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First published online March 20, 2009; doi:10.3732/ajb.0800343 American Journal of Botany 96: 865-876 (2009) © 2009 Botanical Society of America, Inc.

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In vivo study of developmental programmed cell death using the lace plant (Aponogeton madagascariensis; Aponogetonaceae) leaf model system¹

² Atlantic Food and Horticulture Research Center, Agriculture and Agri-Food Canada, Kentville, Nova Scotia, B4N 1J5, Canada ³ Department of Biology, Dalhousie University, Halifax, Nova Scotia, B3H 4J1, Canada ⁴ Mann Laboratory, Department of Plant Sciences, University of California, Davis, California, 95616 USA

ABSTRACT

Programmed cell death (PCD) is required for many morphological changes, but in plants it has been studied in much less detail than in animals. The unique structure and physiology of the lace plant (Aponogeton madagascariensis) is well suited for the in vivo study of developmental PCD. Live streaming video and quantitative analysis, coupled with transmission electron microscopy, were used to better understand the PCD sequence, with an emphasis on the chloroplasts. Dividing, dumbbell-shaped chloroplasts persisted until the late stages of PCD. However, the average size and number of chloroplasts, and the starch granules associated with them, declined steadily in a manner reminiscent of leaf senescence, but distinct from PCD described in the Zinnia tracheary element system. Remaining chloroplasts often formed a ring around the nucleus. Transvacuolar strands, which appeared to be associated with chloroplast transport, first increased and then decreased. Mitochondrial streaming ceased abruptly during the late stages of PCD, apparently due to tonoplast rupture. This rupture occurred shortly before the rapid degradation of the nucleus and plasma membrane collapse, in a manner also reminiscent of the Zinnia model. The presence of numerous objects in the vacuoles suggests increased macro-autophagy before cell death. These objects were rarely observed in cells not undergoing PCD.

Key Words: Aponogeton madagascariensis • Aponogetonaceae • autophagy • chloroplast • cytoplasmic streaming • lace plant • light microscopy • programmed cell death • transmission electron microscopy • transvacuolar strands

Received for publication 9 October 2008. Accepted for publication 5 January 2009.

FOOTNOTES

¹ The authors thank N. Dengler for reviewing this article, G. Rantong for artwork, and V. Hannon for assistance in formatting supplementary videos. The authors thank the Natural Sciences and Engineering Research Council (NSERC) of Canada for Canadian Graduate Studies doctoral funding (CGS D) for H.W. and a discovery and equipment grant for A.G.

⁵ Author for correspondence (e-mail: arunika.gunawardena{at}dal.ca)

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