A Comparison of Oligogalacturonide- and Auxin-Induced Extracellular Alkalinization and Growth Responses in Roots of Intact Cucumber Seedlings

Abstract

Oligogalacturonic acid (OGA) affects plant growth and development in an antagonistic manner to that of the auxin indole-3-acetic acid (IAA), the mechanism by which remains to be determined. This study describes the relationship between IAA and OGA activity in intact cucumber (Cucumis sativus) seedlings. Both OGA and IAA induced rapid and transient extracellular alkalinization; however, the characteristics of the OGA and IAA responses differed in their kinetics, magnitude, calcium dependence, and region of the root in which they induced their maximal response. IAA (1 m) induced a saturating alkalinization response of approximately 0.2 pH unit and a rapid reduction (approximately 80%) in root growth that only partially recovered over 20 h. OGAs, specifically those with a degree of polymerization of 10 to 13, induced a maximal alkalinization response of 0.48 pH unit, but OGA treatment did not alter root growth. Saturating concentrations of OGA did not block IAA-induced alkalinization or the initial IAA-induced inhibition of root growth but allowed IAA-treated roots to recover their initial growth rate within 270 min. IAA-induced alkalinization occurs primarily in the growing apical region of the root, whereas OGA induced its maximal response in the basal region of the root. This study demonstrates that OGA and IAA act by distinct mechanisms and that OGA does not simply act by inhibition of IAA action. These results also suggest that IAA-induced extracellular alkalinization is not sufficient to account for the mechanism by which IAA inhibits root growth.Oligogalacturonic acid (134-linked ␣-d-oligo-Gal-UA; OGA) is a biologically active oligosaccharide produced by hydrolysis of de-esterified pectin (polyGalUA). OGA has been studied extensively in plant tissue cultures and dissected plants and has been shown to alter growth and development, including inhibition of auxin-induced elongation and ethylene accumulation in pea (Pisum sativum) stems (Branca et al., 1988) and regulation of organogenesis in tobacco (Nicotiana tabacum) explants (Eberhard et al., 1989;Bellincampi et al., 1993), to elicit a number of defense responses, including accumulation of phytoalexins (Hahn et al., 1981) and proteinase inhibitors (Bishop et al., 1984), and to induce rapid responses at the plasma membrane, such as trans-membrane ion flux (Mathieu et al., 1991) and phosphorylation of plasma membrane proteins (Farmer et al., 1991). Most of these responses are elicited maximally by OGAs with a degree of polymerization (DP) of 10 to 14 in the concentration range of 10 Ϫ6 to 10 Ϫ9 m; OGAs outside this size range are typically at least 10-fold less active. This indicates that OGA acts by a specific highaffinity mechanism in a manner similar to the classic plant hormones. However, it has not been demonstrated that biologically active OGA of the appropriates size and concentration are present in plant tissues.It has recently been shown that wounding and the wound-induced signal, systemin, induce the systemic accumulation of polygalacturonase, which m...

Production of Reactive Oxygen Intermediates (O2 ˙−, H2O2, and ˙OH) by Maize Roots and Their Role in Wall Loosening and Elongation Growth

“…wall alkalinization and growth responses in cucumber (Cucumis sativus) roots, Spiro et al (2002) concluded that auxin-induced alkalinization is not sufficient to account for the mechanism by which auxin inhibits root growth.…”

Effect of oligogalacturonides on root length, extracellular alkalinization and O2−-accumulation in alfalfa

“…Oligogalacturonic acids (OGAs) are biologically active oligosaccharides produced by the hydrolysis of de-esterified pectins (Spiro et al, 2002). Both plant and pathogen cell walls are a source of the oligosaccharide fragments generated during plant-pathogen interactions through the enzymatic hydrolysis of polysaccharides (Côté and Hahn, 1994;John et al, 1997).…”

Transgenic Expression of a Fungal endo-Polygalacturonase Increases Plant Resistance to Pathogens and Reduces Auxin Sensitivity

“…Furthermore, in tobacco, OGs inhibit the induction of the late auxin-responsive genes Nt114, rolB, and rolD (Mauro et al, 2002). In cucumber (Cucumis sativus) seedlings, OGs allow for a more rapid recovery of root growth in auxin-treated roots (Spiro et al, 2002). To date, the mechanism underlying the antagonistic effect of OGs on auxin-induced responses is not known.…”