Abstract
Salinity leads to reduced plant growth by inhibiting the availability of nutrients especially phosphorous (P). The goal of this work is to demonstrate how phosphate-solubilizing bacteria (PSB) may be used to increase P availability in saline soils. A factorial experiment was carried out to discover the effect of PSB (Bacillus amyloliquefaciens and Bacillus pumilus) on modulating salinity stress (100 mM NaCl) through improving P (50 and 100 µM) availability based on a completely randomized designed (CRD). The results represented that B. pumilus was more effective in modulating salinity in most traits. Under saline conditions, B. pumilus in the presence of P at 50 µM led to increases in shoot dry weight (34%), root dry weight (54%), shoot length (39%), root length (37%), leaf P content (600%), relative water content (RWC, 13%), total chlorophyll (Chl, 32%), proline content (13%), but decreases in malondialdehyde (MDA, 25%), electrolyte leakage (EL, 21%), and soluble sugar (8%). According to principal component analysis (PCA), shoot and root length, root and shoot weight, Chl, and RWC had a negative correlation with MDA and EL. Based on agglomerative hierarchical clustering (AHC), results represented three distinguished clusters, where salinity and P have a noticeable role in this classification. Salinity elevated the expression of TIP41 (Tap42-interacting protein of 41 kDa) but lowered G6PDH (Glucose-6-phosphate dehydrogenase) and ARF15 (auxin response factor 15). Finally, the use of B. pumilus can be recommended to improve the P availability in saline soils through improving the growth, biochemical, and molecular status of chickpea plants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abdel Latef AAH, Abu Alhmad MF, Kordrostami M, Abo-Baker ABAE, Zakir A (2020) Inoculation with Azospirillum lipoferum or Azotobacter chroococcum reinforces maize growth by improving physiological activities under saline conditions. J Plant Growth Regul 39:1293–1306. https://doi.org/10.1007/s00344-020-10065-9
Abdiev A, Khaitov B, Toderich K, Park KW (2019) Growth, nutrient uptake and yield parameters of chickpea (Cicer arietinum L.) enhance by Rhizobium and Azotobacter inoculations in saline soil. J Plant Nutr 42:2703–2714. https://doi.org/10.1080/01904167.2019.1655038
Adnan M, Fahad S, Zamin M, Shah S, Mian IA, Danish S, Datta R (2020) Coupling phosphate-solubilizing bacteria with phosphorus supplements improve maize phosphorus acquisition and growth under lime induced salinity stress. Plants 9:900. https://doi.org/10.3390/plants9070900
Alamzeb M (2022) Management of phosphorus sources in combination with rhizobium and phosphate solubilizing bacteria improve nodulation, yield and phosphorus uptake in chickpea. Gesunde Pflanzen 1–16. https://doi.org/10.1007/s10343-022-00722-2
Alluqmani SM, Alabdallah NM (2022) Dry waste of red tea leaves and rose petals confer salinity stress tolerance in strawberry plants via modulation of growth and physiology. J Saudi Soc Agric Sci 21:511–517. https://doi.org/10.1016/j.jssas.2022.02.003
Amarasinghe T, Madhusha C, Munaweera I, Kottegoda N (2022) Review on mechanisms of phosphate solubilization in rock phosphate fertilizer. Commun Soil Sci Plant Anal 53:944–960. https://doi.org/10.1080/00103624.2022.2034849
Angon PB, Tahjib-Ul-Arif M, Samin SI, Habiba U, Hossain MA, Brestic M (2022) How do plants respond to combined drought and salinity stress?—A systematic review. Plants 11:2884. https://doi.org/10.3390/plants11212884
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta Vulgaris Plant Physiol 24:1. https://doi.org/10.1104/pp.24.1.1
Bates LS, Waldren RA, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207. https://doi.org/10.1007/BF00018060
Bouzroud S, Gouiaa S, Hu N, Bernadac A, Mila I, Bendaou N, Smouni A, Bouzayen M, Zouine M (2018) Auxin response factors (ARFs) are potential mediators of auxin action in tomato response to biotic and abiotic stress (Solanum lycopersicum). PLOS ONE 13:e0193517. https://doi.org/10.1371/journal.pone.0193517
Chapman HD, Pratt PF (1962) Methods of analysis for soils, plants and waters. Soil Sci 93:68. https://doi.org/10.1097/00010694-196201000-00015
Dagar JC, Yadav RK, Sharma PC (Eds.) (2019) Historical perspectives and dynamics of nature, extent, classification and management of salt-affected soils and waters. In: Dagar J, Yadav R, Sharma P (eds) Research developments in saline agriculture. Springer, Singapore. https://doi.org/10.1007/978-981-13-5832-6_1
Dey G, Banerjee P, Sharma RK, Maity JP, Etesami H, Shaw AK, Chen CY (2021) Management of phosphorus in salinity-stressed agriculture for sustainable crop production by salt-tolerant phosphate-solubilizing bacteria—A review. Agronomy 11:1–27. https://doi.org/10.3390/agronomy11081552
El-Esawi MA, Al-Ghamdi AA, Ali HM, Alayafi AA (2019) Azospirillum lipoferum FK1 confers improved salt tolerance in chickpea (Cicer arietinum L.) by modulating osmolytes, antioxidant machinery and stress-related genes expression. Environ Exp Bot 159:55–65. https://doi.org/10.1016/j.envexpbot.2018.12.001
Etesami H, Maheshwari DK (2018) Use of plant growth promoting rhizobacteria (PGPRs) with multiple plant growth promoting traits in stress agriculture: Action mechanisms and future prospects. Ecotoxicol Environ Safe 156:225–246. https://doi.org/10.1016/j.ecoenv.2018.03.013
Fatehi F, Hosseinzadeh A, Alizadeh H, Brimavandi T, Struik PC (2012) The proteome response of salt-resistant and salt-sensitive barley genotypes to long-term salinity stress. Molecul Biol Rep 39:6387–6397. https://doi.org/10.1007/s11033-012-1460-z
Fatehi F, Ebrahimi A, Maleki M (2021) Efficacy of auxin-producing bacillus strains on vegetative traits and relative expression of ARF15 gene in two genotypes of chickpea under salinity stress. Gen Engin Biosaf J 10:93–107 (http://gebsj.ir/article-1-393-en.html)
Fouda A, Hassan SED, Eid AM, El-Din Ewais E (2019) The interaction between plants and bacterial endophytes under salinity stress. In: Jha, S. (eds) Endophytes and secondary metabolites. Reference series in phytochemistry. Springer, Cham. https://doi.org/10.1007/978-3-319-90484-9_15
Gantait S, Sarkar S, Verma SK (2019) Marker‐assisted selection for abiotic stress tolerance in crop plants. Molec Plant Abiotic stress: Biol Biotechnol 335–368. https://doi.org/10.1002/9781119463665.ch18
Gong H, Chen G, Li F, Wang X, Hu Y, Bi Y (2013) Involvement of G6PDH in heat stress tolerance in the calli from Przewalskia tangutica and Nicotiana tabacum. Biol Plant 56:422–430. https://doi.org/10.1007/s10535-012-0072-8
Gul M, Wakeel A, Steffens D, Lindberg S (2019) Potassium-induced decrease in cytosolic Na+ alleviates deleterious effects of salt stress on wheat (Triticum aestivum L.). Plant Biol 21:825–831. https://doi.org/10.1111/plb.12999
Hajiabadi AA, Arani AM, Ghasemi S, Rad MH, Etesami H, Manshadi SS, Dolati A (2021) Mining the rhizosphere of halophytic rangeland plants for halotolerant bacteria to improve growth and yield of salinity-stressed wheat. Plant Physiol Biochem 163:139–153. https://doi.org/10.1016/j.plaphy.2021.03.059
Hassan N, Qadir G, Hassan FU, Akmal M, Sultan T (2021) Impact of phosphate solubilizing bacteria in combination with di-ammonium phosphate on growth and development of sunflower (Helianthus annus L.). J Plant Nutr 44:2359–2370. https://doi.org/10.1080/01904167.2021.1918158
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
Hu W, Zuo J, Hou X, Yan Y, Wei Y, Liu J, Li M, Xu B, Jin Z (2015) The auxin response factor gene family in banana: genome-wide identification and expression analyses during development, ripening, and abiotic stress. Crop Sci Hortic 6:742. https://doi.org/10.3389/fpls.2015.00742
Jain M, Khurana JP (2009) Transcript profiling reveals diverse roles of auxin responsive genes during reproductive development and abiotic stress in rice. FEBS J 276:3148–3162. https://doi.org/10.1111/j.1742-4658.2009.07033.x
Khan N, Bano A, Rahman MA, Guo J, Kan Z, Babar M (2019) Comparative physiological and metabolic analysis reveals a complex mechanism involved in drought tolerance in chickpea (Cicer arietinum L.) induced by PGPR and PGRs. Sci Rep 9:1–19. https://doi.org/10.1016/j.plaphy.2019.11.023
Khosropour E, Weisany W, Tahir NAR, Hakimi L (2021) Vermicompost and biochar can alleviate cadmium stress through minimizing its uptake and optimizing biochemical properties in Berberis integerrima bunge. Environ Sci Pollut Res 1–11. https://doi.org/10.1007/s11356-021-17073-6
Li J, Chen G, Wang X, Zhang Y, Jia H, Bi Y (2011) Glucose-6-phosphate dehydrogenase-dependent hydrogen peroxide production is involved in the regulation of plasma membrane H+-ATPase and Na+/H+ antiporter protein in salt-stressed callus from Carex moorcroftii. Physiol Plant 141:239–250. https://doi.org/10.1111/j.1399-3054.2010.01429.x
Liu J, Wang X, Hu Y, Hu W, Bi Y (2013) Glucose-6-phosphate dehydrogenase plays a pivotal role in tolerance to drought stress in soybean roots. Plant Cell Rep 32:415–429. https://doi.org/10.1007/s00299-012-1374-1
Lutts S, Kinet JM, Bouharmont J (1995) Changes in plant response to NaCl during development of rice (Oryza sativa L.) varieties differing in salinity resistance. J of Exp Bot 46:1843–1852. https://doi.org/10.1093/jxb/46.12.1843
Ma J, Islam F, Ayyaz A, Fang R, Hannan F, Farooq MA, Zhou W (2022) Wood vinegar induces salinity tolerance by alleviating oxidative damages and protecting photosystem II in rapeseed cultivars. Ind Crop Prod 189:115763. https://doi.org/10.1016/j.indcrop.2022.115763
Meena M, Swapnil P, Divyanshu K, Kumar S, Tripathi YN, Zehra A, Upadhyay RS (2020) PGPR-mediated induction of systemic resistance and physiochemical alterations in plants against the pathogens: Current perspectives. J Basic Microbiol 60:828–861. https://doi.org/10.1002/jobm.202000370
Moghaddam M, Panjtandoust FN, Ghanati M, F, (2020) Seed germination, antioxidant enzymes activity and proline content in medicinal plant Tagetes minuta under salinity stress. Plant Biosystems-an Int J Deal Aspect Plant Biol 154:835–842. https://doi.org/10.1080/11263504.2019.1701122
Moreau M, Azzopardi M, Clement G et al (2012) Mutations in the Arabidopsis homolog of LST8/GbetaL, a partner of the target of rapamycin kinase, impair plant growth, flowering, and metabolic adaptation to long days. Plant Cell 24:463–481. https://doi.org/10.1105/tpc.111.091306
Omokolo ND, Boudjeko T, Whitehead CS (2005) Comparative analyses of alterations in carbohydrates, amino acids, phenols and lignin in roots of three cultivars of Xanthosoma sagittifolium infected by Pythium myriotylum. South Afric J Bot 71:432–440. https://doi.org/10.1016/S0254-6299(15)30116-2
Osman HS, Rady A, Awadalla A, Omara AED, Hafez EM (2022) Improving the antioxidants system, growth, and sugar beet quality subjected to long-term osmotic stress by phosphate solubilizing bacteria and compost tea. Int J Plant Prod 16:119–135. https://doi.org/10.1007/s42106-021-00176-y
Parkhurst T, Standish RJ, Prober SM (2022) P is for persistence: Soil phosphorus remains elevated for more than a decade after old field restoration. Ecol Applicat 32:1–12. https://doi.org/10.1002/eap.2547
Paul CS, Mercl F, Száková J, Tejnecký V, Tlustoš P (2021) The role of low molecular weight organic acids in the release of phosphorus from sewage sludge-based biochar. All Life 14:599–609. https://doi.org/10.1080/26895293.2021.1932611
Punzo P, Ruggiero A, Possenti M, Nurcato R, Morelli CA, G, Batelli G, (2018a) The PP 2A-interactor TIP 41 modulates ABA responses in Arabidopsis thaliana. Plant J 94:991–1009. https://doi.org/10.1101/2020.02.07.939421
Punzo P, Ruggiero A, Possenti M, Nurcato R, Costa A, Morelli G, Grillo S, Batelli G (2018b) The PP 2A-interactor TIP 41 modulates ABA responses in Arabidopsis thaliana. Plant J 94:991–1009. https://doi.org/10.1111/tpj.13913
Qin H, Huang R (2020) The phytohormonal regulation of Na+/K+ and reactive oxygen species homeostasis in rice salt response. Molec Breed 40:1–13. https://doi.org/10.1007/s11032-020-1100-6
Reeger JE, Wheatley M, Yang Y, Brown KM (2021) Targeted mutation of transcription factor genes alters metaxylem vessel size and number in rice roots. Plant Direct 5:e00328. https://doi.org/10.1002/pld3.328
Reza DTA, Sohrab M, Hossein Ali A, Masoomeh S (2021) Role of rhizospheric microorganisms in mitigating the adverse effect of salinity stress in Plantago ovata growth, biochemical and photosynthetic traits. Archiv Agron Soil Sci 67:1060–1074. https://doi.org/10.1080/03650340.2020.1775816
Robaglia C, Thomas M, Meyer C (2012) Sensing nutrient and energy status by SnRK1 and TOR Kinases. Curr Opin Plant Biol 15:301–307. https://doi.org/10.1016/j.pbi.2012.01.012
Saghafi D, Delangiz N, Lajayer BA, Ghorbanpour M (2019) An overview on improvement of crop productivity in saline soils by halotolerant and halophilic PGPRs. Biotech 9:1–14. https://doi.org/10.1007/s13205-019-1799-0
Santhi CKV, Rajesh MK, Ramesh SV, Muralikrishna KS, Gangaraj KP, Payal G (2021) Genome-wide exploration of auxin response factors (ARFs) and their expression dynamics in response to abiotic stresses and growth regulators in coconut (Cocos nucifera L.). Plant Gene 28:100344. https://doi.org/10.1016/j.plgene.2021.100344
Singh P, Mahajan MM, Singh NK, Kumar D, Kumar K (2020) Physiological and molecular response under salinity stress in bread wheat (Triticum aestivum L.). J Plant Biochem Biotechnol 29:125–133. https://doi.org/10.1007/s13562-019-00521-3
Sofy MR, Elhawat N, Alshaal T (2020) Glycine betaine counters salinity stress by maintaining high K+/Na+ ratio and antioxidant defense via limiting Na+ uptake in common bean (Phaseolus vulgaris L.). Ecotoxicol Environ Saf 200:110732. https://doi.org/10.1016/j.ecoenv.2020.110732
Tang BL (2019) Neuroprotection by glucose-6-phosphate dehydrogenase and the pentose phosphate pathway. J Cell Biochem 120:14285–14295. https://doi.org/10.1002/jcb.29004
Wang H, Hou J, Li Y, Zhang Y, Huang J, Liang W (2017) Nitric oxide-mediated cytosolic glucose-6-phosphate dehydrogenase is involved in aluminum toxicity of soybean under high aluminum concentration. Plant Soil 416:39–52. https://doi.org/10.1007/s11104-017-3197-x
Wang J, Nan Z, Christensen MJ, Li C (2018) Glucose-6-phosphate dehydrogenase plays a vital role in Achnatherum inebrians plants host to Epichloë gansuensis by improving growth under nitrogen deficiency. Plant Soil 430:37–48. https://doi.org/10.1007/s11104-018-3710-x
Wullschleger S, Loewith R, Hall MN (2006) TOR signaling in growth and metabolism. Cell 124:471–484. https://doi.org/10.1016/j.cell.2006.01.016
Yaghoubian I, Ghassemi S, Nazari M, Smith RY, DL, (2021) Response of physiological traits, antioxidant enzymes and nutrient uptake of soybean to Azotobacter Chroococcum and zinc sulfate under salinity. South Afric J Bot 143:42–51. https://doi.org/10.1016/j.sajb.2021.07.037
Zhao C, Zhang H, Song C, Zhu JK, Shabala S (2020) Mechanisms of plant responses and adaptation to soil salinity. Innovation 1:100017. https://doi.org/10.1016/j.xinn.2020.100017
Author information
Authors and Affiliations
Contributions
The data were prepared by Azam Rahimi Chegeni; the initial draft was prepared by Azam Rahimi Chegeni and Foad Fatehi and revised by others.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Rahimi Chegeni, A., Fatehi, F., Ebrahimi, A. et al. Phosphate-Solubilizing Bacteria Modulated Salinity Stress in the Presence of Phosphorous through Improving Growth, Biochemical Properties, and Gene Expression of Chickpea (Cicer arientnum L.). J Soil Sci Plant Nutr 23, 4450–4462 (2023). https://doi.org/10.1007/s42729-023-01362-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42729-023-01362-9