Abstract
Key message
Herein, the inoculation with strain wp-6 promoted the growth of wheat seedlings by improving the energy production and conversion of wheat seedlings and alleviating salt stress.
Abstract
Soil salinization decreases crop productivity due to high toxicity of sodium ions to plants. Plant growth-promoting rhizobacteria (PGPR) have been demonstrated to alleviate salinity stress. However, the mechanism of PGPR in improving plant salt tolerance remains unclear. In this study, physiological analysis, proteomics, and metabolomics were applied to investigate the changes in wheat seedlings under salt stress (150 mM NaCl), both with and without plant root inoculation with wp-6 (Bacillus sp.). Under salt stress, root inoculation with strain wp-6 increased plant biomass (57%) and root length (25%). The Na+ content was reduced, while the K+ content and K+/Na+ ratio were increased. The content of malondialdehyde was decreased by 31.94% after inoculation of wp-6 under salt stress, while the content of proline, soluble sugar, and soluble protein were increased by 7.48%, 12.34%, and 4.12%, respectively. The peroxidase, catalase, and superoxide dismutase activities were increased after inoculation of wp-6 under salt stress. Galactose metabolism, phenylalanine metabolism, caffeine metabolism, ubiquinone and other terpenoid-quinone biosynthesis, and glutathione metabolism might play an important role in promoting the growth of salt-stressed wheat seedlings after the inoculation with wp-6. Interaction analysis of differentially expressed proteins and metabolites found that energy production and transformation-related proteins and six metabolites (d-arginine, palmitoleic acid, chlorophyllide b, rutin, pheophorbide a, and vanillylamine) were mainly involved in the growth of wheat seedlings after the inoculation with wp-6 under salt stress. Furthermore, correlation analysis found that inoculation with wp-6 promotes the growth of salt-stressed wheat seedlings mainly through regulating amino acid metabolism and porphyrin and chlorophyll metabolism. This study provides an eco-friendly method to increase agricultural productivity and paves a way to sustainable agriculture.
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References
Abid M, Zhang YJ, Li Z et al (2020) Effect of salt stress on growth, physiological and biochemical characters of four kiwifruit genotypes. Sci Hortic 271:109473. https://doi.org/10.1016/j.scienta.2020.109473
Ahmad F, Ahmad I, Khan MS (2008) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 1631:73–181. https://doi.org/10.1016/j.micres.2006.04.001
Barragán V, Leidi EO, Andrés Z et al (2012) Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis. Plant Cell 24:1127–1142. https://doi.org/10.1105/tpc.111.095273
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207. https://doi.org/10.1007/BF00018060
Bharti N, Pandey SS, Barnawal D et al (2016) Plant growth promoting rhizobacteria Dietzia natronolimnaea modulates the expression of stress responsive genes providing protection of wheat from salinity stress. Sci Rep 6:1–16. https://doi.org/10.1038/srep34768
Bhise KK, Bhagwat PK, Dandge PB (2017) Plant growth-promoting characteristics of salt tolerant Enterobacter cloacae strain KBPD and its efficacy in amelioration of salt stress in Vigna radiata L. J Plant Growth Regul 36:215–226. https://doi.org/10.1007/s00344-016-9631-0
Boiteau RM, Markillie LM, Hoyt DW et al (2021) Metabolic interactions between Brachypodium and Pseudomonas fluorescens under controlled iron-limited conditions. Msystems 6:e00580-e620. https://doi.org/10.1128/mSystems.00580-20
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Bruderer R, Bernhardt OM, Gandhi T et al (2015) Extending the limits of quantitative proteome profiling with data-independent acquisition and application to acetaminophen-treated three-dimensional liver microtissues. Mol Cell Proteom 14:1400–1410. https://doi.org/10.1074/mcp.M114.044305
Chen Y, Zhi J, Zhang H et al (2017) Transcriptome analysis of Phytolacca americana L. in response to cadmium stress. PLoS ONE 12:e0184681. https://doi.org/10.1371/journal.pone.0184681
Chen X, Wang H, Li X et al (2019) Molecular cloning and functional analysis of 4-coumarate:coa ligase 4(4cl-like 1) from Fraxinus mandshurica and its role in abiotic stress tolerance and cell wall synthesis. BMC Plant Biol 19:231. https://doi.org/10.1186/s12870-019-1812-0
Chen J, Wang L, Liang H et al (2020) Overexpression of DoUGP enhanced biomass and stress tolerance by promoting polysaccharide accumulation in Dendrobium officinale. Front Plant Sci 11:1673. https://doi.org/10.3389/fpls.2020.533767
Chivasa S, Tomé DF, Slabas AR (2013) UDP-glucose pyrophosphorylase is a novel plant cell death regulator. J Proteome Res 12:1743–1753. https://doi.org/10.1021/pr3010887
Choi M, Chang CY, Clough T et al (2014) MSstats: an R package for statistical analysis of quantitative mass spectrometry-based proteomic experiments. Bioinformatics 30:2524–2526. https://doi.org/10.1093/bioinformatics/btu305
Christian S, Kristina U, Dietrich E et al (2009) A metabolic signature of the beneficial interaction of the endophyte Paenibacillus sp. isolate and in vitro-grown poplar plants revealed by metabolomics. Mol Plant Microbe Int 22:1032–1037. https://doi.org/10.1094/MPMI-22-8-1032
Chrost B, Kolukisaoglu U, Schulz B et al (2007) An α-galactosidase with an essential function during leaf development. Planta 225:311–320. https://doi.org/10.1007/s00425-006-0350-9
Conesa A, Götz S (2008) Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J Genom 2008:619832. https://doi.org/10.1155/2008/619832
Cox J, Michalski A, Mann M (2011) Software lock mass by two-dimensional minimization of peptide mass errors. J Am Soc Mass Spectrom 22:1373–1380. https://doi.org/10.1007/s13361-011-0142-8
Daher Z, Recorbet G, Solymosi K et al (2017) Changes in plastid proteome and structure in arbuscular mycorrhizal roots display a nutrient starvation signature. Physiol Plant 159:13–29. https://doi.org/10.1111/ppl.12505
Danish S, Zafar-ul-Hye M, Mohsin F (2020) ACC-deaminase producing plant growth promoting rhizobacteria and biochar mitigate adverse effects of drought stress on maize growth. PLoS ONE 15:e0230615. https://doi.org/10.1371/journal.pone.0230615
Deng C, Ku X, Cheng LL et al (2020) Metabolite and transcriptome profiling on xanthine alkaloids-fed tea plant (Camellia sinensis) shoot tips and roots reveal the complex metabolic network for caffeine biosynthesis and degradation. Front Plant Sci 11:1339. https://doi.org/10.3389/fpls.2020.551288
Ding X, Zhu X, Zheng W et al (2021) BTH treatment delays the senescence of postharvest pitaya fruit in relation to enhancing antioxidant system and phenylpropanoid pathway. Foods 10:846. https://doi.org/10.3390/foods10040846
dos Santos R, Vergauwen R, Pacolet P et al (2013) Manninotriose is a major carbohydrate in red deadnettle (Lamium purpureum, Lamiaceae). Ann Bot Lond 111:385–393. https://doi.org/10.1093/aob/mcs288
dos Santos RM, Diaz PAE, Lobo LLB et al (2020) Use of plant growth-promoting rhizobacteria in maize and sugarcane: characteristics and applications. Front Sustain Food Syst 4:136. https://doi.org/10.3389/fsufs.2020.00136
Du M, Ding G, Cai Q (2018) The transcriptomic responses of Pinus massoniana to drought stress. Forests 9:326. https://doi.org/10.3390/f9060326
Duan AQ, Tao JP, Jia LL et al (2020) AgNAC1, a celery transcription factor, related to regulation on lignin biosynthesis and salt tolerance. Genomics 112:5254–5264. https://doi.org/10.1016/j.ygeno.2020.09.049
Dubois M, Gilles KA, Hamilton JK et al (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356. https://doi.org/10.1021/AC60111A017
Duke KA, Becker MG, Girard IJ, Millar JL et al (2017) The biocontrol agent Pseudomonas chlororaphis PA23 primes Brassica napus defenses through distinct gene networks. BMC Genom 18:1–16. https://doi.org/10.1186/s12864-017-3848-6
El-Akhdar I, Elsakhawy T, Abo-Koura HA (2020) Alleviation of salt stress on wheat (Triticum aestivum L.) by plant growth promoting bacteria strains Bacillus halotolerans MSR-H4 and Lelliottia amnigenaMSR-M49. J Adv Microbiol 20:44–58. https://doi.org/10.9734/jamb/2020/v20i130208
El-Hefny M, Salem MZ, Behiry SI et al (2020) The potential antibacterial and antifungal activities of wood treated with Withania somnifera fruit extract, and the phenolic, caffeine, and flavonoid composition of the extract according to HPLC. Processes 8:113. https://doi.org/10.3390/pr8010113
El-Saber MM, Mahdi AA, Hassan AH et al (2021) Effects of magnetite nanoparticles on physiological processes to alleviate salinity induced oxidative damage in wheat. J Sci Food Agric. https://doi.org/10.1002/jsfa.11206
Fan H, Pan X, Li Y et al (2008) Evaluation of soil environment after saline soil reclamation of Xinjiang Oasis, China. Agron J 100:471–476. https://doi.org/10.2134/agronj2007.0100
Feussner I, Polle A (2015) What the transcriptome does not tell-proteomics and metabolomics are closer to the plants’patho-phenotype. Cur Opin Plant Biol 26:26–31. https://doi.org/10.1016/j.pbi.2015.05.023
Giri B, Kapoor R, Mukerji KG (2007) Improved tolerance of Acacia nilotica to salt stress by arbuscular mycorrhiza, Glomus fasciculatum may be partly related to elevated K/Na ratios in root and shoot tissues. Microb Ecol 54:753–760. https://doi.org/10.1007/s00248-007-9239-9
Gómez R, Vicino P, Carrillo N et al (2019) Manipulation of oxidative stress responses as a strategy to generate stress-tolerant crops. From damage to signaling to tolerance. Crit Rev Biotechnol 39:693–708. https://doi.org/10.1080/07388551.2019.1597829
Grotto D, Maria LS, Valentini J et al (2009) Importance of the lipid peroxidation biomarkers and methodological aspects for malondialdehyde quantification. Quim Nova 32:169–174. https://doi.org/10.1590/S0100-40422009000100032
Gunnaiah R, Kushalappa AC, Duggavathi R et al (2012) Integrated metabolo-proteomic approach to decipher the mechanisms by which wheat QTL (Fhb1) contributes to resistance against Fusarium graminearum. PLoS ONE 7:e40695. https://doi.org/10.1371/journal.pone.0040695
Guo R, Shi L, Yang Y (2009) Germination, growth, osmotic adjustment and ionic balance of wheat in response to saline and alkaline stresses. Soil Sci Plant Nutr 55:667–679. https://doi.org/10.1111/j.1747-0765.2009.00406.x
Guo Y, Lu Y, Goltsev V et al (2020) Comparative effect of tenuazonic acid, diuron, bentazone, dibromothymoquinone and methyl viologen on the kinetics of Chl a fluorescence rise OJIP and the MR820 signal. Plant Physiol Biochem 156:39–48. https://doi.org/10.1016/j.plaphy.2020.08.044
Hamamoto S, Horie T, Hauser F et al (2015) HKT transporters mediate salt stress resistance in plants: from structure and function to the field. Curr Opin Biotechnol 32:113–120. https://doi.org/10.1016/j.copbio.2014.11.025
Hameeda B, Harini G, Rupela OP et al (2008) Growth promotion of maize by phosphate-solubilizing bacteria isolated from composts and macrofauna. Microbiol Res 163:234–242. https://doi.org/10.1016/j.micres.2006.05.009
Han R, He X, Pan X et al (2020) Enhancing xanthine dehydrogenase activity is an effective way to delay leaf senescence and increase rice yield. Rice 13:1–14. https://doi.org/10.1186/s12284-020-00375-7
Hasanuzzaman M, Bhuyan MHM, Zulfiqar F et al (2020) Reactive oxygen species and antioxidant defense in plants under abiotic stress: revisiting the crucial role of a universal defense regulator. Antioxidants 9:681. https://doi.org/10.3390/antiox9080681
He L, Yue Z, Chen C et al (2020) Enhancing iron uptake and alleviating iron toxicity in wheat by plant growth-promoting bacteria: theories and practices. Int J Agric Biol 23:190–196. https://doi.org/10.17957/IJAB/15.1276
He A, Dean JM, Lodhi IJ (2021) Peroxisomes as cellular adaptors to metabolic and environmental stress. Trends Cell Biol. https://doi.org/10.1016/j.tcb.2021.02.005
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
Jeyaraj A, Elango T, Yu Y et al (2021) Impact of exogenous caffeine on regulatory networks of microRNAs in response to Colletotrichum gloeosporioides in tea plant. Sci Hortic 279:109914. https://doi.org/10.1016/j.scienta.2021.109914
Jia XM, Zhu YF, Hu Y et al (2019) Integrated physiologic, proteomic, and metabolomic analyses of Malus halliana adaptation to saline-alkali stress. Hortic Res 6:1–19. https://doi.org/10.1038/s41438-019-0172-0
Jiang Y, Chen C, Tao X et al (2012) A proteomic analysis of storage stress responses in Ipomoea batatas (L.) Lam. tuberous root. Mol Biol Rep 39:8015–8025. https://doi.org/10.1007/s11033-012-1648-2
Ju Y, Kou M, Zhong R et al (2021) Alleviating salt stress on seedings using plant growth promoting rhizobacteria isolated from the rhizosphere soil of Achnatherum inebrians infected with Epichloë gansuensis endophyte. Plant Soil. https://doi.org/10.1007/s11104-021-05002-y
Kamran M, Parveen A, Ahmar S et al (2020) An overview of hazardous impacts of soil salinity in crops, tolerance mechanisms, and amelioration through selenium supplementation. Int J Mol Sci 21:148. https://doi.org/10.3390/ijms21010148
Kanehisa M, Goto S, Sato Y et al (2012) KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res 40:D109–D114. https://doi.org/10.1093/nar/gkr988
Khan MS, Rizvi A, Saif S et al (2017) Phosphate-solubilizing microorganisms in sustainable production of wheat: current perspective. In: Kumar V, Kumar M, Sharma S, Prasad R (eds) Probiotics in agroecosystem, 1st edn. Springer, Singapore, pp 51–81. https://doi.org/10.1007/978-981-10-4059-7_3
Kubi HAA, Khan MA, Adhikari A et al (2021) Silicon and plant growth-promoting Rhizobacteria Pseudomonas psychrotolerans CS51 mitigates salt stress in Zea mays L. Agriculture 11:272. https://doi.org/10.3390/agriculture11030272
Kumar P, Thakur S, Dhingra GK et al (2018) Inoculation of siderophore producing rhizobacteria and their consortium for growth enhancement of wheat plant. Biocatal Agric Biotechnol 15:264–269. https://doi.org/10.1016/j.bcab.2018.06.019
Lahrmann U, Ding Y, Banhara A et al (2013) Host-related metabolic cues affect colonization strategies of a root endophyte. Proc Natl Acad Sci 110:13965–13970. https://doi.org/10.1073/pnas.1301653110
Lastochkina O, Pusenkova L, Yuldashev R et al (2017) Effects of Bacillus subtilis on some physiological and biochemical parameters of Triticum aestivum L. (wheat) under salinity. Plant Physiol Biochem 121:80–88. https://doi.org/10.1016/j.plaphy.2017.10.020
Lavhale SG, Joshi RS, Kumar Y et al (2021) Functional insights into two Ocimum kilimandscharicum 4-coumarate-CoA ligases involved in phenylpropanoid biosynthesis. Int J Biol Macromol 181:202–210. https://doi.org/10.1016/j.ijbiomac.2021.03.129
Li K, Pidatala VR, Shaik R et al (2014a) Integrated metabolomic and proteomic approaches dissect the effect of metal-resistant bacteria on maize biomass and copper uptake. Environ Sci Technol 48:1184–1193. https://doi.org/10.1021/es4047395
Li H, Yan S, Zhao L (2014b) Histone acetylation associated up-regulation of the cell wall related genes is involved in salt stress induced maize root swelling. BMC Plant Biol 14:1–14. https://doi.org/10.1186/1471-2229-14-105
Li Q, Yang A, Zhang WH (2016) Efficient acquisition of iron confers greater tolerance to saline-alkaline stress in rice (Oryza sativa L.). J Exp Bot 67:6431–6444. https://doi.org/10.1093/jxb/erw407
Li L, Gao S, Yang L, Liu YL et al (2021) Cobalt (II) complex as a fluorescent sensing platform for the selective and sensitive detection of triketone HPPD inhibitors. J Hazard Mater 404:124015. https://doi.org/10.1016/j.jhazmat.2020.124015
Lim JH, Kim SD (2013) Induction of drought stress resistance by multi-functional PGPR Bacillus licheniformis K11 in pepper. Plant Pathol J 29:201. https://doi.org/10.5423/PPJ.SI.02.2013.0021
Lima CVDP, Batista M, Kugeratski FG et al (2014) LM14 defined medium enables continuous growth of Trypanosoma cruzi. BMC Microbiol 14:238. https://doi.org/10.1186/s12866-014-0238-y
Liu SC, Yong J, Li MB et al (2019) Improving plant growth and alleviating photosynthetic inhibition from salt stress using AMF in alfalfa seedlings. J Plant Interact 14:482–491. https://doi.org/10.3389/fpls.2019.00490
Liu S, Zhong H, Wang Q et al (2021) Global analysis of UDP glucose pyrophosphorylase (UDPGP) gene family in plants: conserved evolution involved in cell death. Front Plant Sci 12:924. https://doi.org/10.3389/fpls.2021.681719
Ma Q, Zhou H, Sui X et al (2021) Generation of new salt-tolerant wheat lines and transcriptomic exploration of the responsive genes to ethylene and salt stress. Plant Growth Regul 94:33–48. https://doi.org/10.1007/s10725-021-00694-9
Masmoudi F, Tounsi S, Dunlap CA et al (2021) Halotolerant Bacillus spizizenii FMH45 promoting growth, physiological, and antioxidant parameters of tomato plants exposed to salt stress. Plant Cell Rep. https://doi.org/10.1007/s00299-021-02702-8
Meng J, Wang W, Li L et al (2017) Cadmium effects on DNA and protein metabolism in oyster (Crassostrea gigas) revealed by proteomic analyses. Sci Rep 7:1–16. https://doi.org/10.1038/s41598-017-11894-7
Nakagawa A, Sakamoto S, Takahashi M et al (2007) The RNAi-mediated silencing of xanthine dehydrogenase impairs growth and fertility and accelerates leaf senescence in transgenic arabidopsis plants. Plant Cell Physiol 48:1484–1495. https://doi.org/10.1093/pcp/pcm119
Oleńska E, Małek W, Wójcik M et al (2020) Beneficial features of plant growth-promoting rhizobacteria for improving plant growth and health in challenging conditions: a methodical review. Sci Total Environ. https://doi.org/10.1016/j.scitotenv.2020.140682
Orhan F, Gulluce M (2015) Isolation and characterization of salt-tolerant bacterial strains in salt-affected soils of Erzurum, Turkey. Geomicrobiol J 32:521–529. https://doi.org/10.1080/01490451.2014.962674
Pascual MB, El-Azaz J, de la Torre FN et al (2016) Biosynthesis and metabolic fate of phenylalanine in conifers. Front Plant Sci 7:1030. https://doi.org/10.3389/fpls.2016.01030
Patial M, Pal D, Thakur A et al (2019) Doubled haploidy techniques in wheat (Triticum aestivum L.): an overview. Proc Natl Acad Sci India B 89:27–41. https://doi.org/10.1007/s40011-017-0870-z
Poveda J (2020) Trichoderma parareesei favors the tolerance of rapeseed (Brassica napus L.) to salinity and drought due to a chorismate mutase. Agronomy 10:118. https://doi.org/10.3390/agronomy10010118
Qu L, Huang Y, Zhu C et al (2016) Rhizobia-inoculation enhances the soybean’s tolerance to salt stress. Plant Soil 400:209–222. https://doi.org/10.1007/s11104-015-2728-6
Riahi L, Cherif H, Miladi S et al (2020) Use of plant growth promoting bacteria as an efficient biotechnological tool to enhance the biomass and secondary metabolites production of the industrial crop Pelargonium graveolens L’Hér. under semi-controlled conditions. Ind Crop Prod 154:112721. https://doi.org/10.1016/j.indcrop.2020.112721
Safdarian M, Askari H, Shariati V et al (2019) Transcriptional responses of wheat roots inoculated with Arthrobacter nitroguajacolicus to salt stress. Sci Rep 9:1–12. https://doi.org/10.1038/s41598-018-38398-2
Santander C, Ruiz A, García S et al (2020) Efficiency of two Arbuscular mycorrhizal fungal inocula to improve saline stress tolerance in lettuce plants by changes of antioxidant defense mechanisms. J Sci Food Agric 100:1577–1587. https://doi.org/10.1002/jsfa.10166
Selvakumar G, Shagol CC, Kim K et al (2018) Spore associated bacteria regulates maize root K+/Na+ ion homeostasis to promote salinity tolerance during arbuscular mycorrhizal symbiosis. BMC Plant Biol 18:1–13. https://doi.org/10.1186/s12870-018-1317-2
Shafi M, Bakhat J, Khan MJ et al (2010) Effect of salinity on yield and ion accumulation of wheat genotypes. Pak J Bot 42:4113–4121. https://doi.org/10.1094/MPMI-07-10-0151
Sharma A, Johri BN (2003) Growth promoting influence of siderophore-producing Pseudomonas strains GRP3A and PRS9 in maize (Zea mays L.) under iron limiting conditions. Microbiol Res 158:243–248. https://doi.org/10.1078/0944-5013-00197
Shiferaw B, Smale M, Braun HJ et al (2013) Crops that feed the world 10. Past successes and future challenges to the role played by wheat in global food security. Food Secur 5:291–317. https://doi.org/10.1007/s12571-013-0263-y
Singh RP, Jha P, Jha PN (2015) The plant-growth-promoting bacterium Klebsiella sp. SBP-8 confers induced systemic tolerance in wheat (Triticum aestivum) under salt stress. J Plant Physiol 184:57–67. https://doi.org/10.1016/j.jplph.2015.07.002
Singh RP, Runthala A, Khan S, Jha PN (2017) Quantitative proteomics analysis reveals the tolerance of wheat to salt stress in response to Enterobacter cloacae SBP-8. PLoS ONE 12:e0183513. https://doi.org/10.1371/journal.pone.0183513
Sisó-Terraza P, Luis-Villarroya A, Fourcroy P et al (2016) Accumulation and secretion of coumarinolignans and other coumarins in Arabidopsis thaliana roots in response to iron deficiency at high pH. Front Plant Sci 7:1711. https://doi.org/10.3389/fpls.2016.01711
Song W, Zhou F, Shan C et al (2021) Identification of glutathione S-transferase genes in Hami melon (Cucumis melo var. saccharinus) and their expression analysis under cold stress. Fron Plant Sci 12:672017. https://doi.org/10.3389/fpls.2021.672017
Szymańska S, Płociniczak T, Piotrowska-Seget Z et al (2016) Metabolic potential and community structure of endophytic and rhizosphere bacteria associated with the roots of the halophyte Aster tripolium L. Microbiol Res 182:68–79. https://doi.org/10.1016/j.micres.2015.09.007
Toennes SW, Harder S, Schramm M et al (2003) Pharmacokinetics of cathinone, cathine and norephedrine after the chewing of khat leaves. Brit J Clin Pharmacol 56:125–130. https://doi.org/10.1046/j.1365-2125.2003.01834.x
Tong R, Zhou B, Cao Y et al (2020) Metabolic profiles of moso bamboo in response to drought stress in a field investigation. Sci Total Environ 720:137722. https://doi.org/10.1016/j.scitotenv.2020.137722
Uzoh IM, Babalola OO (2020) Review on increasing iron availability in soil and its content in cowpea (Vigna unguiculata) by plant growth promoting rhizobacteria. AJFAND 20:15779–15799. https://doi.org/10.18697/ajfand.91.18530
Valivand M, Amooaghaie R (2021) Sodium hydrosulfide modulates membrane integrity, cation homeostasis, and accumulation of phenolics and osmolytes in Zucchini under nickel stress. J Plant Growth Regul 40:313–328. https://doi.org/10.1007/s00344-020-10101-8
Vives-Peris V, Gómez-Cadenas A, Pérez-Clemente RM (2018) Salt stress alleviation in citrus plants by plant growth-promoting rhizobacteria Pseudomonas putida and Novosphingobium sp. Plant Cell Rep 37:1557–1569. https://doi.org/10.1007/s00299-018-2328-z
Wang GF, Balint-Kurti PJ (2016) Maize homologs of CCoAOMT and HCT, two key enzymes in lignin biosynthesis, form complexes with the NLR Rp1 protein to modulate the defense response. Plant Physiol 171:2166–2177. https://doi.org/10.1104/pp.16.00224
Wang W, Scali M, Vignani R et al (2003) Protein extraction for two-dimensional electrophoresis from olive leaf, a plant tissue containing high levels of interfering compounds. Electrophoresis 24:2369–2375. https://doi.org/10.1002/elps.200305500
Weckwerth W, Loureiro ME, Wenzel K et al (2004) Differential metabolic networks unravel the effects of silent plant phenotypes. Proc Natl Acad Sci USA 101:7809–7814. https://doi.org/10.1073/pnas.0303415101
Wu CH, Bernard SM, Andersen GL et al (2009) Developing microbe-plant interactions for applications in plant-growth promotion and disease control, production of useful compounds, remediation and carbon sequestration. Microb Biotechnol 2:428–440. https://doi.org/10.1111/j.1751-7915.2009.00109.x
Xing JC, Zhao BQ, Dong J et al (2020) Transcriptome and metabolome profiles revealed molecular mechanisms underlying tolerance of Portulaca oleracea to saline stress. Russ J Plant Physiol 67:146–152. https://doi.org/10.1134/S1021443720010240
Xiong J, Sun Y, Yang Q et al (2017) Proteomic analysis of early salt stress responsive proteins in alfalfa roots and shoots. Proteome Sci 15:19. https://doi.org/10.1186/s12953-017-0127-z
Xu J, Xing XJ, Tian YS et al (2015) Transgenic Arabidopsis plants expressing tomato glutathione S-transferase showed enhanced resistance to salt and drought stress. PLoS ONE 10:e0136960. https://doi.org/10.1371/journal.pone.0136960
Xu B, Wang Y, Zhang S et al (2017a) Transcriptomic and physiological analyses of Medicago sativa L. roots in response to lead stress. PLoS ONE 12:e0175307. https://doi.org/10.1371/journal.pone.0175307
Xu J, Tian YS, Xing XJ et al (2017b) Enhancement of phenol stress tolerance in transgenic Arabidopsis plants overexpressing glutathione S-transferase. Plant Growth Regul 82:37–45. https://doi.org/10.1007/s10725-016-0235-2
Yang Y, Guo Y (2018) Elucidating the molecular mechanisms mediating plant salt-stress responses. New Phytol 217:523–539. https://doi.org/10.1111/nph.14920
Yu D, Boughton BA, Hill CB et al (2020) Insights into oxidized lipid modification in barley roots as an adaptation mechanism to salinity stress. Fronti Plant Sci 11:1. https://doi.org/10.3389/fpls.2020.00001
Zahir ZA, Arshad M, Frankenberger WT (2003) Plant growth-promoting rhizobacteria: applications and perspectives in agriculture. Adv Agron 81:97–168. https://doi.org/10.1016/S0065-2113(03)81003-9
Zhang HH, Xu N, Li X et al (2016a) Overexpression of 2-Cys Prx increased salt tolerance of photosystem II (PSII) in tobacco. PeerJ Prepr. https://doi.org/10.7287/peerj.preprints.2500v1
Zhang SS, Sun L, Dong X et al (2016b) Cellulose synthesis genes CESA6 and CSI1 are important for salt stress tolerance in Arabidopsis. J Integr Plant Biol 58:623–626. https://doi.org/10.1111/jipb.12442
Zhang L, Zhang X, Fan S (2017) Meta-analysis of salt-related gene expression profiles identifies common signatures of salt stress responses in Arabidopsis. Plant Syst Evol 303:757–774. https://doi.org/10.1007/s00606-017-1407-x
Zhang Q, Song X, Bartels D (2018) Sugar metabolism in the desiccation tolerant grass Oropetium thomaeum in response to environmental stresses. Plant Sci 270:30–36. https://doi.org/10.1016/j.plantsci.2018.02.004
Zhang X, Tang H, Du H et al (2020) Comparative N-glycoproteome analysis provides novel insights into the regulation mechanism in tomato (Solanum lycopersicum L.) during fruit ripening process. Plant Sci 293:110413. https://doi.org/10.1016/j.plantsci.2020.110413
Zhao Y, Zhang F, Yang L et al (2019) Response of soil bacterial community structure to different reclamation years of abandoned salinized farmland in arid China. Arch Microbiol 201:1219–1232. https://doi.org/10.1007/s00203-019-01689-x
Zhou C, Zhu L, Xie Y et al (2017) Bacillus licheniformis SA03 confers increased saline-alkaline tolerance in chrysanthemum plants by induction of abscisic acid accumulation. Front Plant Sci 8:1143. https://doi.org/10.3389/fpls.2017.01143
Zvanarou S, Vágnerová R, Mackievic V et al (2020) Salt stress triggers generation of oxygen free radicals and DNA breaks in Physcomitrella patens protonema. Environ Exp Bot 180:104236. https://doi.org/10.1016/j.envexpbot.2020.104236
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This research was financially supported by the National Natural Science Foundation of China (Grant No. 31860360) and the Science and Technology Cooperation Project of Xinjiang (Grant No. 2020BC001).
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YZ and FZ designed and carried out the experiment. YZ collected the data. YZ performed the analysis. YZ, FZ, DW, and WW analysed the results. YZ wrote the manuscript. YZ, FZ, and BM checked and revised the final version of the manuscript.
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Communicated by Prakash Lakshmanan.
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Zhao, Y., Zhang, F., Mickan, B. et al. Physiological, proteomic, and metabolomic analysis provide insights into Bacillus sp.-mediated salt tolerance in wheat. Plant Cell Rep 41, 95–118 (2022). https://doi.org/10.1007/s00299-021-02788-0
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DOI: https://doi.org/10.1007/s00299-021-02788-0