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Ethylene regulates fast apoplastic acidification and expansin A transcription during submergence-induced petiole elongation in Rumex palustris

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Ethylene regulates fast apoplastic acidification and expansin A transcription during submergence-induced petiole elongation in Rumex palustris. / Vreeburg, R A M; Benschop, J J; Peeters, A J M; Colmer, T D; Ammerlaan, A H M; Staal, M; Elzenga, T M; Staals, R H J; Darley, C P; McQueen-Mason, S J; Voesenek, L A C J.

In: Plant Journal, Vol. 43, No. 4, 08.2005, p. 597-610.

Research output: Contribution to journalArticle

Harvard

Vreeburg, RAM, Benschop, JJ, Peeters, AJM, Colmer, TD, Ammerlaan, AHM, Staal, M, Elzenga, TM, Staals, RHJ, Darley, CP, McQueen-Mason, SJ & Voesenek, LACJ 2005, 'Ethylene regulates fast apoplastic acidification and expansin A transcription during submergence-induced petiole elongation in Rumex palustris', Plant Journal, vol. 43, no. 4, pp. 597-610. https://doi.org/10.1111/j.1365-313X.2005.02477.x

APA

Vreeburg, R. A. M., Benschop, J. J., Peeters, A. J. M., Colmer, T. D., Ammerlaan, A. H. M., Staal, M., ... Voesenek, L. A. C. J. (2005). Ethylene regulates fast apoplastic acidification and expansin A transcription during submergence-induced petiole elongation in Rumex palustris. Plant Journal, 43(4), 597-610. https://doi.org/10.1111/j.1365-313X.2005.02477.x

Vancouver

Vreeburg RAM, Benschop JJ, Peeters AJM, Colmer TD, Ammerlaan AHM, Staal M et al. Ethylene regulates fast apoplastic acidification and expansin A transcription during submergence-induced petiole elongation in Rumex palustris. Plant Journal. 2005 Aug;43(4):597-610. https://doi.org/10.1111/j.1365-313X.2005.02477.x

Author

Vreeburg, R A M ; Benschop, J J ; Peeters, A J M ; Colmer, T D ; Ammerlaan, A H M ; Staal, M ; Elzenga, T M ; Staals, R H J ; Darley, C P ; McQueen-Mason, S J ; Voesenek, L A C J. / Ethylene regulates fast apoplastic acidification and expansin A transcription during submergence-induced petiole elongation in Rumex palustris. In: Plant Journal. 2005 ; Vol. 43, No. 4. pp. 597-610.

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@article{d5bed851478c48199d84f0ff92e3237e,
title = "Ethylene regulates fast apoplastic acidification and expansin A transcription during submergence-induced petiole elongation in Rumex palustris",
abstract = "The semi-aquatic dicot Rumex palustris responds to complete submergence by enhanced elongation of young petioles. This elongation of petiole cells brings leaf blades above the water surface, thus reinstating gas exchange with the atmosphere and increasing survival in flood-prone environments. We already know that an enhanced internal level of the gaseous hormone ethylene is the primary signal for underwater escape in R. palustris. Further downstream, concentration changes in abscisic acid (ABA), gibberellin (GA) and auxin are required to gain fast cell elongation under water. A prerequisite for cell elongation in general is cell wall loosening mediated by proteins such as expansins. Expansin genes might, therefore, be important target genes in submergence-induced and plant hormone-mediated petiole elongation. To test this hypothesis we have studied the identity, kinetics and regulation of expansin A mRNA abundance and protein activity, as well as examined pH changes in cell walls associated with this adaptive growth. We found a novel role of ethylene in triggering two processes affecting cell wall loosening during submergence-induced petiole elongation. First, ethylene was shown to promote fast net H+ extrusion, leading to apoplastic acidification. Secondly, ethylene upregulates one expansin A gene (RpEXPA1), as measured with real-time RT-PCR, out of a group of 13 R. palustris expansin A genes tested. Furthermore, a significant accumulation of expansin proteins belonging to the same size class as RpEXPA1, as well as a strong increase in expansin activity, were apparent within 4-6 h of submergence. Regulation of RpEXPA1 transcript levels depends on ethylene action and not on GA and ABA, demonstrating that ethylene evokes at least three, parallel operating pathways that, when integrated at the whole petiole level, lead to coordinated underwater elongation. The first pathway involves ethylene-modulated changes in ABA and GA, these acting on as yet unknown downstream components, whereas the second and third routes encompass ethylene-induced apoplastic acidification and ethylene-induced RpEXPA1 upregulation.",
keywords = "ethylene, expansins, apoplastic acidification, elongation growth, Rumex, DEEP-WATER RICE, TIME QUANTITATIVE PCR, INTOLERANT R-ACETOSA, CELL-WALL EXTENSION, GENE-EXPRESSION, ALPHA-EXPANSIN, ARABIDOPSIS-THALIANA, 1-AMINOCYCLOPROPANE-1-CARBOXYLATE OXIDASE, SHOOT ELONGATION, ABSCISIC-ACID",
author = "Vreeburg, {R A M} and Benschop, {J J} and Peeters, {A J M} and Colmer, {T D} and Ammerlaan, {A H M} and M Staal and Elzenga, {T M} and Staals, {R H J} and Darley, {C P} and McQueen-Mason, {S J} and Voesenek, {L A C J}",
note = "Open access copy available from the journal web site.",
year = "2005",
month = "8",
doi = "10.1111/j.1365-313X.2005.02477.x",
language = "English",
volume = "43",
pages = "597--610",
journal = "The Plant journal",
issn = "0960-7412",
publisher = "Wiley-Blackwell",
number = "4",

}

RIS (suitable for import to EndNote) - Download

TY - JOUR

T1 - Ethylene regulates fast apoplastic acidification and expansin A transcription during submergence-induced petiole elongation in Rumex palustris

AU - Vreeburg, R A M

AU - Benschop, J J

AU - Peeters, A J M

AU - Colmer, T D

AU - Ammerlaan, A H M

AU - Staal, M

AU - Elzenga, T M

AU - Staals, R H J

AU - Darley, C P

AU - McQueen-Mason, S J

AU - Voesenek, L A C J

N1 - Open access copy available from the journal web site.

PY - 2005/8

Y1 - 2005/8

N2 - The semi-aquatic dicot Rumex palustris responds to complete submergence by enhanced elongation of young petioles. This elongation of petiole cells brings leaf blades above the water surface, thus reinstating gas exchange with the atmosphere and increasing survival in flood-prone environments. We already know that an enhanced internal level of the gaseous hormone ethylene is the primary signal for underwater escape in R. palustris. Further downstream, concentration changes in abscisic acid (ABA), gibberellin (GA) and auxin are required to gain fast cell elongation under water. A prerequisite for cell elongation in general is cell wall loosening mediated by proteins such as expansins. Expansin genes might, therefore, be important target genes in submergence-induced and plant hormone-mediated petiole elongation. To test this hypothesis we have studied the identity, kinetics and regulation of expansin A mRNA abundance and protein activity, as well as examined pH changes in cell walls associated with this adaptive growth. We found a novel role of ethylene in triggering two processes affecting cell wall loosening during submergence-induced petiole elongation. First, ethylene was shown to promote fast net H+ extrusion, leading to apoplastic acidification. Secondly, ethylene upregulates one expansin A gene (RpEXPA1), as measured with real-time RT-PCR, out of a group of 13 R. palustris expansin A genes tested. Furthermore, a significant accumulation of expansin proteins belonging to the same size class as RpEXPA1, as well as a strong increase in expansin activity, were apparent within 4-6 h of submergence. Regulation of RpEXPA1 transcript levels depends on ethylene action and not on GA and ABA, demonstrating that ethylene evokes at least three, parallel operating pathways that, when integrated at the whole petiole level, lead to coordinated underwater elongation. The first pathway involves ethylene-modulated changes in ABA and GA, these acting on as yet unknown downstream components, whereas the second and third routes encompass ethylene-induced apoplastic acidification and ethylene-induced RpEXPA1 upregulation.

AB - The semi-aquatic dicot Rumex palustris responds to complete submergence by enhanced elongation of young petioles. This elongation of petiole cells brings leaf blades above the water surface, thus reinstating gas exchange with the atmosphere and increasing survival in flood-prone environments. We already know that an enhanced internal level of the gaseous hormone ethylene is the primary signal for underwater escape in R. palustris. Further downstream, concentration changes in abscisic acid (ABA), gibberellin (GA) and auxin are required to gain fast cell elongation under water. A prerequisite for cell elongation in general is cell wall loosening mediated by proteins such as expansins. Expansin genes might, therefore, be important target genes in submergence-induced and plant hormone-mediated petiole elongation. To test this hypothesis we have studied the identity, kinetics and regulation of expansin A mRNA abundance and protein activity, as well as examined pH changes in cell walls associated with this adaptive growth. We found a novel role of ethylene in triggering two processes affecting cell wall loosening during submergence-induced petiole elongation. First, ethylene was shown to promote fast net H+ extrusion, leading to apoplastic acidification. Secondly, ethylene upregulates one expansin A gene (RpEXPA1), as measured with real-time RT-PCR, out of a group of 13 R. palustris expansin A genes tested. Furthermore, a significant accumulation of expansin proteins belonging to the same size class as RpEXPA1, as well as a strong increase in expansin activity, were apparent within 4-6 h of submergence. Regulation of RpEXPA1 transcript levels depends on ethylene action and not on GA and ABA, demonstrating that ethylene evokes at least three, parallel operating pathways that, when integrated at the whole petiole level, lead to coordinated underwater elongation. The first pathway involves ethylene-modulated changes in ABA and GA, these acting on as yet unknown downstream components, whereas the second and third routes encompass ethylene-induced apoplastic acidification and ethylene-induced RpEXPA1 upregulation.

KW - ethylene

KW - expansins

KW - apoplastic acidification

KW - elongation growth

KW - Rumex

KW - DEEP-WATER RICE

KW - TIME QUANTITATIVE PCR

KW - INTOLERANT R-ACETOSA

KW - CELL-WALL EXTENSION

KW - GENE-EXPRESSION

KW - ALPHA-EXPANSIN

KW - ARABIDOPSIS-THALIANA

KW - 1-AMINOCYCLOPROPANE-1-CARBOXYLATE OXIDASE

KW - SHOOT ELONGATION

KW - ABSCISIC-ACID

U2 - 10.1111/j.1365-313X.2005.02477.x

DO - 10.1111/j.1365-313X.2005.02477.x

M3 - Article

VL - 43

SP - 597

EP - 610

JO - The Plant journal

JF - The Plant journal

SN - 0960-7412

IS - 4

ER -