Exogenous putrescine attenuates the negative impact of drought stress by modulating physio-biochemical traits and gene expression in sugar beet (Beta vulgaris L.)

Drought tolerance is a complex trait controlled by many metabolic pathways and genes and identifying a solution to increase the resilience of plants to drought stress is one of the grand challenges in plant biology. This study provided compelling evidence of increased drought stress tolerance in two...

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Veröffentlicht in:PloS one 2022-01, Vol.17 (1), p.e0262099
Hauptverfasser: Islam, Md Jahirul, Uddin, Md Jalal, Hossain, Mohammad Anwar, Henry, Robert, Begum, Mst Kohinoor, Sohel, Md Abu Taher, Mou, Masuma Akter, Ahn, Juhee, Cheong, Eun Ju, Lim, Young-Seok
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container_issue 1
container_start_page e0262099
container_title PloS one
container_volume 17
creator Islam, Md Jahirul
Uddin, Md Jalal
Hossain, Mohammad Anwar
Henry, Robert
Begum, Mst Kohinoor
Sohel, Md Abu Taher
Mou, Masuma Akter
Ahn, Juhee
Cheong, Eun Ju
Lim, Young-Seok
description Drought tolerance is a complex trait controlled by many metabolic pathways and genes and identifying a solution to increase the resilience of plants to drought stress is one of the grand challenges in plant biology. This study provided compelling evidence of increased drought stress tolerance in two sugar beet genotypes when treated with exogenous putrescine (Put) at the seedling stage. Morpho-physiological and biochemical traits and gene expression were assessed in thirty-day-old sugar beet seedlings subjected to drought stress with or without Put (0.3, 0.6, and 0.9 mM) application. Sugar beet plants exposed to drought stress exhibited a significant decline in growth and development as evidenced by root and shoot growth characteristics, photosynthetic pigments, antioxidant enzyme activities, and gene expression. Drought stress resulted in a sharp increase in hydrogen peroxide (H2O2) (89.4 and 118% in SBT-010 and BSRI Sugar beet 2, respectively) and malondialdehyde (MDA) (35.6 and 27.1% in SBT-010 and BSRI Sugar beet 2, respectively). These changes were strongly linked to growth retardation as evidenced by principal component analysis (PCA) and heatmap clustering. Importantly, Put-sprayed plants suffered from less oxidative stress as indicated by lower H2O2 and MDA accumulation. They better regulated the physiological processes supporting growth, dry matter accumulation, photosynthetic pigmentation and gas exchange, relative water content; modulated biochemical changes including proline, total soluble carbohydrate, total soluble sugar, and ascorbic acid; and enhanced the activities of antioxidant enzymes and gene expression. PCA results strongly suggested that Put conferred drought tolerance mostly by enhancing antioxidant enzymes activities that regulated homeostasis of reactive oxygen species. These findings collectively provide an important illustration of the use of Put in modulating drought tolerance in sugar beet plants.
doi_str_mv 10.1371/journal.pone.0262099
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This study provided compelling evidence of increased drought stress tolerance in two sugar beet genotypes when treated with exogenous putrescine (Put) at the seedling stage. Morpho-physiological and biochemical traits and gene expression were assessed in thirty-day-old sugar beet seedlings subjected to drought stress with or without Put (0.3, 0.6, and 0.9 mM) application. Sugar beet plants exposed to drought stress exhibited a significant decline in growth and development as evidenced by root and shoot growth characteristics, photosynthetic pigments, antioxidant enzyme activities, and gene expression. Drought stress resulted in a sharp increase in hydrogen peroxide (H2O2) (89.4 and 118% in SBT-010 and BSRI Sugar beet 2, respectively) and malondialdehyde (MDA) (35.6 and 27.1% in SBT-010 and BSRI Sugar beet 2, respectively). These changes were strongly linked to growth retardation as evidenced by principal component analysis (PCA) and heatmap clustering. 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These findings collectively provide an important illustration of the use of Put in modulating drought tolerance in sugar beet plants.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0262099</identifier><identifier>PMID: 34995297</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Accumulation ; Agricultural production ; Analysis ; Antioxidants ; Antioxidants - pharmacology ; Ascorbic acid ; Beta vulgaris ; Beta vulgaris - drug effects ; Beta vulgaris - genetics ; Beta vulgaris - metabolism ; Biochemistry ; Biology and Life Sciences ; Carbohydrates ; Clustering ; Drought ; Drought resistance ; Droughts ; Dry matter ; Ecology and Environmental Sciences ; Environmental impact ; Enzymatic activity ; Enzymes ; Gas exchange ; Gene expression ; Gene Expression Regulation, Plant - drug effects ; Genotypes ; Growth rate ; Homeostasis ; Hydrogen ; Hydrogen peroxide ; Influence ; Malondialdehyde ; Metabolic pathways ; Moisture content ; Oxidative Stress ; Oxygen ; Photosynthesis ; Photosynthetic pigments ; Physical Sciences ; Physiology ; Pigmentation ; Pigments ; Plant growth ; Plant physiology ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plant Shoots - drug effects ; Plant Shoots - genetics ; Plant Shoots - metabolism ; Principal components analysis ; Proline ; Putrescine ; Putrescine - pharmacology ; Reactive oxygen species ; Reactive Oxygen Species - metabolism ; Seedlings ; Seeds ; South Korea ; Stress, Physiological ; Sugar ; Sugar beets ; Water content</subject><ispartof>PloS one, 2022-01, Vol.17 (1), p.e0262099</ispartof><rights>COPYRIGHT 2022 Public Library of Science</rights><rights>2022 Islam et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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This study provided compelling evidence of increased drought stress tolerance in two sugar beet genotypes when treated with exogenous putrescine (Put) at the seedling stage. Morpho-physiological and biochemical traits and gene expression were assessed in thirty-day-old sugar beet seedlings subjected to drought stress with or without Put (0.3, 0.6, and 0.9 mM) application. Sugar beet plants exposed to drought stress exhibited a significant decline in growth and development as evidenced by root and shoot growth characteristics, photosynthetic pigments, antioxidant enzyme activities, and gene expression. Drought stress resulted in a sharp increase in hydrogen peroxide (H2O2) (89.4 and 118% in SBT-010 and BSRI Sugar beet 2, respectively) and malondialdehyde (MDA) (35.6 and 27.1% in SBT-010 and BSRI Sugar beet 2, respectively). These changes were strongly linked to growth retardation as evidenced by principal component analysis (PCA) and heatmap clustering. 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These findings collectively provide an important illustration of the use of Put in modulating drought tolerance in sugar beet plants.</description><subject>Accumulation</subject><subject>Agricultural production</subject><subject>Analysis</subject><subject>Antioxidants</subject><subject>Antioxidants - pharmacology</subject><subject>Ascorbic acid</subject><subject>Beta vulgaris</subject><subject>Beta vulgaris - drug effects</subject><subject>Beta vulgaris - genetics</subject><subject>Beta vulgaris - metabolism</subject><subject>Biochemistry</subject><subject>Biology and Life Sciences</subject><subject>Carbohydrates</subject><subject>Clustering</subject><subject>Drought</subject><subject>Drought resistance</subject><subject>Droughts</subject><subject>Dry matter</subject><subject>Ecology and Environmental Sciences</subject><subject>Environmental impact</subject><subject>Enzymatic activity</subject><subject>Enzymes</subject><subject>Gas exchange</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant - drug effects</subject><subject>Genotypes</subject><subject>Growth rate</subject><subject>Homeostasis</subject><subject>Hydrogen</subject><subject>Hydrogen peroxide</subject><subject>Influence</subject><subject>Malondialdehyde</subject><subject>Metabolic pathways</subject><subject>Moisture content</subject><subject>Oxidative Stress</subject><subject>Oxygen</subject><subject>Photosynthesis</subject><subject>Photosynthetic pigments</subject><subject>Physical Sciences</subject><subject>Physiology</subject><subject>Pigmentation</subject><subject>Pigments</subject><subject>Plant growth</subject><subject>Plant physiology</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plant Shoots - drug effects</subject><subject>Plant Shoots - genetics</subject><subject>Plant Shoots - metabolism</subject><subject>Principal components analysis</subject><subject>Proline</subject><subject>Putrescine</subject><subject>Putrescine - pharmacology</subject><subject>Reactive oxygen species</subject><subject>Reactive Oxygen Species - metabolism</subject><subject>Seedlings</subject><subject>Seeds</subject><subject>South Korea</subject><subject>Stress, Physiological</subject><subject>Sugar</subject><subject>Sugar beets</subject><subject>Water content</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>3HK</sourceid><sourceid>DOA</sourceid><recordid>eNqNk91q3DAQhU1padJt36C0gkJpLnYrWbJs3RTSkLaBQKB_t2JWHtsKXsm15LB5nT5ptYkTstBC8YXt0XdmRkeaLHvJ6Irxkr2_9NPooF8N3uGK5jKnSj3KDpni-TL98McPvg-yZyFcUlrwSsqn2QEXShW5Kg-z36db36LzUyDDFEcMxjokECO6CSIGEjskDluI9gqJ3QxgIvENqUc_tV0kYacJZH1NNr6e-oS5lgzddbB-ubbedLixBnoSR7AxEHA1SeWQ4HbYCa13xDoSphZGskaM5N1HjECupj5FbCDnq6Pn2ZMG-oAv5vci-_Hp9PvJl-X5xeezk-PzpSmZjEtu6jLnoqrqQpZQqYoLUzO5rvO1rEvFDSCURaOkoQoAiqKRtcobVaPIJcuBL7LXt3mH3gc92xt0WixLUVFZJeLslqg9XOphtBsYr7UHq28Cfmw1jNGaHjVXtDDCYNkgFawoKiWgMjJt0TAh0pEssg9ztWm9wdqgSxb1e0n3V5ztdOuvdFUKRm8SzO2a5FOyXTs_gmaU8jL1zAuRiDdzidH_mjDEf2xqplpIfVvX-FTObGww-lhWlZI5S74ustVfqPTUuwNOV7CxKb4nONoTJCbiNrYwhaDPvn39f_bi5z779gHbIfSxC76fYrpKYR8Ud_74EEZs7r1lVO8m6M4NvZsgPU9Qkr16eC73oruR4X8AfqQYcw</recordid><startdate>20220107</startdate><enddate>20220107</enddate><creator>Islam, Md Jahirul</creator><creator>Uddin, Md Jalal</creator><creator>Hossain, Mohammad Anwar</creator><creator>Henry, Robert</creator><creator>Begum, Mst Kohinoor</creator><creator>Sohel, Md Abu Taher</creator><creator>Mou, Masuma Akter</creator><creator>Ahn, Juhee</creator><creator>Cheong, Eun Ju</creator><creator>Lim, Young-Seok</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>3HK</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-9415-012X</orcidid><orcidid>https://orcid.org/0000-0002-4060-0292</orcidid><orcidid>https://orcid.org/0000-0003-3950-3599</orcidid><orcidid>https://orcid.org/0000-0002-3349-7741</orcidid><orcidid>https://orcid.org/0000-0001-9341-009X</orcidid></search><sort><creationdate>20220107</creationdate><title>Exogenous putrescine attenuates the negative impact of drought stress by modulating physio-biochemical traits and gene expression in sugar beet (Beta vulgaris L.)</title><author>Islam, Md Jahirul ; Uddin, Md Jalal ; Hossain, Mohammad Anwar ; Henry, Robert ; Begum, Mst Kohinoor ; Sohel, Md Abu Taher ; Mou, Masuma Akter ; Ahn, Juhee ; Cheong, Eun Ju ; Lim, Young-Seok</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c716t-3cd723488d567a89834cd16bd2b6d793caea75f96c09aaa55f6d92f9de42612a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Accumulation</topic><topic>Agricultural production</topic><topic>Analysis</topic><topic>Antioxidants</topic><topic>Antioxidants - pharmacology</topic><topic>Ascorbic acid</topic><topic>Beta vulgaris</topic><topic>Beta vulgaris - drug effects</topic><topic>Beta vulgaris - genetics</topic><topic>Beta vulgaris - metabolism</topic><topic>Biochemistry</topic><topic>Biology and Life Sciences</topic><topic>Carbohydrates</topic><topic>Clustering</topic><topic>Drought</topic><topic>Drought resistance</topic><topic>Droughts</topic><topic>Dry matter</topic><topic>Ecology and Environmental Sciences</topic><topic>Environmental impact</topic><topic>Enzymatic activity</topic><topic>Enzymes</topic><topic>Gas exchange</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Plant - drug effects</topic><topic>Genotypes</topic><topic>Growth rate</topic><topic>Homeostasis</topic><topic>Hydrogen</topic><topic>Hydrogen peroxide</topic><topic>Influence</topic><topic>Malondialdehyde</topic><topic>Metabolic pathways</topic><topic>Moisture content</topic><topic>Oxidative Stress</topic><topic>Oxygen</topic><topic>Photosynthesis</topic><topic>Photosynthetic pigments</topic><topic>Physical Sciences</topic><topic>Physiology</topic><topic>Pigmentation</topic><topic>Pigments</topic><topic>Plant growth</topic><topic>Plant physiology</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plant Shoots - drug effects</topic><topic>Plant Shoots - genetics</topic><topic>Plant Shoots - metabolism</topic><topic>Principal components analysis</topic><topic>Proline</topic><topic>Putrescine</topic><topic>Putrescine - pharmacology</topic><topic>Reactive oxygen species</topic><topic>Reactive Oxygen Species - metabolism</topic><topic>Seedlings</topic><topic>Seeds</topic><topic>South Korea</topic><topic>Stress, Physiological</topic><topic>Sugar</topic><topic>Sugar beets</topic><topic>Water content</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Islam, Md Jahirul</creatorcontrib><creatorcontrib>Uddin, Md Jalal</creatorcontrib><creatorcontrib>Hossain, Mohammad Anwar</creatorcontrib><creatorcontrib>Henry, Robert</creatorcontrib><creatorcontrib>Begum, Mst Kohinoor</creatorcontrib><creatorcontrib>Sohel, Md Abu Taher</creatorcontrib><creatorcontrib>Mou, Masuma Akter</creatorcontrib><creatorcontrib>Ahn, Juhee</creatorcontrib><creatorcontrib>Cheong, Eun Ju</creatorcontrib><creatorcontrib>Lim, Young-Seok</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing &amp; Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological &amp; Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health &amp; Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science &amp; Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies &amp; Aerospace Collection</collection><collection>Agricultural &amp; Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing &amp; Allied Health Database (Alumni Edition)</collection><collection>Meteorological &amp; Geoastrophysical Abstracts - 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Norwegian Open Research Archives</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Islam, Md Jahirul</au><au>Uddin, Md Jalal</au><au>Hossain, Mohammad Anwar</au><au>Henry, Robert</au><au>Begum, Mst Kohinoor</au><au>Sohel, Md Abu Taher</au><au>Mou, Masuma Akter</au><au>Ahn, Juhee</au><au>Cheong, Eun Ju</au><au>Lim, Young-Seok</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Exogenous putrescine attenuates the negative impact of drought stress by modulating physio-biochemical traits and gene expression in sugar beet (Beta vulgaris L.)</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2022-01-07</date><risdate>2022</risdate><volume>17</volume><issue>1</issue><spage>e0262099</spage><pages>e0262099-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Drought tolerance is a complex trait controlled by many metabolic pathways and genes and identifying a solution to increase the resilience of plants to drought stress is one of the grand challenges in plant biology. This study provided compelling evidence of increased drought stress tolerance in two sugar beet genotypes when treated with exogenous putrescine (Put) at the seedling stage. Morpho-physiological and biochemical traits and gene expression were assessed in thirty-day-old sugar beet seedlings subjected to drought stress with or without Put (0.3, 0.6, and 0.9 mM) application. Sugar beet plants exposed to drought stress exhibited a significant decline in growth and development as evidenced by root and shoot growth characteristics, photosynthetic pigments, antioxidant enzyme activities, and gene expression. Drought stress resulted in a sharp increase in hydrogen peroxide (H2O2) (89.4 and 118% in SBT-010 and BSRI Sugar beet 2, respectively) and malondialdehyde (MDA) (35.6 and 27.1% in SBT-010 and BSRI Sugar beet 2, respectively). These changes were strongly linked to growth retardation as evidenced by principal component analysis (PCA) and heatmap clustering. Importantly, Put-sprayed plants suffered from less oxidative stress as indicated by lower H2O2 and MDA accumulation. They better regulated the physiological processes supporting growth, dry matter accumulation, photosynthetic pigmentation and gas exchange, relative water content; modulated biochemical changes including proline, total soluble carbohydrate, total soluble sugar, and ascorbic acid; and enhanced the activities of antioxidant enzymes and gene expression. PCA results strongly suggested that Put conferred drought tolerance mostly by enhancing antioxidant enzymes activities that regulated homeostasis of reactive oxygen species. These findings collectively provide an important illustration of the use of Put in modulating drought tolerance in sugar beet plants.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>34995297</pmid><doi>10.1371/journal.pone.0262099</doi><tpages>e0262099</tpages><orcidid>https://orcid.org/0000-0001-9415-012X</orcidid><orcidid>https://orcid.org/0000-0002-4060-0292</orcidid><orcidid>https://orcid.org/0000-0003-3950-3599</orcidid><orcidid>https://orcid.org/0000-0002-3349-7741</orcidid><orcidid>https://orcid.org/0000-0001-9341-009X</orcidid><oa>free_for_read</oa></addata></record>
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1932-6203
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subjects Accumulation
Agricultural production
Analysis
Antioxidants
Antioxidants - pharmacology
Ascorbic acid
Beta vulgaris
Beta vulgaris - drug effects
Beta vulgaris - genetics
Beta vulgaris - metabolism
Biochemistry
Biology and Life Sciences
Carbohydrates
Clustering
Drought
Drought resistance
Droughts
Dry matter
Ecology and Environmental Sciences
Environmental impact
Enzymatic activity
Enzymes
Gas exchange
Gene expression
Gene Expression Regulation, Plant - drug effects
Genotypes
Growth rate
Homeostasis
Hydrogen
Hydrogen peroxide
Influence
Malondialdehyde
Metabolic pathways
Moisture content
Oxidative Stress
Oxygen
Photosynthesis
Photosynthetic pigments
Physical Sciences
Physiology
Pigmentation
Pigments
Plant growth
Plant physiology
Plant Proteins - genetics
Plant Proteins - metabolism
Plant Shoots - drug effects
Plant Shoots - genetics
Plant Shoots - metabolism
Principal components analysis
Proline
Putrescine
Putrescine - pharmacology
Reactive oxygen species
Reactive Oxygen Species - metabolism
Seedlings
Seeds
South Korea
Stress, Physiological
Sugar
Sugar beets
Water content
title Exogenous putrescine attenuates the negative impact of drought stress by modulating physio-biochemical traits and gene expression in sugar beet (Beta vulgaris L.)
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