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Developmental analyses reveal early arrests of the spore-bearing parts of reproductive organs in unisexual flowers of cucumber (Cucumis sativus L.)

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Abstract

To understand the regulatory mechanisms governing unisexual flower development in cucumber, we conducted a systematic morphogenetic analysis of male and female flower development, examined the dynamic changes in expression of the C-class floral organ identity gene CUM1, and assessed the extent of DNA damage in inappropriate carpels of male flowers. Accordingly, based on the occurrence of distinct morphological events, we divided the floral development into 12 stages ranging from floral meristem initiation to anthesis. As a result of our investigation we found that the arrest of stamen development in female flowers, which occurs just after the differentiation between the anther and filament, is mainly restricted to the primordial anther, and that it is coincident with down-regulation of CUM1 gene expression. In contrast, the arrest of carpel development in the male flowers occurs prior to the differentiation between the stigma and ovary, given that no indication of ovary differentiation was observed even though CUM1 gene expression remained detectable throughout the development of the stigma-like structures. Although the male and female reproductive organs have distinctive characteristics in terms of organ differentiation, there are two common features regarding organ arrest. The first is that the arrest of the inappropriate organ does not affect the entirety of the organ uniformly but occurs only in portions of the organs. The second feature is that all the arrested portions in both reproductive organs are spore-bearing parts.

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Fig. 1a–m
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Fig. 4a–p
Fig. 5a–j
Fig. 6a–c
Fig. 7a–c

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Abbreviations

SEM:

Scanning electron microscopy

TEM:

Transmission electron microscopy

TUNEL:

TdT-mediated dUTP nick-end labeling

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Acknowledgements

The authors thank Ms Min Chen at the University of Arizona, USA, for her pilot work on the cucumber morphogenesis in this laboratory; Dr. Yu-Jin Hao at the National Institute of Fruit Tree Science, Japan, for his involvement in discussion of the implication of the putative critical point in cucumber unisexual flower development; Prof. C.X. He of the Institute of Vegetables and Flowers, CAAS for his help in growing plants; Prof. Xiansheng Zhang of Shangdong Agricultural University for his gift of the CUM1 gene as a probe; Prof. Zheng Meng and Wen-Liang Lu for their help in the establishment of the in situ technique in our laboratory; Profs. T.H. Tsao and S.Y. Hu of PKU, Prof. Z.R. Sung of UC Berkeley, Prof. H. Ma of Penn State University and Prof. V. Irish of Yale University for their critical reading of the manuscript; This work was supported by grants to S-N.B. from MST (J00-A-005, G19990116), NSFC (30070361), and to Z-H.X from MST.

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Correspondence to Shu-Nong Bai.

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Bai, SL., Peng, YB., Cui, JX. et al. Developmental analyses reveal early arrests of the spore-bearing parts of reproductive organs in unisexual flowers of cucumber (Cucumis sativus L.). Planta 220, 230–240 (2004). https://doi.org/10.1007/s00425-004-1342-2

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