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Changes in mitochondrial membrane potential and accumulation of reactive oxygen species precede ultrastructural changes during ovule abortion

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Abstract

In many species, environmental stress reduces plant fertility. In Arabidopsis thaliana, a significant fraction of this reduction in plant fertility results from ovule abortion and embryo senescence. In this species, environmental conditions were identified that induced 94% of the developing ovules to either undergo stress-induced ovule abortion or embryo senescence (Sun et al. Plant Physiol 135:2358–2367, 2004). Following salt stress, physiological and anatomical changes were first detected in the female gametophyte of an aborting ovule. Two to four hours after a period of salt stress that induces most ovules to abort, the mitochondrial membrane potential dissipated. Subsequently, cells in the gametophyte accumulated reactive oxygen species, which are known to be molecules that promote programmed cell death (PCD). Because mitochondria often play an important role in PCD, these organelles were closely examined for changes in structure. Although the anatomy of mitochondria varied, reproducible changes in mitochondria structure were not observed. Nonetheless, other changes in ultrastructure were found. In some aborting gametophytes, concentric rings of endoplasmic reticulum were formed. In a fraction of the aborting ovules, cytoplasmic contents and organelles were invaginated into the vacuole. Even in cryofixed sections, many of these bodies appeared indistinct, which is consistent with the degradation of their contents.

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Abbreviations

CH2DCFDA:

5-(and-6)-carboxy-2′, 7′-dichlorodihydrofluorescein diacetate

ER:

endoplasmic reticulum

JC-1:

5,5′, 6,6′-tetrachloro-1, 1′, 3, 3′-tetraethyl-benzimidazolylcarbocyanine iodide

MMC:

Megaspore mother cell

PCD:

Programmed cell death

ROS:

Reactive oxygen species

TEM:

Transmission electron microscopy

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Acknowledgements

We thank Greg Erdos and Karen Kelley for assistance with electron microscopy, and Margaret Joyner and anonymous reviewers for helpful comments. The National Research Initiative of the USDA Cooperative State Research, Education and Extension Service (grant number 2002-35100-12109), and the UF Alumni Fellowship Program supported this research.

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Authors and Affiliations

  1. Department of Botany, UF Genetics Institute, and Plant Molecular and Cellular Biology Program, University of Florida, 220 Bartram Hall, Gainesville, FL, 32611-8526, USA

    Bernard A. Hauser, Kelian Sun & David G. Oppenheimer

  2. Department of Botany, University of Toronto, 25 Wilcock St., Toronto, ON, Canada, M5S 3B2

    Tammy L. Sage

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  1. Bernard A. Hauser
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Correspondence to Bernard A. Hauser.

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Hauser, B.A., Sun, K., Oppenheimer, D.G. et al. Changes in mitochondrial membrane potential and accumulation of reactive oxygen species precede ultrastructural changes during ovule abortion. Planta 223, 492–499 (2006). https://doi.org/10.1007/s00425-005-0107-x

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