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ENVIRONMENTAL STRESS AND ADAPTATION TO STRESS

Regulation of Respiration and the Oxygen Diffusion Barrier in Soybean Protect Symbiotic Nitrogen Fixation from Chilling-Induced Inhibition and Shoots from Premature Senescence^1,[W],[OA]

Plant Sciences Department, Rothamsted Research, Harpenden, Hertshire AL5 2JQ, United Kingdom (P.D.R.v.H., G.K., T.K.P., P.W.M., U.S., C.H.F.); School of Environmental Sciences and Development, Section Botany, North-West University, Potchefstroom 2520, South Africa (P.D.R.v.H., A.J., A.J.S., M.d.B.); Department of Biodiversity, University of Limpopo, Sovenga 0727, South Africa (P.W.M.); Forestry and Agricultural Biotechnology Institute, University of Pretoria, Pretoria 0002, South Africa (U.S., K.J.K.); and School of Agriculture, Food, and Rural Development, University of Newcastle upon Tyne, Newcastle upon Tyne NE1 7RU, United Kingdom (C.H.F.)

Symbiotic nitrogen fixation is sensitive to dark chilling (7°C–15°C)-induced inhibition in soybean (Glycine max). To characterize the mechanisms that cause the stress-induced loss of nodule function, we examined nodule structure, carbon-nitrogen interactions, and respiration in two soybean genotypes that differ in chilling sensitivity: PAN809 (PAN), which is chilling sensitive, and Highveld Top (HT), which is more chilling resistant. Nodule numbers were unaffected by dark chilling, as was the abundance of the nitrogenase and leghemoglobin proteins. However, dark chilling decreased nodule respiration rates, nitrogenase activities, and NifH and NifK mRNAs and increased nodule starch, sucrose, and glucose in both genotypes. Ureide and fructose contents decreased only in PAN nodules. While the chilling-induced decreases in nodule respiration persisted in PAN even after return to optimal temperatures, respiration started to recover in HT by the end of the chilling period. The area of the intercellular spaces in the nodule cortex and infected zone was greatly decreased in HT after three nights of chilling, an acclimatory response that was absent from PAN. These data show that HT nodules are able to regulate both respiration and the area of the intercellular spaces during chilling and in this way control the oxygen diffusion barrier, which is a key component of the nodule stress response. We conclude that chilling-induced loss of symbiotic nitrogen fixation in PAN is caused by the inhibition of respiration coupled to the failure to regulate the oxygen diffusion barrier effectively. The resultant limitations on nitrogen availability contribute to the greater chilling-induced inhibition of photosynthesis in PAN than in HT.

² Present address: South African Sugarcane Research Institute, 170 Flanders Drive, Mount Edgecombe 4300, South Africa.

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: Christine H. Foyer (christine.foyer{at}ncl.ac.uk).

^[W] The online version of this article contains Web-only data.

^[OA] Open Access articles can be viewed online without a subscription.

www.plantphysiol.org/cgi/doi/10.1104/pp.108.123422

^* Corresponding author; e-mail christine.foyer{at}ncl.ac.uk.

Received May 23, 2008; accepted July 16, 2008; published July 30, 2008.

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