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First published online December 23, 2005; 10.1104/pp.105.073015

Plant Physiology 140:326-335 (2006)
© 2006 American Society of Plant Biologists

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ENVIRONMENTAL STRESS AND ADAPTATION TO STRESS

Pea Seed Mitochondria Are Endowed with a Remarkable Tolerance to Extreme Physiological Temperatures1

Irina Stupnikova, Abdelilah Benamar, Dimitri Tolleter, Johann Grelet, Genadii Borovskii, Albert-Jean Dorne and David Macherel*

Siberian Institute for Plant Physiology and Biochemistry, 664033 Irkutsk, Russia (I.S., G.B.); Unité Mixte de Recherche 1191 Physiologie Moléculaire des Semences, Université d'Angers/l'Institut National d'Horticulture/Institut National de la Recherche Agronomique, ARES, 49045 Angers cedex 01, France (A.B., J.G., D.M.); and Unité Mixte de Recherche 5019 Physiologie Cellulaire Végétale, Centre National de la Recherche Scientifique/Commissariat à l'Energie Atomique/Université Joseph Fourier, 38054 Grenoble cedex 9, France (A.-J.D.)

Most seeds are anhydrobiotes, relying on an array of protective and repair mechanisms, and seed mitochondria have previously been shown to harbor stress proteins probably involved in desiccation tolerance. Since temperature stress is a major issue for germinating seeds, the temperature response of pea (Pisum sativum) seed mitochondria was examined in comparison with that of mitochondria from etiolated epicotyl, a desiccation-sensitive tissue. The functional analysis illustrated the remarkable temperature tolerance of seed mitochondria in response to both cold and heat stress. The mitochondria maintained a well-coupled respiration between –3.5°C and 40°C, while epicotyl mitochondria were not efficient below 0°C and collapsed above 30°C. Both mitochondria exhibited a similar Arrhenius break temperature at 7°C, although they differed in phospholipid composition. Seed mitochondria had a lower phosphatidylethanolamine-to-phosphatidylcholine ratio, fewer unsaturated fatty acids, and appeared less susceptible to lipid peroxidation. They also accumulated large amounts of heat shock protein HSP22 and late-embryogenesis abundant protein PsLEAm. The combination of membrane composition and stress protein accumulation required for desiccation tolerance is expected to lead to an unusually wide temperature tolerance, contributing to the fitness of germinating seeds in adverse conditions. The unique oxidation of external NADH at low temperatures found with several types of mitochondria may play a central role in maintaining energy homeostasis during cold shock, a situation often encountered by sessile and ectothermic higher plants.


1 This work was supported by a postdoctoral fellowship from the Région Pays-de-la-Loire (to I.S.); by the Contrat de Plan Etat-Région Pays-de-la-Loire, program "Semences"; and by the Russian Fund of Basic Researches (project N 05–04–48966–a).

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: David Macherel (david.macherel{at}univ-angers.fr).

Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.073015.

* Corresponding author; e-mail david.macherel{at}univ-angers.fr; fax 33–241–225–549.

Received October 18, 2005; returned for revision October 18, 2005; accepted November 8, 2005.




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