Transcriptomes of eight Arabidopsis thaliana accessions reveal core conserved, genotype- and organ-specific responses to flooding stress

Hans van Veen, Divya Vashisht, Melis Akman, Thomas Girke, Angelika Mustroph, Emilie Reinen, Sjon Hartman, Maarten Kooiker, Peter van Tienderen, Eric Schranz, Julia Bailey-Serres, Laurentius A.C.J. Voesenek, Rashmi Sasidharan*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

30 Citations (Scopus)

Abstract

Climate change has increased the frequency and severity of flooding events, with significant negative impact on agricultural productivity. These events often submerge plant aerial organs and roots, limiting growth and survival due to a severe reduction in light reactions and gas exchange necessary for photosynthesis and respiration, respectively. To distinguish molecular responses to the compound stress imposed by submergence, we investigated transcriptomic adjustments to darkness in air and under submerged conditions using eight Arabidopsis (Arabidopsis thaliana) accessions differing significantly in sensitivity to submergence. Evaluation of root and rosette transcriptomes revealed an early transcriptional and posttranscriptional response signature that was conserved primarily across genotypes, although flooding susceptibility-associated and genotype-specific responses also were uncovered. Posttranscriptional regulation encompassed darkness- and submergence-induced alternative splicing of transcripts from pathways involved in the alternative mobilization of energy reserves. The organ-specific transcriptome adjustments reflected the distinct physiological status of roots and shoots. Root-specific transcriptome changes included marked up-regulation of chloroplast-encoded photosynthesis and redox-related genes, whereas those of the rosette were related to the regulation of development and growth processes. We identified a novel set of tolerance genes, recognized mainly by quantitative differences. These included a transcriptome signature of more pronounced gluconeogenesis in tolerant accessions, a response that included stress-induced alternative splicing. This study provides organ-specific molecular resolution of genetic variation in submergence responses involving interactions between darkness and low-oxygen constraints of flooding stress and demonstrates that early transcriptome plasticity, including alternative splicing, is associated with the ability to cope with a compound environmental stress.

Original languageEnglish
Pages (from-to)668-689
JournalPlant Physiology
Volume172
Issue number2
DOIs
Publication statusPublished - 2016

Fingerprint

Transcriptome
Arabidopsis
transcriptome
submergence
Arabidopsis thaliana
Genotype
Darkness
alternative splicing
Alternative Splicing
genotype
Photosynthesis
photosynthesis
Gluconeogenesis
gluconeogenesis
Climate Change
renewable energy sources
Chloroplasts
physiological state
transcriptomics
Growth and Development

Cite this

van Veen, Hans ; Vashisht, Divya ; Akman, Melis ; Girke, Thomas ; Mustroph, Angelika ; Reinen, Emilie ; Hartman, Sjon ; Kooiker, Maarten ; van Tienderen, Peter ; Schranz, Eric ; Bailey-Serres, Julia ; Voesenek, Laurentius A.C.J. ; Sasidharan, Rashmi. / Transcriptomes of eight Arabidopsis thaliana accessions reveal core conserved, genotype- and organ-specific responses to flooding stress. In: Plant Physiology. 2016 ; Vol. 172, No. 2. pp. 668-689.
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abstract = "Climate change has increased the frequency and severity of flooding events, with significant negative impact on agricultural productivity. These events often submerge plant aerial organs and roots, limiting growth and survival due to a severe reduction in light reactions and gas exchange necessary for photosynthesis and respiration, respectively. To distinguish molecular responses to the compound stress imposed by submergence, we investigated transcriptomic adjustments to darkness in air and under submerged conditions using eight Arabidopsis (Arabidopsis thaliana) accessions differing significantly in sensitivity to submergence. Evaluation of root and rosette transcriptomes revealed an early transcriptional and posttranscriptional response signature that was conserved primarily across genotypes, although flooding susceptibility-associated and genotype-specific responses also were uncovered. Posttranscriptional regulation encompassed darkness- and submergence-induced alternative splicing of transcripts from pathways involved in the alternative mobilization of energy reserves. The organ-specific transcriptome adjustments reflected the distinct physiological status of roots and shoots. Root-specific transcriptome changes included marked up-regulation of chloroplast-encoded photosynthesis and redox-related genes, whereas those of the rosette were related to the regulation of development and growth processes. We identified a novel set of tolerance genes, recognized mainly by quantitative differences. These included a transcriptome signature of more pronounced gluconeogenesis in tolerant accessions, a response that included stress-induced alternative splicing. This study provides organ-specific molecular resolution of genetic variation in submergence responses involving interactions between darkness and low-oxygen constraints of flooding stress and demonstrates that early transcriptome plasticity, including alternative splicing, is associated with the ability to cope with a compound environmental stress.",
author = "{van Veen}, Hans and Divya Vashisht and Melis Akman and Thomas Girke and Angelika Mustroph and Emilie Reinen and Sjon Hartman and Maarten Kooiker and {van Tienderen}, Peter and Eric Schranz and Julia Bailey-Serres and Voesenek, {Laurentius A.C.J.} and Rashmi Sasidharan",
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van Veen, H, Vashisht, D, Akman, M, Girke, T, Mustroph, A, Reinen, E, Hartman, S, Kooiker, M, van Tienderen, P, Schranz, E, Bailey-Serres, J, Voesenek, LACJ & Sasidharan, R 2016, 'Transcriptomes of eight Arabidopsis thaliana accessions reveal core conserved, genotype- and organ-specific responses to flooding stress', Plant Physiology, vol. 172, no. 2, pp. 668-689. https://doi.org/10.1104/pp.16.00472

Transcriptomes of eight Arabidopsis thaliana accessions reveal core conserved, genotype- and organ-specific responses to flooding stress. / van Veen, Hans; Vashisht, Divya; Akman, Melis; Girke, Thomas; Mustroph, Angelika; Reinen, Emilie; Hartman, Sjon; Kooiker, Maarten; van Tienderen, Peter; Schranz, Eric; Bailey-Serres, Julia; Voesenek, Laurentius A.C.J.; Sasidharan, Rashmi.

In: Plant Physiology, Vol. 172, No. 2, 2016, p. 668-689.

Research output: Contribution to journalArticleAcademicpeer-review

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AU - van Veen, Hans

AU - Vashisht, Divya

AU - Akman, Melis

AU - Girke, Thomas

AU - Mustroph, Angelika

AU - Reinen, Emilie

AU - Hartman, Sjon

AU - Kooiker, Maarten

AU - van Tienderen, Peter

AU - Schranz, Eric

AU - Bailey-Serres, Julia

AU - Voesenek, Laurentius A.C.J.

AU - Sasidharan, Rashmi

PY - 2016

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N2 - Climate change has increased the frequency and severity of flooding events, with significant negative impact on agricultural productivity. These events often submerge plant aerial organs and roots, limiting growth and survival due to a severe reduction in light reactions and gas exchange necessary for photosynthesis and respiration, respectively. To distinguish molecular responses to the compound stress imposed by submergence, we investigated transcriptomic adjustments to darkness in air and under submerged conditions using eight Arabidopsis (Arabidopsis thaliana) accessions differing significantly in sensitivity to submergence. Evaluation of root and rosette transcriptomes revealed an early transcriptional and posttranscriptional response signature that was conserved primarily across genotypes, although flooding susceptibility-associated and genotype-specific responses also were uncovered. Posttranscriptional regulation encompassed darkness- and submergence-induced alternative splicing of transcripts from pathways involved in the alternative mobilization of energy reserves. The organ-specific transcriptome adjustments reflected the distinct physiological status of roots and shoots. Root-specific transcriptome changes included marked up-regulation of chloroplast-encoded photosynthesis and redox-related genes, whereas those of the rosette were related to the regulation of development and growth processes. We identified a novel set of tolerance genes, recognized mainly by quantitative differences. These included a transcriptome signature of more pronounced gluconeogenesis in tolerant accessions, a response that included stress-induced alternative splicing. This study provides organ-specific molecular resolution of genetic variation in submergence responses involving interactions between darkness and low-oxygen constraints of flooding stress and demonstrates that early transcriptome plasticity, including alternative splicing, is associated with the ability to cope with a compound environmental stress.

AB - Climate change has increased the frequency and severity of flooding events, with significant negative impact on agricultural productivity. These events often submerge plant aerial organs and roots, limiting growth and survival due to a severe reduction in light reactions and gas exchange necessary for photosynthesis and respiration, respectively. To distinguish molecular responses to the compound stress imposed by submergence, we investigated transcriptomic adjustments to darkness in air and under submerged conditions using eight Arabidopsis (Arabidopsis thaliana) accessions differing significantly in sensitivity to submergence. Evaluation of root and rosette transcriptomes revealed an early transcriptional and posttranscriptional response signature that was conserved primarily across genotypes, although flooding susceptibility-associated and genotype-specific responses also were uncovered. Posttranscriptional regulation encompassed darkness- and submergence-induced alternative splicing of transcripts from pathways involved in the alternative mobilization of energy reserves. The organ-specific transcriptome adjustments reflected the distinct physiological status of roots and shoots. Root-specific transcriptome changes included marked up-regulation of chloroplast-encoded photosynthesis and redox-related genes, whereas those of the rosette were related to the regulation of development and growth processes. We identified a novel set of tolerance genes, recognized mainly by quantitative differences. These included a transcriptome signature of more pronounced gluconeogenesis in tolerant accessions, a response that included stress-induced alternative splicing. This study provides organ-specific molecular resolution of genetic variation in submergence responses involving interactions between darkness and low-oxygen constraints of flooding stress and demonstrates that early transcriptome plasticity, including alternative splicing, is associated with the ability to cope with a compound environmental stress.

U2 - 10.1104/pp.16.00472

DO - 10.1104/pp.16.00472

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EP - 689

JO - Plant Physiology

JF - Plant Physiology

SN - 0032-0889

IS - 2

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