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Vascular Aerenchyma and PCD

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Plant Programmed Cell Death

Abstract

Aerenchyma is tissue in a plant organ with larger than typical intercellular spaces. Historically the presumed function of aerenchyma has been enhanced oxygen distribution within the organ under otherwise suboptimal gas exchange conditions. Ultimately, however, other functions have been attributed to aerenchyma tissue, depending on its type and the organ involved, including floatation, reduced respiratory demand, improved mineral absorption, and enhanced interactions with other species. Generally there are two broad types: developmentally constitutive and stress-induced aerenchyma. The former typically results from cell separation during growth (schizogeny) and the latter from cell removal by degradation (lysigeny). Lysigenous aerenchyma, which usually forms within the ground tissue system, has been characterized in several species as being the result of programmed cell death (PCD). The discovery of extensive lysigenous destruction of the central vascular tissue in primary roots of pea (Pisum sativum) under certain conditions began as a straightforward observation that led to a controversy that spanned decades. The controversy stimulated an investigation by our research group. Step by step we accumulated the evidence that this process, as improbable as it seemed, is PCD-mediated aerenchyma formation. Vascular cavities were first correlated to temperatures above 15 °C; then it was shown that warm temperatures were necessary but not sufficient. Cavity formation was observed to be correlated also to the degree of water saturation of the root medium. We discovered that by manipulating the water content of the medium, we could regulate the frequency of cavity formation and induce cavities very rapidly by sudden flooding. Observed ultrastructural changes, such as nuclear invagination, chromatin condensation, and tonoplast rupture in affected cells, were consistent with contemporary reports emerging about PCD in other plant species. Further investigations in P. sativum revealed that ethylene was a critical mediator of the process, that systematic DNA fragmentation occurred, and that cytochrome c was released from mitochondria. In Glycine max caspase-like proteases were shown to be part of the induction pathway. Finally, direct evidence from a study using Phaseolus coccineus showed that vascular cavities enhance oxygen availability for the apical meristem and therefore are a form of functional aerenchyma. Further work is proceeding to evaluate gene expression changes during vascular cavity formation in G. max. The ultimate goal is to fully understand the signal transduction pathway for the formation of vascular cavities, an unusual form of aerenchyma.

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Acknowledgments

The author thanks his mentors and collaborators, Teruo Niki, Tom Rost, Pengzhe Lu, and Mitsuo Takahashi, and his hardworking students, Purbasha Sarkar, Suma Sreekanta, and Hans Waldenmaier, for their many significant contributions to the studies reported in this chapter. I also thank Bill Biasi and Rob Veltman of the University of California-Davis Pomology Post-Harvest Laboratory and Richard Edelmann and Matt Duley of the Miami University Center for Advanced Microscopy and Imaging for excellent advice and technical assistance. Sachiko Ishii, Prof. Niki’s longtime technical assistant, deserves special mention for her precision, organization skills, and tolerance for our many bad jokes.

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  1. Department of Biology, Miami University, Hamilton, OH, USA

    Daniel K. Gladish

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  1. Department of Biology, Dalhousie University, Halifax, NS, Canada

    Arunika N. Gunawardena

  2. School of Biology and Environmental Science, University College Dublin, Dublin, Ireland

    Paul F. McCabe

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Gladish, D.K. (2015). Vascular Aerenchyma and PCD. In: Gunawardena, A.N., McCabe, P.F. (eds) Plant Programmed Cell Death. Springer, Cham. https://doi.org/10.1007/978-3-319-21033-9_5

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