Abstract

Genotypic, developmental, and environmental factors converge to determine the degree of Crassulacean acid metabolism (CAM) expression. To characterize the signaling events controlling CAM expression in young pineapple (Ananas comosus) plants, this photosynthetic pathway was modulated through manipulations in water availability. Rapid, intense, and completely reversible up-regulation in CAM expression was triggered by water deficit, as indicated by the rise in nocturnal malate accumulation and in the expression and activity of important CAM enzymes. During both up- and down-regulation of CAM, the degree of CAM expression was positively and negatively correlated with the endogenous levels of abscisic acid (ABA) and cytokinins, respectively. When exogenously applied, ABA stimulated and cytokinins repressed the expression of CAM. However, inhibition of water deficit-induced ABA accumulation did not block the up-regulation of CAM, suggesting that a parallel, non-ABA-dependent signaling route was also operating. Moreover, strong evidence revealed that nitric oxide (NO) may fulfill an important role during CAM signaling. Up-regulation of CAM was clearly observed in NO-treated plants, and a conspicuous temporal and spatial correlation was also evident between NO production and CAM expression. Removal of NO from the tissues either by adding NO scavenger or by inhibiting NO production significantly impaired ABA-induced up-regulation of CAM, indicating that NO likely acts as a key downstream component in the ABA-dependent signaling pathway. Finally, tungstate or glutamine inhibition of the NO-generating enzyme nitrate reductase completely blocked NO production during ABA-induced up-regulation of CAM, characterizing this enzyme as responsible for NO synthesis during CAM signaling in pineapple plants.

Highlights

  • Genotypic, developmental, and environmental factors converge to determine the degree of Crassulacean acid metabolism (CAM) expression

  • On the other hand, when water deficit was imposed by incubating the plants in a growth medium containing 30% polyethylene glycol (PEG), a progressive rise in the expression of these CAM enzymes was observed after 5 d of treatment (Fig. 1, A, C, and E), revealing a relatively rapid up-regulation of CAM in response to this abiotic stress

  • When water deficit-treated plants were subjected to a recovery period in the absence of PEG, a gradual decrease in transcript abundance and activities of CAM enzymes was observed (Fig. 2, A–F), which was associated with a corresponding reduction in the D malate (Fig. 2G)

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Summary

Introduction

Developmental, and environmental factors converge to determine the degree of Crassulacean acid metabolism (CAM) expression. In the facultative CAM species Mesembryanthemum crystallinum, the most intensively studied CAM model, elevations in endogenous abscisic acid (ABA) are usually observed during the CAM induction by salt or water stress (Thomas et al, 1992; Taybi et al, 1995; Taybi and Cushman, 2002), while exogenous ABA can induce the expression and activity of several CAM enzymes even in the absence of environmental constraints (Chu et al, 1990; Taybi et al, 1995) These observations strongly suggest that ABA is involved in CAM induction, the inhibition of ABA synthesis did not block the salt- or drought-induced CAM expression in M. crystallinum, suggesting that an ABA-independent signaling pathway mediates the C3-CAM transition process in this plant (Thomas et al, 1992; Taybi and Cushman, 2002). Based on these limited data, auxins and ethylene (ET) seem to have no effect on CAM induction (Dai et al, 1994; Hurst et al, 2004), whereas GA3 and methyl jasmonate were found to have a limited influence on CAM expression, acting as positive and negative regulators, respectively (Taybi et al, 2002)

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