Down to the wire: late season changes in sex expression in a sexually labile tree species, Acer pensylvanicum (Sapindaceae)
In sexually plastic Acer pensylvanicum, determination of sex can occur extremely late, within three weeks of spring flowering. Physical damage causing complete vascular tissue severance results in increased female expression.
Species with environmental sex determination are rare amongst angiosperms but widely distributed across taxa. The timing of floral development in species that change sex based on environmental cues is unexplored. We investigated the timing of differentiation of sexual organs in buds of Acer pensylvanicum, an understory tree in eastern North America with environmental sex determination. We collected branches from individuals at three collection times in the early spring of 2016 and kept them in a warm greenhouse until anthesis. All individuals exhibited complete or partial female inflorescences in the greenhouse in one or more collection. However, none of these same individuals produced only female flowers in the field. Unlike many other woody species that differentiate bud sexual primordia 9–12 months prior to flowering, A. pensylvanicum may differentiate the sexual organs in its flower buds as late as three weeks prior to anthesis. In a separate series of branch collections in 2017, we found that the stress response to cutting leads to increased female sex expression in branches, while earlier warm temperatures (e.g., those caused by growing in a protected greenhouse environment) or increased carbohydrate availability does not. Given the labile sex determination system of A. pensylvanicum, the ability to delay differentiation of buds into male or female until shortly before spring flowering would allow individual trees to respond to sex-determining damage cues as late as mid-spring. This supports the hypothesis that A. pensylvanicum may not exhibit the lag-time characteristic of temperate spring and early-summer flowering woody species and may change sex expression in response to stress.
KeywordsAcer Dioecy Environmental sex determination Flowering Phenology Sex expression
We would like to thank Dr. Jason Grabosky, Dr. Peter Morin, Dr. Greg Anderson, the Research and Horticultural greenhouse staff, Carlos Olivares, Anny Marchioni, and Pepe Bowman for help with this research. Research permits were obtained from the New Jersey Department of Environmental Protection. This work was supported by the Ecology and Evolution Graduate Program, Rutgers University; the Torrey Botanical Society; the Botanical Society of America, and NSF IGERT Grant (NSF-DGE/IGERT 0903675).
J. Blake-Mahmud designed and conducted the experiments, collected and analyzed data, and wrote the manuscript as part of a doctoral dissertation. L. Struwe co-led the embedding and sectioning investigation and serves as the doctoral dissertation advisor.
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Conflict of interest
The authors declare that they have no conflict of interest.
- Blake J, Struwe L (2015) Temporal and environmental dimensions of variable sex expression in striped maple, Acer pensylvanicum (Sapindaceae). In: Botany. Edmonton, Alberta, Canada. http://2015.botanyconference.org/engine/search/index.php?func=detail&aid=1844. Accessed 22 Dec 2017
- Blake J, Struwe L (2017) Sugars, stress, and sex-change: environmental sex determination in striped maple. In: Botany. Fort Worth, TX. http://2017.botanyconference.org/engine/search/index.php?func=detail&aid=235. Accessed 22 Dec 2017
- Blake-Mahmud J, Struwe L (2016) Late season changes in sex expression in striped maple,Acer pensylvanicum (Sapindaceae). In: Botany. Savannah, GA. http://2016.botanyconference.org/engine/search/index.php?func=detail&aid=852. Accessed 22 Dec 2017
- Davis MB (1986) Climatic instability, time lags, and community disequilibrium. In: Diamond JCTJ (ed) Community ecology. Harper and Row Publishers, New York, pp 269–284Google Scholar
- de Jong PC (1976) Flowering and sex expression in Acer L.: a biosystematic study. Dissertation, Agricultural University Wageningen, The NetherlandsGoogle Scholar
- Guimond CM, Andrews PK, Lang GA (1998) Scanning electron microscopy of floral initiation in sweet cherry. J Am Soc Hortic Sci 123:509–512Google Scholar
- Haas TP (1933) Untersuchung an der Gattung Acer. Dissertation, Universität München, GermanyGoogle Scholar
- Holmes RT, Likens GE (2016) Hubbard Brook: the story of a forest ecosystem. Yale University Press, New Haven, CT, USAGoogle Scholar
- Immelman KL (1984) Simaroubaceae flowering in Kirkia wilmsii Engl. Bothalia 102:151–152Google Scholar
- Kozlowski TT, Kramer PJ, Pallardy SG (1991) The physiological ecology of woody plants. Academic Press, New YorkGoogle Scholar
- Lavender DP (1986) Angiospermous forest trees of temperate zones. In: Halevy AH (ed) Handbook of Flowering. CRC Press, Inc, Boca Raton, pp 15–23Google Scholar
- Longman KA, Coutts MP (1974) Physiology of the oak tree. In: Morris MG, Perring FH (eds) The British oak. The Botanical Society of the British Isles, Berkshire, pp 194–221Google Scholar
- Sedgley M (1989) Floral development, anthesis, and pollination. Acta Hortic 177–184Google Scholar
- Sedgley M, Griffin AR (1989) Sexual reproduction of tree crops. Academic Press, San DiegoGoogle Scholar
- Wetzstein HY, Sparks D (1986) Flowering in Pecan. In: Janick J (ed) Horticultural reviews, vol 8. Wiley, NJ, pp 217–255Google Scholar
- Woodroof JG, Chapman-Woodroof N (1926) Fruit-bud differentiation and subsequent development of the flowers in the Hicoria Pecan. J Agric Res 33:677–685Google Scholar
- Yonemori K, Sugiura A, Tanaka K, Kameda K (1993) Floral ontogeny and sex determination in monoecious-type persimmons. J Am Soc Hortic Sci 118:293–297Google Scholar