Short- and long-term effects of UVA on arabidopsis are mediated by a novel cGMP phosphodiesterase

Jean Charles Isner; Vlad Aris Olteanu; Alexander J. Hetherington; Aude Coupel-Ledru; Peng Sun; Ashley J. Pridgeon; Glyndyr S. Jones; Matthew Oates; Tom A. Williams; Frans J.M. Maathuis; Richard Kift; Ann R. Webb; Julian Gough; Keara A. Franklin; Alistair M. Hetherington

doi:10.1016/j.cub.2019.06.071

Short- and long-term effects of UVA on arabidopsis are mediated by a novel cGMP phosphodiesterase

Jean Charles Isner, Vlad Aris Olteanu, Alexander J. Hetherington, Aude Coupel-Ledru, Peng Sun, Ashley J. Pridgeon, Glyndyr S. Jones, Matthew Oates, Tom A. Williams, Frans J.M. Maathuis, Richard Kift, Ann R. Webb, Julian Gough, Keara A. Franklin, Alistair M. Hetherington^*

^*Corresponding author for this work

School of Biological Sciences

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

Abstract / Description of output

Although UVA radiation (315–400 nm) represents 95% of the UV radiation reaching the earth's surface, surprisingly little is known about its effects on plants [1]. We show that in Arabidopsis, short-term exposure to UVA inhibits the opening of stomata, and this requires a reduction in the cytosolic level of cGMP. This process is independent of UVR8, the UVB receptor. A cGMP-activated phosphodiesterase (AtCN-PDE1) was responsible for the UVA-induced decrease in cGMP in Arabidopsis. AtCN-PDE1-like proteins form a clade within the large HD-domain/PDEase-like protein superfamily, but no eukaryotic members of this subfamily have been functionally characterized. These genes have been lost from the genomes of metazoans but are otherwise conserved as single-copy genes across the tree of life. In longer-term experiments, UVA radiation increased growth and decreased water-use efficiency. These experiments revealed that PDE1 is also a negative regulator of growth. As the PDE1 gene is ancient and not represented in animal lineages, it is likely that at least one element of cGMP signaling in plants has evolved differently to the system present in metazoans.

Original language	English
Pages (from-to)	2580-2585.e4
Number of pages	6
Journal	Current Biology
Volume	29
Issue number	15
DOIs	https://doi.org/10.1016/j.cub.2019.06.071
Publication status	Published - 5 Aug 2019

Keywords / Materials (for Non-textual outputs)

arabidopsis
cGMP
cGMP-phosphodiesterase
cyclic nucleotides
guard cell signaling
light signaling
UVA
water-use efficiency
evolution

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HetheringtonEtalCB2019ShortAndLongTermEffectsOfUVAFinal published version, 1.53 MBLicence: Creative Commons: Attribution (CC-BY)

Cite this

Isner, J. C., Olteanu, V. A., Hetherington, A. J., Coupel-Ledru, A., Sun, P., Pridgeon, A. J., Jones, G. S., Oates, M., Williams, T. A., Maathuis, F. J. M., Kift, R., Webb, A. R., Gough, J., Franklin, K. A., & Hetherington, A. M. (2019). Short- and long-term effects of UVA on arabidopsis are mediated by a novel cGMP phosphodiesterase. Current Biology, 29(15), 2580-2585.e4. https://doi.org/10.1016/j.cub.2019.06.071

@article{0657da8689f2443a89623eec2dc9b28c,

title = "Short- and long-term effects of UVA on arabidopsis are mediated by a novel cGMP phosphodiesterase",

abstract = "Although UVA radiation (315–400 nm) represents 95% of the UV radiation reaching the earth's surface, surprisingly little is known about its effects on plants [1]. We show that in Arabidopsis, short-term exposure to UVA inhibits the opening of stomata, and this requires a reduction in the cytosolic level of cGMP. This process is independent of UVR8, the UVB receptor. A cGMP-activated phosphodiesterase (AtCN-PDE1) was responsible for the UVA-induced decrease in cGMP in Arabidopsis. AtCN-PDE1-like proteins form a clade within the large HD-domain/PDEase-like protein superfamily, but no eukaryotic members of this subfamily have been functionally characterized. These genes have been lost from the genomes of metazoans but are otherwise conserved as single-copy genes across the tree of life. In longer-term experiments, UVA radiation increased growth and decreased water-use efficiency. These experiments revealed that PDE1 is also a negative regulator of growth. As the PDE1 gene is ancient and not represented in animal lineages, it is likely that at least one element of cGMP signaling in plants has evolved differently to the system present in metazoans.",

keywords = "arabidopsis, cGMP, cGMP-phosphodiesterase, cyclic nucleotides, guard cell signaling, light signaling, UVA, water-use efficiency, evolution",

author = "Isner, {Jean Charles} and Olteanu, {Vlad Aris} and Hetherington, {Alexander J.} and Aude Coupel-Ledru and Peng Sun and Pridgeon, {Ashley J.} and Jones, {Glyndyr S.} and Matthew Oates and Williams, {Tom A.} and Maathuis, {Frans J.M.} and Richard Kift and Webb, {Ann R.} and Julian Gough and Franklin, {Keara A.} and Hetherington, {Alistair M.}",

year = "2019",

month = aug,

day = "5",

doi = "10.1016/j.cub.2019.06.071",

language = "English",

volume = "29",

pages = "2580--2585.e4",

journal = "Current Biology",

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publisher = "Cell Press",

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Isner, JC, Olteanu, VA, Hetherington, AJ, Coupel-Ledru, A, Sun, P, Pridgeon, AJ, Jones, GS, Oates, M, Williams, TA, Maathuis, FJM, Kift, R, Webb, AR, Gough, J, Franklin, KA & Hetherington, AM 2019, 'Short- and long-term effects of UVA on arabidopsis are mediated by a novel cGMP phosphodiesterase', Current Biology, vol. 29, no. 15, pp. 2580-2585.e4. https://doi.org/10.1016/j.cub.2019.06.071

TY - JOUR

T1 - Short- and long-term effects of UVA on arabidopsis are mediated by a novel cGMP phosphodiesterase

AU - Isner, Jean Charles

AU - Olteanu, Vlad Aris

AU - Hetherington, Alexander J.

AU - Coupel-Ledru, Aude

AU - Sun, Peng

AU - Pridgeon, Ashley J.

AU - Jones, Glyndyr S.

AU - Oates, Matthew

AU - Williams, Tom A.

AU - Maathuis, Frans J.M.

AU - Kift, Richard

AU - Webb, Ann R.

AU - Gough, Julian

AU - Franklin, Keara A.

AU - Hetherington, Alistair M.

PY - 2019/8/5

Y1 - 2019/8/5

N2 - Although UVA radiation (315–400 nm) represents 95% of the UV radiation reaching the earth's surface, surprisingly little is known about its effects on plants [1]. We show that in Arabidopsis, short-term exposure to UVA inhibits the opening of stomata, and this requires a reduction in the cytosolic level of cGMP. This process is independent of UVR8, the UVB receptor. A cGMP-activated phosphodiesterase (AtCN-PDE1) was responsible for the UVA-induced decrease in cGMP in Arabidopsis. AtCN-PDE1-like proteins form a clade within the large HD-domain/PDEase-like protein superfamily, but no eukaryotic members of this subfamily have been functionally characterized. These genes have been lost from the genomes of metazoans but are otherwise conserved as single-copy genes across the tree of life. In longer-term experiments, UVA radiation increased growth and decreased water-use efficiency. These experiments revealed that PDE1 is also a negative regulator of growth. As the PDE1 gene is ancient and not represented in animal lineages, it is likely that at least one element of cGMP signaling in plants has evolved differently to the system present in metazoans.

AB - Although UVA radiation (315–400 nm) represents 95% of the UV radiation reaching the earth's surface, surprisingly little is known about its effects on plants [1]. We show that in Arabidopsis, short-term exposure to UVA inhibits the opening of stomata, and this requires a reduction in the cytosolic level of cGMP. This process is independent of UVR8, the UVB receptor. A cGMP-activated phosphodiesterase (AtCN-PDE1) was responsible for the UVA-induced decrease in cGMP in Arabidopsis. AtCN-PDE1-like proteins form a clade within the large HD-domain/PDEase-like protein superfamily, but no eukaryotic members of this subfamily have been functionally characterized. These genes have been lost from the genomes of metazoans but are otherwise conserved as single-copy genes across the tree of life. In longer-term experiments, UVA radiation increased growth and decreased water-use efficiency. These experiments revealed that PDE1 is also a negative regulator of growth. As the PDE1 gene is ancient and not represented in animal lineages, it is likely that at least one element of cGMP signaling in plants has evolved differently to the system present in metazoans.

KW - arabidopsis

KW - cGMP

KW - cGMP-phosphodiesterase

KW - cyclic nucleotides

KW - guard cell signaling

KW - light signaling

KW - UVA

KW - water-use efficiency

KW - evolution

U2 - 10.1016/j.cub.2019.06.071

DO - 10.1016/j.cub.2019.06.071

M3 - Article

C2 - 31353185

AN - SCOPUS:85069895061

SN - 0960-9822

VL - 29

SP - 2580-2585.e4

JO - Current Biology

JF - Current Biology

IS - 15

ER -

Short- and long-term effects of UVA on arabidopsis are mediated by a novel cGMP phosphodiesterase

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Keywords / Materials (for Non-textual outputs)

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