Apoplasmic Barriers and Oxygen Transport Properties of Hypodermal Cell Walls in Roots from Four Amazonian Tree Species

Abstract

The formation of suberized and lignified barriers in the exodermis is suggested to be part of a suite of adaptations to flooded or waterlogged conditions, adjusting transport of solutes and gases in and out of roots. In this study, the composition of apoplasmic barriers in hypodermal cell walls and oxygen profiles in roots and the surrounding medium of four Amazon tree species that are subjected to long-term flooding at their habitat was analyzed. In hypodermal cell walls of the deciduous tree Crateva benthami, suberization is very weak and dominated by monoacids, 2-hydroxy acids, and -hydroxycarboxylic acids. This species does not show any morphological adaptations to flooding and overcomes the aquatic period in a dormant state. Hypodermal cells of Tabernaemontana juruana, a tree which is able to maintain its leaf system during the aquatic phase, are characterized by extensively suberized walls, incrusted mainly by the unsaturated C 18 -hydroxycarboxylic acid and the ␣,-dicarboxylic acid analogon, known as typical suberin markers. Two other evergreen species, Laetia corymbulosa and Salix martiana, contained 3-to 4-fold less aliphatic suberin in the exodermis, but more than 85% of the aromatic moiety of suberin are composed of para-hydroxybenzoic acid, suggesting a function of suberin in pathogen defense. No major differences in the lignin content among the species were observed. Determination of oxygen distribution in the roots and rhizosphere of the four species revealed that radial loss of oxygen can be effectively restricted by the formation of suberized barriers but not by lignification of exodermal cell walls.Suberin is a heterogeneous extracellular biopolymer closely attached to the inner primary cell wall (Schreiber et al., 1999). On the basis of chemical analysis of enzymatically isolated cell walls, the composition of suberin in the exodermis was shown to consist of long-chain aliphatic monomers esterified with aromatic compounds like ferulic and coumaric acids and cell wall carbohydrates (Zeier and Schreiber, 1997; Kolattukudy, 2001). Recently, glycerol has been identified as a new important structural element in the suberin macromolecule, which is supposed to cross-link the aliphatic and aromatic suberin domains (Moire et al., 1999; Pereira, 2000a, 2000b). The aliphatic monomers of suberin are synthesized via the fatty acid biosynthetic pathway, catalyzed by fatty acid elongases in the root cells (Domeregue et al., 1998;Schreiber et al., 2000). Hydroxylation is mediated by cytochrome P450-dependent enzymes, converting -hydroxyacids to either 1,-dicarboxylic acids or alcohols (Agrawal and Kolattukudy, 1978;Le Bouquin et al., 2001). The assembly of the aromatic moiety of suberin, in most cases cinnamic acid derivatives, proceeds via the general phenylpropanoid pathway with Phe ammonia-lyase as the central enzyme (Kolattukudy, 2001). Similar to suberin, lignin is a highly variable biopolymer synthesized in a complex pathway. The basic lignin molecule is derived from the oxidative polymerization of the ...

Waterlogging tolerance and capacity for oxygen transport in Brachypodium distachyon (Bd21)

“…Plants have three major strategies for acclimating to waterlogged conditions (Shiono et al 2008, Colmer andVoesenek 2009): developing newly formed adventitious roots, forming aerenchyma and forming a barrier to ROL by accumulating suberin and/or lignin in the outer part of roots (De Simone et al 2003, Garthwaite et al 2008, Soukup et al 2007, Kotula et al 2009a, Kotula et al 2009b, Ranathunge et al 2011, Watanabe et al 2013. In B. distachyon, newly formed adventitious roots were not increased.…”

“…The barrier might also impede entry of phytotoxins from chemically-reduced waterlogged soils (Armstrong 1979). In Amazonian tree species (De Simone et al 2003), Glyceria maxima and Phragmites australis (Soukup et al 2007), the barrier to ROL has been linked to suberin deposits in the exodermis/hypodermis. In Oryza sativa (rice) and Hordeum marinum, suberin and/or lignin in the outer part of roots are thought to contribute to the barrier (Garthwaite et al 2008, Kotula et al 2009a, Kotula et al 2009b, Ranathunge et al 2011 can be detected ).…”

Anatomical and morphological modifications in response to flooding by six Cerrado tree species

“…Non spaces can form channels that are connected throughout the plant, and serve as routes of low resistance to the diffusion of gases and toxic products derived from the metabolism (Kozlowski 1997;Simone et al 2003;Shimamura et al 2010). Among the six species studied, only T. rosea formed aerenchyma in the roots and stem.…”

De novo assembly of Zea nicaraguensis root transcriptome identified 5 261 full-length transcripts

“…Therefore, we believe that most of the full-length transcripts we defined in the present study contain the complete coding region and are close to the true transcripts. Highly developed aerenchyma and suberized exodermis are typical characteristics of aquatic and wetland plant species (De Simone et al 2003;Jackson et al 2009). Compared with cultivated maize, Z. nicaraguensis can form constitutive aerenchyma and a well-developed suberin lamella in the exodermis even in well-drained soil Abiko et al 2012).…”