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

• Published in: The Plant journal : for cell and molecular biology Vol. 43; no. 4; pp. 597 - 610
• Main Authors: 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
• Format: Journal Article
• Language: English
• Published: Oxford, UK Blackwell Science Ltd 01.08.2005; Blackwell Science; Blackwell Publishing Ltd
• Subjects: Abscisic Acid - pharmacology; acidification; apoplast; apoplastic acidification; Biological and medical sciences; Botany; elongation growth; ethylene; Ethylenes - pharmacology; expansins; Flowers - growth & development; Fundamental and applied biological sciences. Psychology; gene expression regulation; Gene Expression Regulation, Developmental - drug effects; Gene Expression Regulation, Developmental - physiology; Gene Expression Regulation, Plant - drug effects; Gene Expression Regulation, Plant - physiology; Gibberellins - pharmacology; Hormones; messenger RNA; molecular sequence data; Naphthaleneacetic Acids - pharmacology; nucleotide sequences; petioles; Physical agents; Physical growth; plant growth; Plant Growth Regulators - physiology; Plant physiology and development; Plant Proteins - biosynthesis; Proteins; Rumex; Rumex - drug effects; Rumex - growth & development; Rumex - metabolism; Rumex palustris; Signal transduction; submerged aquatic plants; Time Factors; transcription (genetics); Transcription, Genetic - physiology; Triazoles - pharmacology; Vegetative apparatus, growth and morphogenesis. Senescence; Water; Water - metabolism; Polygonaceae; Growth; Ethylene; Rumex; Submersion; elongation growth; Protein; Regulation(control); expansins; Dicotyledones; Angiospermae; Plant growth substance; Spermatophyta; Aquatic plant; Gas exchange; apoplastic acidification; Elongation; Petiole
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/j.1365-313x.2005.02477.x

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.