Summary
Cell-to-cell transport of small molecules and ions occurs in plants through plasmodesmata. Plant roots are frequently subjected to localized anaerobic stress, with a resultant decrease in ATP. In order to determine the effect of this stress on plasmodesmal transport, fluorescent dyes of increasing molecular weight (0.46 to 10 kDa) were injected into epidermal and cortical cells of 3-day-old wheat roots, and their movement into neighboring cells was determined by fluorescence microscopy. Anaerobiosis was generated by N2 gas or simulated by the presence of sodium azide, both of which reduced the ATP levels in the tissue by over 80%. In the absence of such stress, the upper limit for movement, or size exclusion limit (SEL), of cortical plasmodesmata was <1 kDa. The ATP analogue TNP-ADP (mw 681) moved across the plasmodesmata of unstressed roots, indicating that plasmodesmata may be conduits for nucleotide (ATP and ADP) exchange between cells. Upon imposition of stress, the SEL rose to between 5 and 10 kDa. This response of plasmodesmata to a decrease in the level of ATP suggests that they are constricted by an ATP-dependent process so as to maintain a restricted SEL. When roots are subjected to anaerobic stress, an increase in SEL may permit enhanced delivery of sugars to the affected cells of the root where anaerobic respiration could regenerate the needed ATP.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- F-dextran:
-
fluorescein-coupled dextran
- LYCH:
-
Lucifer Yellow CH
- SEL:
-
size exclusion limit
- TNP-ADP:
-
2′-O-(trinitrophenyl)adenosine-5″-diphosphate
References
Baron-Epel O, Hernandez D, Jiang L-W, Meiners S, Schindler M (1988) Dynamic continuity of cytoplasmic and membrane compartments between plant cells. J Cell Biol 106: 715–721
Citovsky V, McLean BG, Zupan JR, Zambryski P (1993) Phosphorylation of tobacco mosaic virus cell-to-cell movement protein by a developmentally regulated plant cell wall-associated protein kinase. Genes Dev 7: 904–910
Derrick PM, Barker H, Oparka KJ (1992) Increase in plasmodesmatal permeability during cell-to-spread of tobacco rattle virus from individually inoculated cells. Plant Cell 4: 1405–1412
Ding B, Haudenshield JS, Hull RJ, Wolf S, Beachy RN, Lucas WJ (1992) Secondary plasmodesmata are specific sites of localization of the tobacco virus movement protein in transgenic tobacco plants. Plant Cell 4: 915–928
— —, Willmitzer L, Lucas WJ (1993) Correlation between arrested secondary plasmodesmal development and onset of accelerated senescence in yeast acid invertase transgenic tobacco. Plant J 4: 179–189
Drake G (1979) Electrical coupling, potentials, and resistances in oat coleoptiles: effects of azide and cyanide. J Exp Bot 30: 719–725
Erwee MG, Goodwin PB (1983) Characterization of theEgeria densa symplast. Inhibition of the intercellular movement of fluorescent probes by group II ions. Planta 158: 320–328
— — (1985) Symplastic domains in extrastelar tissues ofEgeria densa Planch. Planta 163: 9–19
Eschrich W, Heyser W (1975) Biochemistry of phloem constituents. In: Zimmermann MH, Milburn JA (eds) Transport in plants, I. phloem transport. Springer, Berlin Heidelberg New York, pp 1101–1136 [Pirson A, Zimmermann MH (eds) Encyclopedia of plant physiology, NS, vol 1]
Giaquinta RT, Lin W, Sadler NL, Franceschi VR (1983) Pathway of phloem unloading of sucrose in corn roots. Plant Physiol 72: 362–367
Grubmayer C, Penefsky HS (1981) The presence of two hydrolytic sites on beef heart mitochondrial adenosine triphosphatase. J Bil Chem 256: 3718–3727
Lüttge U, Higinbotham N (1979) Transport in plants. Springer, Berlin Heidelberg New York
Meiners S, Xu A, Schindler M (1991) Gap junction protein homologue fromArabidopsis thaliana: evidence for connexin in plants. Proc Natl Acad Sci USA 88: 4119–4122
Mushegian AR, Koonin EV (1993) The proposed plant connexin is a protein kinase-like protein. Plant Cell 5: 998–999
Robards AW, Lucas WJ (1990) Plasmodesmata. Annu Rev Plant Physiol Plant Mol Biol 41: 369–419
Tucker EB (1993) Azide treatment enhances cell-to-cell diffusion in staminal hairs ofSetcreasea purpurea. Protoplasma 174: 45–49
White RG, Badelt K, Overall RL, Vesk M (1992) Actin associated with plasmodesmata. In: Abstracts 2nd International Workshop on Basic and Applied Research in Plasmodesmatal Biology, pp 12–14
Wiedenroth E-M (1993) Responses of roots to hypoxia: their structural and energy relations with the whole plant. Environ Exp Bot 33: 41–51
Wilson C, Oross JW, Lucas WJ (1985) Sugar uptake intoAllium cepa leaf tissue: an integrated approach. Planta 164: 227–240
Wolf S, Deom CM, Beachy RN, Lucas WJ (1989) Movement protein of tobacco mosaic virus modifies plasmodesmatal size exclusion limit. Science 246: 377–379
— — — — (1991) Plasmodesmatal function is probed using transgenic tobacco plants that express a virus movement protein. Plant Cell 3: 593–604
Yahalom A, Warmbrodt RD, Laird DW, Traub O, Revel J-P, Willecke K, Epel BL (1991) Maize mesocotyl plasmodesmata proteins cross-react with connexin gap junction protein antibodies. Plant Cell 3: 407–417
Zhang WH, Tyerman SD (1991) Effect of low O2 concentration and azide on hydraulic conductivity and osmotic volume of the cortical cells of wheat roots. Aust J Plant Physiol 18: 603–613
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Cleland, R.E., Fujiwara, T. & Lucas, W.J. Plasmodesmal-mediated cell-to-cell transport in wheat roots is modulated by anaerobic stress. Protoplasma 178, 81–85 (1994). https://doi.org/10.1007/BF01404123
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01404123