Abstract
Low-temperature stress can seriously impair plant physiology. Chilling injury leads to a complex array of cellular dysfunctions, and symptoms include chlorosis, sterility, loss of vigor, wilting, and even death of the plants. Furthermore, phosphorus limitations additionally halt the growth of plants. Low-temperature adaptive plant growth–promoting microbes through various direct and indirect mechanisms help in the survival of plants under stress conditions. The present investigation deals with isolation of P-solubilizing psychrotrophic bacteria from diverse cultivars of wheat grown in the Keylong region of Himachal Pradesh. A total of 33 P-solubilizing bacterial isolates were obtained. P-solubilizers were screened for different plant growth–promoting (PGP) attributes of K and Zn solubilization, production of IAA, siderophores, and different hydrolytic enzymes. Among 33 P-solubilizers, 8 efficient strains exhibiting multiple PGP attributes were used as bioinoculants for wheat under low-temperature stress in different in vitro and in vivo experiments. The psychrotrophic bacterial isolates positively influenced the growth and physiological parameters as well as nutrient uptake and yield of wheat and efficiently alleviated low-temperature stress. The potential of low-temperature stress adaptive and PGP microbes can be utilized in agricultural sector for amelioration of low-temperature stress and plant growth promotion. The present study deals with the isolation of psychrotrophic P-solubilizers with multiple PGP attributes and their role in alleviation of cold stress in wheat.
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References
Yadav AN, Sachan SG, Verma P, Saxena AK (2016) Bioprospecting of plant growth promoting psychrotrophic Bacilli from cold desert of north western Indian Himalayas. Indian J Exp Biol 54:142–150
Mishra PK, Bisht SC, Ruwari P, Selvakumar G, Joshi GK, Bisht JK et al (2011) Alleviation of cold stress in inoculated wheat (Triticum aestivum L.) seedlings with psychrotolerant Pseudomonads from NW Himalayas. Arch Microbiol 193:497–513. https://doi.org/10.1007/s00203-011-0693-x
Sharma P, Sharma N, Deswal R (2005) The molecular biology of the low-temperature response in plants. Bioessays 27:1048–1059. https://doi.org/10.1002/bies.20307
Subramanian P, Kim K, Krishnamoorthy R, Mageswari A, Selvakumar G, Sa T (2016) Cold stress tolerance in psychrotolerant soil bacteria and their conferred chilling resistance in tomato (Solanum lycopersicum Mill.) under low temperatures. PloS one 11:e0161592. https://doi.org/10.1371/journal.pone.0161592
Theocharis A, Clément C, Barka EA (2012) Physiological and molecular changes in plants grown at low temperatures. Planta 235:1091–1105. https://doi.org/10.1007/s00425-012-1641-y
Chen Y, Rekha P, Arun A, Shen F, Lai W-A, Young CC (2006) Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Appl Soil Ecol 34:33–41. https://doi.org/10.1016/j.apsoil.2005.12.002
Verma P, Yadav AN, Kazy SK, Saxena AK, Suman A (2014) Evaluating the diversity and phylogeny of plant growth promoting bacteria associated with wheat (Triticum aestivum) growing in central zone of India. Int J Curr Microbiol Appl Sci 3:432–447
Verma P, Yadav AN, Khannam KS, Kumar S, Saxena AK, Suman A (2016) Molecular diversity and multifarious plant growth promoting attributes of Bacilli associated with wheat (Triticum aestivum L.) rhizosphere from six diverse agro-ecological zones of India. J Basic Microbiol 56:44–58. https://doi.org/10.1002/jobm.201500459
Verma P, Yadav AN, Khannam KS, Panjiar N, Kumar S, Saxena AK et al (2015) Assessment of genetic diversity and plant growth promoting attributes of psychrotolerant bacteria allied with wheat (Triticum aestivum) from the northern hills zone of India. Ann Microbiol 65:1885–1899. https://doi.org/10.1007/s13213-014-1027-4
Yadav AN, Sachan SG, Verma P, Saxena AK (2015a) Prospecting cold deserts of north western Himalayas for microbial diversity and plant growth promoting attributes. J Biosci Bioeng 119:683–693. https://doi.org/10.1016/j.jbiosc.2014.11.006
Yadav AN, Sachan SG, Verma P, Tyagi SP, Kaushik R, Saxena AK (2015b) Culturable diversity and functional annotation of psychrotrophic bacteria from cold desert of Leh Ladakh (India). World J Microbiol Biotechnol 31:95–108. https://doi.org/10.1007/s11274-014-1768-z
Bhardwaj D, Ansari MW, Sahoo RK, Tuteja N (2014) Biofertilizers function as key player in sustainable agriculture by improving soil fertility, plant tolerance and crop productivity. Microb Cell Fact 13:1–10. https://doi.org/10.1186/1475-2859-13-66
Tapia-Vázquez I, Sánchez-Cruz R, Arroyo-Domínguez M, Lira-Ruan V, Sánchez-Reyes A, del Rayo S-CM et al (2020) Isolation and characterization of psychrophilic and psychrotolerant plant-growth promoting microorganisms from a high-altitude volcano crater in Mexico. Microbiol Res 232:126394. https://doi.org/10.1016/j.micres.2019.126394
Yadav AN, Rastegari AA, Yadav N (2020) Microbiomes of extreme environments: biodiversity and biotechnological applications. CRC Press, Taylor & Francis, Boca Raton, USA
Singh JS, Singh D (2013) Plant growth promoting rhizobacteria (PGPR): microbes in sustainable agriculture. In: Management of microbial resources in the environment. Springer, pp 361–385. https://doi.org/10.1007/978-94-007-5931-2_14
Naik K, Mishra S, Srichandan H, Singh PK, Sarangi PK (2019) Plant growth promoting microbes: potential link to sustainable agriculture and environment. Biocatal Agric Biotechnol 21:101326. https://doi.org/10.1016/j.bcab.2019.101326
Joshi A, Mishra B, Chatrath R, Ferrara GO, Singh RP (2007) Wheat improvement in India: present status, emerging challenges and future prospects. Euphytica 157:431–446. https://doi.org/10.1007/s10681-007-9385-7
Verma P, Yadav A, Kazy S, Saxena A, Suman A (2013) Elucidating the diversity and plant growth promoting attributes of wheat (Triticum aestivum) associated acidotolerant bacteria from southern hills zone of India. Natl J Life Sci 10:219–226
Pikovskaya R (1948) Mobilization of phosphorus in soil in connection with vital activity of some microbial species. Mikrobiologiya 17:362–370
Hu X, Chen J, Guo J (2006) Two phosphate-and potassium-solubilizing bacteria isolated from Tianmu Mountain, Zhejiang, China. World J Microbiol Biotechnol 22:983–990. https://doi.org/10.1007/s11274-006-9144-2
Saravanan VS, Subramoniam SR, Raj SA (2004) Assessing in vitro solubilization potential of different zinc solubilizing bacterial (zsb) isolates. Braz J Microbiol 35:121–125. https://doi.org/10.1590/S1517-83822004000100020
Bric JM, Bostock RM, Silverstone SE (1991) Rapid in situ assay for indoleacetic acid production by bacteria immobilized on a nitrocellulose membrane. Appl Environ Microbiol 57:535–538
Schwyn B, Neilands J (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56. https://doi.org/10.1016/0003-2697(87)90612-9
Cappucino JC, Sherman N (1992) Nitrogen cycle. In: Microbiology: A Laboratory Manual, 4th edn. Benjamin/Cumming Pub. Co., New York, pp 311–312
Castro G, Ferrero M, Méndez B, Sineriz F (1993) Screening and selection of bacteria with high amylolytic activity. Acta Biotechnol 13:197–201. https://doi.org/10.1002/abio.370130220
Zhou X, Chen H, Li Z (2004) CMCase activity assay as a method for cellulase adsorption analysis. Enzyme Microb Technol 35:455–459. https://doi.org/10.1016/j.enzmictec.2004.07.005
Kanekar P, Nilegaonkar S, Sarnaik S, Kelkar A (2002) Optimization of protease activity of alkaliphilic bacteria isolated from an alkaline lake in India. Biores Technol 85:87–93. https://doi.org/10.1016/S0960-8524(02)00018-4
Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36. https://doi.org/10.1080/00103624.2020.1729379
Elliott L, Lynch J (1984) Pseudomonads as a factor in the growth of winter wheat (Triticum aestivum L.). Soil Biol Biochem 16:69–71. https://doi.org/10.1016/0038-0717(84)90128-7
Bates L, Waldren R, Teare I (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207. https://doi.org/10.1007/BF00018060
Grieve C, Grattan S (1983) Rapid assay for determination of water soluble quaternary ammonium compounds. Plant Soil 70:303–307. https://doi.org/10.1007/BF02374789
Irigoyen J, Einerich D, Sánchez-Díaz M (1992) Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants. Physiol Plant 84:55–60. https://doi.org/10.1111/j.1399-3054.1992.tb08764.x
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198. https://doi.org/10.1016/0003-9861(68)90654-1
Dhindsa RS, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101
Smith IK, Vierheller TL, Thorne CA (1988) Assay of glutathione reductase in crude tissue homogenates using 5, 5′-dithiobis (2-nitrobenzoic acid). Anal Biochem 175:408–413. https://doi.org/10.1016/0003-2697(88)90564-7
Sharma P, Sheikh I, Singh D, Kumar S, Verma SK, Kumar R et al (2017) Uptake, distribution, and remobilization of iron and zinc among various tissues of wheat–Aegilops substitution lines at different growth stages. Acta Physiol Plant 39:185. https://doi.org/10.1007/s11738-017-2456-z
Kushwaha P, Kashyap PL, Kuppusamy P (2020) Microbes for cold stress resistance in plants: mechanism, opportunities, and challenges. In: Microbiological Advancements for Higher Altitude Agro-Ecosystems & Sustainability. Springer, pp 269–292. https://doi.org/10.1007/978-981-15-1902-4_14
Ruelland E, Zachowski A (2010) How plants sense temperature. Environ Exp Bot 69:225–232. https://doi.org/10.1016/j.envexpbot.2010.05.011
Vega-Celedón P, Bravo G, Velásquez A, Cid FP, Valenzuela M, Ramírez I et al (2021) Microbial diversity of psychrotolerant bacteria isolated from wild flora of Andes Mountains and Patagonia of Chile towards the selection of plant growth-promoting bacterial consortia to alleviate cold stress in plants. Microorganisms 9:538. https://doi.org/10.3390/microorganisms9030538
De Souza M-J, Nair S, Bharathi PL, Chandramohan D (2006) Metal and antibiotic-resistance in psychrotrophic bacteria from Antarctic Marine waters. Ecotoxicology 15:379–384. https://doi.org/10.1007/s10646-006-0068-2
Schloss PD, Allen HK, Klimowicz AK, Mlot C, Gross JA, Savengsuksa S et al (2010) Psychrotrophic strain of Janthinobacterium lividum from a cold Alaskan soil produces prodigiosin. DNA Cell Biol 29:533–541. https://doi.org/10.1089/dna.2010.1020
Maharana AK, Ray P (2013) Isolation and screening of cold active extracellular enzymes producing psychrotrophic bacteria from soil of Jammu City. Biosci Biotechnol Res Asia 10:267–273. https://doi.org/10.13005/BBRA/1120
Przemieniecki SW, Kurowski TP, Korzekwa K, Karwowska A (2014) The effect of psychrotrophic bacteria isolated from the root zone of winter wheat on selected biotic and abiotic factors. J Plant Prot Res 54:407–413. https://doi.org/10.2478/jppr-2014-0061
Mitra D, Anđelković S, Panneerselvam P, Senapati A, Vasić T, Ganeshamurthy A et al (2020) Phosphate-solubilizing microbes and biocontrol agent for plant nutrition and protection: current perspective. Commun Soil Sci Plant Anal 51:645–657
Uphoff N, Ball AS, Fernandes E, Herren H, Husson O, Laing M et al (2006) Biological approaches to sustainable soil systems. CRC Press, Taylor & Francis, Boca Raton, London, New York
Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 126:45–51. https://doi.org/10.1111/j.0031-9317.2005.00582.x
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930. https://doi.org/10.1016/j.plaphy.2010.08.016
Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216. https://doi.org/10.1016/j.envexpbot.2005.12.006
Siddique A, Kandpal G, Kumar P (2018) Proline accumulation and its defensive role under diverse stress condition in plants: an overview. J Pure Appl Microbiol 12:1655–1659. https://doi.org/10.22207/JPAM.12.3.73
Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino acids 35:753–759. https://doi.org/10.1007/s00726-008-0061-6
Forlani G, Trovato M, Funck D, Signorelli S (2019) Regulation of proline accumulation and its molecular and physiological functions in stress defence. In: Osmoprotectant-mediated abiotic stress tolerance in plants. Springer, pp 73–97. https://doi.org/10.1007/978-3-030-27423-8_3
Nayyar H, Chander K, Kumar S, Bains T (2005) Glycine betaine mitigates cold stress damage in chickpea. Agron Sustain Dev 25:381–388
Yuanyuan M, Yali Z, Jiang L, Hongbo S (2009) Roles of plant soluble sugars and their responses to plant cold stress. Afr J Biotechnol 8
Choudhury S, Panda P, Sahoo L, Panda SK (2013) Reactive oxygen species signaling in plants under abiotic stress. Plant Signal Behav 8:e23681. https://doi.org/10.4161/psb.23681
Aydin SS, Büyük I, Aras S (2013) Relationships among lipid peroxidation, SOD enzyme activity, and SOD gene expression profile in Lycopersicum esculentum L. exposed to cold stress. Genet Mol Res 12:3220–3229. https://doi.org/10.4238/2013
Kumar V, Yadav SK (2009) Proline and betaine provide protection to antioxidant and methylglyoxal detoxification systems during cold stress in Camellia sinensis (L.) O. Kuntze. Acta Physiol Plant 31:261–269. https://doi.org/10.1007/s11738-008-0227-6
Gill SS, Anjum NA, Hasanuzzaman M, Gill R, Trivedi DK, Ahmad I et al (2013) Glutathione and glutathione reductase: a boon in disguise for plant abiotic stress defense operations. Plant Physiol Biochem 70:204–212. https://doi.org/10.1016/j.plaphy.2013.05.032
Yousuf PY, Hakeem KUR, Chandna R, Ahmad P (2012) Role of glutathione reductase in plant abiotic stress. In: Abiotic stress responses in plants. Springer, pp 149–158. https://doi.org/10.1007/978-1-4614-0634-1_8
Tiryaki D, Aydın İ, Atıcı Ö (2019) Psychrotolerant bacteria isolated from the leaf apoplast of cold-adapted wild plants improve the cold resistance of bean (Phaseolus vulgaris L.) under low temperature. Cryobiology 86:111–119. https://doi.org/10.1016/j.cryobiol.2018.11.001
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 58:371–377. https://doi.org/10.1007/s00284-008-9339-x
Acknowledgements
The authors are grateful to Department of Biotechnology, Dr. Khem Singh Gill Akal College of Agriculture, Eternal University, Baru Sahib and the Department of Environment, Science & Technology (DEST), Shimla-funded project “Development of Microbial Consortium as Bio-inoculants for Drought and Low Temperature Growing Crops for Organic Farming in Himachal Pradesh” for providing the facilities, to undertake the investigations.
Funding
The Department of Environment, Science & Technology (DEST), Shimla-funded project “Development of Microbial Consortium as Bio-inoculants for Drought and Low Temperature Growing Crops for Organic Farming in Himachal Pradesh” provided financial support, to undertake the investigations.
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Kour, D., Yadav, A.N. Alleviation of cold stress in wheat with psychrotrophic phosphorus solubilizing Acinetobacter rhizosphaerae EU-KL44. Braz J Microbiol 54, 371–383 (2023). https://doi.org/10.1007/s42770-023-00913-7
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DOI: https://doi.org/10.1007/s42770-023-00913-7