of bacterial ice nucleation gene evolution. Molecular Biology and Evolution. 11(6), 911-920.

Fahy PC, Persley GJ (20002) Plant Bacterial Diseases A Diagnostic Guide. Sydney, Australia. Academic Press. pp. 393. 337-375.

Hill TC, Moffett BF, DeMott PJ, Georgakopoulos DG, Stump WL, Franc GD (2014) Measurement of ice nucleation-active bacteria on plants and in precipitation by quantitative PCR. Applied and Environmental Microbiology. 80(4), 1256-1267.

Hirano SS, Nordheim EV, Arny DC, Upper CD (1982) Lognormal distribution of epiphytic bacterial populations on leaf surfaces. Applied and Environmental Microbiology. 44(3), 695-700.

 Hokmabadi H (2011) Pistachio frost damage in Iran and new methods of frost protection. In XIV GREMPA Meeting on Pistachios and Almonds Zaragoza: CIHEAM-IAMZ/FAO/AUA/TEI Kalamatas/NAGREF. pp. 71-78.‏

Karimi E (2017) Solid state fermentation effects on pistachio hulls antioxidant activities. Asia-Pacific Journal of Science and Technology. 15(5), 360-366.‏

Lagzian M, Latifi AM, Bassami MR, Mirzaei M (2014) An ice nucleation protein from Fusarium acuminatum: cloning, expression, biochemical characterization and computational modeling. Biotechnology letters. 36(10), 2043-2051.

Lindow SE, Arny DC, Upper CD (1982a) Bacterial ice nucleation: a factor in frost injury to plants. Plant Physiology. 70(4), 1084-1089.

Lindow SE, Hirano SS, Barchet WR, Arny DC, Upper CD (1982b) Relationship between ice nucleation frequency of bacteria and frost injury. Plant Physiology. 70(4), 1090-1093.

Lindow SE (1983) The role of bacterial ice nucleation in frost injury to plants. Annual Review of Phytopathology. 21, 363-384.

Lindow SE, Arny DC, Upper CD (1978) Distribution of ice nucleation-active bacteria on plants in nature. Applied and Environmental Microbiology. 36(6), 831-838.

Love J, Lesser W (1989)The Potential Impact of Ice-Minus Bacteria as a Frost Protestant in New York Tree Fruit Production. Northeastern Journal of Agricultural and Resource Economics. 18(1), 26-34.

Maki LR, Galyan EL, Chang-Chien MM, Caldwell DR (1974) Ice nucleation induced by Pseudomonas syringae.  Journal of Applied  Microbiology. 28(3), 456-459.‏

Maki LR, Willoughby Kj (1978) Bacteria as biogenic sources of freezing nuclei. Journal of Applied Meteorology. 17(7), 1049-1053.

Morris CE, Sands DC, Vanneste JL, Montarry J, Oakley B, Guilbaud C (2010).Inferring the evolutionary history of the plant pathogen Pseudomonas syringae from its biogeography in headwaters of rivers in North America, Europe and New Zealand. mBio. 1, 00107–10.

Mulet M, Lalucat J, García-Valdés E (2010) DNA sequence-based analysis of the Pseudomonas species. Environ Microbiol. 12, 1513–30.

Obata H, Muryoi N, Kawahara H, Yamade K, Nishikawa J (1999) Identification of a novel ice-nucleating bacterium of Antarctic origin and its ice nucleation properties. Cryobiology. 38(2), 131-139.

Parkinson N, Bryant R, Bew J, Elphinstone J (2011) Rapid phylogenetic identification of members of the Pseudomonas syringae species complex using the rpoD locus. Plant Pathology. 60(2), 338–344.

Rostami M, Hasanzadeh N, Khodaygan P, Riahi-Madvar A (2018) Ice nucleation active bacteria from pistachio in Kerman Province, Iran. Journal of Plant Pathology. 51-58.‏

Sarris PF, Trantas EA, Mpalantinaki E, Ververidis F, Goumas DE (2012) Pseudomonas viridiflava, a multi host plant pathogen with significant genetic variation at the molecular level. PloS One 7: e36090.

Schaad NW, Jones JB, Chun W (2001) Laboratory Guide for Identification of Plant Pathogenic Bacteria. 3rd ed. Saint Paul Minnesota. American phytopathological society (APS) Press. pp. 373.

Tang C, Sun F, Zhao T (2003) Construction of ice nucleation active Enterobacter cloacae for control of insect pests.  Chinese Science Bulletin. 48(2), 175-180.‏

 Vali G (1971) Quantitative evaluation of experimental results the heterogeneous freezing nucleation of supercooled liquids. Journal of the Atmospheric Sciences. 28(3), 402-409.

Varvaro L, Fabi A (1992) The role of ice nucleation active Pseudomonas viridiflava in frost injury to kiwifruit plants. Rivista di Patologia Vegetale. 85-90.‏

Watanabe K, Abe K, Sato M (2000) Biological control of an insect pest by gut‐colonizing Enterobacter cloacae transformed with ice nucleation gene. Journal of Applied Microbiology. 88(1), 90-97.

Weaver DJ (1978) Interaction of Pseudomonas syringae and freezing in bacterial canker on excised peach twigs. Phytopathology. 68(10), 1460-1463.‏

Wisniewski, M, Fuller M, Glenn DM, Palta J, Carter J, Gusta L, Duman J (2001) Factors involved in ice nucleation and propagation in plants: an overview based on new insights gained from the use of infrared thermography. Icelandic Agricultural Sciences. 14, 41-47.

Wolber PK, Warren GJ (2012) Evolutionary Perspective on the Ice Nucleation Gene-Encoded Membrane Protein. In: Andrews JH, Hirano SS (eds) Microbial Ecology of Leaves. Springer, New York.

Wowk B, Fahy GM (2002) Inhibition of bacterial ice nucleation by polyglycerol polymers. Cryobiology. 44(1), 14-23.

Yadav KK, Bora A, Datta S, Chandel K, Gogoi HK, Prasad  GBKS, Veer V (2015) Molecular characterization of midgut microbiota of Aedes albopictus and Aedes  aegypti from Arunachal Pradesh, India. Parasites Vectors. 8(1), 641-649.