Alleviation of salt stress in winter wheat by Pantoea spp. endophytes isolated from spontaneous desert plants of the Sahara

References

• Arnold AE, Mejía LC, Kyllo D, Rojas EI, Maynard Z, Robbins N, Herre EA. 2003. Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci U S A. 100(26):15649–15654.
   PubMed Web of Science ®Google Scholar
• Asif MA, Pearson AS, Schilling RK, Roy SJ. 2018. Opportunities for developing salt-tolerant wheat and barley varieties. Annu Rev Plant Biol. 2:157–218.
   Google Scholar
• Bashan Y, De-Bashan LE. 2010. Chapter two: How the plant growth-promoting bacterium Azospirillum promotes plant growth—a critical assessment. Adv Agron. 108:77–136.
   Web of Science ®Google Scholar
• Ben Ahmed C, Ben Rouina B, Sensoy S, Boukhriss M, Ben Abdullah F. 2010. Exogenous proline effects on photosynthetic performance and antioxidant defense system of young olive tree. J Agric Food Chem. 58(7):4216–4222.
   PubMed Web of Science ®Google Scholar
• Bernstein N, Sela Saldinger S, Dudai N, Gorbatsevich E. 2017. Salinity stress does not affect root uptake, dissemination and persistence of salmonella in sweet-basil (Ocimum basilicum). Front Plant Sci. 2(8):675.
   Web of Science ®Google Scholar
• Bhise KK, Dandge PB. 2019. Alleviation of salinity stress in rice plant by encapsulated salt tolerant plant growth-promoting bacteria Pantoea agglomerans strain KL and its root colonization ability. Arch Agron Soil Sci. 65(14):1955–1968.
   Web of Science ®Google Scholar
• Bowyer C, Withana S, Fenn I, Bassi S, Lewis M, Cooper T, Benito P, Mudgal S. 2009. Land Degradation and Desertification Policy Department Economic and Scientific Policy IP/A/ENVI/ST/2008-23. Brussel, Belgium.
   Google Scholar
• Brady CL, Cleenwerck I, Venter SN, Engelbeen K, De Vos P, Coutinho TA. 2010. Emended description of the genus Pantoea, description of four species from human clinical samples, Pantoea septica sp. nov., Pantoea eucrina sp. nov., Pantoea brenneri sp. nov. and Pantoea conspicua sp. nov., and transfer of Pectobacterium cypripedii (Hor. Int J Syst Evol Microbiol. 60(Pt 10):2430–2440.
   PubMed Web of Science ®Google Scholar
• Brady C, Cleenwerck I, Venter S, Vancanneyt M, Swings J, Coutinho T. 2008. Phylogeny and identification of Pantoea species associated with plants, humans and the natural environment based on multilocus sequence analysis (MLSA). Syst Appl Microbiol. 31(6-8):447–460.
   PubMed Web of Science ®Google Scholar
• Brown VI, Lowbury EJ. 1965. Use of an improved cetrimide agar medium and other culture methods for Pseudomonas aeruginosa. J Clin Pathol. 18(6):752–756.
   PubMed Web of Science ®Google Scholar
• Chen C, Xin K, Liu H, Cheng J, Shen X, Wang Y, Zhang L. 2017. Pantoea alhagi, a novel endophytic bacterium with ability to improve growth and drought tolerance in wheat. Sci Rep. 7(1):41564.
   PubMed Web of Science ®Google Scholar
• Cherif-Silini H, Thissera B, Bouket AC, Saadaoui N, Silini A, Eshelli M, Alenezi FN, Vallat A, Luptakova L, Yahiaoui B, et al. 2019. Durum wheat stress tolerance induced by endophyte Pantoea agglomerans with genes contributing to plant functions and secondary metabolite Arsenal. IJMS. 20(16):3989.
   Web of Science ®Google Scholar
• Coleman-Derr D, Tringe SG. 2014. Building the crops of tomorrow: advantages of symbiont-based approaches to improving abiotic stress tolerance. Front Microbiol. 5:283.
   PubMed Web of Science ®Google Scholar
• Debez A, Chaibi W, Bouzid S. 2001. Effect du NaCl et de regulatoeurs de croissance sur la germination d’Atriplex halimus L. Cah Agric. 10:135–138.
   Google Scholar
• Del Amor FM, Cuadra-Crespo P. 2012. Plant growth-promoting bacteria as a tool to improve salinity tolerance in sweet pepper. Funct Plant Biol. 39(1):82–90.
   PubMed Web of Science ®Google Scholar
• Dias MP, Bastos MS, Xavier VB, Cassel E, Astarita LV, Santarém ER. 2017. Plant growth and resistance promoted by Streptomyces spp. in tomato. Plant Physiol Biochem. 118:479–493.
   PubMed Web of Science ®Google Scholar
• Dutkiewicz J, Mackiewicz B, Lemieszek MK, Golec M, Milanowski J. 2016a. Pantoea agglomerans: a mysterious bacterium of evil and good. Part IV. Beneficial effects. Ann Agric Environ Med. 23(2):206–222.
   PubMed Web of Science ®Google Scholar
• Dutkiewicz J, Mackiewicz B, Lemieszek MK, Golec M, Milanowski J. 2016b. Pantoea agglomerans: a mysterious bacterium of evil and good. Part III. Deleterious effects: infections of humans, animals and plants. Ann Agric Environ Med. 23(2):197–205.
   PubMed Web of Science ®Google Scholar
• Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32(5):1792–1797.
   PubMed Web of Science ®Google Scholar
• Edwards U, Rogall T, Blöcker H, Emde M, Böttger EC. 1989. Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res. 17(19):7843–7853.
   PubMed Web of Science ®Google Scholar
• Egamberdieva D. 2009. Alleviation of salt stress by plant growth regulators and IAA producing bacteria in wheat. Acta Physiol Plant. 31(4):861–864.
   Web of Science ®Google Scholar
• Felsenstein J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution. ). 39(4):783–791.
   PubMed Web of Science ®Google Scholar
• Frankenberger WTJ, Arshad M. 1995. Phytohormones in soils. Microbial production and function. New York: Marcel Dekker.
   Google Scholar
• Gavini F, Mergaert J, Beji A, Mielcarek C, Izard D, Kersters K, De Ley J. 1989. Transfer of Enterobacter agglomerans (Beijerinck 1888) Ewing and Fife 1972 to Pantoea gen. nov. as Pantoea agglomerans comb. nov. and description of Pantoea dispersa sp. nov. Int J Syst Bacteriol. 39(3):337–345.
   Google Scholar
• Ghatak A, Chaturvedi P, Weckwerth W. 2017. Cereal crop proteomics: systemic analysis of crop drought stress responses towards marker-assisted selection breeding. Front Plant Sci. 2(8):757.
   Web of Science ®Google Scholar
• Gond SK, Torres MS, Bergen MS, Helsel Z, White JF. 2015. Induction of salt tolerance and up-regulation of aquaporin genes in tropical corn by rhizobacterium Pantoea agglomerans. Lett Appl Microbiol. 60(4):392–399.
   PubMed Web of Science ®Google Scholar
• Hu XJ, Li ZJ, Cao YC, Zhang J, Gong YX, Yang YF. 2010. Isolation and identification of a phosphate-solubilizing bacterium Pantoea stewartii subsp. stewartii g6, and effects of temperature, salinity, and pH on its growth under indoor culture conditions. Aquacult Int. 18(6):1079–1091.
   Web of Science ®Google Scholar
• Husen E. 2016. Screening of soil bacteria for plant growth promotion activities in vitro. Indones J Agric Sci. 4(1):27–31.
   Google Scholar
• Jamil M, Lee D, Jung K, Ashraf M, Lee S, Rhal E. 2006. Effect of salt (NaCl) stress on germination and early seedling growth of four vegetables species. Cent Eur Agric. 7:273–282.
   Google Scholar
• Khalid A, Arshad M, Zahir ZA. 2004. Screening plant growth-promoting rhizobacteria for improving growth and yield of wheat. J Appl Microbiol. 96(3):473–480.
   PubMed Web of Science ®Google Scholar
• Kharbikar LL, Nandanwar SK, Shanware AS, Yele YM, Sivalingam PN, Kaushal P, Kumar J. 2018. Microbe-mediated salinity tolerance in plants. Nature Portfolio Microbiology Community. 15 Mars 2018. https://microbiologycommunity.nature.com/posts/31111-microbe-mediated-salinity-tolerance-in-plants.
   Google Scholar
• Kong Z, Glick BR. 2017. The role of plant growth-promoting bacteria in metal phytoremediation. Adv Microb Physiol. 71:97–132.
   PubMed Web of Science ®Google Scholar
• Krishnan N, Dickman MB, Becker DF. 2008. Proline modulates the intracellular redox environment and protects mammalian cells against oxidative stress. Free Radic Biol Med. 44(4):671–681.
   PubMed Web of Science ®Google Scholar
• Kumar P, Sharma PK. 2020. Soil salinity and food security in India. Front Sustain Food Syst. 4:533781.
   Google Scholar
• Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol. 33(7):1870–1874.
   PubMed Web of Science ®Google Scholar
• Lambers H. 2003. Dryland salinity: a key environmental issue in southern Australia. Plant Soil. 257(2):V–VII.
   Web of Science ®Google Scholar
• Letunic I, Bork P. 2019. Interactive Tree of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 47(W1):W256–W259.
   PubMed Web of Science ®Google Scholar
• Li X, Geng X, Xie R, Fu L, Jiang J, Gao L, Sun J. 2016. The endophytic bacteria isolated from elephant grass (Pennisetum purpureum Schumach) promote plant growth and enhance salt tolerance of Hybrid Pennisetum. Biotechnol Biofuels. 9(1):190.
   PubMed Web of Science ®Google Scholar
• Li H, Lei P, Pang X, Li S, Xu H, Xu Z, Feng X. 2017. Enhanced tolerance to salt stress in canola (Brassica napus L.) seedlings inoculated with the halotolerant Enterobacter cloacae HSNJ4. Appl Soil Ecol. 119:26–34.
   Web of Science ®Google Scholar
• Lim JA, Lee DH, Kim BY, Heu S. 2014. Draft genome sequence of Pantoea agglomerans R190, a producer of antibiotics against phytopathogens and foodborne pathogens. J Biotechnol. 188:7–8.
   PubMed Web of Science ®Google Scholar
• Machado RMA, Serralheiro RP. 2017. Soil salinity: effect on vegetable crop growth. Management practices to prevent and mitigate soil salinization. Horticulturae. 3(2):30.
   Web of Science ®Google Scholar
• Mayak S, Tirosh T, Glick BR. 2004. Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem. 42(6):565–572.
   PubMed Web of Science ®Google Scholar
• Meena KK, Sorty AM, Bitla UM, Choudhary K, Gupta P, Pareek A, Singh DP, Prabha R, Sahu PK, Gupta VK, et al. 2017. Abiotic stress responses and microbe-mediated mitigation in plants: the omics strategies. Front Plant Sci. 8:172.
   PubMed Web of Science ®Google Scholar
• Miche L, Balandreau J. 2001. Effects of rice seed surface sterilization with hypochlorite on inoculated Burkholderia vietnamiensis. Appl Environ Microbiol. 67(7):3046–3052.
   PubMed Web of Science ®Google Scholar
• Mishra A, Chauhan PS, Chaudhry V, Tripathi M, Nautiyal CS. 2011. Rhizosphere competent Pantoea agglomerans enhances maize (Zea mays) and chickpea (Cicera rietinum L.) growth, without altering the rhizosphere functional diversity. Antonie Van Leeuwenhoek. 100(3):405–413.
   PubMed Web of Science ®Google Scholar
• 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(2):429–448.
   PubMed Web of Science ®Google Scholar
• Nautiyal CS. 1999. An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett. 170(1):265–270.
   PubMed Web of Science ®Google Scholar
• Nei M, Kumar S. 2000. Molecular evolution and phylogenetics. Oxford Uni. Oxford.
   Google Scholar
• Ngumbi E, Kloepper J. 2016. Bacterial-mediated drought tolerance: current and future prospects. Appl Soil Ecol. 105:109–125.
   Web of Science ®Google Scholar
• Noori F, Etesami H, Noori S, Forouzan E, Salehi Jouzani G, Malboobi MA. 2021. Whole-genome sequence of Pantoea agglomerans ANP8, a salinity and drought stress–resistant bacterium isolated from alfalfa (Medicago sativa L.) root nodules. Biotechnol Rep (Amst). 29:e00600.
   PubMedGoogle Scholar
• Panwar M, Tewari R, Gulati A, Nayyar H. 2016a. Indigenous salt-tolerant rhizobacterium Pantoea dispersa (PSB3) reduces sodium uptake and mitigates the effects of salt stress on growth and yield of chickpea. Acta Physiol Plant. 38(12):278.
   Web of Science ®Google Scholar
• Panwar M, Tewari R, Nayyar H. 2016b. Native halo-tolerant plant growth-promoting rhizobacteria Enterococcus and Pantoea sp. improve seed yield of Mung bean (Vigna radiata L.) under soil salinity by reducing sodium uptake and stress injury. Physiol Mol Biol Plants. 22(4):445–459.
   PubMed Web of Science ®Google Scholar
• Paredes-Páliz KI, Caviedes MA, Doukkali B, Mateos-Naranjo E, Rodríguez-Llorente ID, Pajuelo E. 2016a. Screening beneficial rhizobacteria from Spartina maritima for phytoremediation of metal polluted salt marshes: comparison of gram-positive and gram-negative strains. Environ Sci Pollut Res Int. 23(19):19825–19837.
   PubMed Web of Science ®Google Scholar
• Paredes-Páliz KI, Pajuelo E, Doukkali B, Caviedes MÁ, Rodríguez-Llorente ID, Mateos-Naranjo E. 2016b. Bacterial inoculants for enhanced seed germination of Spartina densiflora: implications for restoration of metal polluted areas. Mar Pollut Bull. 110(1):396–400.
   PubMed Web of Science ®Google Scholar
• Pikovskaya RI. 1948. Mobilization of phosphorus in soil in connection with vital activity of some microbial species. Mikrobiologiya. 17:362–370.
   Google Scholar
• Popp A, Cleenwerck I, Iversen C, De Vos P, Stephan R. 2010. Pantoea gaviniae sp. nov. and Pantoea calida sp. nov., isolated from infant formula and an infant formula production environment. Int J Syst Evol Microbiol. 60(Pt 12):2786–2792.
   PubMed Web of Science ®Google Scholar
• Qin Y, Druzhinina IS, Pan X, Yuan Z. 2016. Microbially Mediated Plant Salt Tolerance and Microbiome-based Solutions for Saline Agriculture. Biotechnol Adv. 34(7):1245–1259.
   PubMed Web of Science ®Google Scholar
• Redman RS, Kim YO, Woodward CJDA, Greer C, Espino L, Doty SL, Rodriguez RJ. 2011. Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: a strategy for mitigating impacts of climate change. PLoS One. 6(7):e14823.
   PubMed Web of Science ®Google Scholar
• Reiter B, Pfeifer U, Schwab H, Sessitsch A. 2002. Response of endophytic bacterial communities in potato plants to infection with Erwinia carotovora subsp. atroseptica. Appl Environ Microbiol. 68(5):2261–2268.
   PubMed Web of Science ®Google Scholar
• Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim YO, Redman RS. 2008. Stress tolerance in plants via habitat-adapted symbiosis. Isme J. 2(4):404–416.
   PubMed Web of Science ®Google Scholar
• Rosenblueth M, Martínez-Romero E. 2006. Bacterial endophytes and their interactions with hosts. Mol Plant Microbe Interact. 19(8):827–837.
   PubMed Web of Science ®Google Scholar
• Rubini MR, Silva-Ribeiro RT, Pomella AWV, Maki CS, Araújo WL, Dos Santos DR, Azevedo JL. 2005. Diversity of endophytic fungal community of cacao (Theobroma cacao L.) and biological control of Crinipellis perniciosa, causal agent of Witches’ Broom Disease. Int J Biol Sci. 1(1):24–33.
   PubMed Web of Science ®Google Scholar
• Ruchi S, Ritika K, AK, Amit K, Sandip P, Shobit T, Mohinder K. 2012. Evaluation of plant growth-promoting attributes and lytic enzyme production by fluorescent Pseudomonas diversity associated with apple and pear. Int J Sci Res Publ. 2:1–8.
   Google Scholar
• Rzhetsky A, Nei M. 1992. A simple method for estimating and testing minimum-evolution trees. Mol Biol Evol. 9(5):945–967.
   Web of Science ®Google Scholar
• Sahoo S, Baranda, B, Nitesh. 2018. Salinity tolerance in wheat. Marumegh. 3:61–65.
   Google Scholar
• Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 4(4):406–425.
   PubMed Web of Science ®Google Scholar
• Santoyo G, Moreno-Hagelsieb G, d C, Orozco-Mosqueda M, Glick BR. 2016. Plant growth-promoting bacterial endophytes. Microbiol Res. 183:92–99.
   PubMed Web of Science ®Google Scholar
• Sarker U, Oba S. 2020. The response of salinity stress-induced A. tricolor to growth, anatomy, physiology, non-enzymatic and enzymatic antioxidants. Front Plant Sci. 11:559876.
   PubMed Web of Science ®Google Scholar
• Sarker U, Oba S. 2021. Color attributes, betacyanin, and carotenoid profiles, bioactive components, and radical quenching capacity in selected Amaranthus gangeticus leafy vegetables. Sci Rep. 11(1):11559.
   PubMed Web of Science ®Google Scholar
• Schwyn B, Neiland JB. 1987. Universal chemical assay for the detection and determination of siderophores. Anal Biochem. 160(1):47–56.
   PubMed Web of Science ®Google Scholar
• Shariati V, Malboobi MA, Tabrizi Z, Tavakol E, Owlia P, Safari M. 2017. Comprehensive genomic analysis of a plant growth-promoting rhizobacterium Pantoea agglomerans strain P5. Sci Rep. 7(1):15610.
   PubMed Web of Science ®Google Scholar
• Shrivastava P, Kumar R. 2015. Soil salinity: a serious environmental issue and plant growth-promoting bacteria as one of the tools for its alleviation. Saudi J Biol Sci. 22(2):123–131.
   PubMed Web of Science ®Google Scholar
• Soares MA, Li HY, Kowalski KP, Bergen M, Torres MS, White JF. 2016. Evaluation of the functional roles of fungal endophytes of Phragmites australis from high saline and low saline habitats. Biol Invasions. 18(9):2689–2702.
   Web of Science ®Google Scholar
• Štajner D, Kevrešan S, Gašić O, Mimica-Dukić N, Zongli H. 1997. Nitrogen and Azotobacter chroococcum enhance oxidative stress tolerance in sugar beet. Biol Plant. 39(3):441–445.
   Web of Science ®Google Scholar
• Sun L, Lei P, Wang Q, Ma J, Zhan Y, Jiang K, Xu Z, Xu H. 2019. The Endophyte Pantoea alhagi NX-11 alleviates salt stress damage to rice seedlings by secreting exopolysaccharides. Front Microbiol. 10:3112.
   PubMed Web of Science ®Google Scholar
• Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R. 2014. Abiotic and biotic stress combinations. New Phytol. 203(1):32–43.
   PubMed Web of Science ®Google Scholar
• Tiwari S, Lata C, Chauhan PS, Nautiyal CS. 2016. Pseudomonas putida attunes morphophysiological, biochemical and molecular responses in Cicer arietinum L. during drought stress and recovery. Plant Physiol Biochem. 99:108–117.
   PubMed Web of Science ®Google Scholar
• Vidhyasekaran P, Rabindran R, Muthamilan M, Nayar K, Rajappan K, Subramanian N, Vasumathi K. 1997. Development of a powder formulation of Pseudomonas fluorescens for control of rice blast. Plant Pathol. 46(3):291–297.
   Web of Science ®Google Scholar
• Vurukonda SSKP, Vardharajula S, Shrivastava M, SkZ A. 2016. Enhancement of drought stress tolerance in crops by plant growth-promoting rhizobacteria. Microbiol Res. 184:13–24.
   PubMed Web of Science ®Google Scholar
• Walitang DI, Kim CG, Kim K, Kang Y, Kim YK, Sa T. 2018. The influence of host genotype and salt stress on the seed endophytic community of salt-sensitive and salt-tolerant rice cultivars. BMC Plant Biol. 18(1):51.
   PubMed Web of Science ®Google Scholar
• Walitang DI, Kim K, Madhaiyan M, Kim YK, Kang Y, Sa T. 2017. Characterizing endophytic competence and plant growth promotion of bacterial endophytes inhabiting the seed endosphere of Rice. BMC Microbiol. 17(1):209.
   PubMed Web of Science ®Google Scholar
• Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 1991. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol. 173(2):697–703.
   PubMed Web of Science ®Google Scholar
• Widmer F, Shaffer BT, Porteous LA, Seidler RJ. 1999. Analysis of nifH gene pool complexity in soil and litter at a douglas fir forest site in the oregon cascade mountain range. Appl Environ Microbiol. 65(2):374–380.
   PubMed Web of Science ®Google Scholar
• Yan N, Marschner P, Cao W, Zuo C, Qin W. 2015. Influence of salinity and water content on soil microorganisms. Int Soil Water Conserv Res. 3(4):316–323.
   Web of Science ®Google Scholar