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.
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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
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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)