Comparative root transcriptome analysis of Kandelia candel Druce and Rhizophora mucronata Lam. germinating propagules under salinity gradients reveal their tolerance mechanisms and ecological adaptations
The mangrove ecosystems are characterised by high salinity and hypoxia. When viviparous mangrove propagules detach from the mother plants and find a substratum, their roots must respond appropriately to the external environment. Therefore, for an improved understanding of the dynamics of mangrove ad...
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description | The mangrove ecosystems are characterised by high salinity and hypoxia. When viviparous mangrove propagules detach from the mother plants and find a substratum, their roots must respond appropriately to the external environment. Therefore, for an improved understanding of the dynamics of mangrove adaptations to fluctuating intertidal habitats, root transcriptomic and anatomical responses of the germinated propagules of
Rhizophora mucronata
Lam. and
Kandelia candel
Druce were analysed. Both species had larger cortexes with aerenchyma spaces, and root cortical/stelar area decreased above five parts per thousand (ppt) of salinity treatment after 60 days. The percentage of suberised endodermal cells in
R. mucronata
was above 80%, while it increased in
K. candel
after 60 days of treatment. De novo transcriptome sequencing of
K. candel
and
R. mucronata
at 45 and 60 days after salinity treatments identified 766,040 and 558,190 transcripts with predicted open reading frames, respectively, and differential gene expression analysis unveiled ~ 16,000 salt-responsive transcripts. Gene ontology analysis showed enrichment of transcripts related to cell wall biosynthesis (cellulose synthase, expansins), membrane transporters (aquaporins, salt overly sensitive 1, vacuolar ATPase), and hormone signal transduction (delay of germination 1 domain-containing protein, auxin-responsive protein). Interestingly, the differentially expressed solute transporter protein transcripts were higher in
K. candel
than in
R. mucronata.
Pathway enrichment analysis revealed the significant expression of flavonoid/flavonol and taurine/hypotaurine biosynthesis pathways, indicating the role of specialised metabolites in stress response. A total of 10 differentially expressed transcripts were validated using qRT-PCR, and a positive correlation of 0.62 (
K. candel
) and 0.68 (
R. mucronata
) was observed between the RNA sequencing data and qRT-PCR. Overall, this study contributes to understanding mangrove ecological adaptations and stress response mechanisms to salinity stress in the early developing propagules. |
doi_str_mv | 10.1007/s10725-024-01125-1 |
format | Article |
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Rhizophora mucronata
Lam. and
Kandelia candel
Druce were analysed. Both species had larger cortexes with aerenchyma spaces, and root cortical/stelar area decreased above five parts per thousand (ppt) of salinity treatment after 60 days. The percentage of suberised endodermal cells in
R. mucronata
was above 80%, while it increased in
K. candel
after 60 days of treatment. De novo transcriptome sequencing of
K. candel
and
R. mucronata
at 45 and 60 days after salinity treatments identified 766,040 and 558,190 transcripts with predicted open reading frames, respectively, and differential gene expression analysis unveiled ~ 16,000 salt-responsive transcripts. Gene ontology analysis showed enrichment of transcripts related to cell wall biosynthesis (cellulose synthase, expansins), membrane transporters (aquaporins, salt overly sensitive 1, vacuolar ATPase), and hormone signal transduction (delay of germination 1 domain-containing protein, auxin-responsive protein). Interestingly, the differentially expressed solute transporter protein transcripts were higher in
K. candel
than in
R. mucronata.
Pathway enrichment analysis revealed the significant expression of flavonoid/flavonol and taurine/hypotaurine biosynthesis pathways, indicating the role of specialised metabolites in stress response. A total of 10 differentially expressed transcripts were validated using qRT-PCR, and a positive correlation of 0.62 (
K. candel
) and 0.68 (
R. mucronata
) was observed between the RNA sequencing data and qRT-PCR. Overall, this study contributes to understanding mangrove ecological adaptations and stress response mechanisms to salinity stress in the early developing propagules.</description><identifier>ISSN: 0167-6903</identifier><identifier>EISSN: 1573-5087</identifier><identifier>DOI: 10.1007/s10725-024-01125-1</identifier><language>eng</language><publisher>Dordrecht: Springer Netherlands</publisher><subject>Adaptation ; Agriculture ; Aquaporins ; Biomedical and Life Sciences ; Biosynthesis ; Cell walls ; Cellulose ; Cellulose synthase ; Ecological adaptation ; Flavonoids ; Flavonols ; Gene expression ; Gene sequencing ; Germination ; Hypoxia ; Kandelia candel ; Life Sciences ; Mangroves ; Metabolites ; Open reading frames ; Original Paper ; Plant Anatomy/Development ; Plant Physiology ; Plant Sciences ; Propagules ; Protein transport ; Proteins ; Rhizophora mucronata ; Salinity ; Salinity effects ; Signal transduction ; Taurine ; Transcriptomes ; Transcriptomics</subject><ispartof>Plant growth regulation, 2024-07, Vol.103 (3), p.539-563</ispartof><rights>The Author(s), under exclusive licence to Springer Nature B.V. 2024. 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.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c270t-4982a3e79a6928c710d6149cf8675efd088e2a741620bceb9b71f8610f7d6db73</cites><orcidid>0000-0001-7436-5000</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s10725-024-01125-1$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s10725-024-01125-1$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,780,784,27924,27925,41488,42557,51319</link.rule.ids></links><search><creatorcontrib>Nizam, Ashifa</creatorcontrib><creatorcontrib>Rawoof, Abdul</creatorcontrib><creatorcontrib>Adot, Vivek</creatorcontrib><creatorcontrib>Madhavan, Chithra</creatorcontrib><creatorcontrib>Ramchiary, Nirala</creatorcontrib><creatorcontrib>Kumar, Ajay</creatorcontrib><title>Comparative root transcriptome analysis of Kandelia candel Druce and Rhizophora mucronata Lam. germinating propagules under salinity gradients reveal their tolerance mechanisms and ecological adaptations</title><title>Plant growth regulation</title><addtitle>Plant Growth Regul</addtitle><description>The mangrove ecosystems are characterised by high salinity and hypoxia. When viviparous mangrove propagules detach from the mother plants and find a substratum, their roots must respond appropriately to the external environment. Therefore, for an improved understanding of the dynamics of mangrove adaptations to fluctuating intertidal habitats, root transcriptomic and anatomical responses of the germinated propagules of
Rhizophora mucronata
Lam. and
Kandelia candel
Druce were analysed. Both species had larger cortexes with aerenchyma spaces, and root cortical/stelar area decreased above five parts per thousand (ppt) of salinity treatment after 60 days. The percentage of suberised endodermal cells in
R. mucronata
was above 80%, while it increased in
K. candel
after 60 days of treatment. De novo transcriptome sequencing of
K. candel
and
R. mucronata
at 45 and 60 days after salinity treatments identified 766,040 and 558,190 transcripts with predicted open reading frames, respectively, and differential gene expression analysis unveiled ~ 16,000 salt-responsive transcripts. Gene ontology analysis showed enrichment of transcripts related to cell wall biosynthesis (cellulose synthase, expansins), membrane transporters (aquaporins, salt overly sensitive 1, vacuolar ATPase), and hormone signal transduction (delay of germination 1 domain-containing protein, auxin-responsive protein). Interestingly, the differentially expressed solute transporter protein transcripts were higher in
K. candel
than in
R. mucronata.
Pathway enrichment analysis revealed the significant expression of flavonoid/flavonol and taurine/hypotaurine biosynthesis pathways, indicating the role of specialised metabolites in stress response. A total of 10 differentially expressed transcripts were validated using qRT-PCR, and a positive correlation of 0.62 (
K. candel
) and 0.68 (
R. mucronata
) was observed between the RNA sequencing data and qRT-PCR. Overall, this study contributes to understanding mangrove ecological adaptations and stress response mechanisms to salinity stress in the early developing propagules.</description><subject>Adaptation</subject><subject>Agriculture</subject><subject>Aquaporins</subject><subject>Biomedical and Life Sciences</subject><subject>Biosynthesis</subject><subject>Cell walls</subject><subject>Cellulose</subject><subject>Cellulose synthase</subject><subject>Ecological adaptation</subject><subject>Flavonoids</subject><subject>Flavonols</subject><subject>Gene expression</subject><subject>Gene sequencing</subject><subject>Germination</subject><subject>Hypoxia</subject><subject>Kandelia candel</subject><subject>Life Sciences</subject><subject>Mangroves</subject><subject>Metabolites</subject><subject>Open reading frames</subject><subject>Original Paper</subject><subject>Plant Anatomy/Development</subject><subject>Plant Physiology</subject><subject>Plant Sciences</subject><subject>Propagules</subject><subject>Protein transport</subject><subject>Proteins</subject><subject>Rhizophora mucronata</subject><subject>Salinity</subject><subject>Salinity effects</subject><subject>Signal transduction</subject><subject>Taurine</subject><subject>Transcriptomes</subject><subject>Transcriptomics</subject><issn>0167-6903</issn><issn>1573-5087</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>8G5</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNp9UcFu1DAQtRBILG1_gNNInFPGySZOjmiBglgJCdGzNetMsq4SO9hOpeUX-1O4u0jcOM2M_N6b8XtCvJV4KxHV-yhRlXWB5bZAKXMnX4iNrFVV1Niql2KDslFF02H1WryJ8QER27aWG_G08_NCgZJ9ZAjeJ0iBXDTBLsnPDORoOkUbwQ_wjVzPkyUw5wY-htU8I3r4cbS__XL0gWBeTfCOEsGe5lsYOcw2j9aNsAS_0LhOHGHNAgEiTdbZdIIxUG_ZpQiBH5kmSEe2AZKfOF-Tl8xsjuRsnON5Hxs_-dGajKSelpT1vYvX4tVAU-Sbv_VK3H_-9HP3pdh_v_u6-7AvTKkwFduuLali1VHTla1REvtGbjsztI2qeeizM1yS2sqmxIPhQ3dQMr9JHFTf9AdVXYl3F938oV8rx6Qf_BqyUVFXqGrVtgq7jCovqOxHjIEHvQQ7Uzhpifo5NH0JTefQ9Dk0LTOpupBiBrts3j_p_7D-AGz5oE8</recordid><startdate>20240701</startdate><enddate>20240701</enddate><creator>Nizam, Ashifa</creator><creator>Rawoof, Abdul</creator><creator>Adot, Vivek</creator><creator>Madhavan, Chithra</creator><creator>Ramchiary, Nirala</creator><creator>Kumar, Ajay</creator><general>Springer Netherlands</general><general>Springer Nature B.V</general><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7X2</scope><scope>7XB</scope><scope>8FE</scope><scope>8FH</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>HCIFZ</scope><scope>LK8</scope><scope>M0K</scope><scope>M2O</scope><scope>M7P</scope><scope>MBDVC</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><orcidid>https://orcid.org/0000-0001-7436-5000</orcidid></search><sort><creationdate>20240701</creationdate><title>Comparative root transcriptome analysis of Kandelia candel Druce and Rhizophora mucronata Lam. germinating propagules under salinity gradients reveal their tolerance mechanisms and ecological adaptations</title><author>Nizam, Ashifa ; Rawoof, Abdul ; Adot, Vivek ; Madhavan, Chithra ; Ramchiary, Nirala ; Kumar, Ajay</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c270t-4982a3e79a6928c710d6149cf8675efd088e2a741620bceb9b71f8610f7d6db73</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Adaptation</topic><topic>Agriculture</topic><topic>Aquaporins</topic><topic>Biomedical and Life Sciences</topic><topic>Biosynthesis</topic><topic>Cell walls</topic><topic>Cellulose</topic><topic>Cellulose synthase</topic><topic>Ecological adaptation</topic><topic>Flavonoids</topic><topic>Flavonols</topic><topic>Gene expression</topic><topic>Gene sequencing</topic><topic>Germination</topic><topic>Hypoxia</topic><topic>Kandelia candel</topic><topic>Life Sciences</topic><topic>Mangroves</topic><topic>Metabolites</topic><topic>Open reading frames</topic><topic>Original Paper</topic><topic>Plant Anatomy/Development</topic><topic>Plant Physiology</topic><topic>Plant Sciences</topic><topic>Propagules</topic><topic>Protein transport</topic><topic>Proteins</topic><topic>Rhizophora mucronata</topic><topic>Salinity</topic><topic>Salinity effects</topic><topic>Signal transduction</topic><topic>Taurine</topic><topic>Transcriptomes</topic><topic>Transcriptomics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Nizam, Ashifa</creatorcontrib><creatorcontrib>Rawoof, Abdul</creatorcontrib><creatorcontrib>Adot, Vivek</creatorcontrib><creatorcontrib>Madhavan, Chithra</creatorcontrib><creatorcontrib>Ramchiary, Nirala</creatorcontrib><creatorcontrib>Kumar, Ajay</creatorcontrib><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Agricultural Science Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Research Library (Alumni Edition)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>ProQuest Central Student</collection><collection>Research Library Prep</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Research Library</collection><collection>Biological Science Database</collection><collection>Research Library (Corporate)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central Basic</collection><jtitle>Plant growth regulation</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Nizam, Ashifa</au><au>Rawoof, Abdul</au><au>Adot, Vivek</au><au>Madhavan, Chithra</au><au>Ramchiary, Nirala</au><au>Kumar, Ajay</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Comparative root transcriptome analysis of Kandelia candel Druce and Rhizophora mucronata Lam. germinating propagules under salinity gradients reveal their tolerance mechanisms and ecological adaptations</atitle><jtitle>Plant growth regulation</jtitle><stitle>Plant Growth Regul</stitle><date>2024-07-01</date><risdate>2024</risdate><volume>103</volume><issue>3</issue><spage>539</spage><epage>563</epage><pages>539-563</pages><issn>0167-6903</issn><eissn>1573-5087</eissn><abstract>The mangrove ecosystems are characterised by high salinity and hypoxia. When viviparous mangrove propagules detach from the mother plants and find a substratum, their roots must respond appropriately to the external environment. Therefore, for an improved understanding of the dynamics of mangrove adaptations to fluctuating intertidal habitats, root transcriptomic and anatomical responses of the germinated propagules of
Rhizophora mucronata
Lam. and
Kandelia candel
Druce were analysed. Both species had larger cortexes with aerenchyma spaces, and root cortical/stelar area decreased above five parts per thousand (ppt) of salinity treatment after 60 days. The percentage of suberised endodermal cells in
R. mucronata
was above 80%, while it increased in
K. candel
after 60 days of treatment. De novo transcriptome sequencing of
K. candel
and
R. mucronata
at 45 and 60 days after salinity treatments identified 766,040 and 558,190 transcripts with predicted open reading frames, respectively, and differential gene expression analysis unveiled ~ 16,000 salt-responsive transcripts. Gene ontology analysis showed enrichment of transcripts related to cell wall biosynthesis (cellulose synthase, expansins), membrane transporters (aquaporins, salt overly sensitive 1, vacuolar ATPase), and hormone signal transduction (delay of germination 1 domain-containing protein, auxin-responsive protein). Interestingly, the differentially expressed solute transporter protein transcripts were higher in
K. candel
than in
R. mucronata.
Pathway enrichment analysis revealed the significant expression of flavonoid/flavonol and taurine/hypotaurine biosynthesis pathways, indicating the role of specialised metabolites in stress response. A total of 10 differentially expressed transcripts were validated using qRT-PCR, and a positive correlation of 0.62 (
K. candel
) and 0.68 (
R. mucronata
) was observed between the RNA sequencing data and qRT-PCR. Overall, this study contributes to understanding mangrove ecological adaptations and stress response mechanisms to salinity stress in the early developing propagules.</abstract><cop>Dordrecht</cop><pub>Springer Netherlands</pub><doi>10.1007/s10725-024-01125-1</doi><tpages>25</tpages><orcidid>https://orcid.org/0000-0001-7436-5000</orcidid></addata></record> |
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subjects | Adaptation Agriculture Aquaporins Biomedical and Life Sciences Biosynthesis Cell walls Cellulose Cellulose synthase Ecological adaptation Flavonoids Flavonols Gene expression Gene sequencing Germination Hypoxia Kandelia candel Life Sciences Mangroves Metabolites Open reading frames Original Paper Plant Anatomy/Development Plant Physiology Plant Sciences Propagules Protein transport Proteins Rhizophora mucronata Salinity Salinity effects Signal transduction Taurine Transcriptomes Transcriptomics |
title | Comparative root transcriptome analysis of Kandelia candel Druce and Rhizophora mucronata Lam. germinating propagules under salinity gradients reveal their tolerance mechanisms and ecological adaptations |
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