The Marine Endophytic Polyamine-Producing Streptomyces mutabilis UAE1 Isolated From Extreme Niches in the Arabian Gulf Promotes the Performance of Mangrove (Avicennia marina) Seedlings Under Greenhouse Conditions

Mangrove forests in the Arabian Gulf are under continuous threat. To increase plantations of gray mangrove (Avicennia marina) in the United Arab Emirates (UAE), 27 endophytic actinobacterial isolates obtained from mangrove roots were in vitro pre-screened to detect the polyamines (PAs) [putrescine (...

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Main Authors: Khaled A. El-Tarabily, Gaber A. Ramadan, Alaa A. Elbadawi, Amira H. Hassan, Saeed Tariq, Eman W. Ghazal, Mohammad I. Abo Gamar, Synan F. AbuQamar
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-07-01
Series:Frontiers in Marine Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmars.2021.710200/full
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author Khaled A. El-Tarabily
Khaled A. El-Tarabily
Gaber A. Ramadan
Alaa A. Elbadawi
Amira H. Hassan
Saeed Tariq
Eman W. Ghazal
Mohammad I. Abo Gamar
Synan F. AbuQamar
author_facet Khaled A. El-Tarabily
Khaled A. El-Tarabily
Gaber A. Ramadan
Alaa A. Elbadawi
Amira H. Hassan
Saeed Tariq
Eman W. Ghazal
Mohammad I. Abo Gamar
Synan F. AbuQamar
author_sort Khaled A. El-Tarabily
collection DOAJ
description Mangrove forests in the Arabian Gulf are under continuous threat. To increase plantations of gray mangrove (Avicennia marina) in the United Arab Emirates (UAE), 27 endophytic actinobacterial isolates obtained from mangrove roots were in vitro pre-screened to detect the polyamines (PAs) [putrescine (Put), spermidine (Spd), and spermine (Spm)]. We also determined the abilities of the endophytic PA-producing actinobacterial isolates in enhancing the growth of A. marina under greenhouse conditions. Although three highly PA-producing isolates were recovered from inside mangrove root tissues, Streptomyces mutabilis UAE1 constantly colonized root and stem inner tissues for 12 weeks, suggesting an endophytic association between this actinobacterial isolate and mangrove seedlings. When roots were inoculated with S. mutabilis, mangrove growth was remarkably enhanced under gnotobiotic and greenhouse conditions. This was evident from the significant (P < 0.05) increases in dry weight and length of root (66.7 and 65.5%, respectively) and shoot (64.8 and 58.0%, respectively), number of branches (64.3%), total leaf area (40.2%), and photosynthetic pigments (54.5% chlorophyll a; 40.0% chlorophyll b; and 53.1% carotenoids) of mangrove compared to the PA-non-producing Streptomyces sp. or control treatment. Growth promotion in plants treated with S. mutabilis was also supported by significant (P < 0.05) elevations in the contents of mangrove in planta PAs, auxins, and cytokinins, accompanied by a decrease in abscisic acid levels. No difference was, however, detected in growth and amounts of PAs or any plant growth regulators (PGRs) in plants treated with or without the PA-non-producing isolate. Our findings indicate that plant growth parameters can be enhanced as a consequence of secretion of Put, Spd, and Spm by S. mutabilis resulting in regulation of endogenous PAs and other PGRs in mangrove tissues. This study is the first record that aims to improve sustainable agricultural management practices using plant growth promoting (PGP) actinobacteria, endophytic in mangrove tissues to promote mangrove growth under greenhouse conditions. Such research may allow this region to be a model to study the synergistic S. mutabilis–mangrove interactions and the future impacts on mangrove reforestation in the Arabian Gulf and elsewhere where mangrove forests are in threat.
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spelling doaj.art-57c3dd9e5d494d9a9f13cae6e679578a2022-12-21T22:12:25ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452021-07-01810.3389/fmars.2021.710200710200The Marine Endophytic Polyamine-Producing Streptomyces mutabilis UAE1 Isolated From Extreme Niches in the Arabian Gulf Promotes the Performance of Mangrove (Avicennia marina) Seedlings Under Greenhouse ConditionsKhaled A. El-Tarabily0Khaled A. El-Tarabily1Gaber A. Ramadan2Alaa A. Elbadawi3Amira H. Hassan4Saeed Tariq5Eman W. Ghazal6Mohammad I. Abo Gamar7Synan F. AbuQamar8Department of Biology, United Arab Emirates University, Al-Ain, United Arab EmiratesHarry Butler Institute, Murdoch University, Murdoch, WA, AustraliaDepartment of Biology, United Arab Emirates University, Al-Ain, United Arab EmiratesDepartment of Biology, United Arab Emirates University, Al-Ain, United Arab EmiratesDepartment of Biology, United Arab Emirates University, Al-Ain, United Arab EmiratesDepartment of Anatomy, College of Medicine and Health Sciences, United Arab Emirates University, Al-Ain, United Arab EmiratesDepartment of Nutrition and Health, College of Medicine and Health Sciences, United Arab Emirates University, Al-Ain, United Arab EmiratesDepartment of Biological Sciences, Faculty of Science, Yarmouk University, Irbid, JordanDepartment of Biology, United Arab Emirates University, Al-Ain, United Arab EmiratesMangrove forests in the Arabian Gulf are under continuous threat. To increase plantations of gray mangrove (Avicennia marina) in the United Arab Emirates (UAE), 27 endophytic actinobacterial isolates obtained from mangrove roots were in vitro pre-screened to detect the polyamines (PAs) [putrescine (Put), spermidine (Spd), and spermine (Spm)]. We also determined the abilities of the endophytic PA-producing actinobacterial isolates in enhancing the growth of A. marina under greenhouse conditions. Although three highly PA-producing isolates were recovered from inside mangrove root tissues, Streptomyces mutabilis UAE1 constantly colonized root and stem inner tissues for 12 weeks, suggesting an endophytic association between this actinobacterial isolate and mangrove seedlings. When roots were inoculated with S. mutabilis, mangrove growth was remarkably enhanced under gnotobiotic and greenhouse conditions. This was evident from the significant (P < 0.05) increases in dry weight and length of root (66.7 and 65.5%, respectively) and shoot (64.8 and 58.0%, respectively), number of branches (64.3%), total leaf area (40.2%), and photosynthetic pigments (54.5% chlorophyll a; 40.0% chlorophyll b; and 53.1% carotenoids) of mangrove compared to the PA-non-producing Streptomyces sp. or control treatment. Growth promotion in plants treated with S. mutabilis was also supported by significant (P < 0.05) elevations in the contents of mangrove in planta PAs, auxins, and cytokinins, accompanied by a decrease in abscisic acid levels. No difference was, however, detected in growth and amounts of PAs or any plant growth regulators (PGRs) in plants treated with or without the PA-non-producing isolate. Our findings indicate that plant growth parameters can be enhanced as a consequence of secretion of Put, Spd, and Spm by S. mutabilis resulting in regulation of endogenous PAs and other PGRs in mangrove tissues. This study is the first record that aims to improve sustainable agricultural management practices using plant growth promoting (PGP) actinobacteria, endophytic in mangrove tissues to promote mangrove growth under greenhouse conditions. Such research may allow this region to be a model to study the synergistic S. mutabilis–mangrove interactions and the future impacts on mangrove reforestation in the Arabian Gulf and elsewhere where mangrove forests are in threat.https://www.frontiersin.org/articles/10.3389/fmars.2021.710200/fullendophytic actinobacteriahalophytemangroveplant growth promotionpolyamines
spellingShingle Khaled A. El-Tarabily
Khaled A. El-Tarabily
Gaber A. Ramadan
Alaa A. Elbadawi
Amira H. Hassan
Saeed Tariq
Eman W. Ghazal
Mohammad I. Abo Gamar
Synan F. AbuQamar
The Marine Endophytic Polyamine-Producing Streptomyces mutabilis UAE1 Isolated From Extreme Niches in the Arabian Gulf Promotes the Performance of Mangrove (Avicennia marina) Seedlings Under Greenhouse Conditions
Frontiers in Marine Science
endophytic actinobacteria
halophyte
mangrove
plant growth promotion
polyamines
title The Marine Endophytic Polyamine-Producing Streptomyces mutabilis UAE1 Isolated From Extreme Niches in the Arabian Gulf Promotes the Performance of Mangrove (Avicennia marina) Seedlings Under Greenhouse Conditions
title_full The Marine Endophytic Polyamine-Producing Streptomyces mutabilis UAE1 Isolated From Extreme Niches in the Arabian Gulf Promotes the Performance of Mangrove (Avicennia marina) Seedlings Under Greenhouse Conditions
title_fullStr The Marine Endophytic Polyamine-Producing Streptomyces mutabilis UAE1 Isolated From Extreme Niches in the Arabian Gulf Promotes the Performance of Mangrove (Avicennia marina) Seedlings Under Greenhouse Conditions
title_full_unstemmed The Marine Endophytic Polyamine-Producing Streptomyces mutabilis UAE1 Isolated From Extreme Niches in the Arabian Gulf Promotes the Performance of Mangrove (Avicennia marina) Seedlings Under Greenhouse Conditions
title_short The Marine Endophytic Polyamine-Producing Streptomyces mutabilis UAE1 Isolated From Extreme Niches in the Arabian Gulf Promotes the Performance of Mangrove (Avicennia marina) Seedlings Under Greenhouse Conditions
title_sort marine endophytic polyamine producing streptomyces mutabilis uae1 isolated from extreme niches in the arabian gulf promotes the performance of mangrove avicennia marina seedlings under greenhouse conditions
topic endophytic actinobacteria
halophyte
mangrove
plant growth promotion
polyamines
url https://www.frontiersin.org/articles/10.3389/fmars.2021.710200/full
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