The Plant Cell 21: 3803-3822 (2009)

Ethylene interacts with abscisic acid to regulate endosperm rupture during germination: a comparative approach using Lepidium sativum and Arabidopsis thaliana  [W][OA]

Ada Linkies, Kerstin Müller, Karl Morris, Veronika Turecková, Meike Wenk, Cassandra S. C. Cadman, Françoise Corbineau, Miroslav Strnad, James R. Lynn, William E. Finch-Savage, Gerhard Leubner-Metzger
University of Freiburg, Faculty of Biology, Institute for Biology II, Botany / Plant Physiology, D-79104 Freiburg, Germany, Web: 'The Seed Biology Place' (A.L., Ke.M., M.W., G.L.-M.)
Warwick Horticulture Research International (HRI), Warwick University, Wellesbourne, Warwick CV35 9EF, United Kingdom (Ka.M., C.S.C.C., J.R.L., W.E.F.-S.)
Palacky University and Institute of Experimental Botany Academy of Sciences of the Czech Republic, Laboratory of Growth Regulators, CZ-78371 Olomouc, Czech Republic (V.T., M.S.)
Université Pierre et Marie Curie-Paris 6, Germination et Dormance des Semences, UR5, Site d'Ivry, F-75005 Paris, France (F.C.)

Received July 23, 2009; Returned for revision October 12, 2009; Accepted November 17, 2009; Published December 18, 2009

Abstract. The micropylar endosperm cap covering the radicle in the mature seeds of most angiosperms acts as a constraint that regulates seed germination. Here, we report on a comparative seed biology study with the close Brassicaceae relatives Lepidium sativum and Arabidopsis thaliana showing that ethylene biosynthesis and signaling regulate seed germination by a mechanism that requires the coordinated action of the radicle and the endosperm cap. The larger seed size of Lepidium allows direct tissue-specific biomechanical, biochemical, and transcriptome analyses. We show that ethylene promotes endosperm cap weakening of Lepidium and endosperm rupture of both species and that it counteracts the inhibitory action of abscisic acid (ABA) on these two processes. Cross-species microarrays of the Lepidium micropylar endosperm cap and the radicle show that the ethylene-ABA antagonism involves both tissues and has the micropylar endosperm cap as a major target. Ethylene counteracts the ABA-induced inhibition without affecting seed ABA levels. The Arabidopsis loss-of-function mutants ACC oxidase2 (aco2; ethylene biosynthesis) and constitutive triple response1 (ethylene signaling) are impaired in the 1-aminocyclopropane-1-carboxylic acid (ACC)-mediated reversion of the ABA-induced inhibition of seed germination. Ethylene production by the ACC oxidase orthologs Lepidium ACO2 and Arabidopsis ACO2 appears to be a key regulatory step. Endosperm cap weakening and rupture are promoted by ethylene and inhibited by ABA to regulate germination in a process conserved across the Brassicaceae.

Key words: abscisic acid (ABA), ACC oxidase ACO2, Brassicaceae cross-species work, endosperm rupture, endosperm weakening, ethylene, ethylene-ABA antagonism, micropylar endosperm (cap), radicle, seed germination, transcriptome

Synopsis: Tissue weakening of the endosperm is required to allow radicle protrusion during seed germination. Cross-species work including tissue-specific transcriptome analysis and biomechanical measurement of endosperm weakening provided a new mechanistic model that explains how ethylene promotes seed germination and counteracts the inhibition of endosperm cap weakening by abscisic acid.

Financial support: Our work is funded by grants of the Deutsche Forschungsgemeinschaft (grant no. DFG LE720/6) and the Deutscher Akademischer Austauschdienst (grant no. DAAD D/0628197) to G.L.-M., the Wissenschaftliche Gesellschaft Freiburg to G.L.-M. and A.L., the UK Department for the Environment, Food and Rural Affairs and the Biotechnology and Biological Sciences Research Council (grant no. BB/E006418/1) to W.F.-S., the Hubert Curien Program (Proscope grant no. 14896 UL) to F.C., and the Czech Ministry of Education grant MSM 6198959216 to M.S. which are gratefully acknowledged.

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