A stress recovery signaling network for enhanced flooding tolerance in Arabidopsis thaliana

Elaine Yeung; Hans van Veen; Divya Vashisht; Ana Luiza Sobral Paiva; Maureen Hummel; Tom Rankenberg; Bianka Steffens; Anja Steffen-Heins; Margret Sauter; Michel de Vries; Robert C. Schuurink; Jérémie Bazin; Julia Bailey-Serres; Laurentius A.C.J. Voesenek; Rashmi Sasidharan

doi:10.1073/pnas.1803841115

A stress recovery signaling network for enhanced flooding tolerance in Arabidopsis thaliana

Elaine Yeung, Hans van Veen, Divya Vashisht, Ana Luiza Sobral Paiva, Maureen Hummel, Tom Rankenberg, Bianka Steffens, Anja Steffen-Heins, Margret Sauter, Michel de Vries, Robert C. Schuurink, Jérémie Bazin, Julia Bailey-Serres^*, Laurentius A.C.J. Voesenek, Rashmi Sasidharan

^*Corresponding author for this work

Sub Plant Ecophysiology

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

Abstract

Abiotic stresses in plants are often transient, and the recovery phase following stress removal is critical. Flooding, a major abiotic stress that negatively impacts plant biodiversity and agriculture, is a sequential stress where tolerance is strongly dependent on viability underwater and during the postflooding period. Here we show that in Arabidopsis thaliana accessions (Bay-0 and Lp2-6), different rates of submergence recovery correlate with submergence tolerance and fecundity. A genome-wide assessment of ribosome-associated transcripts in Bay-0 and Lp2-6 revealed a signaling network regulating recovery processes. Differential recovery between the accessions was related to the activity of three genes: RESPIRATORY BURST OXIDASE HOMOLOG D, SENESCENCE-ASSOCIATED GENE113, and ORESARA1, which function in a regulatory network involving a reactive oxygen species (ROS) burst upon desubmergence and the hormones abscisic acid and ethylene. This regulatory module controls ROS homeostasis, stomatal aperture, and chlorophyll degradation during submergence recovery. This work uncovers a signaling network that regulates recovery processes following flooding to hasten the return to prestress homeostasis.

Original language	English
Pages (from-to)	E6085-E6094
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	115
Issue number	26
DOIs	https://doi.org/10.1073/pnas.1803841115
Publication status	Published - 26 Jun 2018

Funding

ACKNOWLEDGMENTS. At Utrecht University, we thank Rob Welschen for managing the growth facilities, Emilie Reinen and Zeguang Liu for genotyping mutant lines, Yorrit van de Kaa for seed harvesting, and Sven Teurlincx and Ankie Ammerlaan for experimental assistance. We appreciate Timo Staffel at the University of Kiel for assisting with plant growth for EPR measurements. We thank Thomas Girke of the University of California, Riverside for guidance on the Ribo-seq workflow in R/Bioconductor. This work was supported by grants (to R.S.) from the Netherlands Organisation for Scientific Research (NWO 016. VIDI.171.006 and NWO-VENI 863.12.013) and grants (to J.B.-S.) from the US National Science Foundation (MCB-1021969) and the US Department of Agriculture National Institute of Food and Agriculture Hatch program. E.Y. was supported by a PhD scholarship from Utrecht University.

Keywords

Dehydration
Flooding
Reactive oxygen species
Recovery
Ribosome footprinting

Access to Document

10.1073/pnas.1803841115

E6085.fullFinal published version, 1.98 MB

Cite this

Yeung, E., van Veen, H., Vashisht, D., Paiva, A. L. S., Hummel, M., Rankenberg, T., Steffens, B., Steffen-Heins, A., Sauter, M., de Vries, M., Schuurink, R. C., Bazin, J., Bailey-Serres, J., Voesenek, L. A. C. J., & Sasidharan, R. (2018). A stress recovery signaling network for enhanced flooding tolerance in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America, 115(26), E6085-E6094. https://doi.org/10.1073/pnas.1803841115

@article{2e67c69b6868435f8576c7aaa38f4cc7,

title = "A stress recovery signaling network for enhanced flooding tolerance in Arabidopsis thaliana",

abstract = "Abiotic stresses in plants are often transient, and the recovery phase following stress removal is critical. Flooding, a major abiotic stress that negatively impacts plant biodiversity and agriculture, is a sequential stress where tolerance is strongly dependent on viability underwater and during the postflooding period. Here we show that in Arabidopsis thaliana accessions (Bay-0 and Lp2-6), different rates of submergence recovery correlate with submergence tolerance and fecundity. A genome-wide assessment of ribosome-associated transcripts in Bay-0 and Lp2-6 revealed a signaling network regulating recovery processes. Differential recovery between the accessions was related to the activity of three genes: RESPIRATORY BURST OXIDASE HOMOLOG D, SENESCENCE-ASSOCIATED GENE113, and ORESARA1, which function in a regulatory network involving a reactive oxygen species (ROS) burst upon desubmergence and the hormones abscisic acid and ethylene. This regulatory module controls ROS homeostasis, stomatal aperture, and chlorophyll degradation during submergence recovery. This work uncovers a signaling network that regulates recovery processes following flooding to hasten the return to prestress homeostasis.",

keywords = "Dehydration, Flooding, Reactive oxygen species, Recovery, Ribosome footprinting",

author = "Elaine Yeung and {van Veen}, Hans and Divya Vashisht and Paiva, {Ana Luiza Sobral} and Maureen Hummel and Tom Rankenberg and Bianka Steffens and Anja Steffen-Heins and Margret Sauter and {de Vries}, Michel and Schuurink, {Robert C.} and J{\'e}r{\'e}mie Bazin and Julia Bailey-Serres and Voesenek, {Laurentius A.C.J.} and Rashmi Sasidharan",

year = "2018",

month = jun,

day = "26",

doi = "10.1073/pnas.1803841115",

language = "English",

volume = "115",

pages = "E6085--E6094",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

issn = "0027-8424",

publisher = "National Academy of Sciences",

number = "26",

}

Yeung, E, van Veen, H, Vashisht, D, Paiva, ALS, Hummel, M, Rankenberg, T, Steffens, B, Steffen-Heins, A, Sauter, M, de Vries, M, Schuurink, RC, Bazin, J, Bailey-Serres, J, Voesenek, LACJ & Sasidharan, R 2018, 'A stress recovery signaling network for enhanced flooding tolerance in Arabidopsis thaliana', Proceedings of the National Academy of Sciences of the United States of America, vol. 115, no. 26, pp. E6085-E6094. https://doi.org/10.1073/pnas.1803841115

TY - JOUR

T1 - A stress recovery signaling network for enhanced flooding tolerance in Arabidopsis thaliana

AU - Yeung, Elaine

AU - van Veen, Hans

AU - Vashisht, Divya

AU - Paiva, Ana Luiza Sobral

AU - Hummel, Maureen

AU - Rankenberg, Tom

AU - Steffens, Bianka

AU - Steffen-Heins, Anja

AU - Sauter, Margret

AU - de Vries, Michel

AU - Schuurink, Robert C.

AU - Bazin, Jérémie

AU - Bailey-Serres, Julia

AU - Voesenek, Laurentius A.C.J.

AU - Sasidharan, Rashmi

PY - 2018/6/26

Y1 - 2018/6/26

N2 - Abiotic stresses in plants are often transient, and the recovery phase following stress removal is critical. Flooding, a major abiotic stress that negatively impacts plant biodiversity and agriculture, is a sequential stress where tolerance is strongly dependent on viability underwater and during the postflooding period. Here we show that in Arabidopsis thaliana accessions (Bay-0 and Lp2-6), different rates of submergence recovery correlate with submergence tolerance and fecundity. A genome-wide assessment of ribosome-associated transcripts in Bay-0 and Lp2-6 revealed a signaling network regulating recovery processes. Differential recovery between the accessions was related to the activity of three genes: RESPIRATORY BURST OXIDASE HOMOLOG D, SENESCENCE-ASSOCIATED GENE113, and ORESARA1, which function in a regulatory network involving a reactive oxygen species (ROS) burst upon desubmergence and the hormones abscisic acid and ethylene. This regulatory module controls ROS homeostasis, stomatal aperture, and chlorophyll degradation during submergence recovery. This work uncovers a signaling network that regulates recovery processes following flooding to hasten the return to prestress homeostasis.

AB - Abiotic stresses in plants are often transient, and the recovery phase following stress removal is critical. Flooding, a major abiotic stress that negatively impacts plant biodiversity and agriculture, is a sequential stress where tolerance is strongly dependent on viability underwater and during the postflooding period. Here we show that in Arabidopsis thaliana accessions (Bay-0 and Lp2-6), different rates of submergence recovery correlate with submergence tolerance and fecundity. A genome-wide assessment of ribosome-associated transcripts in Bay-0 and Lp2-6 revealed a signaling network regulating recovery processes. Differential recovery between the accessions was related to the activity of three genes: RESPIRATORY BURST OXIDASE HOMOLOG D, SENESCENCE-ASSOCIATED GENE113, and ORESARA1, which function in a regulatory network involving a reactive oxygen species (ROS) burst upon desubmergence and the hormones abscisic acid and ethylene. This regulatory module controls ROS homeostasis, stomatal aperture, and chlorophyll degradation during submergence recovery. This work uncovers a signaling network that regulates recovery processes following flooding to hasten the return to prestress homeostasis.

KW - Dehydration

KW - Flooding

KW - Reactive oxygen species

KW - Recovery

KW - Ribosome footprinting

UR - http://www.scopus.com/inward/record.url?scp=85049005922&partnerID=8YFLogxK

U2 - 10.1073/pnas.1803841115

DO - 10.1073/pnas.1803841115

M3 - Article

AN - SCOPUS:85049005922

SN - 0027-8424

VL - 115

SP - E6085-E6094

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 26

ER -

A stress recovery signaling network for enhanced flooding tolerance in Arabidopsis thaliana

Abstract

Funding

Keywords

Access to Document

Other files and links

Fingerprint

Cite this