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

Abstract

Spermidine (Spd) treatment inhibited root cell elongation, promoted deposition of phenolics in cell walls of rhizodermis, xylem elements, and vascular parenchyma, and resulted in a higher number of cells resting in G 1 and G 2 phases in the maize (Zea mays) primary root apex. Furthermore, Spd treatment induced nuclear condensation and DNA fragmentation as well as precocious differentiation and cell death in both early metaxylem and late metaxylem precursors. Treatment with either N-prenylagmatine, a selective inhibitor of polyamine oxidase (PAO) enzyme activity, or N,N 1 -dimethylthiourea, a hydrogen peroxide (H 2 O 2 ) scavenger, reverted Spd-induced autofluorescence intensification, DNA fragmentation, inhibition of root cell elongation, as well as reduction of percentage of nuclei in S phase. Transmission electron microscopy showed that N-prenylagmatine inhibited the differentiation of the secondary wall of early and late metaxylem elements, and xylem parenchymal cells. Moreover, although root growth and xylem differentiation in antisense PAO tobacco (Nicotiana tabacum) plants were unaltered, overexpression of maize PAO (SZmPAO) as well as down-regulation of the gene encoding S-adenosyl-L-methionine decarboxylase via RNAi in tobacco plants promoted vascular cell differentiation and induced programmed cell death in root cap cells. Furthermore, following Spd treatment in maize and ZmPAO overexpression in tobacco, the in vivo H 2 O 2 production was enhanced in xylem tissues. Overall, our results suggest that, after Spd supply or PAO overexpression, H 2 O 2 derived from polyamine catabolism behaves as a signal for secondary wall deposition and for induction of developmental programmed cell death.

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

“…The altered PA content of the mutant (e.g. increased Put) may lead to increased PA oxidase activity and H 2 O 2 , a documented signal for increased vascular tissue differentiation (Tisi et al, 2011). However, we did not detect increased H 2 O 2 in 14-d-old mtn1-1mtn2-1 seedlings using a histochemical stain (Supplemental Fig.…”

“…Tspm may induce more normal xylem differentiation and restore sufficient transport of compounds essential for seed development, including phytohormones and metal cofactors. Interestingly, a recent report by Tisi et al (2011) shows that increased xylem differentiation and secondary wall deposition are induced in maize (Zea mays) roots by exogenous Spd feeding. This is apparently induced by H 2 O 2 arising from PA catabolism.…”

“…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).…”

The Apoplastic Copper AMINE OXIDASE1 Mediates Jasmonic Acid-Induced Protoxylem Differentiation in Arabidopsis Roots

“…During the plant response to stresses, a faster apoplastic oxidation of PAs has been supposed to occur, allowed by the concurrent increase of PA secretion and catabolism in the cell wall, and the PA-derived H 2 O 2 has been demonstrated to trigger signal transduction pathways leading to the induction of defense gene expression, stress tolerance, or PCD (Moschou et al, 2008;Tisi et al, 2011a). Recently, the dual role of PAs as either signaling compounds or the source of the second messenger H 2 O 2 has been highlighted, and it has been hypothesized that AOs may have a role in PA/H 2 O 2 balance (Moschou et al, 2008;Tisi et al, 2011aTisi et al, , 2011b. In fact, the coordinated modulation of PA metabolism and secretion in the cell wall may represent a crucial mechanism in the control of the PA-H 2 O 2 ratio, which has been suggested to be a significant player in fixing cell fate and behavior under stress conditions (Moschou et al, 2008;Tisi et al, 2011a).…”

“…H 2 O 2 derived from the extracellular catabolism of PAs by cell wall-localized AOs has been shown to be involved in both developmental processes, such as the light-induced inhibition of mesocotyl growth (Cona et al, 2003) and the PCD occurring in differentiating tracheary elements (Tisi et al, 2011b), as well as defense responses during wound healing (Angelini et al, 2008), salt stress (Moschou et al, 2008), and pathogen attack (Moschou et al, 2009). In this regard, AOs have also been suggested to act as stress-responsive genes whose expression strongly increases in response to both pathogen infection and abiotic stresses (Moschou et al, 2008;Tavladoraki et al, 2012).…”