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First published online February 26, 2004; 10.1104/pp.103.037382

Plant Physiology 134:1227-1239 (2004)
© 2004 American Society of Plant Biologists

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CELL BIOLOGY AND SIGNAL TRANSDUCTION

Geminating Pollen Has Tubular Vacuoles, Displays Highly Dynamic Vacuole Biogenesis, and Requires VACUOLESS1 for Proper Function1,[w]

Glenn R. Hicks, Enrique Rojo2, Seho Hong3, David G. Carter and Natasha V. Raikhel*

Center for Plant Cell Biology and Department of Botany and Plant Sciences, University of California, Riverside, Riverside, California 92521

Vacuoles perform multiple functions in plants, and VCL1 (VACUOLESS1) is essential for biogenesis with loss of expression in the vcl1 mutant leading to lethality. Vacuole biogenesis plays a prominent role in gametophytes, yet is poorly understood. Given the importance of VCL1, we asked if it contributes to vacuole biogenesis during pollen germination. To address this question, it was essential to first understand the dynamics of vacuoles. A tonoplast marker, {delta}-TIP::GFP, under a pollen-specific promoter permitted the examination of vacuole morphology in germinating pollen of Arabidopsis. Our results demonstrate that germination involves a complex, yet definable, progression of vacuole biogenesis. Pollen vacuoles are extremely dynamic with remarkable features such as elongated (tubular) vacuoles and highly mobile cytoplasmic invaginations. Surprisingly, vcl1 did not adversely impact vacuole morphology in pollen germinated in vitro. To focus further on VCL1 in pollen, reciprocal backcrosses demonstrated reduced transmission of vcl1 through male gametophytes, indicating that vcl1 was expressive after germination. Interestingly, vcl1 affected the fertility of female gametophytes that undergo similarly complex vacuole biogenesis. Our results indicate that vcl1 is lethal in the sporophyte but is not fully expressive in the gametophytes. They also point to the complexity of pollen vacuoles and suggest that the mechanism of vacuole biogenesis in pollen may differ from that in other plant tissues.

Article, publication date, and citation information can be found at http://www.plantphysiol.org/cgi/doi/10.1104/pp.103.037382.

1 This work was supported by the Department of Energy (grant no. DE–FG03–02ER15295/A000 to N.V.R.).

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

2 Present address: Departamento de Genetica Molecular de Plantas, Centro Nacional de Biotecnologia, Consejo Superior de Investigaciones Cientifas, E–28049 Madrid, Spain.

3 Present address: Department of Biological Sciences, KAISTYu-song Gu, Daejon, Republic of Korea.

* Corresponding author; e-mail natasha.raikhel{at}ucr.edu; fax 909–787–4437.

Received December 9, 2003; returned for revision January 2, 2004; accepted January 28, 2004.




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