Salinity-induced changes in the nutritional status of expanding cells may impact leaf growth inhibition in maize
Beatriz G. Neves-Piestun A and Nirit Bernstein A BA Institute of Soil, Water and Environmental Sciences, Agricultural Research Organization, The Volcani Center, PO Box 6, Bet-Dagan 50-250, Israel.
B Corresponding author. Email: nirit@agri.gov.il
Functional Plant Biology 32(2) 141-152 https://doi.org/10.1071/FP04113
Submitted: 29 June 2004 Accepted: 28 October 2004 Published: 24 February 2005
Abstract
Salinity-induced excess or deficiency of specific nutrients are often hypothesised to operate as causes of growth inhibition and to trigger primary responses, which directly affect growth. Information concerning salinity effects on microelement nutrition in the growing cells is limited. In this study, salinity-(80 mm NaCl) inflicted alterations in spatial profiles of essential elements (N, P, K, S, Ca, Mg, Fe, Zn, Mn, Cu) and the salinity source (Na and Cl) were studied along the growing zone of leaf 4 of maize (Zea mays L.). Correlations between spatial profiles of growth and nutritional status of the tissue were tested for evaluation of the hypothesis that a disturbance of specific mineral nutritional factors in the growing cells might serve as causes of salt-induced growth inhibition. Examined nutritional elements exhibited unique distribution patterns, all of which were disturbed by salinity. With the exception of Na, Cl and Fe, the deposition rates of all the studied mineral elements were reduced by salinity throughout the elongating tissue. Localised contents of Ca, K and Fe in the growing tissue of the salt-stressed leaf were highly correlated with the intensity of localised tissue volumetric expansion, suggesting reduced levels of Ca and K, and toxic levels of Fe as possible causes of growth inhibition. Na and Cl accumulation were not correlated with growth inhibition under salinity.
Keywords: growing zone, leaves, macroelements, microelements, salinity, Zea mays.
Acknowledgments
Special thanks to Professor U. Kafkafi for advice concerning N determinations and interpretation of the results. We thank Dr Marcus and Mrs M Zarchi for statistical guidance. The seeds used in this project were a gift from Galilee-seeds, Israel. The project was supported by BARD fund, project number 2360–93.
Abd-El Baki GK,
Siefritz F,
Man H-M,
Weiner H,
Kaldenhoff R, Kaiser WM
(2000) Nitrate reductase in Zea mays L. under salinity. Plant, Cell and Environment 23, 515–521.
| Crossref | GoogleScholarGoogle Scholar |
Bernstein N,
Läuchli A, Silk WK
(1993a) Kinematics and dynamics of sorghum (Sorghum bicolor L.) leaf development at various Na/Ca salinities. I. Elongation growth. Plant Physiology 103, 1107–1114.
| PubMed |
Bernstein N,
Silk WK, Läuchli A
(1993b) Growth and development of sorghum leaves under conditions of NaCl stress: spatial and temporal aspects of leaf growth inhibition. Planta 191, 433–439.
| Crossref | GoogleScholarGoogle Scholar |
Bernstein N,
Silk WK, Läuchli A
(1995) Growth and development of sorghum leaves under conditions of NaCl stress: possible role of some mineral elements in growth inhibition. Planta 196, 699–705.
| Crossref | GoogleScholarGoogle Scholar |
Bressan RA,
Hasegawa PM, Pardo JM
(1998) Plants use calcium to resolve salt stress. Trends in Plant Science 3, 411–412.
| Crossref | GoogleScholarGoogle Scholar |
Cheeseman JM
(1988) Mechanisms of salinity tolerance in plants. Plant Physiology 87, 547–550.
Cramer GR
(1992) Kinetics of maize leaf elongation. II. Responses of a Na-excluding cultivar and a Na-including cultivar to varying Na / Ca salinities. Journal of Experimental Botany 43, 857–864.
Epstein, E (1972). ‘Mineral nutrition of plants: principles and perspectives.’ (John Wiley and Sons: New York)
Fricke W, Flowers TJ
(1998) Control of leaf cell elongation in barley. Generation rates of osmotic pressure and turgor, and growth-associated water potential gradients. Planta 206, 53–65.
| Crossref | GoogleScholarGoogle Scholar |
Grattan SR, Grieve CM
(1998) Salinity-mineral nutrient relations in horticultural crops. Scientia Horticulturae 78, 127–157.
| Crossref | GoogleScholarGoogle Scholar |
Green PB
(1976) Growth and cell pattern formation on an axis: critique of concepts, terminology, and modes of study. Botanical Gazette 137, 187–202.
| Crossref | GoogleScholarGoogle Scholar |
Haussling N,
Römheld V, Marschner H
(1985) Bezeiehungen zwischen Cholorosegrad, Eisengehalten und Blattwachstun von Weinreben auf verschiedenen Standorten. Vitis 24, 158–168.
Hu Y, Schmidhalter U
(1998) Spatial distribution and net deposition rates of mineral elements in the elongating wheat (Triticum aestivum L.) leaf under saline soil conditions. Planta 204, 212–219.
| Crossref | GoogleScholarGoogle Scholar |
Hu Y,
von Tucher S, Schmidhalter U
(2000) Spatial distribution and net deposition rates of Fe, Mn and Zn in the elongating leaves of wheat under saline soil conditions. Australian Journal of Plant Physiology 24, 53–59.
Jeschke WD, Wolf O
(1985) Na dependent net K retranslocation in leaves of Hordeum vulgare, cv California Mariout and Hordeum distichon cv. Villa under salt stress. Journal of Plant Physiology 121, 211–223.
Kafkafi U, Ganmore-Neumann R
(1997) Ammonium in plant tissue: real or artifact? Journal of Plant Nutrition 20, 107–118.
Lazof, DB ,
and
Bernstein, N (1999a). The NaCl-induced inhibition of shoot growth: The case for disturbed nutrition with special consideration of Calcium nutrition. In ‘Advances in botanical research incorporating advances in plant pathology’. a. pp. 113–189. (Academic Press: London)
Lazof DB, Bernstein N
(1999b) Effects of salinization on nutrient transport to lettuce leaves: consideration of leaf developmental stage. New Phytologist 144, 85–94.
| Crossref | GoogleScholarGoogle Scholar |
Lazof DB, Läuchli A
(1991) The nutritional status of the apical meristem of Lactuca sativa as affected by NaCl salinization: an electron probe microanalytic study. Planta 184, 334–342.
Lynch J,
Thiel G, Läuchli A
(1988) Effect of salinity on the extensibility and Ca availability in the expanding region of growing barley leaves. Botanica Acta 101, 355–361.
MacAdam JW, Nelson CJ
(2002) Secondary cell wall deposition causes radial growth of fibre cells in the maturation zone of elongating tall fescue leaf blades. Annals of Botany 89, 89–96.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Marschner, H (1995). ‘Mineral nutrition of higher plants.’ (2nd edn) (Academic Press: London)
Maurice I,
Gastal F, Durand J-L
(1997) Generation of form and associated mass deposition during leaf development in grasses: a kinematic approach for non-steady growth. Annals of Botany 80, 673–683.
| Crossref | GoogleScholarGoogle Scholar |
Munns R
(1985) Na, K, and Cl, in xylem sap flowing to shoots of NaCl-treated barley. Journal of Experimental Botany 36, 1032–1042.
Munns R
(1993) Physiological processes limiting plant growth in saline soils: some dogmas and hypotheses. Plant, Cell and Environment 16, 15–24.
Munns R,
Passioura JB,
Guo J,
Chazen O, Cramer GR
(2000) Water relations and leaf expansion: importance of time scale. Journal of Experimental Botany 51, 1495–1504.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Munns R
(2002) Comparative physiology of salt and water stress. Plant, Cell and Environment 25, 239–250.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Neves-Piestun BG, Bernstein N
(2001) Salinity-induced inhibition of leaf elongation in maize is not mediated by changes in cell wall acidification capacity. Plant Physiology 125, 1419–1428.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Peters WS, Bernstein N
(1997) The determination of relative elemental growth rate profiles from segmental growth rates: a methodological evaluation. Plant Physiology 113, 1395–1404.
| PubMed |
Roberts JKM,
Linker CS,
Benoit AG,
Jardetzky O, Nieman RH
(1984) Salt stimulation of phosphate uptake root tips studied by 31P nuclear magnetic resonance. Plant Physiology 75, 947–950.
Rus A,
Yokoi S,
Sharkhuu A,
Reddy M,
Lee BH,
Matsumoto TK,
Koiwa H,
Zhu JK,
Bressan RH, Hasegawa PM
(2001) AtHKT1 is a salt tolerance determinant that controls Na+ entry into plant roots. Proceedings of the National Academy of Sciences USA 98, 14150–14155.
| Crossref | GoogleScholarGoogle Scholar |
Schnyder H, Nelson CJ
(1988) Diurnal growth of tall fescue leaf blades I. Spatial distribution of growth, deposition of water and assimilate import in the elongation zone. Plant Physiology 86, 1070–1076.
Shabala S,
Shabala L, Van Volkenburgh E
(2003) Effect of Ca on root development and root ion fluxes in salinised barley seedlings. Functional Plant Biology 30, 507–514.
| Crossref | GoogleScholarGoogle Scholar |
Silk WK,
Walker RC, Labavitch J
(1984) Uridine deposition rates in the primary root of Zea mays.
Plant Physiology 74, 721–726.
Silk WK,
Hsiao TC,
Diedenhofen U, Matson C
(1986) Spatial distribution of potassium, solutes, and their deposition rates in the growth zone of the primary corn root. Plant Physiology 82, 853–858.
Smith VR
(1980) A phenol-hypochlorite manual determination of ammonium-nitrogen in Kjeldahl digests of plant tissue. Communications in Soil Science and Plant Analysis 11, 709–722.
Smith GS,
Cornforth IS, Henderson HV
(1984) Iron requirements of C3 and C4 plants. New Phytologist 97, 543–556.
Su H,
Golldack D,
Zhao C, Bohnert HJ
(2002) The expression of HAK-type K(+) transporters is regulated in response to salinity stress in common ice plant. Plant Physiology 129, 1482–1493.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tang AC, Boyer JS
(2002) Growth-induced water potentials and the growth of maize leaves. Journal of Experimental Botany 53, 489–503.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Walter A,
Silk WK, Schurr U
(2000) Effect of soil pH on growth and cation deposition in the root tip of Zea mays L. Journal of Plant Growth Regulation 19, 65–76.
| PubMed |
Walter A,
Feil R, Schurr U
(2003) Expansion dynamics, metabolite composition and substance transfer of the primary root growth zone of Zea mays L. grown in different external nutrient availabilities. Plant, Cell and Environment 26, 1451–1466.
| Crossref | GoogleScholarGoogle Scholar |
Yamuchi M
(1989) Rice bronzing in Nigeria caused by nutrient imbalances and its control by potassium sulfate application. Plant and Soil 117, 275–286.
Zhu JK
(2001) Plant salt tolerance. Trends in Plant Science 6, 66–71.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zhu JK
(2003) Regulation of ion homeostasis under salt stress. Current Opinion in Plant Biology 6, 441–445.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
