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First published online July 21, 2006; 10.1104/pp.106.081430

Plant Physiology 142:220-232 (2006)
© 2006 American Society of Plant Biologists

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WHOLE PLANT AND ECOPHYSIOLOGY

A Shift of Phloem Unloading from Symplasmic to Apoplasmic Pathway Is Involved in Developmental Onset of Ripening in Grape Berry1

Xiao-Yan Zhang2, Xiu-Ling Wang2, Xiao-Fang Wang2, Guo-Hai Xia, Qiu-Hong Pan, Ren-Chun Fan, Fu-Qing Wu, Xiang-Chun Yu and Da-Peng Zhang*

China State Key Laboratory of Plant Physiology and Biochemistry, China Agricultural University, 100094 Beijing, China

It remains unclear whether the phloem unloading pathway alters to adapt to developmental transition in fleshy fruits that accumulate high level of soluble sugars. Using a combination of electron microscopy, transport of the phloem-mobile symplasmic tracer carboxyfluorescein, movement of the companion cell-expressed and the green fluorescent protein-tagged viral movement protein, and assays of the sucrose cleavage enzymes, the pathway of phloem unloading was studied in the berries of a hybrid grape (Vitis vinifera x Vitis labrusca). Structural investigations showed that the sieve element-companion cell complex is apparently symplasmically connected through plasmodesmata with surrounding parenchyma cells throughout fruit development, though a small portion of plasmodesmata are apparently blocked in the ripening stage. Both carboxyfluorescein and the green fluorescent protein-tagged viral movement protein were released from the functional phloem strands during the early and middle stages of fruit development, whereas the two symplasmic tracers were confined to the phloem strands during the late stage. This reveals a shift of phloem unloading from symplasmic to apoplasmic pathway during fruit development. The turning point of the phloem unloading pathways was further shown to be at or just before onset of ripening, an important developmental checkpoint of grape berry. In addition, the levels of both the expression and activities of cell wall acid invertase increased around the onset of ripening and reached a high level in the late stage, providing further evidence for an operation of the apoplasmic unloading pathway after onset of ripening. These data demonstrate clearly the occurrence of an adaptive shift of phloem unloading pathway to developmental transition from growing phase to ripening in grape berry.

1 This work was supported by the grants from China National Natural Science Foundation (grant nos. 30421002, 30330420, and 30471193 to D.-P.Z.), the National Key Basic Research Program of China (grant no. 2003CB114302 to D.-P.Z.), and a "948" Research Program from the China Ministry of Agriculture (to D.-P.Z).

2 These authors contributed equally to the paper.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instruction for Authors (www.plantphysiol.org) is: Da-Peng Zhang (zhangdp{at}sohu.net).

www.plantphysiol.org/cgi/doi/10.1104/pp.106.081430

* Corresponding author; e-mail zhangdp{at}sohu.net; fax 86–10–62731899.

Received April 3, 2006; accepted July 15, 2006.




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