Metal-tolerant morganella morganii isolates can potentially mediate nickel stress tolerance in Arabidopsis by upregulating antioxidative enzyme activities

Plant growth-promoting rhizobacteria (PGPRs) have been utilized to immobilize heavy metals, limiting their translocation in metal contaminated settings. However, studies on the mechanisms and interactions that elucidate how PGPRs mediate Nickel (Ni) tolerance in plants are rare. Thus, in this study...

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Main Authors: Tahir Naqqash, Aeman Aziz, Muhammad Baber, Muhammad Shahid, Muhammad Sajid, Radicetti Emanuele, Abdel-Rhman Z. Gaafar, Mohamed S. Hodhod, Ghulam Haider
Format: Article
Language:English
Published: Taylor & Francis Group 2024-12-01
Series:Plant Signaling & Behavior
Subjects:
Online Access:http://dx.doi.org/10.1080/15592324.2024.2318513
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author Tahir Naqqash
Aeman Aziz
Muhammad Baber
Muhammad Shahid
Muhammad Sajid
Radicetti Emanuele
Abdel-Rhman Z. Gaafar
Mohamed S. Hodhod
Ghulam Haider
author_facet Tahir Naqqash
Aeman Aziz
Muhammad Baber
Muhammad Shahid
Muhammad Sajid
Radicetti Emanuele
Abdel-Rhman Z. Gaafar
Mohamed S. Hodhod
Ghulam Haider
author_sort Tahir Naqqash
collection DOAJ
description Plant growth-promoting rhizobacteria (PGPRs) have been utilized to immobilize heavy metals, limiting their translocation in metal contaminated settings. However, studies on the mechanisms and interactions that elucidate how PGPRs mediate Nickel (Ni) tolerance in plants are rare. Thus, in this study we investigated how two pre-characterized heavy metal tolerant isolates of Morganella morganii (ABT9 and ABT3) improve Ni stress tolerance in Arabidopsis while enhancing its growth and yield. Arabidopsis seedlings were grown for five weeks in control/Ni contaminated (control, 1.5 mM and 2.5 mM) potted soil, in the presence or absence of PGPRs. Plant growth characteristics, quantum yield, and antioxidative enzymatic activities were analyzed to assess the influence of PGPRs on plant physiology. Oxidative stress tolerance was quantified by measuring MDA accumulation in Arabidopsis plants. As expected, Ni stress substantially reduced plant growth (shoot and root fresh weight by 53.25% and 58.77%, dry weight by 49.80% and 57.41% and length by 47.16% and 64.63% over control), chlorophyll content and quantum yield (by 40.21% and 54.37% over control). It also increased MDA content by 84.28% at higher (2.5 mM) Ni concentrations. In contrast, inoculation with M. morganii led to significant improvements in leaf chlorophyll, quantum yield, and Arabidopsis biomass production. The mitigation of adverse effects of Ni stress on biomass observed in M. morganii-inoculated plants was attributed to the enhancement of antioxidative enzyme activities compared to Ni-treated plants. This upregulation of the antioxidative defense mechanism mitigated Ni-induced oxidative stress, leading to improved performance of the photosynthetic machinery, which, in turn, enhanced chlorophyll content and quantum yield. Understanding the underlying mechanisms of these tolerance-inducing processes will help to complete the picture of PGPRs-mediated defense signaling. Thus, it suggests that M. morganii PGPRs candidate can potentially be utilized for plant growth promotion by reducing oxidative stress via upregulating antioxidant defense systems in Ni-contaminated soils and reducing Ni metal uptake.
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spelling doaj.art-c2425a63f8f64408800496294646aea32025-01-02T11:44:26ZengTaylor & Francis GroupPlant Signaling & Behavior1559-23161559-23242024-12-0119110.1080/15592324.2024.23185132318513Metal-tolerant morganella morganii isolates can potentially mediate nickel stress tolerance in Arabidopsis by upregulating antioxidative enzyme activitiesTahir Naqqash0Aeman Aziz1Muhammad Baber2Muhammad Shahid3Muhammad Sajid4Radicetti Emanuele5Abdel-Rhman Z. Gaafar6Mohamed S. Hodhod7Ghulam Haider8Bahauddin Zakariya UniversityBahauddin Zakariya UniversityBahauddin Zakariya UniversityGovernment College UniversityUniversity of OkaraUniversity of FerraraKing Saud UniversityOctober University for Modern Sciences & ArtsNational University of Sciences and TechnologyPlant growth-promoting rhizobacteria (PGPRs) have been utilized to immobilize heavy metals, limiting their translocation in metal contaminated settings. However, studies on the mechanisms and interactions that elucidate how PGPRs mediate Nickel (Ni) tolerance in plants are rare. Thus, in this study we investigated how two pre-characterized heavy metal tolerant isolates of Morganella morganii (ABT9 and ABT3) improve Ni stress tolerance in Arabidopsis while enhancing its growth and yield. Arabidopsis seedlings were grown for five weeks in control/Ni contaminated (control, 1.5 mM and 2.5 mM) potted soil, in the presence or absence of PGPRs. Plant growth characteristics, quantum yield, and antioxidative enzymatic activities were analyzed to assess the influence of PGPRs on plant physiology. Oxidative stress tolerance was quantified by measuring MDA accumulation in Arabidopsis plants. As expected, Ni stress substantially reduced plant growth (shoot and root fresh weight by 53.25% and 58.77%, dry weight by 49.80% and 57.41% and length by 47.16% and 64.63% over control), chlorophyll content and quantum yield (by 40.21% and 54.37% over control). It also increased MDA content by 84.28% at higher (2.5 mM) Ni concentrations. In contrast, inoculation with M. morganii led to significant improvements in leaf chlorophyll, quantum yield, and Arabidopsis biomass production. The mitigation of adverse effects of Ni stress on biomass observed in M. morganii-inoculated plants was attributed to the enhancement of antioxidative enzyme activities compared to Ni-treated plants. This upregulation of the antioxidative defense mechanism mitigated Ni-induced oxidative stress, leading to improved performance of the photosynthetic machinery, which, in turn, enhanced chlorophyll content and quantum yield. Understanding the underlying mechanisms of these tolerance-inducing processes will help to complete the picture of PGPRs-mediated defense signaling. Thus, it suggests that M. morganii PGPRs candidate can potentially be utilized for plant growth promotion by reducing oxidative stress via upregulating antioxidant defense systems in Ni-contaminated soils and reducing Ni metal uptake.http://dx.doi.org/10.1080/15592324.2024.2318513heavy metalarabidopsis thalianaplant-growth-promoting rhizobacteriaquantum yieldmdasod
spellingShingle Tahir Naqqash
Aeman Aziz
Muhammad Baber
Muhammad Shahid
Muhammad Sajid
Radicetti Emanuele
Abdel-Rhman Z. Gaafar
Mohamed S. Hodhod
Ghulam Haider
Metal-tolerant morganella morganii isolates can potentially mediate nickel stress tolerance in Arabidopsis by upregulating antioxidative enzyme activities
Plant Signaling & Behavior
heavy metal
arabidopsis thaliana
plant-growth-promoting rhizobacteria
quantum yield
mda
sod
title Metal-tolerant morganella morganii isolates can potentially mediate nickel stress tolerance in Arabidopsis by upregulating antioxidative enzyme activities
title_full Metal-tolerant morganella morganii isolates can potentially mediate nickel stress tolerance in Arabidopsis by upregulating antioxidative enzyme activities
title_fullStr Metal-tolerant morganella morganii isolates can potentially mediate nickel stress tolerance in Arabidopsis by upregulating antioxidative enzyme activities
title_full_unstemmed Metal-tolerant morganella morganii isolates can potentially mediate nickel stress tolerance in Arabidopsis by upregulating antioxidative enzyme activities
title_short Metal-tolerant morganella morganii isolates can potentially mediate nickel stress tolerance in Arabidopsis by upregulating antioxidative enzyme activities
title_sort metal tolerant morganella morganii isolates can potentially mediate nickel stress tolerance in arabidopsis by upregulating antioxidative enzyme activities
topic heavy metal
arabidopsis thaliana
plant-growth-promoting rhizobacteria
quantum yield
mda
sod
url http://dx.doi.org/10.1080/15592324.2024.2318513
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