Abstract
Root hair formation is induced by low pH in lettuce (Lactuca sativa L. cv. Grand Rapids) seedlings cultured in mineral medium. The role of mineral concentrations in this phenomenon was investigated, especially for manganese. When lettuce seedlings were cultured in media that were deficient in calcium (Ca), manganese (Mn), boron (B) or molybdenum (Mo), morphological changes were induced in roots. Deficiency of other nutrients had little effect on root hair formation. Ca or B deficiency inhibited the growth of the main root and the formation of root hairs, regardless of pH. Mn or Mo deficiency increased root hair formation at pH 6 and suppressed main root growth slightly. In contrast, increasing the Mn concentration suppressed low-pH-induced root hair formation. The Mn content of roots grown at pH 4 was only about 15% of that at pH 6. In contrast, the Mo content of roots grown at low pH was about six times that of roots grown at neutral pH. These results suggest that root hair formation induced by low pH is at least partly mediated by decreased Mn uptake in root cells.
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References
Alonso JM, Hirayama T, Roman G, Nourizadeh S, Ecker JR (1999) EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284:2148–2152
Bates TR, Lynch JP (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ 19:529–538
Cheniae GM, Martin IF (1968) Site of manganese function in photosynthesis. Biochim Biophys Acta 153:819–837
De Simone S, Oka Y, Inoue Y (2000) Photoperceptive site of the photoinduction of root hairs in lettuce (Lactuca sativa L. cv. Grand rapids) seedlings under low pH conditions. J Plant Res 113:55–62
Fleischer A, Titel C, Ehwald R (1998) The boron requirement and cell wall properties of growing- and stationary-phase suspension-cultured Chenopodium album L. cells. Plant Physiol 117:1401–1410
Gamble RL, Coonfield ML, Schaller AG (1998) Histidine kinase activity of the ETR1 ethylene receptor from Arabidopsis. Proc Natl Acad Sci USA 95:7825–7829
Glüsenkamp K-H, Kosegarten H, Mengal K, Grolig F, Esch A, Goldbach HE (1997) A fluorescein boronic acid conjugate as a marker for borate binding sites in the apoplast of growing roots of Zea mays L. and Helianthus annuus L. In: Bell RW, Rerkasen B (eds) Boron in soils and plants. Kluwer, Dordrecht, pp 229–235
Hamilton CA, Good AG, Taylor GJ (2001) Induction of vacuolar ATPase and mitochondrial ATP synthase by aluminum in an aluminum-resistant cultivar of wheat. Plant Physiol 125:2068–2077
Hofer R-M (1996) Root hairs. In: Y Waisel, A Eshel, U Kafkafi (eds) Plant roots. The hidden half. Dekker, New York, pp 111–126
Inoue Y, Yamaoka K, Kimura K, Sawai K (1995) Image processing-aided simple analysis method for root hair formation in plants. Bioimages 3:31–36
Inoue Y, Yamaoka K, Kimura K, Sawai K, Arai T (2000) Effects of low pH on the induction of root hair formation in young lettuce (Lactuca sativa L. cv. Grand Rapids) seedlings. J Plant Res 113:39–44
Kawaguchi M, Imaizumi-Anraku H, Koiwa H, Niwa S, Ikuta A, Shono K, Akao S (2002) Root, root hair, and symbiotic mutants of the model legume Lotus japonicus. Mol Plant Microbe Interact 15:17–26
Kidd PS, Llugany M, Poschenrieder C, Gunse B, Barcelo J (2001) The role of root exudates in aluminium resistance and silicon-induced amelioration of aluminium toxicity in three varieties of maize (Zea mays L.). J Exp Bot 52(359):1339–1352
Kobayashi M, Matoh T and Azuma J (1996) Two chains of rhamnogalacturonan II are cross-linked by borate-diol ester bonds in higher plant cell walls. Plant Physiol 110:1017–1020
Kobayashi M, Nakagawa H, Asaka T, Matoh T (1999) Borate-rhamnogalacturonan II bonding reinforced by Ca2+ retains pectic polysaccharides in higher-plant cell walls. Plant Physiol 119:199–203
Kollmeier M, Dietrich P, Bauer CS, Horst WJ, Hedrich R (2001) Aluminum activates a citrate-permeable anion channel in the aluminum-sensitive zone of the maize root apex. A comparison between an aluminum-sensitive and an aluminum-resistant cultivar. Plant Physiol 126:397–410
Koyama H, Toda T, Hara T (2001) Brief exposure to low-pH stress causes irreversible damage to the growing root in Arabidopsis thaliana: pectin-Ca interaction may play an important role in proton rhizotoxicity. J Exp Bot 52:361–368
Landsberg EC (1996) Hormonal regulation of iron-stress response in sunflower roots: a morphological and cytological investigation. Protoplasma 194:69–80
Ma Z, Bielenberg DG, Brown KM, Lynch JP (2001) Regulation of root hair density by phosphorus availability in Arabidopsis thaliana. Plant Cell Environ 24:459–467
Mendel RR, Schwarz G (1999) Molybdoenzymes and molybdenum cofactor in plants. Crit Rev Plant Sci 18: 33–69
Moog PR, Kooij TAW, Brüggemann W, Schiefelbein JW, Kuiper PJ (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
Ohki K (1976) Manganese deficiency and toxicity levels for 'Bragg' soybeans. Agron J 68:861–864
Ohki K (1985) Manganese deficiency and toxicity effects on photosynthesis, chlorophyll, and transpiration in wheat. Crop Sci 25:187–191
O'Neill MA, Warrenfeltz D, Kates K, Pellerin P, Doco T, Darvill AG, Albersheim P (1996) Rhamnogalacturonan-II, a pectic polysaccharide in the walls of growing plants, forms a dimer that is covalently cross-linked by a borate ester. In vitro conditions for the formation and hydrolysis of the dimer. J Biol Chem 271:22923–22930
Pitts RJ, Cernac A, Estelle M (1998) Auxin and ethylene promote root hair elongation in Arabidopsis. Plant J 16:553–560
Reid ID, Paice MG (1998) Effects of manganese peroxidase on residual lignin of softwood Kraft pulp. Appl Environ Microbiol 64:2273–2274
Ringbom A (1963) Complexation in analytical chemistry. A guide for the critical selection of analytical methods based on complexation reactions. Wiley, New York
Sarker AN, Wyn Jones RG (1982) Effect of rhizosphere pH on the availability and uptake of Fe, Mn and Zn. Plant Soil 66:361–372
Schmidt W, Schikora A (2001) Different pathways are involved in phosphate and iron stress-induced alterations of root epidermal cell development. Plant Physiol 125:2078–2084
Schmidt W, Tittel J, Schikora A (2000) Role of hormones in the induction of iron deficiency responses in Arabidopsis roots. Plant Physiol 122:1109–1118
Shuman LM (1994) Mineral nutrition. In: Wilkinson RE (ed) Plant-environment interactions. Dekker, New York, pp 149–182
Tanimoto M, Roberts K, Dolan L (1995) Ethylene is a positive regulator of root hair development in Arabidopsis thaliana. Plant J 8:943–948
Whittaker JW (2000) Manganese superoxide dismutase. Met Ions Biol Syst 37:587–611
Wilkinson RE (1994) Acid soil stress and plant growth. In: Wilkinson RE (ed) Plant-environment interactions. Dekker, New York, pp 125–148
Wymer CL, Bibikova TN, Gilroy S (1997) Cytoplasmic free calcium distributions during the development of root hairs of Arabidopsis thaliana. Plant J 12:427–439
Acknowledgements
We thank Professor Kunihiro Watanabe, Tokyo University of Science, and Professor Yuko Hasegawa, Tokyo University of Science, for valuable suggestions and discussions on investigating the uptake of nutrients by lettuce seedlings.
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Konno, M., Ooishi, M. & Inoue, Y. Role of manganese in low-pH-induced root hair formation in Lactuca sativa cv. Grand Rapids seedlings. J Plant Res 116, 301–307 (2003). https://doi.org/10.1007/s10265-003-0100-z
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DOI: https://doi.org/10.1007/s10265-003-0100-z