ACAULIS5 controlsArabidopsisxylem specification through the prevention of premature cell death

Abstract

Cell size and secondary cell wall patterning are crucial for the proper functioning of xylem vessel elements in the vascular tissues of plants. Through detailed anatomical characterization of Arabidopsis thaliana hypocotyls, we observed that mutations in the putative spermine biosynthetic gene ACL5 severely affected xylem specification: the xylem vessel elements of the acl5 mutant were small and mainly of the spiral type, and the normally predominant pitted vessels as well as the xylem fibers were completely missing. The cell-specific expression of ACL5 in the early developing vessel elements, as detected by in situ hybridization and reporter gene analyses, suggested that the observed xylem vessel defects were caused directly by the acl5 mutation. Exogenous spermine prolonged xylem element differentiation and stimulated cell expansion and cell wall elaboration in xylogenic cell cultures of Zinnia elegans, suggesting that ACL5 prevents premature death of the developing vessel elements to allow complete expansion and secondary cell wall patterning. This was further supported by our observations that the vessel elements of acl5 seemed to initiate the cell death program too early and that the xylem defects associated with acl5 could be largely phenocopied by induction of premature, diphtheria toxin-mediated cell death in the ACL5-expressing vessel elements. We therefore provide, for the first time, mechanistic evidence for the function of ACL5 in xylem specification through its action on the duration of xylem element differentiation.

Perturbation of Polyamine Catabolism Can Strongly Affect Root Development and Xylem Differentiation

“…4). In apparent contradiction with our hypothesis about the role played by PA in xylem differentiation and cell death, is the finding that exogenous Spm prolongs xylem element differentiation in xylogenic Zinnia elegans cell cultures, reducing the time of appearance and the rate of tracheal element differentiation as well as the finding that ACL5 controls xylem specification through the prevention of premature cell death in Arabidopsis (Muñ iz et al, 2008). However, this incongruity can be explained by two considerations: (1) contrary to Z. elegans or Arabidopsis plants, PAO expression levels are particularly high in the cytoplasm and cell wall of monocotyledons (Cohen, 1998;Cona et al, 2005) and thus the physiological role of PAs in maize root may depend on the H 2 O 2 released upon PAO-mediated PA oxidation; (2) ACL5, actually being a thermospermine synthase (Knott et al, 2007), may exert its function through a specific effect of thermospermine (Kakehi et al, 2008) that is indeed a poor substrate of ZmPAO (P. Tavladoraki, personal communication).…”

“…This acl5 mutant shows severely reduced secondary growth of the vascular tissue, dramatically altered morphology of the vessel element, and total lack of xylem fibers (Clay and Nelson, 2005). It has been hypothesized that under physiological conditions, ACL5 prevents premature death of the developing vessel elements to allow complete expansion and secondary cell wall patterning (Muñ iz et al, 2008).…”

Recycling of Methylthioadenosine Is Essential for Normal Vascular Development and Reproduction in Arabidopsis

“…The increased vein thickness of the MTN mutant rosette leaves is similar to that reported for tkv (Clay and Nelson, 2005). Since our modeling predicted that Tspm synthase activity is inhibited by MTA, and Tspm is required for normal xylem differentiation (Muñ iz et al, 2008), it was of interest to examine Tspm content. Unfortunately, Tspm quantification is a challenge due to its low abundance; Tspm was not detected in our system.…”

“…Some of the documented roles of PAs include vascular differentiation, embryogenesis, cell division, and responses to abiotic stresses such as salt, osmotic, drought, and wounding (Takahashi and Kakehi, 2010;Vera-Sirera et al, 2010). For example, recent evidence suggests roles for both Tspm and hydrogen peroxide (H 2 O 2 ) produced from PA catabolism in the control of xylem differentiation (Muñ iz et al, 2008;Tisi et al, 2011). PAs have also been implicated in RNA processing, chromatin remodeling, membrane fluidity, and protein activation (Baron and Stasolla, 2008;Takahashi and Kakehi, 2010).…”

Bacterial and Plant Signal Integration via D3-Type Cyclins Enhances Symptom Development in the Arabidopsis-Rhodococcus fasciansInteraction

“…Indeed, expression of polyamine biosynthesis genes and polyamine levels are altered in response to treatment with cytokinins, auxins, abscisic acid, gibberellins, and jasmonates (Altman, 1989;Biondi et al, 2001;Hanzawa et al, 2002;Imai et al, 2004a;Urano et al, 2004;Muñ iz et al, 2008;Cui et al, 2010). The reverse is also true: whereas abscisic acid and cytokinin biosynthesis are induced by polyamines (Cuevas et al, 2009;Wang et al, 2009;Cui et al, 2010), ethylene and gibberellin production are down-regulated (Alcázar et al, 2005;Hu et al, 2006).…”