Functional and chemical comparison of apoplastic barriers to radial oxygen loss in roots of rice (Oryza sativa L.) grown in aerated or deoxygenated solution

Journal of Experimental Botany, May 2009

Radial oxygen loss (ROL) and root porosity of rice (Oryza sativa L.) plants grown in either aerated or deoxygenated (stagnant) conditions were combined for the first time with extensive histochemical and biochemical studies of the apoplastic barriers in the roots’ peripheral cell layers. Growth in stagnant solution significantly affected structural and, consequently, the physiological features of rice roots. It increased adventitious root porosity by about 20% and decreased the ROL towards the base to zero at a distance of 40 mm from the apex. By contrast, roots of plants grown in aerated solutions revealed the highest rates of ROL at 30 mm from the apex. Differences in the ROL pattern along the root were related to histochemical studies, which showed an early development of Casparian bands and suberin lamellae in the exodermis, and lignified sclerenchyma cells in roots of plants grown in deoxygenated solution. In agreement with anatomical studies, absolute contents of suberin and lignin in the outer part of the roots (OPR) were higher in plants grown in deoxygenated solution. Regardless of growth conditions, the levels of suberin and lignin increased along the roots towards the base. It is concluded that radial oxygen loss can be effectively restricted by the formation of a suberized exodermis and/or lignified sclerenchyma in the OPR. However, the relative contribution of suberin and lignin in the formation of a tight barrier is unclear. Knowing the permeability coefficient across OPR for roots of plants grown in both conditions will allow a more precise understanding of the mechanisms controlling ROL.

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Functional and chemical comparison of apoplastic barriers to radial oxygen loss in roots of rice (Oryza sativa L.) grown in aerated or deoxygenated solution

Lukasz Kotula 1 Kosala Ranathunge 0 Lukas Schreiber 0 Ernst Steudle 1 0 Department of Ecophysiology, Institute of Cellular and Molecular Botany, University of Bonn , Germany 1 Department of Plant Ecology, University of Bayreuth , Germany Radial oxygen loss (ROL) and root porosity of rice (Oryza sativa L.) plants grown in either aerated or deoxygenated (stagnant) conditions were combined for the first time with extensive histochemical and biochemical studies of the apoplastic barriers in the roots' peripheral cell layers. Growth in stagnant solution significantly affected structural and, consequently, the physiological features of rice roots. It increased adventitious root porosity by about 20% and decreased the ROL towards the base to zero at a distance of 40 mm from the apex. By contrast, roots of plants grown in aerated solutions revealed the highest rates of ROL at 30 mm from the apex. Differences in the ROL pattern along the root were related to histochemical studies, which showed an early development of Casparian bands and suberin lamellae in the exodermis, and lignified sclerenchyma cells in roots of plants grown in deoxygenated solution. In agreement with anatomical studies, absolute contents of suberin and lignin in the outer part of the roots (OPR) were higher in plants grown in deoxygenated solution. Regardless of growth conditions, the levels of suberin and lignin increased along the roots towards the base. It is concluded that radial oxygen loss can be effectively restricted by the formation of a suberized exodermis and/or lignified sclerenchyma in the OPR. However, the relative contribution of suberin and lignin in the formation of a tight barrier is unclear. Knowing the permeability coefficient across OPR for roots of plants grown in both conditions will allow a more precise understanding of the mechanisms controlling ROL. - Rice (Oryza sativa L.) is often cultivated in flood-prone environments, which are usually anaerobic and chemically reduced, because of the slow diffusion of oxygen in water and the rapid consumption of oxygen by soil microorganisms (Ponnamperuma, 1984; Laanbroek, 1990). To overcome these threats, rice, as other aquatic plants, is adapted both metabolically and structurally in numerous ways. The main adaptations include (i) internal aeration by the formation of aerenchyma along the entire plant, connecting the aerial parts with submerged organs, and (ii) the induction of strong barriers in the root peripheral layers external to aerenchyma to impede radial oxygen loss (ROL; Armstrong, 1979; Colmer, 2003b). Usually, the barrier to ROL in roots is related to suberization and/or lignification of the walls of root peripheral layers (Armstrong et al., 2000; De Simone et al., 2003; Soukup et al., 2006). In rice, the well-developed outer part of the root (OPR) consists of four cell layers: rhizodermis, exodermis, sclerenchyma cells, and one layer of cortical cells (Ranathunge et al., 2003). It is known that the suberized exodermis and/or lignified sclerenchyma cells act as a barrier to impede ROL (Kotula and Steudle, 2008). There are two consecutive developmental stages of the exodermis: (i) the formation of Casparian bands in radial and transverse walls impregnating primary cell wall pores with liphophilic and aromatic substances and (ii) the * To whom correspondence should be addressed. E-mail: The Author [2009]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved. For Permissions, please e-mail: deposition of suberin lamellae to the inner surface of anticlinal and tangential cell walls (Clark and Harris, 1981; Peterson, 1989; Ranathunge et al., 2004). Modifications of apoplastic barriers, investigated by using histochemical staining techniques, allowed the description of developmental stages of roots in terms of structural changes in cell walls. An insight into the chemical composition of modified cell walls can be obtained only by directly analysing the compounds occurring in such walls (Schreiber et al., 1999; De Simone et al., 2003). There is an enzymatic method for the isolation of modified root cell walls and for analysing them after chemical modification using gas chromatography and mass spectrometry (Schreiber et al., 1994, 1999). Suberin is a heterogeneous extracellular biopolymer closely attached to the inner primary cell walls (Schreiber et al., 1999; Bernards, 2002). It consists of aliphatic monomers (x-hydroxy acids, diacids, primary fatty acids, primary alcohols, and 2-hydroxy acids) esterified with aromatic compounds like ferulic acid and coumaric acid, and of cell wall carbohydrates (Zeier and Schreiber, 1997; Kolattukudy, 2001). Lignin is a biopolymer bearing the three aromatic residues p-hydroxyphenyl, guaiacyl, and syringyl (Freudenberg, 1965; Boudet, 1998; De Simone et al., 2003). It has been suggested that suberin and lignin biopolymers are involved in pathogen defence, by a breakdown of the (...truncated)


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Lukasz Kotula, Kosala Ranathunge, Lukas Schreiber, Ernst Steudle. Functional and chemical comparison of apoplastic barriers to radial oxygen loss in roots of rice (Oryza sativa L.) grown in aerated or deoxygenated solution, Journal of Experimental Botany, 2009, pp. 2155-2167, 60/7, DOI: 10.1093/jxb/erp089