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Pollen tube development in two species of Trithuria (Hydatellaceae) with contrasting breeding systems

Abstract

Trithuria (Hydatellaceae; Nymphaeales) is unique among early-divergent angiosperms in that its species are extremely small and most have exceptionally short, annual life histories. Given the evolution of these extremes of size and development, we sought to understand whether post-pollination processes still varied predictably with breeding system in Trithuria. To address this question, we studied two Western Australian species, Trithuria austinensis (dioecious, obligately outcrossing) and Trithuria submersa (bisexual, highly selfing). To document developmental timing, carpels were hand-pollinated, collected at sequential time points, and examined with light and fluorescence microscopy. In both species, pollen tubes first entered ovules <1 h after pollination, but the pollen tube pathway of outcrossing T. austinensis was almost four times longer and its pollen tube growth rates were up to six times faster (≤2,166 vs. 321 μm/h) than those of T. submersa. T. austinensis also exhibited greater male investment, slower pollen germination, and greater pollen tube attrition. These differences in male gametophyte development are predicted for outcrossers versus selfers in phylogenetically derived angiosperms. These new data for Hydatellaceae reinforce the idea that an acceleration of pollen tube development occurred in the Nymphaeales stem lineage, before the origin of Hydatellaceae. We infer that a recent evolutionary transition to selfing in T. submersa has been accompanied by predictable modifications to reproductive development, which, because of the ancient relationship between Hydatellaceae and all other angiosperms, suggests that traits underlying the lability of flowering plant post-pollination biology were present early in their history.

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Acknowledgments

The authors thank the Western Australia Department of Environment and Conservation in Manjimup, particularly Robyn Bowles and Rich Robinson for providing logistical support and use of facilities, as well as Roger Hearn for insightful conversations about the ecology of the area wetlands. We especially thank Terry Macfarlane for his assistance in locating populations and identifying plants, as well as for valuable discussion. We also thank Anna Becker and M. Steven Furches for assistance with field collections, Andrew Moffat for laboratory assistance, and Nicholas Buckley and Matthew Lettre for comments on early drafts of this manuscript. This work was supported by a National Science Foundation (NSF) Doctoral Dissertation Improvement Grant to M. L. T. (DEB 0910171) and by NSF award IOS 1052291 to J. H. W.

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Correspondence to Mackenzie L. Taylor.

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Communicated by Scott Russell.

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Taylor, M.L., Williams, J.H. Pollen tube development in two species of Trithuria (Hydatellaceae) with contrasting breeding systems. Sex Plant Reprod 25, 83–96 (2012). https://doi.org/10.1007/s00497-012-0183-6

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