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Trees

, Volume 33, Issue 6, pp 1571–1582 | Cite as

Floral development and the formation of functionally unisexual flowers in Xanthoceras sorbifolium (Sapindaceae), a morphologically andromonoecious tree endemic to northern China

  • Qingyuan ZhouEmail author
  • Qing Cai
  • Yuanrun Zheng
  • Zhiyan Wu
  • Jianfeng Mao
Original Article
  • 92 Downloads

Abstract

Key message

Xanthoceras sorbifolium is apparently andromonoecious but exhibits a cryptically monoecious breeding system. Sexual differentiation in male and functional female flowers occurs 2 weeks before flowering.

Abstract

Individual trees of Xanthoceras sorbifolium bear male and morphologically bisexual flowers but functionally female flowers, and show labile sex expression. Investigations of the floral development are of significant value for understanding the breeding system and elucidating the systematic relationships. We studied floral development of male and bisexual flowers using scanning electron and light microscopy. The early stages of floral development were essentially the same, and all floral organ primordia were initiated in the two types of flowers of X. sorbifolium. Later, the stamens in bisexual flowers and the gynoecium in male flowers were aborted. We divided floral development into nine stages. Morphological differences between male and bisexual flowers appeared first at stage 8, when the style elongated obviously and the stigma papillae began to expand in the bisexual flowers but not in the male flowers. Ovule development was arrested shortly after formation of megaspore mother cells or during meiosis in the male flowers, whereas anther development was aberrant in the bisexual flowers. Morphologically bisexual flowers of X. sorbifolium do not have male function and are functionally female. Comparison of floral developmental characters did not support the separation of the Chinese monotypic genus Xanthoceras from the family Sapindaceae.

Keywords

Floral development Andromonoecy Monoecy Systematic relationship Xanthoceras sorbifolium 

Notes

Acknowledgements

We would like to thank Xiuping Xu, Jie Wen, and Fengqin Dong for technical help. This work was supported by National Natural Science Foundation of China (30972344, 31370611 and 31570680) and Beijing Natural Science Foundation (6172028).

References

  1. Acevedo-Rodríguez P, van Welzen PC, Adema F, van der Ham RWJM (2010) Sapindaceae. In: Kubitzki K (ed) Flowering plants, Eudicots: Sapindales, Cucurbitales, Myrtaceae. The families and genera of vascular plants, vol 10. Springer, Berlin.Google Scholar
  2. Ainsworth CS, Buchanan-Wollaston CM, Thangavelu CM, Parker J (1995) Male and female flowers of the dioecious plant sorrel show different patterns of MADS box gene expression. Plant Cell 7:1583–1598PubMedPubMedCentralGoogle Scholar
  3. Beardsell DV, Williams EG, Knox RB (1989) The structure and histochemistry of the nectary and anther secretory tissue of the flowers of Tryptomene calycina (Lindl.) Stapf (Myrtaceae). Aust J Bot 37:65–80CrossRefGoogle Scholar
  4. Buerki S, Forest F, Acevedo-Rodríguez P, Callmander MW, Nylander JAA, Harrington M, Sanmartín I, Küpfer P, Alvarez N (2009) Plastid and nuclear DNA markers reveal intricate relationships at subfamilial and tribal levels in the soapberry family (Sapindaceae). Mol Phylogenet Evol 51:238–258CrossRefGoogle Scholar
  5. Buerki S, Porter P, Lowry II, Alvarez N, Razafimandimbison SG, Kuepfer P, Callmander MW (2010) Phylogeny and circumscription of Sapindaceae revisited: molecular sequence data, morphology and biogeography support recognition of a new family, Xanthoceraceae. Plant Ecol Evol 143:148–159CrossRefGoogle Scholar
  6. Cao LM, Xia NH (2009) Floral organogenesis of Delavaya toxocarpa (Sapindaceae; Sapindales). J Syst Evol 47:237–244CrossRefGoogle Scholar
  7. Cao LM, Xia NH, Deng YF (2008) Embryology of Handeliodendron bodinieri (Sapindaceae) and its systematic value: development of male and female gametophytes. Plant Syst Evol 274:17–23CrossRefGoogle Scholar
  8. Cao LM, Ronse De Craene LP, Wang ZX, Wang YH (2017) The floral organogenesis of Eurycorymbus cavaleriei (Sapindaceae) and its systematic implications. Phytotaxa 297:234–244CrossRefGoogle Scholar
  9. Cao LM, Liu J, Lin Q, Ronse De Craene LP (2018) The floral organogenesis of Koelreuteria bipinnata and its variety K. bipinnata var. integrifolia (Sapindaceae): evidence of floral constraints on the evolution of monosymmetry. Plant Syst Evol 304:923–935CrossRefGoogle Scholar
  10. de Long A, Calderon-Urrea A (1994) The sex determination process in maize. Science 266:1501–1505CrossRefGoogle Scholar
  11. de Barros TC, Pedersoli GD, Teixeira SP (2017) Anther glands in Mimosoideae (Leguminosae) are emergences with a conserved meristematic origin. Flora 226:1–9CrossRefGoogle Scholar
  12. de Lima HA, Somner GV, Giulietti AM (2016) Duodichogamy and sex lability in Sapindaceae: the case of Paullinia weinmanniifolia. Plant Syst Evol 302:109–120CrossRefGoogle Scholar
  13. Dellinger AS, Penneys DS, Staedler YM, Fragner L, Weckwerth W, Schönenberger J (2014) A specialized bird pollination system with a bellows mechanism for pollen transfer and staminal food body rewards. Curr Biol 24:1615–1619CrossRefGoogle Scholar
  14. Diggle PK (1993) Developmental plasticity, genetic variation, and the evolution of andromonoecy in Solanum hirtum (Solanaceae). Am J Bot 80:967–973CrossRefGoogle Scholar
  15. Endress PK, Stumpf S (1991) The diversity of stamen structures in ‘lower’ Rosidae (Rosales, Fabales, Proteales, Sapindales). Bot J Linn Soc 107:217–293CrossRefGoogle Scholar
  16. Freeman DC, Harper KT, Charnov EL (1980) Sex change in plants: old and new observations and new hypotheses. Oecologia 47:222–232CrossRefGoogle Scholar
  17. Gagliardi KB, Cordeiro I, Demarco D (2018) Structure and development of flowers and inflorescences in Peraceae and Euphorbiaceae and the evolution of pseudanthia in Malpighiales. PLoS ONE 13(10):e0203954.  https://doi.org/10.1371/journal.pone.0203954 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Heslop-Harrison J (1964) Sex expression in flowering plants. Brookhaven Symposia in Biology No. 16, 109-125. Brookhaven National Laboratory, Upton, NYGoogle Scholar
  19. Heslop-Harrison Y (1981) Stigma characteristics and angiosperm taxonomy. Nord J Bot 1:401–420CrossRefGoogle Scholar
  20. Le Roux Lucia G, Kellogg EA (1999) Floral development and the formation of unisexual spikelets in the Andropoganeae (Poaceae). Amer J Bot 86:354–366CrossRefGoogle Scholar
  21. Luo YB, Yu JL, Tong ZK, Zhao HB (2017) Flower development of different genders in the morphologically andromonoecious but functionally monoecious plant Acer elegantulum Fang et P. L. Chiu. Flora 233:179–185CrossRefGoogle Scholar
  22. Mitchell CH, Diggle PK (2005) The evolution of unisexual flowers: morphological and functional convergence results from diverse developmental transitions. Am J Bot 92:1068–1076CrossRefGoogle Scholar
  23. Renner SS (2014) The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database. Am J Bot 101:1588–1596CrossRefGoogle Scholar
  24. Reuther K, Claßen-Bockhoff R (2013) Andromonoecy and developmental plasticity in Chaerophyllum bulbosum (Apiaceae–Apioideae). Ann Bot 112:1495–1503CrossRefGoogle Scholar
  25. Richards AJ (1986) Plant breeding systems. George Allen and Unwin, LondonGoogle Scholar
  26. Ronse De Craene LP, Smets E, Clinckemaillie D (2000) Floral ontogeny and anatomy in Koelreuteria with special emphasis on monosymmetry and septal cavities. Plant Syst Evol 223:91–107CrossRefGoogle Scholar
  27. Sherry RA, Eckard KJ, Lord EM (1993) Flower development in dioecious Spinacia oleracea (Chenopodiaceae). Am J Bot 80:283–291CrossRefGoogle Scholar
  28. Tucker SC (1998) Floral ontogeny in legume genera Petalostylis, Labichea, and Dialium (Caesalpinioideae: Cassieae), a series in floral reduction. Am J Bot 85:184–208CrossRefGoogle Scholar
  29. Vary LB, Sakai AK, Weller SG (2011) Morphological and functional sex expression in the Malagary endemic Tina striata (Sapindaceae). Am J Bot 98:1040–1048CrossRefGoogle Scholar
  30. Xia NH, Gadek PA (2007) Sapindaceae. In: Wu ZY, Raven PH (eds) Flora of China Vol. 12. Science Press, Beijing.Google Scholar
  31. Yampolsky C, Yampolsky H (1922) Distribution of sex forms in the phanerogamic flora. Bibl Gen 3:1–62Google Scholar
  32. Zhou QY, Cai Q (2018) The superoxide dismutase genes might be required for appropriate development of the ovule after fertilization in Xanthoceras sorbifolium. Plant Cell Rep 37:727–739CrossRefGoogle Scholar
  33. Zhou QY, Liu GS (2012) The embryology of Xanthoceras and its phylogenetic implications. Plant Syst Evol 298:457–468CrossRefGoogle Scholar
  34. Zhou QY, Zheng YR, Lai LM, Du H (2017) Observations on sexual reproduction in Xanthoceras sorbifolium (Sapindaceae). Acta Bot Occid Sin 37:0014–0022Google Scholar
  35. Zimmerman E, Prenner G, Bruneau A (2013) Floral ontogeny in Dialiinae (Caesalpiniodeae: Cassieae): a study in organ loss and instability. South Afr J Bot 89:188–209CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Key Laboratory of Plant Resources, Institute of BotanyChinese Academy of SciencesBeijingChina
  2. 2.Shinyleaf Yellowhorn Engineering and Technology Research Center of National Forestry and Grassland AdministrationChifengChina
  3. 3.College of Biological Sciences and TechnologyBeijing Forestry UniversityBeijingChina

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