Abstract
Patterning of epidermal cells is subject to genetic regulation but also influenced by environmental stimuli. To adapt to unfavorable environmental conditions plants have developed various mechanisms to increase the plasma membrane's surface area of epidermal root cells, for example through the formation of root hairs and differentiation of rhizodermal transfer cells. Mechanisms controlling cell fate speciation in the rhizodermis were investigated by application of hormones and hormone antagonists. In addition, the effect of Fe deficiency on root epidermal patterning and Fe(III)-reduction activity was examined. In the iron-hyperaccumulating pea mutants dgl and brz and in the Arabidopsis mutant man1 Fe(III)-reduction activity was found to be up-regulated under both high and low iron supply. In contrast, morphological responses such as the development of transfer cells and extranumerary root hairs was repressed by a high iron concentration in the external medium. All morphological responses can be mimicked by exogenous application of the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) or the auxin analog 2,4-dichlorophenoxyacetic acid (2,4-D). Conversely, Fe(III)-reduction rates were not influenced or only slightly affected by the hormone treatment. Application of inhibitors of ethylene synthesis, ethylene action or auxin transport was effective only in inhibiting the formation of extra root hairs, indicating that these hormones are not required for transfer cell formation or expression of Fe(III) reduction. These data suggest that the Fe reductase induced by iron stress does not depend on the formation of transfer cells and further imply separate regulatory pathways for the two responses. The data are compatible with a model in which root reduction activity is modulated by a shoot-borne signal coordinating iron uptake with the shoot demand, while the epidermal phenotype is primarily dependent on the intracellular iron concentration of root cells.
Similar content being viewed by others
References
Aisen P, Wessling-Resnick M and Leibold E A 1999 Iron metabolism. Curr. Opin. Chem. Biol. 3, 2000-2006.
Cohen C K, Fox T C, Garvin D F and Kochian L V 1998 The role of iron-deficiency stress responses in stimulating heavy-metal transport in plants. Plant Physiol. 116, 1063-1072.
Curie C, Alonso J M, Le Jean M, Ecker J R, Briat J F 2000 Involvement of NRAMP1 from Arabidopsis in iron transport. Biochem. J. 347, 749-755.
Delhaize E 1996 A metal-accumulator mutant of Arabidopsis thaliana. Plant Physiol. 111, 849-855.
Dell'Orto M, Santi S, De Nisi, Cesco S, Varanini Z, Zocchi G and Pinton R 2000 Development of Fe-deficiency responses in cucumber (Cucumis sativus L.) roots: involvement of plasma membrane H+-ATPase activity. J. Exp. Bot. 51, 695-701.
Eide D, Broderius M, Feit J and Guerinot M L 1996 A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc. Natl. Acad. Sci. USA 93, 5624-5628.
Eisenstein R S and Blemings K P 1998 Iron regulatory proteins, iron responsive elements and iron homeostasis. J. Nutr. 128, 2295-2298.
Estelle M A and Somerville C 1987 Auxin-resistant mutants of Arabidopsis thaliana with an altered morphology. Mol. Gen. Genet. 206, 200-206.
Fox T C and Guerinot M L 1998 Molecular biology of cation transport in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 669-696.
Galway M E, Masucci J D, Lloyd A M, Walbot V, Davis R W and Schiefelbein J W 1994 The TTG gene is required to specify epidermal cell fate and cell patterning in the Arabidopsis root. Dev. Biol. 166, 740-754.
Guerinot M L 2000 The ZIP family of metal transporters. Biochim. Biophys. Acta 1465, 190-198.
Grusak M A and Pezeshgi S 1996 Shoot-to-root signal transmission regulates root Fe(III) reductase activity in the dgl mutant of pea. Plant Physiol. 110, 329-334.
Landsberg E C 1982 Transfer cell formation in the root epidermis: a prerequisite for Fe-efficiency? J. Plant Nutr. 5, 415-432.
Landsberg E C 1996 Hormonal regulation of ron-stress response in sunflower roots: a morphological and cytological investigation. Protoplasma 194, 69-80.
Masucci J D and Schiefelbein J W 1996 Hormones act downstream of TTG and GL2 to promote root hair outgrowth during epidermis development in the Arabidopsis root. Plant Cell 8, 1505-1517.
Masucci J D, Rerie W G, Foreman D R, Zhang M, Galway M E, Marks D M and Schiefelbein J W 1996 The homeobox gene GLABRA2 is required for position dependent cell differentiation in the root epidermis of Arabidopsis thaliana. Development 122, 1253-1260.
Moog P R, van der Kooij T A W, Brüggemann W, Schiefelbein J W and Kuiper P J C 1995 Responses to iron deficiency in Arabidopsis thaliana: the turbo iron reductase does not depend on the formation of root hairs and transfer cells. Planta 195, 505-513.
Pate J S and Gunning B E S 1972 Transfer cells. Annu. Rev. Plant Physiol. 23, 173-196.
Pitts R J, Cernac A and Estelle M 1999 Auxin and ethylene promote root hair elongation in Arabidopsis. Plant J. 16, 553-560.
Robinson N J, Procter C M, Conolly E L and Guerinot M L 1999 A ferric-chelate reductase for iron uptake from soils. Nature 397, 694-697.
Romera F J and Alcántara E 1994 Iron-deficiency stress responses in cucumber (Cucumis sativus L.) roots. Plant Physiol. 105, 1133-12138.
Romera F J, Alcántara E and de la Guardia M D 1999 Ethylene production by Fe-deficient roots and its involvement in the regulation of Fe-deficiency stress responses by strategy I plants. Ann. Bot. 83, 51-55.
Römheld V and Marschner H 1986 Evidence for a specific uptake system for iron phytosiderophores in roots of grasses. Plant Physiol. 80, 175-180.
Schmidt W 1994 Effects of various inhibitors on in vivo reduction by Plantago lanceolata L. roots. Plant Soil 165, 207-212.
Schmidt W 1999 Mechanisms and regulation of reduction-based iron uptake in plants. New Phytol. 141, 1-26.
Schmidt W and Bartels M 1996 Formation of root epidermal transfer cells in Plantago. Plant Physiol. 110, 217-225.
Schmidt W, Bartels M, Tittel J and Fühner C 1997 Physiological effects of copper on iron acquisition processes in Plantago. New Phytol. 135, 659-666.
Schmidt W, Schikora A, Pich A and Bartels M 2000a Hormones induce an Fe-deficiency-like root epidermal cell pattern in the Fe-inefficient tomato mutant fer. Protoplasma 213, 67-73.
Schmidt W, Tittel J and Schikora A 2000b Role of hormones in the induction of Fe deficiency responses in Arabidopsis roots. Plant Physiol. 122, 1109-1118.
Tanimoto M, Roberts K and Dolan L 1995 Ethylene is a positive regulator of root hair development in Arabidopsis thaliana. Plant J. 8, 943-948.
Wada T, Tachibana T, Shimura Y and Okada K 1997 Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. Science 277, 1113-1116.
Waters B M, Blevins D G and Eide D J 2000 psFRO, a Pisum sativum ferric reductase involved in Fe uptake. Abstracts 10th International Symposium on Iron Nutrition and Interactions in Plants, Houston.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Schikora, A., Schmidt, W. Modulation of the root epidermal phenotype by hormones, inhibitors and iron regime. Plant and Soil 241, 87–96 (2002). https://doi.org/10.1023/A:1016089209891
Issue Date:
DOI: https://doi.org/10.1023/A:1016089209891