Tissue-Specific Transcriptomes Outline Halophyte Adaptive Strategies in the Gray Mangrove (Avicennia marina)

David R. Nelson; Amphun Chaiboonchoe; Khaled M. Hazzouri; Basel Khraiwesh; Amnah Alzahmi; Ashish Jaiswal; Guillermo Friis; John A. Burt; Khaled M. A. Amiri; Kourosh Salehi-Ashtiani

doi:10.3390/agronomy12092030

Tissue-Specific Transcriptomes Outline Halophyte Adaptive Strategies in the Gray Mangrove (Avicennia marina)

David R. Nelson, Amphun Chaiboonchoe, Khaled M. Hazzouri, Basel Khraiwesh, Amnah Alzahmi, Ashish Jaiswal, Guillermo Friis, John A. Burt, Khaled M. A. Amiri, Kourosh Salehi-Ashtiani

Research output: Contribution to journal › Article › peer-review

3 Scopus citations

Abstract

Avicennia marina forests fulfill essential blue carbon and ecosystem services, including halting coastal erosion and supporting fisheries. Genetic studies of A. marina tissues could yield insight into halophyte adaptive strategies, empowering saline agriculture research. We compare transcriptomes from A. marina pneumatophores, stems, leaves, flowers, seeds, and transcriptomes across four widely divergent environments in the Indo-Pacific (Red Sea, Arabian Gulf, Bay of Bengal, and Red River Delta) to decipher the shared and location-, tissue-, and condition-specific functions. On average, 4.8% of transcripts per tissue were uniquely expressed in that tissue, and 12.2% were shared in all five tissues. Flowers’ transcript expression was the most distinct, with domain-centric gene ontology analysis showing high enrichment for stimulus-responsive processes, as well as genes implicated in flowering (hydroxygeraniol dehydrogenase, TPM = 3687) and floral scent biosynthesis (e.g., benzoyl_coenzyme_A, 2497.2 TPM). Pneumatophores highly expressed antioxidant genes, such as glutathione S-transferase (GST, TPM = 4759) and thioredoxin (TRX, TPM = 936.2), as well as proteins in the GO term ‘Hydroquinone:oxygen oxidoreductase activity’ (enrichment Z = 7.69, FDR-corr. p = 0.000785). Tissue-specific metabolic pathway reconstruction revealed unique processes in the five tissues; for example, seeds showed the most complete expression of lipid biosynthetic and degradation pathways. The leaf transcriptome had the lowest functional diversity among the expressed genes in any tissue, but highly expressed a catalase (TPM = 4181) and was enriched for the GO term ‘transmembrane transporter activity’ (GO:0015238; Z = 11.83; FDR-corr. p = 1.58 × 10−9), underscoring the genes for salt exporters. Metallothioneins (MTs) were the highest-expressed genes in all tissues from the cultivars of all locations; the dominant expression of these metal-binding and oxidative-stress control genes indicates they are essential for A. marina in its natural habitats. Our study yields insight into how A. marina tissue-specific gene expression supports halotolerance and other coastal adaptative strategies in this halophytic angiosperm.

Original language	English (US)
Pages (from-to)	2030
Journal	Agronomy
Volume	12
Issue number	9
DOIs	https://doi.org/10.3390/agronomy12092030
State	Published - Aug 26 2022
Externally published	Yes

Bibliographical note

KAUST Repository Item: Exported on 2022-09-14
Acknowledgements: This research was supported by KAUST Laboratory Baseline Funds and by New York University Abu Dhabi (NYUAD) Faculty Research fund AD060 and NYUAD Research Institute grant 73 71210 CGSB9. JB was supported by the NYUAD Water Research Center grant CG007, while GF was supported by the NYUAD-CGSB grant CGSB5. We thank the New York University Abu Dhabi High-Performance Computing Facility for computational resources. We thank Alexey Sergeev for permission to use the Avicennia photographs and NASA for the Jeddah satellite image. This manuscript is dedicated to the memory of Basel Khraiwesh.
This publication acknowledges KAUST support, but has no KAUST affiliated authors.

ASJC Scopus subject areas

Agronomy and Crop Science

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access to Document

10.3390/agronomy12092030

Cite this

@article{f372dd8c23d448b88df5d070a000ef25,

title = "Tissue-Specific Transcriptomes Outline Halophyte Adaptive Strategies in the Gray Mangrove (Avicennia marina)",

abstract = "Avicennia marina forests fulfill essential blue carbon and ecosystem services, including halting coastal erosion and supporting fisheries. Genetic studies of A. marina tissues could yield insight into halophyte adaptive strategies, empowering saline agriculture research. We compare transcriptomes from A. marina pneumatophores, stems, leaves, flowers, seeds, and transcriptomes across four widely divergent environments in the Indo-Pacific (Red Sea, Arabian Gulf, Bay of Bengal, and Red River Delta) to decipher the shared and location-, tissue-, and condition-specific functions. On average, 4.8% of transcripts per tissue were uniquely expressed in that tissue, and 12.2% were shared in all five tissues. Flowers{\textquoteright} transcript expression was the most distinct, with domain-centric gene ontology analysis showing high enrichment for stimulus-responsive processes, as well as genes implicated in flowering (hydroxygeraniol dehydrogenase, TPM = 3687) and floral scent biosynthesis (e.g., benzoyl_coenzyme_A, 2497.2 TPM). Pneumatophores highly expressed antioxidant genes, such as glutathione S-transferase (GST, TPM = 4759) and thioredoxin (TRX, TPM = 936.2), as well as proteins in the GO term {\textquoteleft}Hydroquinone:oxygen oxidoreductase activity{\textquoteright} (enrichment Z = 7.69, FDR-corr. p = 0.000785). Tissue-specific metabolic pathway reconstruction revealed unique processes in the five tissues; for example, seeds showed the most complete expression of lipid biosynthetic and degradation pathways. The leaf transcriptome had the lowest functional diversity among the expressed genes in any tissue, but highly expressed a catalase (TPM = 4181) and was enriched for the GO term {\textquoteleft}transmembrane transporter activity{\textquoteright} (GO:0015238; Z = 11.83; FDR-corr. p = 1.58 × 10−9), underscoring the genes for salt exporters. Metallothioneins (MTs) were the highest-expressed genes in all tissues from the cultivars of all locations; the dominant expression of these metal-binding and oxidative-stress control genes indicates they are essential for A. marina in its natural habitats. Our study yields insight into how A. marina tissue-specific gene expression supports halotolerance and other coastal adaptative strategies in this halophytic angiosperm.",

author = "Nelson, {David R.} and Amphun Chaiboonchoe and Hazzouri, {Khaled M.} and Basel Khraiwesh and Amnah Alzahmi and Ashish Jaiswal and Guillermo Friis and Burt, {John A.} and Amiri, {Khaled M. A.} and Kourosh Salehi-Ashtiani",

note = "KAUST Repository Item: Exported on 2022-09-14 Acknowledgements: This research was supported by KAUST Laboratory Baseline Funds and by New York University Abu Dhabi (NYUAD) Faculty Research fund AD060 and NYUAD Research Institute grant 73 71210 CGSB9. JB was supported by the NYUAD Water Research Center grant CG007, while GF was supported by the NYUAD-CGSB grant CGSB5. We thank the New York University Abu Dhabi High-Performance Computing Facility for computational resources. We thank Alexey Sergeev for permission to use the Avicennia photographs and NASA for the Jeddah satellite image. This manuscript is dedicated to the memory of Basel Khraiwesh. This publication acknowledges KAUST support, but has no KAUST affiliated authors.",

year = "2022",

month = aug,

day = "26",

doi = "10.3390/agronomy12092030",

language = "English (US)",

volume = "12",

pages = "2030",

journal = "Agronomy",

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TY - JOUR

T1 - Tissue-Specific Transcriptomes Outline Halophyte Adaptive Strategies in the Gray Mangrove (Avicennia marina)

AU - Nelson, David R.

AU - Chaiboonchoe, Amphun

AU - Hazzouri, Khaled M.

AU - Khraiwesh, Basel

AU - Alzahmi, Amnah

AU - Jaiswal, Ashish

AU - Friis, Guillermo

AU - Burt, John A.

AU - Amiri, Khaled M. A.

AU - Salehi-Ashtiani, Kourosh

N1 - KAUST Repository Item: Exported on 2022-09-14 Acknowledgements: This research was supported by KAUST Laboratory Baseline Funds and by New York University Abu Dhabi (NYUAD) Faculty Research fund AD060 and NYUAD Research Institute grant 73 71210 CGSB9. JB was supported by the NYUAD Water Research Center grant CG007, while GF was supported by the NYUAD-CGSB grant CGSB5. We thank the New York University Abu Dhabi High-Performance Computing Facility for computational resources. We thank Alexey Sergeev for permission to use the Avicennia photographs and NASA for the Jeddah satellite image. This manuscript is dedicated to the memory of Basel Khraiwesh. This publication acknowledges KAUST support, but has no KAUST affiliated authors.

PY - 2022/8/26

Y1 - 2022/8/26

N2 - Avicennia marina forests fulfill essential blue carbon and ecosystem services, including halting coastal erosion and supporting fisheries. Genetic studies of A. marina tissues could yield insight into halophyte adaptive strategies, empowering saline agriculture research. We compare transcriptomes from A. marina pneumatophores, stems, leaves, flowers, seeds, and transcriptomes across four widely divergent environments in the Indo-Pacific (Red Sea, Arabian Gulf, Bay of Bengal, and Red River Delta) to decipher the shared and location-, tissue-, and condition-specific functions. On average, 4.8% of transcripts per tissue were uniquely expressed in that tissue, and 12.2% were shared in all five tissues. Flowers’ transcript expression was the most distinct, with domain-centric gene ontology analysis showing high enrichment for stimulus-responsive processes, as well as genes implicated in flowering (hydroxygeraniol dehydrogenase, TPM = 3687) and floral scent biosynthesis (e.g., benzoyl_coenzyme_A, 2497.2 TPM). Pneumatophores highly expressed antioxidant genes, such as glutathione S-transferase (GST, TPM = 4759) and thioredoxin (TRX, TPM = 936.2), as well as proteins in the GO term ‘Hydroquinone:oxygen oxidoreductase activity’ (enrichment Z = 7.69, FDR-corr. p = 0.000785). Tissue-specific metabolic pathway reconstruction revealed unique processes in the five tissues; for example, seeds showed the most complete expression of lipid biosynthetic and degradation pathways. The leaf transcriptome had the lowest functional diversity among the expressed genes in any tissue, but highly expressed a catalase (TPM = 4181) and was enriched for the GO term ‘transmembrane transporter activity’ (GO:0015238; Z = 11.83; FDR-corr. p = 1.58 × 10−9), underscoring the genes for salt exporters. Metallothioneins (MTs) were the highest-expressed genes in all tissues from the cultivars of all locations; the dominant expression of these metal-binding and oxidative-stress control genes indicates they are essential for A. marina in its natural habitats. Our study yields insight into how A. marina tissue-specific gene expression supports halotolerance and other coastal adaptative strategies in this halophytic angiosperm.

AB - Avicennia marina forests fulfill essential blue carbon and ecosystem services, including halting coastal erosion and supporting fisheries. Genetic studies of A. marina tissues could yield insight into halophyte adaptive strategies, empowering saline agriculture research. We compare transcriptomes from A. marina pneumatophores, stems, leaves, flowers, seeds, and transcriptomes across four widely divergent environments in the Indo-Pacific (Red Sea, Arabian Gulf, Bay of Bengal, and Red River Delta) to decipher the shared and location-, tissue-, and condition-specific functions. On average, 4.8% of transcripts per tissue were uniquely expressed in that tissue, and 12.2% were shared in all five tissues. Flowers’ transcript expression was the most distinct, with domain-centric gene ontology analysis showing high enrichment for stimulus-responsive processes, as well as genes implicated in flowering (hydroxygeraniol dehydrogenase, TPM = 3687) and floral scent biosynthesis (e.g., benzoyl_coenzyme_A, 2497.2 TPM). Pneumatophores highly expressed antioxidant genes, such as glutathione S-transferase (GST, TPM = 4759) and thioredoxin (TRX, TPM = 936.2), as well as proteins in the GO term ‘Hydroquinone:oxygen oxidoreductase activity’ (enrichment Z = 7.69, FDR-corr. p = 0.000785). Tissue-specific metabolic pathway reconstruction revealed unique processes in the five tissues; for example, seeds showed the most complete expression of lipid biosynthetic and degradation pathways. The leaf transcriptome had the lowest functional diversity among the expressed genes in any tissue, but highly expressed a catalase (TPM = 4181) and was enriched for the GO term ‘transmembrane transporter activity’ (GO:0015238; Z = 11.83; FDR-corr. p = 1.58 × 10−9), underscoring the genes for salt exporters. Metallothioneins (MTs) were the highest-expressed genes in all tissues from the cultivars of all locations; the dominant expression of these metal-binding and oxidative-stress control genes indicates they are essential for A. marina in its natural habitats. Our study yields insight into how A. marina tissue-specific gene expression supports halotolerance and other coastal adaptative strategies in this halophytic angiosperm.

UR - http://hdl.handle.net/10754/680803

UR - https://www.mdpi.com/2073-4395/12/9/2030

U2 - 10.3390/agronomy12092030

DO - 10.3390/agronomy12092030

M3 - Article

SN - 2073-4395

VL - 12

SP - 2030

JO - Agronomy

JF - Agronomy

IS - 9

ER -

Tissue-Specific Transcriptomes Outline Halophyte Adaptive Strategies in the Gray Mangrove (Avicennia marina)

Abstract

Bibliographical note

ASJC Scopus subject areas

UN SDGs

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