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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Veröffentlicht in:Plant growth regulation 2024-07, Vol.103 (3), p.539-563
Hauptverfasser: Nizam, Ashifa, Rawoof, Abdul, Adot, Vivek, Madhavan, Chithra, Ramchiary, Nirala, Kumar, Ajay
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creator Nizam, Ashifa
Rawoof, Abdul
Adot, Vivek
Madhavan, Chithra
Ramchiary, Nirala
Kumar, Ajay
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
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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. 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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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