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The interrelationship between the lower oxygen limit, chlorophyll fluorescence and the xanthophyll cycle in plants

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Abstract

The lower oxygen limit (LOL) in plants may be identified through the measure of respiratory gases [i.e. the anaerobic compensation point (ACP) or the respiratory quotient breakpoint (RQB)], but recent work shows it may also be identified by a sudden rise in dark minimum fluorescence (F o). The interrelationship between aerobic respiration and fermentative metabolism, which occur in the mitochondria and cytosol, respectively, and fluorescence, which emanates from the chloroplasts, is not well documented in the literature. Using spinach (Spinacia oleracea), this study showed that Fo and photochemical quenching (q P) remained relatively unchanged until O2 levels dropped below the LOL. An over-reduction of the plastoquinone (PQ) pool is believed to increase F o under dark + anoxic conditions. It is proposed that excess cytosolic reductant due to inhibition of the mitochondria’s cytochrome oxidase under low-O2, may be the primary reductant source. The maximum fluorescence (F m) is largely unaffected by low-O2 in the dark, but was severely quenched, mirroring changes to the xanthophyll de-epoxidation state (DEPS), under even low-intensity light (≈4 μmol m−2 s−1). In low light, the low-O2-induced increase in F o was also quenched, likely by non-photochemical and photochemical means. The degree of quenching in the light was negatively correlated with the level of ethanol fermentation in the dark. A discussion detailing the possible roles of cyclic electron flow, the xanthophyll cycle, chlororespiration and a pathway we termed ‘chlorofermentation’ were used to interpret fluorescence phenomena of both spinach and apple (Malus domestica) over a range of atmospheric conditions under both dark and low-light.

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Notes

  1. This was comparable to a study by Watada et al. (1996) that found the LOL in spinach to be between 0.2 and 0.4 kPa O2, based on the RQB and the ACP, at 5°C.

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Acknowledgments

We would like to thank Dr. David M. Kramer (Washington State University, WA, USA) and Dr. Douglas Campbell (Mount Allison University, NB, Canada) for reviewing this article. This is contribution no. 2377 of the Atlantic Food and Horticulture Research Centre, Agriculture and Agri-Food Canada. The authors would like to thank P. Harrison and C. Bishop for technical assistance. We gratefully acknowledge the Natural Sciences and Engineering Research Council (NSERC) of Canada for Canadian Graduate Studies doctoral funding (CGS D) for H. Wright.

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  1. Atlantic Food and Horticulture Research Centre, Agriculture and Agri-Food Canada, 32 Main Street, Kentville, NS, B4N 1J5, Canada

    A. Harrison Wright, John M. DeLong & Robert K. Prange

  2. Department of Biology, Dalhousie University, Halifax, NS, B3H 4J1, Canada

    A. Harrison Wright & Arunika H. L. A. N. Gunawardena

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  1. A. Harrison Wright
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Correspondence to A. Harrison Wright.

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Wright, A.H., DeLong, J.M., Gunawardena, A.H.L.A.N. et al. The interrelationship between the lower oxygen limit, chlorophyll fluorescence and the xanthophyll cycle in plants. Photosynth Res 107, 223–235 (2011). https://doi.org/10.1007/s11120-011-9621-9

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