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Inoculation with Lysinibacillus fusiformis Strain YJ4 and Lysinibacillus sphaericus Strain YJ5 Alleviates the Effects of Cold Stress in Maize Plants

Die Inokulation mit dem Lysinibacillus fusiformis-Stamm YJ4 und dem Lysinibacillus sphaericus-Stamm YJ5 mildert die Auswirkungen von Kältestress bei Maispflanzen

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Abstract

Low temperature is an important abiotic variable that inhibits plant growth and yield by restricting plant distribution on land. Cold-tolerant plant growth-promoting rhizobacteria (PGPR) improve nutrient absorption and availability in plants through biochemical and physiological mechanisms. Furthermore, they increase the tolerance of plants to cold stress. Different strains of bacteria were isolated from the roots of Suaeda nudiflora. These isolates were identified using 16SrDNA as Lysinibacillus fusiformis strain YJ4 and Lysinibacillus sphaericus strain YJ5 and were used to study their role in alleviating the harmful effect of cold stress. The two bacterial strains have the ability to solubilize phosphorus and to produce gluconic acid, phytohormones, catechol and hydroxymate siderophores. The present study aimed to study the effect of inoculating maize seeds with PGPR and its use to alleviate the adverse effects of cold stress. The results showed that cold stress (4 °C) reduces germination, growth criteria, photosynthetic pigments (i.e., chl a, chl b, and carotenoids), photosynthetic rate, membrane stability index, phytohormones (auxin and gibberellin), and mineral contents (N, P, K, and Ca) while increasing conductivity, malondialdehyde (MDA), lignin, cell viability, osmolytes (proline, glycine betaine, and soluble sugars), phenolic content, abscisic acid, 1‑aminocyclopropane-1-carboxylic acid (ACC) content and the antioxidant defense system in maize plants. Besides, the lignification, osmolytes, phenolic content, phytohormones, the enzymatic antioxidant defenses (i.e., superoxide dismutase, catalase, and phenylalanine ammonia-lyase), and mineral contents of maize plants increased after inoculation with L. fusiformis and L. sphaericus alone or in combination as compared to normal and cold stress conditions. In conclusion, the inoculation with L. fusiformis and L. sphaericus in maize plants induced resistance of osmotic and oxidative stress caused due to exposure to cold stress by upregulation of osmolytes, phenolics, phytohormones, and antioxidant enzymes. Also, L. sphaericus strains is more effective in tolerance to cold stress than L. fusiformis.

Zusammenfassung

Niedrige Temperaturen sind eine wichtige abiotische Variable, die das Pflanzenwachstum und den Ertrag hemmt, indem sie die Verteilung der Pflanzen auf dem Boden einschränkt. Kältetolerante pflanzenwachstumsfördernde Rhizobakterien (plant growth-promoting rhizobacteria, PGPR) verbessern die Nährstoffaufnahme und -verfügbarkeit in Pflanzen durch biochemische und physiologische Mechanismen. Außerdem erhöhen sie die Toleranz der Pflanzen gegenüber Kältestress. Verschiedene Bakterienstämme wurden aus den Wurzeln von Suaeda nudiflora isoliert. Diese Isolate wurden anhand der 16SrDNA als Lysinibacillus fusiformis-Stamm YJ4 und Lysinibacillus sphaericus-Stamm YJ5 identifiziert und zur Untersuchung ihrer Rolle bei der Abschwächung der schädlichen Auswirkungen von Kältestress verwendet. Die beiden Bakterienstämme sind in der Lage, Phosphor zu solubilisieren und Gluconsäure, Phytohormone, Catechin und Hydroxymat-Siderophore zu produzieren. Ziel der vorliegenden Studie war es, die Wirkung der Beimpfung von Maissaatgut mit PGPR und dessen Einsatz zur Abschwächung der negativen Auswirkungen von Kältestress zu untersuchen. Die Ergebnisse zeigten, dass Kältestress (4 °C) die Keimung, die Wachstumskriterien und die photosynthetischen Pigmente (Chl a, Chl b und Carotinoide), die Photosyntheserate, den Membranstabilitätsindex, die Phytohormone (Auxin und Gibberellin) und den Mineralstoffgehalt (N, P, K und Ca) reduziert, während die Leitfähigkeit, Malondialdehyd (MDA) Lignin, Zelllebensfähigkeit, Osmolyte (Prolin, Glycinbetain und lösliche Zucker), Phenolgehalt, Abscisinsäure, Gehalt an 1‑Aminocyclopropan-1-carbonsäure (ACC) und das antioxidative Abwehrsystem in Maispflanzen erhöht wurden. Außerdem stiegen die Lignifizierung, die Osmolyte, der Phenolgehalt, die Phytohormone, die enzymatische antioxidative Abwehr (d. h. Superoxid-Dismutase, Katalase und Phenylalanin-Ammoniak-Lyase) und der Mineralstoffgehalt der Maispflanzen nach der Inokulation mit L. fusiformis und L. sphaericus allein oder in Kombination im Vergleich zu normalen und Kältestressbedingungen. Zusammenfassend lässt sich sagen, dass die Inokulation mit L. fusiformis und L. sphaericus in Maispflanzen die Resistenz gegen osmotischen und oxidativen Stress, der durch Kältestress verursacht wird, durch die Hochregulierung von Osmolyten, Phenolen, Phytohormonen und antioxidativen Enzymen induziert. Außerdem sind die L. sphaericus-Stämme bei der Toleranz gegenüber Kältestress effektiver als L. fusiformis.

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References

  • Abd El-Rahman SS, Mohamed HI (2014) Application of benzothiadiazole and Trichoderma harzianum to control faba bean chocolate spot disease and their effect on some physiological and biochemical traits. Acta Physiol Plant 36(2):343–354

    Article  CAS  Google Scholar 

  • Abu-Shahba MS, Mansour MM, Mohamed HI, Sofy MR (2021) Comparative cultivation and biochemical analysis of iceberg lettuce grown in sand soil and hydroponics with or without microbubble and microbubble. J Soil Sci Plant Nutr 21:389–403

    Article  CAS  Google Scholar 

  • Alexander A, Singh VK, Mishra A, Jha B (2019) Plant growth promoting rhizobacterium Stenotrophomonas maltophilia BJ01 augments endurance against N2 starvation by modulating physiology and biochemical activities of Arachis hypogea. PLoS ONE 14(9):e222405

    Article  CAS  Google Scholar 

  • Aly AA, Mohamed HI, Mansour MTM, Omar MR (2013) Suppression of powdery mildew on flax by foliar application of essential oils. J Phytopathol l161:376–381

    Article  Google Scholar 

  • Aly AA, Mansour MTM, Mohamed HI (2017) Association of increase in some biochemical components with flax resistance to powdery mildew. Gesunde Pflanz 69(1):47–52

    Article  CAS  Google Scholar 

  • Ames BN (1966) Assay of inorganic phosphate, total phosphate and phosphatases. Methods Enzymol 8:115–118

    Article  CAS  Google Scholar 

  • Amna S, Sarfraz B, Din Y, Xia MA, Kamran MT, Javed TS, Chaudhary HJ (2019) Mechanistic elucidation of germination potential and growth of wheat inoculated with exopolysaccharide and ACC-deaminase producing bacillus strains under induced salinity stress. Eco Toxicol Environ Saf 183:109466

    Article  CAS  Google Scholar 

  • Anderson JT, Panetta AM, Mitchell-Olds T (2012) Evolutionary and ecological responses to anthropogenic climate change: update on anthropogenic climate change. Plant Physiol 160:1728–1740

    Article  CAS  Google Scholar 

  • Arbona V, Manzi M, Zandalinas SI, Vives-Peris V, Pérez-Clemente RM, Gómez-Cadenas A (2017) Physiological, metabolic and molecular responses of plants to abiotic stress. In stress signaling in plants. Genom Proteom Perspect 2:1–35

    Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts phenoloxidase in Beta vulgaris. Plant Physiol 24:1

    Article  CAS  Google Scholar 

  • Ashrostaghi T, Aliniaeifard S, Shomali A, Azizinia S, Abbasi Koohpalekani J, Moosavi-Nezhad M, Gruda NS (2022) Light Intensity: The Role Player in Cucumber Response to Cold Stress. Agronomy 12:201. https://doi.org/10.3390/agronomy12010201

    Article  CAS  Google Scholar 

  • Auh CK, Scandalios JG (1997) Spatial and temporal responses of the maize catalases to low temperature. Physiol Plant 101:149–156

    Article  CAS  Google Scholar 

  • Basit A, Shah ST, Ullah I, Muntha ST, Mohamed HI (2021) Microbe-assisted phytoremediation of environmental pollutants and energy recycling in sustainable agriculture. Arch Microbiol 203:5859–5885

    Article  CAS  Google Scholar 

  • Bates LS, Waldrfn RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Boinot M, Karakas E, Koehl K, Pagter M, Zuther E (2022) Cold stress and freezing tolerance negatively affect the fitness of Arabidopsis thaliana accessions under field and controlled conditions. Planta 255(2):1–8

    Article  Google Scholar 

  • Chandran H, Meena M, Swapnil P (2021) Plant growth-promoting rhizobacteria as a green alternative for sustainable agriculture. Sustainability 13:10986. https://doi.org/10.3390/su131910986

    Article  CAS  Google Scholar 

  • Costa MA, Pinheiro HA, Shimizu ES, Fonseca FT, dos Santos Filho BG, Moraes FK, de Figueiredo DM (2010) Lipid peroxidation, chloroplastic pigments and antioxidant strategies in Carapa guianensis (Aubl.) subjected to water-deficit and short-term rewetting. Trees 24(2):275–283

    Article  CAS  Google Scholar 

  • Damam M, Kaloori K, Gaddam B, Kausar R (2016) Plant growth promoting substances (phytohormones) produced by rhizobacterial strains isolated from the rhizosphere of medicinal plants. Int J Pharm Sci Rev 37:130–136

    CAS  Google Scholar 

  • Dey S, Biswas A, Huang S, Li D, Liu L, Deng Y, Xiao A, Birhanie ZM, Zhang J, Li J, Gong Y (2021) Low Temperature Effect on Different Varieties of Corchorus capsularis and Corchorus olitorius at Seedling Stage. Agronomy 11(12):2547

    Article  CAS  Google Scholar 

  • Dickerson DP, Pascholati SF, Hagerman AE, Butler LG, Nicholson RL (1984) Phenylalanine ammonia-lyase and hydroxycinnamate: CoA ligase in maize mesocotyls inoculated with Helminthosporium maydis or Helminthosporium carbonum. Physiol Plant Pathol 25(2):111–123

    Article  CAS  Google Scholar 

  • Ding S, Huang CL, Sheng HM, Song CL, Li YB, An LZ (2011) Effect of inoculation with the endophyte Clavibacter sp. strain Enf12 on chilling tolerance in Chorispora bungeana. Physiol Plant 141:141–151

    Article  CAS  Google Scholar 

  • El-Beltagi HS, Mohamed HI, Abdelazeem AS, Youssef R, Safwat G (2019) GC-MS analysis, antioxidant, antimicrobial and anticancer activities of extracts from Ficus sycomorus fruits and leaves. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 47(2):493–505

    Article  CAS  Google Scholar 

  • El-Mahdy OM, Mohamed HI, Mogazy AM (2021) Biosorption effect of Aspergillus niger and Penicillium chrysosporium for Cd and Pb contaminated soil and their physiological effects on Vicia faba L. Environ Sci Pollut Res 28(47):67608–67631

    Article  CAS  Google Scholar 

  • Fernandez O, Vandesteene L, Feil R, Baillieul F, Lunn JE, Clément C (2012) Trehalose metabolism is activated upon chilling in grapevine and might participate in Burkholderia phytofirmans induced chilling tolerance. Planta 236(2):355–369

    Article  CAS  Google Scholar 

  • Galluzzi L, Vitale I, Aaronson S (2018) Molecular mechanisms of cell death: recommendations of the Nomenclature Committee on Cell Death. Cell Death Differ 25:486–541

    Article  Google Scholar 

  • Gao J, Wang H, Yuan Q, Feng Y (2018) Structure and function of the photosystem supercomplexes. Front Plant Sci 9:357

    Article  Google Scholar 

  • Ghonaim MM, Mohamed HI, Omran AAA (2021) Evaluation of wheat salt stress tolerance using physiological parameters and retrotransposon-based markers. Genet Resour Crop Evol 68:227–242

    Article  CAS  Google Scholar 

  • Grieve CM, Grattan SR (1983) Rapid assay for determination of water soluble quaternary ammonium compounds. Plant Soil 70:303–307

    Article  CAS  Google Scholar 

  • Hassan MA, Xiang C, Farooq M, Muhammad N, Yan Z, Hui X, Yuanyuan K, Bruno AK, Lele Z, Jincai L (2021) Cold stress in wheat: plant acclimation responses and management strategies. Front Plant Sci 12:676884. https://doi.org/10.3389/fpls.2021.676884

    Article  Google Scholar 

  • Helmi A, Mohamed HI (2016) Biochemical and ultrastructural changes of some tomato cultivars to infestation with Aphis gossypii Glover (Hemiptera: Aphididae) at Qalyubiya, Egypt. Gesunde Pflanz 68:41–50

    Article  CAS  Google Scholar 

  • Holbrook A, Edge W, Bailey F (1961) Spectrophotometric method for determination of gibberellic acid. Adv Chem Ser 28:159–167

    Article  Google Scholar 

  • Hussain HA, Hussain S, Khaliq A, Ashraf U, Anjum SA, Men S, Wang L (2018) Chilling and drought stresses in crop plants: implications, cross talk, and potential management opportunities. Front Plant Sci 9:393. https://doi.org/10.3389/fpls.2018.00393

    Article  Google Scholar 

  • Hussain HA, Shengnan M, Hussain S, Ashraf U, Zhang Q, Anjum SA, Ali I, Wang L (2019) Individual and concurrent effects of drought and chilling stresses on morpho-physiological characteristics and oxidative metabolism of maize cultivars. BioRxiv 829309

    Book  Google Scholar 

  • Hussain T, KhanA A, Mohamed HI (2022) Potential efficacy of biofilm-forming biosurfactant Bacillus firmus HussainT-Lab.66 against Rhizoctonia solani and mass spectrometry analysis of their metabolites. Int J Peptide Res Therap 28:3. https://doi.org/10.1007/s10989-021-10318-5

    Article  CAS  Google Scholar 

  • Irigoyen JJ, Emerich DW, Sa’nchez-Dı’az M (1992) Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants. Physiol Plant 84:67–72

    Article  CAS  Google Scholar 

  • Jha Y (2017a) Potassium mobilizing bacteria: enhance potassium intake in paddy to regulate membrane permeability and accumulate carbohydrates under salinity stress. Braz J Bio Sci 4(8):333–344

    Article  Google Scholar 

  • Jha Y (2017b) Cell water content and lignification in maize regulated by rhizobacteria under salinity. Braz J Bio Sci 4(7):9–18

    Article  Google Scholar 

  • Jha Y (2019a) Endophytic bacteria as a modern tool for sustainable crop management under stress. In: Giri B, Prasad R, Wu QS, Varma A (eds) Biofertilizers for sustainable agriculture and environment. Soil Biology, vol 55. Springer, Cham

    Chapter  Google Scholar 

  • Jha Y (2019b) Endophytic bacteria-mediated regulation of secondary metabolites for the growth induction in Hyptis suaveolens under stress. In: Egamberdieva D, Tiezzi A (eds) Medically important plant biomes: source of secondary metabolites. Microorganisms for Sustainability, vol 15. Springer, Singapore

    Google Scholar 

  • Jha Y (2019c) Higher induction of defense enzymes and cell wall reinforcement in maize by root associated bacteria for better protection against Aspergillus niger. J Plant Prot Res 59(3):341–349

    CAS  Google Scholar 

  • Jha Y, Subramanian RB (2011) Endophytic pseudomonas pseudoalcaligenes shows better response against the Magnaporthe grisea than a rhizospheric Bacillus pumilus in Oryza sativa (Rice). Arch Phytopathol Plant Protect 44:592–604

    Article  Google Scholar 

  • Jha Y, Subramanian RB (2015) Reduced cell death and improved cell membrane integrity in rice under salinity by root associated bacteria. Theor Exp Plant Phys 3:227–235

    Article  Google Scholar 

  • Jha Y, Subramanian RB (2018) From interaction to gene induction: an Eco-friendly mechanism of PGPR-mediated stress management in the plant. In: Egamberdieva D, Ahmad P (eds) Plant microbiome: stress response. Microorganisms for sustainability, vol 5. Springer, Singapore

    Google Scholar 

  • Jha Y, Subramanian RB, Patel S (2011) Combination of endophytic and rhizospheric plant growth promoting rhizobacteria in Oryza sativa shows higher accumulation of osmoprotectant against saline stress. Acta Physiol Plant 33:797–802

    Article  Google Scholar 

  • Jha Y, Subramanian RB, Patel S (2012) Endophytic bacteria induced enzymes against M. grisea in O. sativa under biotic stress. Afr J Basic Appl Sci 3(4):136–146

    Google Scholar 

  • Jha Y, Subramanian RB, Patel N, Jithwa R (2014) Identification of plant growth promoting rhizobacteria from Suaeda nudiflora plant and its effect on maize. Ind J Plant Protect 42(4):422–429

    Google Scholar 

  • Jha Y, Kulkarni A, Subramanian RB (2021) Psychrotrophic soil microbes and their role in alleviation of cold stress in plants. In: Yadav AN (ed) Soil microbiomes for sustainable agriculture. Sustainable Development and Biodiversity, vol 27. Springer, Cham

    Chapter  Google Scholar 

  • Jha Y, Dehury B, Kumar SPJ, Chaurasia A, Singh UB, Yadav MK, Angadi UB, Ranjan R, Tripathy M, Subramanian RB, Kumar S, Simal-Gandara J (2022) Delineation of molecular interactions of plant growth promoting bacteria induced β‑1,3‑glucanases and guanosine triphosphate ligand for antifungal response in rice: a molecular dynamics approach. Mol Biol Rep 49:2579–2589

    Article  CAS  Google Scholar 

  • Kamble PN, Giri SP, Mane RS, Tiwana A (2015) Estimation of Chlorophyll content in young and adult leaves of some selected plants. Universal J Environ Res Technol 5(6):306–310

    CAS  Google Scholar 

  • Kamnev A, Shchelochkov A, Perfiliev YD, Tarantilis PA, Polissiou MG (2001) Spectroscopic investigation of indole-3-acetic acid interaction with iron(III). J Mol Struct 563:565–572

    Article  Google Scholar 

  • Karabudak T, Bor M, Özdemir F, Türkan İ (2014) Glycine betaine protects tomato (Solanum lycopersicum) plants at low temperature by inducing fatty acid desaturase 7 and lipoxygenase gene expression. Mol Biol Rep 41:1401–1410

    Article  CAS  Google Scholar 

  • Kong X, Wei B, Gao Z, Zhou Y, Shi F, Zhou X, Zhou Q, Ji S (2018) Changes in membrane lipid composition and function accompanying chilling injury in bell peppers. Plant Cell Physiol 59(1):167–178

    Article  CAS  Google Scholar 

  • Kour D, Rana KL, Kaur T, Sheikh I, Yadav AN, Kumar V (2020) Microbe-mediated alleviation of drought stress and acquisition of phosphorus in great millet (Sorghum bicolor L.) by drought-adaptive and phosphorus-solubilizing microbes. Biocatal Agric Biotechnol 23:101501

    Article  Google Scholar 

  • Kova’cik J, Klejdus B (2008) Dynamics of phenolic acids and ˇ lignin accumulation in metal-treated Matricaria chamomilla roots. Plant Cell Rep 27(3):605–615

    Article  Google Scholar 

  • Li H, Luo W, Ji R, Xu Y, Xu G, Qiu S, Tang H (2021) A comparative proteomic study of cold responses in potato leaves. Heliyon 7(2):e6002

    Article  CAS  Google Scholar 

  • Liu W, Yu K, He T, Li F, Zhang D, Liu J (2013) The low temperature induced physiological responses of Avena nuda L., a cold-tolerant plant species. Sci World J. https://doi.org/10.1155/2013/658793

    Article  Google Scholar 

  • Materán M, Fernandez M, Valenzuela S, Sáez K, Seeman P, Sánchez-Olate M, Ríos D (2009) Abscisic acid and 3‑indolacetic acid levels during the reinvigoration process of Pinus radiata D. Don adult material. Plant Growth Regul 59:171–177

    Article  Google Scholar 

  • Mayer JM, Abdallah MA (1978) The fluorescent pigment of Pseudomonas fluorescens biosynthesis, purification and physicochemical properties. J Gen Microbiol 107:319–332

    Article  Google Scholar 

  • Mesa T, Polo J, Arabia A, Caselles V, Munné-Bosch S (2022) Differential physiological response to heat and cold stress of tomato plants and its implication on fruit quality. J Plant Physiol 268:153581

    Article  CAS  Google Scholar 

  • Mohamed HI, Abdel-Hamid AME (2013) Molecular and biochemical studies for heat tolerance on four cotton genotypes (Gossypium hirsutum L.). Romanian Biotechnol Lett 18(6):7223–7231

    Google Scholar 

  • Mohamed HI, Gomaa EZ (2012) Effect of plant growth promoting Bacillus subtilis and Pseudomonas fluorescens on growth and pigment composition of radish plants (Raphanus sativus) under NaCl stress. Photosynthetica 50(2):263–272

    Article  CAS  Google Scholar 

  • Mohamed HI, Hameed A‑EAG (2014) Molecular and biochemical markers of some Vicia faba L. genotype in response to storage insect pests infestation. J Plant Int 9(1):618–626

    CAS  Google Scholar 

  • Mohamed HI, Elsherbiny EA, Abdelhamid MT (2016) Physiological and biochemical responses of Vicia faba plants to foliar application with zinc and iron. Gesunde Pflanz 68:201–212

    Article  CAS  Google Scholar 

  • Mohamed HI, Ashry NA, Ghonaim MM (2019) Physiological analysis for heat shock induced biochemical (responsive) compounds and molecular characterizations of ESTs expressed for heat tolerance in some Egyptian maize hybrids. Gesunde Pflanz 71:213–222

    Article  CAS  Google Scholar 

  • Moustafa-Farag M, Mohamed HI, Mahmoud A, Elkelish A, Misra AN, Guy KM, Kamran M, Ai S, Zhang M (2020) Salicylic acid stimulates antioxidant defense and osmolyte metabolism to alleviate oxidative stress in watermelons under excess boron. Plants 9(6):724

    Article  CAS  Google Scholar 

  • Naeem M, Basit A, Ahmad I, Mohamed HI, Wasila H (2020) Effect of salicylic acid and salinity stress on the performance of tomato. Gesunde Pflanz 72:393–402

    Article  CAS  Google Scholar 

  • Penrose DM, Barbara M, Glick BR (2001) Determination of ACC to assess the effect of ACC-deaminase-containing bacteria on roots of canola seedlings. Can J Microbiol 47:77–80

    Article  CAS  Google Scholar 

  • Pradhan N, Sukla LB (2005) Solubilization of inorganic phosphates by fungi isolated from agriculture soil. African J Biotechnol 5(10):850–854

    Google Scholar 

  • Rajawat MVS, Singh R, Singh D, Yadav AN, Singh S, Kumar M (2020) Spatial distribution and identification of bacteria in stressed environments capable to weather potassium aluminosilicate mineral. Braz J Microbiol 51:751–764

    Article  CAS  Google Scholar 

  • Ramalingam R, In-Jung L (2013) Ameliorative effects of spermine against osmotic stress through antioxidants and abscisic acid changes in soybean pods and seeds. Acta Physiol Plant 35:263–269

    Article  Google Scholar 

  • Rao KVM, Sresty TVS (2000) Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan L Millspaugh) in response to Zn and Ni stresses. Plant Sci 157:113–128

    Article  Google Scholar 

  • Rejeb BK, Abdelly C, Savouré A (2014) How reactive oxygen species and proline face stress together. Plant Physiol Biochem 80:278–284

    Article  Google Scholar 

  • Rioux C, Jordan DC, Rattray JB (1983) Colorimetric determination of catechol siderophores in microbial cultures. Anal Biochem 133(1):163–169

    Article  CAS  Google Scholar 

  • Ritonga FN, Chen S (2020) Physiological and molecular mechanism involved in cold stress tolerance in plants. Plants 9:560. https://doi.org/10.3390/plants9050560

    Article  CAS  Google Scholar 

  • Sanevas N, Sunohara Y, Matsumoto H (2007) Characterization of reactive oxygen species-involved oxidative damage in Hapalosiphon species crude extract-treated wheat and onion roots. Weed Biol Mana 7:172–177

    Article  CAS  Google Scholar 

  • Santoyo G, Moreno-Hagelsieb G, del Carmen Orozco-Mosqueda M, Glick BR (2016) Plant growth-promoting bacterial endophytes. Microbiol Rese 183:92–99

    Article  CAS  Google Scholar 

  • Santoyo G, Urtis-Flores CA, Loeza-Lara PD, Orozco-Mosqueda MDC, Glick BR (2021) Rhizosphere colonization determinants by plant growth-promoting rhizobacteria (PGPR). Biology 10:475

    Article  CAS  Google Scholar 

  • Shahidi F, Wanasundara PKJPD (1992) Phenolic antioxidants. Crit Rev Food Sci Nutr 32:67–103

    Article  CAS  Google Scholar 

  • Singh A, Kumar R, Yadav AN, Mishra S, Sachan S, Sachan SG (2020) Tiny microbes, big yields: microorganisms for enhancing food crop production sustainable development. In: Rastegari AA, Yadav AN, Yadav N (eds) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspectives. Elsevier, Amsterdam, pp 1–15

    Google Scholar 

  • Skyba M, Petijová L, Košuth J, Koleva DP, Ganeva TG, Kapchina-Toteva VM, Cellárová E (2012) Oxidative stress and antioxidant response in Hypericum perforatum L. plants subjected to low temperature treatment. J Plant Physiol 169:955–964

    Article  CAS  Google Scholar 

  • Sofy MR, Aboseidah AA, Heneidak SA, Ahmed HR (2021a) ACC deaminase containing endophytic bacteria ameliorate salt stress in Pisum sativum through reduced oxidative damage and induction of antioxidative defense systems. Environ Sci Pollut Res 28(30):40971–40991

    Article  CAS  Google Scholar 

  • Sofy AR, Sofy MR, Hmed AA, Dawoud RA, Refaey EE, Mohamed HI, El-Dougdoug NK (2021b) Molecular characterization of the Alfalfa mosaic virus infecting Solanum melongena in Egypt and control of its deleterious effects with melatonin and salicylic acid. Plants 10(3):459. https://doi.org/10.3390/plants10030459

    Article  CAS  Google Scholar 

  • Su F, Jacquard C, Villaume S, Michel J, Rabenoelina F, Clément C, Barka EA, Dhondt-Cordelier S, Vaillant-Gaveau N (2015) Burkholderia phytofirmans PsJN reduces impact of freezing temperatures on photosynthesis in Arabidopsis thaliana. Front Plant Sci 6:810

    Article  Google Scholar 

  • Subramanian P, Mageswari A, Kim K, Lee Y, Sa T (2015) Psychrotolerant endophytic Pseudomonas sp. strains OB155 and OS261 induced chilling resistance in tomato plants (Solanum lycopersicum Mill.) by activation of their antioxidant capacity. Mol Plant-microbe Int 28(10):1073–1081

    Article  CAS  Google Scholar 

  • 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(8):e161592

    Article  Google Scholar 

  • Sullivan C, Ross WM (1979) Selecting for drought and heatresistance sorghum. In: Mussell H, Taples T (eds) Stress physiology in crops plants. John Willey and Sons, USA, pp 264–281

    Google Scholar 

  • Szechyńska-Hebda M, Hebda M, Mirek M (2016) Cold-induced changes in cell wall stability determine the resistance of winter triticale to fungal pathogen Microdochium nivale. J Therm Anal Calorim 126:77–90

    Article  Google Scholar 

  • Takahashi D, Gorka M, Erban A, Graf A, Kopka J, Zuther E, Hincha DK (2019) Both cold and sub-zero acclimation induce cell wall modification and changes in the extracellular proteome in Arabidopsis thaliana. Sci Rep 9:2289

    Article  Google Scholar 

  • Theocharis A, Bordiec S, Fernandez O, Paquis S, Dhondt-Cordelier S, Baillieul F, Clément C, Barka EA (2012) Burkholderia phytofirmans PsJN primes Vitis vinifera L. and confers a better tolerance to low nonfreezing temperatures. Mol Plant Microbe Int 25(2):241–249

    Article  CAS  Google Scholar 

  • Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599

    Article  CAS  Google Scholar 

  • Tiwari S, Prasad V, Chauhan PS, Lata C (2017) Bacillus amyloliquefaciens confers tolerance to various abiotic stresses and modulates plant response to phytohormones through osmoprotection and gene expression regulation in rice. Front Plant Sci 8:1510

    Article  Google Scholar 

  • Vaishnav A, Varma A, Tuteja N, Choudhary DK (2016) PGPR-mediated amelioration of crops under salt stress. In: Plant-Microbe Interaction: an approach to sustainable agriculture. Springer, Singapore, pp 205–226

    Chapter  Google Scholar 

  • Vijayraghavan V, Soole K (2010) Effect of short- and long-term phosphate stress on the non-phosphorylating pathway of mitochondrial electron transport in Arabidopsis thaliana. Funct Plant Biol 37:455–466

    Article  CAS  Google Scholar 

  • Welcher FJ (1958) The analytical uses of ethylene diamine tetraacetic acid (EDTA). D. Van Nostrand company, New Jersey

    Google Scholar 

  • Whitelaw MA, Harden TJ, Helyar KR (1999) Phosphate solubilisation in solution culture by the soil fungus Penicillium radicum. Soil Biol Biochem 31:655–665

    Article  CAS  Google Scholar 

  • Wijewardana C, Henry WB, Hock MW, Reddy KR (2016) Growth and physiological trait variation among corn hybrids for cold tolerance. Can J Plant Sci 96:639–656

    Article  CAS  Google Scholar 

  • Xu SC, Li YP, Jin H, Guan YJ, Zheng YY, Zhu SJ (2010) Responses of antioxidant enzymes to chilling stress in tobacco seedlings. Agri Sci China 9(11):1594–1601

    Article  CAS  Google Scholar 

  • Zhou R, Hyldgaard B, Yu X, Rosenqvist E, Ugarte RM, Yu S, Wu Z, Ottosen CO, Zhao T (2018) Phenotyping of faba beans (Vicia faba L.) under cold and heat stresses using chlorophyll fluorescence. Euphytica 214:68

    Article  Google Scholar 

  • Zubair M, Hanif A, Farzand A, Sheikh TM, Khan AR, Suleman M, Ayaz M, Gao X (2019) Genetic screening and expression analysis of psychrophilic Bacillus spp. reveal their potential to alleviate cold stress and modulate phytohormones in wheat. Microorganisms 7:337. https://doi.org/10.3390/microorganisms7090337

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. N. V. Patel College of Pure & Applied Sciences, S. P. University, V.V. Nagar, Anand (Gujarat), India

    Yachana Jha

  2. Biological and Geological Science Department, Faculty of Education, Ain Shams University, 11566, Cairo, Egypt

    Heba I. Mohamed

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  1. Yachana Jha
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  2. Heba I. Mohamed
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Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Yachana Jhaand Heba I. Mohamed. The first draft of the manuscript was written by Yachana Jha and Heba I. Mohamed and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Heba I. Mohamed.

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Y. Jha and H.I. Mohamed declare that they have no competing interests.

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Jha, Y., Mohamed, H.I. Inoculation with Lysinibacillus fusiformis Strain YJ4 and Lysinibacillus sphaericus Strain YJ5 Alleviates the Effects of Cold Stress in Maize Plants. Gesunde Pflanzen 75, 77–95 (2023). https://doi.org/10.1007/s10343-022-00666-7

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  • DOI: https://doi.org/10.1007/s10343-022-00666-7

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