Abstract
Polyamines are low molecular weight, aliphatic polycations found in the cells of all living organisms. Due to their positive charges, polyamines bind to macromolecules such as DNA, RNA, and proteins. They are involved in diverse processes, including regulation of gene expression, translation, cell proliferation, modulation of cell signalling, and membrane stabilization. They also modulate the activities of certain sets of ion channels. Because of these multifaceted functions, the homeostasis of polyamines is crucial and is ensured through regulation of biosynthesis, catabolism, and transport. Through isolation of the genes involved in plant polyamine biosynthesis and loss-of-function experiments on the corresponding genes, their essentiality for growth is reconfirmed. Polyamines are also involved in stress responses and diseases in plants, indicating their importance for plant survival. This review summarizes the recent advances in polyamine research in the field of plant science compared with the knowledge obtained in microorganisms and animal systems.
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Introduction
Polyamines are low molecular weight aliphatic cations that are ubiquitous to all living organisms. Their initial discovery was made as early as 1678, when “three-sided” crystals from human semen were first described (van Leeuwenhoek 1678). Because the described polyamine occurs in high concentration in sperm, the name spermine [N,N′-bis(3-aminopropyl)butane-1,4-diamine] was designated (Ladenburg and Abel 1888). The structure and chemical synthesis of this compound were not established until much later (1926) (Dudley et al. 1926; Wrede 1925). Accordingly, the name spermidine was given to a previously chemically synthesized bovine pancreatic polyamine [N-(3-aminopropyl)butane-1,4-diamine] (Dudley et al. 1927). Spermine and spermidine are responsible for the typical odor of semen. Two other naturally occurring polyamines, putrescine (butane-1,4-diamine) and cadaverine (pentane-1,5-diamine), are bacterial decomposition compounds that are also fragrant volatile compounds (Brieger 1885). Both contribute to the foul odor of the putrefying flesh of cadaver, which gives them their names. Their structures were established, as was spermidine, by comparison with the already synthesized molecules (Ladenburg 1886; von Udransky and Baumann 1888) (Fig. 1). Since their discovery, the cellular functions of the physiological polyamines putrescine, spermidine, and spermine have been the focus of much study. Due to their positive charge, these compounds can bind various cellular macromolecules, including DNA, RNA, chromatin and proteins by electrostatic linkages which can cause stabilization or destabilisation. Furthermore, covalent linkages can lead to cross-link formation of proteins forming cytotoxic derivatives. Thus, they have been implicated in myriad fundamental cellular processes, including regulation of gene expression, translation, cell proliferation, modulation of cell signaling, and membrane stabilization (Tabor and Tabor 1984; Cohen 1998; Igarashi and Kashiwagi 2000). Polyamines can also regulate cell death, particularly apoptosis (Thomas and Thomas 2001; Seiler and Raul 2005).
The most abundant polyamines in bacteria are putrescine and spermidine. Cadaverine is also present but is less abundant. Various unique functions for bacterial polyamines have been uncovered (Wortham et al. 2007); they (1) are often components of outer membrane of gram-negative bacteria, (2) are involved in the biosynthesis of siderophores, (3) are important in acid resistance, (4) protect from oxygen toxicity, (5) play a potent role in signaling for cellular differentiation (as suggested through their action as an extracellular signal for swarming), and (6) are essential for plaque biofilm formation. Additionally, putrescine is known to activate the transcription of the genes involved in polyamine uptake and utilization. Thermophilic bacteria contain two additional categories of unique polyamines (Hamana et al. 1998; Oshima 2007). These include polyamines with longer chains such as caldopentamine and caldohexamine, and branched polyamines such as tris(3-aminopropyl)amine (so-called mitsubisine) and tetrakis(3-aminopropyl)ammonium (Fig. 1).
Intensive research on polyamine function in mammals has revealed that they are, as in bacteria, essential regulators of growth, gene transcription, and ribosome-mediated translation (Thomas and Thomas 2003; Childs et al. 2003; Umekage and Ueda 2006). Polyamines and their metabolism are of clear medical and pharmacological importance. They are present at relatively high concentrations in the mammalian brain and are believed to be involved in the pathophysiological processes underlying brain ischemia (Li et al. 2007). Owing to the high turnover of the intestinal mucosal cells, those cells have a high requirement for polyamines. They contribute to the maintenance of normal gut function, the maturation of the intestinal mucosa and its repair after injury (Seiler and Raul 2007). In addition, the polyamine metabolic pathway is a recognized drug target for cancer prevention, as there is a strong positive correlation between polyamine content and cancer cell growth (Saunder and Wallace 2007; Casero and Marton 2007).
In plants, the three major polyamines are putrescine, spermidine, and spermine. Cadaverine is also present in legumes. Plant polyamines have been suggested to play important roles in morphogenesis, growth, embryogenesis, organ development, leaf senescence, and abiotic and biotic stress response (Kumar et al. 1997; Walden et al. 1997; Malmberg et al. 1998; Bouchereau et al. 1999; Liu et al. 2000; Alcázar et al. 2006; Groppa and Benavides 2007; Kusano et al. 2007b). Plant polyamines are also responsible for characteristics of agro-economical importance, including phytonutrient content, fruit quality, and vine life (Mehta et al. 2002; Matto et al. 2006).
In this review, we summarize what is known about polyamine metabolism and function in plants, with particular emphasis on stress responses.
Polyamine biosynthesis
With some variations, the biosynthetic pathways for the polyamines are conserved from bacteria to animals and plants (Tabor and Tabor 1984). The synthesis essentially starts from the two amino acid precursor molecules, l-arginine and l-methionine. An overview of the general pathway is given in Fig. 2a.
Polyamine biosynthesis and degradation pathways. a Biosynthesis; b degradation. Plant pathways are indicated by green bold arrows. Blue and red arrows indicate bacterial and animal pathways, respectively
In plants, polyamines have not only been localized in the cytoplasm but also in organelles such as vacuoles, mitochondria, and chloroplasts (Kumar et al. 1997). Two alternative synthesis pathways have been verified and the genes encoding enzymes for the polyamine biosynthesis pathway have been cloned and characterized from various plant species (Bell and Malmberg 1990; Michael et al. 1996; see also the reviews, Bagni and Tassoni 2001; Liu et al. 2007). Starting from arginine, the diamine putrescine is synthesized via ornithine by arginase (EC 3.5.3.1) and ornithine decarboxylase (ODC, EC 4.1.1.17). Putrescine can also be synthesized via agmatine by three sequential reactions catalyzed by arginine decarboxylase (ADC, EC 4.1.1.19), agmatine iminohydrolase (AIH, EC 3.5.3.12), and N-carbamoylputrescine amidohydrolase (CPA, EC 3.5.1.53), respectively. Putrescine is converted to spermidine by action of spermidine synthase (SPDS, EC 2.5.1.16). An aminopropyl group is transferred from the decarboxylated S-adenosylmethionine, which is synthesized from methionine in two sequential reactions of methionine adenosyltransferase (EC 2.5.1.6) and S-adenosylmethionine decarboxylase (SAMDC, EC 4.1.1.50), respectively. In legumes, where also cadaverine is present, this diamine is derived from lysine via a reaction of lysine decarboxylase (LDC, EC 4.1.1.18).
Interestingly, the sequenced genome of the model plant Arabidopsis thaliana does not contain a gene coding for ornithine decarboxylase (ODC) (Hanfrey et al. 2001). So far, absence of this enzyme has only been reported in one other organism, the protozoan eukaryote Trypanosoma cruzi. All other polyamine biosynthesis genes have been assigned in A. thaliana: there are two genes (ADC1 and ADC2) for arginine decarboxylase (Watson and Malmberg 1996; Watson et al. 1997), and one each (AIH and CPA) for agmatine iminohydrolase and N-carbamoylputrescine amidohydrolase (Janowitz et al. 2003; Piotrowski et al. 2003). Spermidine synthase is encoded by two genes (SPDS1 and SPDS2) (Hanzawa et al. 2002). ACL5 and SPMS (formally SPDS3) were identified as the genes encoding spermine synthase (Hanzawa et al. 2000; Panicot et al. 2002; Clay and Nelson 2005; see also the next paragraph). There are at least four genes (SAMDC1, SAMDC2, SAMDC3 and SAMDC4) for S-adenosylmethionine decarboxylase (Urano et al. 2003; Ge et al. 2006). A study of the interactions of these gene products revealed that SPMS but not ACL5 associates with the spermidine synthases (SPDS1 and SPDS2) to form “polyamine metabolon complexes” (Panicot et al. 2002). The dynamics of these complexes during environmental changes have yet to be investigated.
In 2007, Knott et al. reported that a putative spermine synthase from the diatom Thalassiosira pseudonana has thermospermine synthase activity, and that A. thaliana ACL5 has the same enzymatic activity. Thermospermine is an isomer of spermine (Fig. 1). The substrate binding sites of spermidine synthases were identified by X-ray analysis (Korolev et al. 2002; Dufe et al. 2005). By sequence comparison, spermine and thermospermine synthases exhibit a similar spatial arrangement of these binding sites. The conserved amino acid sequence GGGDG constitutes the binding site for decarboxylated S-adenosylmethionine in spermidine synthase (Korolev et al. 2002), and this domain is also found in spermine synthase. The aspartate (D) residue in this sequence is responsible for an ionic interaction with the amino group of the aminopropyl moiety of decarboxylated S-adenosylmethionine (Dufe et al. 2005) and is replaced by a glutamate (E) in all ACL5 group sequences. Besides ACL5 from A. thaliana, MdACL5-1 and -2 from apple (Kitashiba et al. 2005), and a number of other genes deposited in the DNA database are classified as thermospermine synthases (Knott et al. 2007). A knockout mutation on ACL5 leads to defects in stem elongation (Hanzawa et al. 1997) and in vascular development (Clay and Nelson 2005). One (sac51) of the acl5-suppressor mutants, which recovers normal stem growth, was mapped to a gene encoding a bHLH-type transcription factor (Imai et al. 2006). Future work should uncover the physiological roles of thermospermine synthase in plants.
In bacteria, in addition to the pathways which are effective in plants putrescine can be synthesized directly from agmatine by agmatinase (EC 3.5.3.11). Spermine is not synthesized in Escherichia coli as its genome does not encode spermine synthase (SPMS, EC 2.5.1.22) (Wortham et al. 2007). Recent studies on polyamine biosynthesis in the extreme thermophile Thermus thermophilus revealed a new metabolic pathway for spermidine synthesis in this organism. T. thermophilus spermidine, the precursor for the unique polyamines described above, is derived from arginine but not putrescine (Oshima 2007).
Polyamine synthesis in animals also starts from ornithine, and can be formed directly from proline by ornithine aminotransferase (Wu et al. 2005). The arginine decarboxylase pathway via agmatine as described for bacteria and plants has not been demonstrated in animal cells. Ornithine decarboxylase, spermidine synthase, and spermine synthase accomplish the sequential synthesis of putrescine, spermidine, and spermine, respectively.
Polyamine catabolism
The major pathways of polyamine degradation are depicted in Fig. 2b. The enzyme polyamine oxidase (PAO, EC 1.5.3.11) has been characterized as a flavine adenine dinucleotide (FAD)-containing enzyme that uses N 1-acetyl derivatives as substrates (Bolenius and Seiler 1981). In plants, it was demonstrated that PAOs catalyze the conversion of spermidine and spermine to 4-aminobutanal and N-(3-aminopropyl)-4-aminobutanal, respectively, along with the production of 1,3-diaminopropane and H2O2 (Federico et al. 1990; Šebela et al. 2001; Cona et al. 2006). This means that plant PAOs are involved in the terminal catabolism of polyamines. The first described plant PAO was ZmPAO derived from the apoplast of maize cells. ZmPAO is a 53-kDa monomeric glycoprotein containing one molecule of FAD (Tavladoraki et al. 1998). Two isoforms, HvPAO1 and HvPAO2, have been isolated from barley; the latter targets to the vacuole. A C-terminal eight amino acid-extension observed only in HvPAO2 was identified as a sorting-signal for this organelle (Cervelli et al. 2001, 2004, 2006).
Spermine oxidase (SMO), a FAD-dependent amine oxidase that directs the back-conversion of spermine to spermidine with concomitant production of 3-aminopropanal and H2O2, was initially identified in mammalian cells (Wang et al. 2001; Vujcic et al 2002; Cervelli et al. 2003). An enzyme (Fms1) with the same enzymatic activity was found in yeast (Landry and Sternglanz 2003). The genome of the model plant Arabidopsis contains five PAO-like genes (see the review, Alcázar et al. 2006). Of those, AtPAO1 catalyzes the same reaction as SMO/Fms1 (Tavladoraki et al. 2006), indicating that a back-conversion pathway of polyamines also exists in plants. Whether any of the plant PAOs can convert spermidine to putrescine, thus completing a full back-conversion cycle should be assessed in the future.
The other class of enzymes that catabolizes polyamines is the copper-containing diamine oxidase (DAO, EC 1.4.3.6), which prefers diamines as substrates (Zeller 1938; Brazeau et al. 2004). DAO catalyzes the oxidation of putrescine to 4-aminobutanal with concomitant production of NH3 and H2O2, and the resulting aldehyde is further metabolized to γ-aminobutyric acid via Δ1-pyrroline (Bagni and Tassoni 2001). Arabidopsis contains 12 DAO-like genes (see review Alcázar et al. 2006). Among them, only ATAO1 is characterized biochemically (Møller and McPherson 1998). Thus, the functional analysis of the remaining 11 genes with sequence similarity to ATAO1 is awaiting. As has been demonstrated, all polyamine-oxidizing enzymes generate H2O2. The importance of this will be addressed later in the review.
Post-translational modification of histone N-terminal tails impacts chromatin structure, in which human LSD1 (lysine-specific demethylase 1), a nuclear homolog of amine oxidase, is involved. LSD1 protein consists of three major domains, and, of these, the C-terminal domain has significantly high sequence homology to polyamine oxidases that belong to the FAD-dependent enzyme family (Binda et al. 2002; Anand and Marmostein 2007). LSD1 functions as a transcriptional corepressor through histone demethylase activity specifically to histone H3 lysine 4, which is linked to active transcription. The protein is evolutionarily conserved from yeast (Schizosaccharomyces pombe) to animals and plants (Shi et al. 2004; Culhane and Cole 2007). A. thaliana homologs of LSD1 promote floral transition through repressing the expression of floral repressor genes (Jiang et al. 2007). In this context, again, the functional characterization of the members whose sequences have enough homology either to ATAO1 or to AtPAO1 might be informative.
Plant polyamines serve as substrates for secondary metabolites. Putrescine, for instance, is a common precursor of nicotine and tropane alkaloids, which are present abundantly in the Solanaceae (Leete 1980). In the first step of the pathway, putrescine is methylated by N-methyltransferase (Hibi et al. 1994). This methyl derivative is then deaminated oxidatively to 4-methylaminobutanal, which spontaneously cyclizes to give the N-methylpyrrolinium cation. This reaction is catalyzed by N-methylputrescine oxidase (MPO) (Katoh et al. 2007; Heim et al. 2007). Tobacco plants have two MPO genes (MPO1 and MPO2) that share 88% identity (Katoh et al. 2007). MPO1 has 43% homology each to Pisum sativum amine oxidase (Tipping and McPherson 1995) and to A. thaliana amine oxidase1 (Møller and McPherson 1998).
In animals, polyamine catabolism starts with the inducible enzyme spermidine/spermine N 1-acetyltransferase (SSAT, EC 2.3.1.57) (Casero and Pegg 1993; Seiler 2004), which catalyzes the formation of N 1-acetyl derivatives by the transfer of the acetyl group from acetyl-coenzyme A to the N 1 position of spermine/spermidine. The acetyl derivatives are then converted to spermidine or putrescine along with the production of 3-aceto-aminopropanal and hydrogen peroxide (H2O2) by the peroxisomal and constitutive PAO (Bolenius and Seiler 1981). The aldehyde can be further catabolized to β-alanine by sequential reactions of aldehyde dehydrogenase and N-acetyl-β-alanine deacetylase. Mice chronically treated with the PAO inhibitor MDL72527 [N 1,N 4-bis(2,3-butadienyl)-1,4-butanediamine] die, due to spermine accumulation in red blood cells and blood plasma. This result indicates that blockage of polyamine catabolism, especially spermine catabolism, can be fatal in these animals (Seiler et al. 2002), and symbolizes the importance of polyamine catabolism.
Polyamine transport
Polyamine transport systems in plant and animal cells have been proposed, but none have been identified at the molecular level. Results from uptake-experiments of putrescine and spermidine into carrot cells suggested that the entry of polyamines into the cells is driven by a transmembrane electrical gradient, with a possible antiport mechanism between external and internal polyamines (Pistocchi et al. 1987). Other results suggested that in maize roots the bulk of exogenously applied putrescine is transported across the plasmalemma by a carrier-mediated process, similar to that proposed for animal systems (DiTomaso et al. 1992).
In mammalian cells, two transport systems for polyamines have been suggested. In one model, polyamines are transported into cells through unidentified membrane transporters/carriers driven by a membrane potential. The polyamines then are sequestered into vesicles by proton exchange over a pH gradient built by a vacuolar ATPase (Soulet et al. 2004; Casero and Marton 2007). The second model proposes a role for the heparin sulphate side chains of recycling glypican 1 (GPC1) in the transport of spermine, and assumes that GPC1 recycling is a basis of polyamine transport (Belting et al. 2003). In addition to these suggested transport mechanisms that also act as control points for the adjustment of intracellular polyamine levels, two additional mammalian mechanisms have also been proposed (Wallace et al. 2003). For plant cells a model for a polyamine transport system is yet not available.
In microorganisms such as E. coli and yeast polyamine transport systems have been investigated in-depth. In E. coli, four systems, (1) spermidine-preferential uptake system (PotABCD), (2) putrescine-specific uptake system (PotFGHI), (3) putrescine transport system (PotE), and (4) cadaverine transport system (CadB), have been identified (Igarashi and Kashiwagi 1999; Igarashi 2006). Of those, the former two uptake systems are ATP-binding cassette transporters. Recently, a novel putrescine utilization pathway in E. coli was identified (Kurihara et al. 2005). The pathway components are encoded by the ycj gene cluster, and include a novel putrescine importer gene, ycjJ (now renamed puuP). In yeast, nine proteins were identified as polyamine transport proteins: TPO1–5, UGA4, GAP1, DUR3, and SAM3. TPO1–4 are efflux-pumps for xenobiotics that also recognize polyamines. TPO5, which localizes in the post-Golgi complex, is an efflux-pump for polyamines. UGA4, which resides in vacuoles, takes up putrescine along with γ-aminobutyric acid. The cytoplasmic membrane protein GAP, takes up polyamines into the cytoplasm along with amino acids. DUR3 and SAM3 also carry polyamines preferentially into the cytoplasm (Igarashi 2006).
Polyamine homeostasis
The overall intracellular concentration of polyamines is in the range of several hundred micromolar to a few millimolars and is tightly regulated, as higher levels of polyamines are toxic to cells and lead to cell death. Polyamine levels are elegantly regulated at various steps including de novo synthesis, degradation, and transport.
S-adenosylmethionine decarboxylase (SAMDC) was found to be an important enzyme in regulation of polyamine homeostasis in all organisms. E. coli SAMDC is first synthesized as a proenzyme, and thereafter cleaved posttranslationally to form α and β subunits (Li et al. 2001). The former subunit is modified by covalent attachment of a pyruvoyl group derived from serine, which is essential for enzyme activity. The mature enzyme takes (αβ)4 configuration. Subsequent work revealed that SAMDC enzymes from other organisms including plants are also synthesized as a proenzyme and then processed to form the active pyruvoyl-containing enzyme (Kashiwagi et al. 1990). The processing and activity of SAMDC are increased by putrescine, indicating that the increased concentration of putrescine raises the formation of decarboxylated SAM which is required for the spermidine synthase (Pegg 1986; Kameji and Pegg 1987; Xiong et al. 1997). The active enzyme is further modified irreversibly at the cysteine residue of α subunit by the product of enzyme reaction, decarboxylated S-adenosylmethionine (Li et al. 2001). This modification causes the inactivation of the enzyme and contributes to polyamine homeostasis.
A further regulation mechansim for SAMDC has been uncovered. For the plant model it is outlined in Fig. 3. First it was shown for the mammalian SAMDC transcript that it contains a small open reading frame (ORF) encoding the hexapeptide MAGDIS upstream of the main ORF. This type of ORF is termed an upstream ORF (uORF). SAMDC is regulated at the translation level in response to cellular polyamine levels through interactions between the peptide product and polyamines. These interactions results in ribosomal stalling near the stop codon of the uORF (Ruan et al 1996). Plant SAMDC genes have an unusually long 5′-UTR where two uORFs are well conserved (Franceschetti et al. 2001). The first uORFs (termed tiny uORFs) distal to the 5′ end are 3–4 codons long, while the second (termed small uORFs) encode 50–54 peptides. The small uORF-encoded peptide sequences are conserved among different plant species (Hanfrey et al. 2002, 2003, 2005). The small uORF-encoded peptide is responsible for translational repression of the main ORF under conditions of excess polyamine concentration; while the tiny uORF is required for induced translation of the main ORF during conditions of low polyamine concentration (Hanfrey et al. 2002, 2005) (Fig. 3). Interestingly, this tiny/small uORFs’ configuration with one-nucleotide-overlap is highly conserved from Chlamydomonas reinhardtii, to Physcomitrella patens, to higher plants. These results demonstrate two things: first, that the dual uORF-based control mechanism of SAMDC has been maintained during plant evolution; and second, that the translational regulation of SAMDC mRNA is critically important for plant polyamine homeostasis.
Regulation of the translation of plant SAMDC main ORF mediated by the dual uORFs. This circuit model is based on the reference by Hanfrey et al. (2005)
A main modulator of polyamine concentration, antizyme, although it is generally presumed that it does not exist in plants, should be briefly described in this review. The antizyme proteins are encoded by a small gene family and details of the individual members are known but will not be touched upon here (see reviews, Mangold 2005; Pegg 2006). In response to increasing polyamine levels, antizyme binds to ODC, the key enzyme of polyamine biosynthesis. Besides non-competitively inhibiting ODC activity, antizyme recruits ODC to the 26S proteasome for destruction without ubiquitin-modification. Antizyme transcription is not modulated by polyamine concentration, however, higher concentrations of polyamine cause a +1 programmed frameshift of the antizyme mRNA, resulting in decoding of a full-length antizyme mRNA and production of the mature antizyme protein (Matsufuji et al. 1995; Hayashi et al. 1996; Ivanov et al. 2000). Antizyme also regulates polyamine transport (Mitchell et al. 1994; He et al. 1994). The bacterial ODC is also regulated by an antizyme-like molecule, AtoC (Canellakis et al. 1993; Lioliou and Kyriakidis 2004). Putrescine induces atoC expression, and the resulting AtoC protein inhibits ODC activity. Although antizyme-like properties of AtoC have been demonstrated, its expression is not regulated by frameshifting. An antizyme-like protein of 22 kDa has been identified in the anaerobic, gram-negative bacterium Selenomonas ruminantium (Yamaguchi et al. 2002) that contains cadaverine as a membrane component (Kamio et al. 1981). The lysine decarboxylase of S. ruminantium has ODC activity and is completely inhibited by the ODC inhibitor 2-difluoromethylornithine. Furthermore, the antizyme-like protein is induced upon addition of putrescine and is able to bind to lysine decarboxylase. Interestingly, this protein has sequence similarity to the ribosomal L10 protein of Gram-positive bacteria (Yamaguchi et al. 2006).
As mentioned, at the moment, it is generally presumed that plants do not have antizyme-type proteins. The model plant Arabidopsis lacks the antizyme target, ODC (Hanfrey et al. 2001); and other plants possess two alternative biosynthetic pathways. These results suggest that plants are equipped with distinct but still veiled mechanism(s) to control intracellular polyamine levels. At least plant PAO and DAO activities contribute to the regulation of polyamine homeostasis (Šebela et al. 2001).
Polyamines as regulators of ion channels
In mammals, polyamines have direct effects on several ion channels and receptors, resulting in the regulation of Ca2+, Na+, and K+ homeostasis (Li et al. 2007; Johnson 1996; William 1997a, b). Intracellular polyamines are involved in the regulation of intrinsic gating and rectification of inward rectifier K+ channels (Ficker et al. 1994; Lopatin et al. 1994; Oliver et al. 2000). Furthermore, they are responsible for inward rectification of AMPA (α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid) and kainite receptors through blocking the pore of the receptor channel, thus preventing Na+ or Ca2+ influx. Extracellular polyamines, particularly spermine, have stimulatory effects on the NMDA (N-methyl-d-aspartate) receptor, which is a glutamate receptor (William 1997a, b). Polyamines also interact with voltage-activated Ca2+-channels (Li et al. 2007) and cyclic nucleotide-gated channels (Lu and Ding 1999). Therefore, changes in intracellular or extracellular levels of polyamines could alter K+, Na+, or Ca2+ trafficking.
Studies of the effects of polyamines on ion channels have been extended to plants. Intracellular polyamines block a fast-activating vacuolar (FV) cation channel from barley (Brüggemann et al. 1998, 1999). FV and slow-activating channels in red beet vacuoles are also inhibited by polyamines (Dobrovinskaya et al. 1999a, b). Cytoplasmic polyamines block the inward K+ currents across the plasma membrane of guard cells (Liu et al. 2000). Non-selective cation channels are another target of polyamines, and channel blockage by polyamines leads to the prevention of K+ efflux from pea mesophyll cells (Shabala et al. 2007). Cyclic nucleotide-gated channels and glutamate receptor-like proteins are the major candidates for non-selective cation channels in plants (Davenport 2002). In addition to the direct effect of polyamines on the ion channels, it has also been reported that polyamines, particularly spermine, enhance the activity of plasma membrane H+-ATPase through increased associations between the 14-3-3 protein and the enzyme (Garufi et al. 2007). More detailed analyses of polyamine action on ion channels in plants will be one of the most challenging and fruitful targets in polyamine research, and may uncover how these cationic molecules modulate ion cross-networks in plant cells.
Polyamines for growth
Polyamines are considered to be essential for life, as inhibition of polyamine biosynthesis blocks cell growth (Cohen 1998; Igarashi and Kashiwagi 2000; Thomas and Thomas 2001; Hanfrey et al. 2001). Early evidence for this comes from data on sea urchin eggs (Kusunoki and Yasumasu 1978). When the egg cells are treated with an ODC inhibitor, egg cleavage is significantly blocked, which inhibition is reversed in the presence of polyamines. Current genetic data now substantiates this notion: deletion of either the ODC gene or the SAMDC gene prevents spermidine synthesis and is lethal at very early embryonic stages in mice (Wang et al. 2004). Thus, spermidine is essential for eukaryotic viability.
Most bacteria do not contain a gene encoding spermine synthase (Wortham et al. 2007); and although yeast cells carry genes for the synthase, spermine is not essential for their growth (Hamasaki-Katagiri et al. 1998). The same is also the case in mice (Lorenz et al. 1998; Mackintosh and Pegg 2000). These findings suggest that spermine is not essential in all mammals or all prokaryotes. Recent evidence indicates that this is also the case in plants (Fig. 4). Urano et al. (2005) isolated T-DNA insertional mutants for two ADC genes, ADC1 and ADC2. After crossing, these researchers generated an Arabidopsis double mutation on ADC1 and ADC2 that was found to cause a lethal defect in embryo development. A double mutation on two spermidine synthase-encoded genes, SPDS1 and SPDS2, leads to a similar developmental defect in the embryo (Imai et al. 2004b). Furthermore, a dual mutation on SAMDC1 and SAMDC4 is embryonic lethal (Ge et al. 2006).
Putrescine and spermidine, but not spermine, are essential for normal growth of Arabidopsis. Polyamine biosynthesis pathway in A. thaliana and the genes involved are depicted
One molecular basis of the spermidine requirement for eukaryotic viability is that spermidine is a precursor of the unusual amino acid hypusine. Hypusine is involved in post-translational modification of the epsilon-amino group of one specific lysine residue of the eukaryotic translational initiation factor 5A (eIF5A) (Park 2006). In contrast with spermidine requirements, an acl5/spms double knockout mutant plant that cannot produce spermine grows well and sets fertile seeds (Imai et al. 2004a). Collectively, these data indicate that putrescine and spermidine are essential for plant embryogenesis and possibly for further growth, but that spermine is not essential for normal growth in Arabidopsis (Fig. 4).
These results raise the question of what role spermine has in growth and development. Interestingly, the above mentioned mice lacking spermine synthase have a variety of defects, including severe growth retardation, inner ear abnormalities, very short life spans, deafness, sterility, and neurological defects reflecting to abnormal behavior such as circling (Lorenz et al. 1998; Mackintosh and Pegg 2000). It has also been reported that Snyder–Robinson syndrome, an X-linked mental retardation disorder, is caused by a deficiency in spermine synthase (Cason et al. 2003). It is likely, therefore, that spermine is required not only for growth (Wang et al. 2004) but also for functionality of organs such as the brain in mammals. It is possible that the role of spermine in growth can be substituted by spermidine, whereas spermine is essential for organ functionality. This topic will be touched upon later in this review.
Polyamines can act as intracellular growth factors by increasing the rate of cell growth. The molecular mechanism underlying polyamine-enhanced growth has been discovered gradually. Igarashi et al. proposed a “polyamine modulon” theory to explain how polyamines enhance bacterial cell growth (Yoshida et al. 2004; Terui et al. 2004; Igarashi and Kashiwagi 2006): polyamines stimulate the synthesis of several key factors including oligopeptide binding protein (a periplasmic substrate-binding protein of the oligopeptide uptake system), adenylate cyclase, RNA polymerase sigma subunit (for transcription of stationary-phase genes), and several transcription factors. With the use of microarray analysis, these researchers further found that the expression of about 300 genes in E. coli are enhanced more than 2-fold by polyamines, and that 97 of those genes were under the control of transcription factors from the polyamine modulon (Terui et al. 2004).
Polyamines in plant survival
Mutants of E. coli and yeast strains with reduced levels of polyamines are more sensitive to oxidative damage (Chattopadhyay et al. 2003, 2006; Jung et al. 2003). Polyamines protect DNA from damage caused by alkylating reagents and from free radical attack in mammals (Ha et al. 1998; Mackintosh and Pegg 2000). Rider et al. (2007) used spermine synthase-deficient mouse fibroblast cells to demonstrate the protective potential of polyamines against oxidative damage caused by H2O2. A recent review summarizes that polyamines have a protective role against various stresses, including oxidative, acidic, osmotic, and neuronal stresses, and pathogen attacks (Rhee et al. 2007).
Plant polyamines frequently accumulate in response to abiotic and biotic stresses (Bouchereau et al. 1999; Urano et al. 2003; Walters 2003a, b). There is an extensive literature describing the correlation of changes in polyamine levels and physiological perturbations and on the protective effect of polyamines on environmental stresses (see reviews Alcázar et al. 2006; Groppa and Benavides 2007; Liu et al. 2007, and references therein). It was initially observed that exogenously applied polyamines protect plants from abiotic stress (Chattopadhayay et al. 2002). The improvement of stress tolerance in the transgenic plants overexpressing polyamine biosynthetic genes was then demonstrated; for instance, overexpression of Cucurbita ficifolia SPDS gene confers multi-stress tolerance to Arabidopsis and sweet potato (Kasukabe et al. 2004, 2006). Rice plants overexpressing Datura stramonium ADC gene are tolerant to drought (Capell et al. 2004). Even in woody plants, the enhancement of polyamine synthesis via a transgenic approach confers multi-stress tolerance (Wen et al. 2007). Data obtained by loss-of-function experiments also support the above notions; i.e., deletion of Arabidopsis ADC2 results in host plants that are more sensitive to salt stress relative to control plants (Urano et al. 2004). The Arabidopsis acl5/spms mutant plant, which is unable to produce spermine, is hypersensitive to salt and drought stresses relative to wild type plant (Yamaguchi et al. 2006, 2007). These stress-sensitive phenotypes were reversed by the addition of exogenous polyamines, putrescine in the former case and spermine in the latter.
Curiously, the acl5/spms mutant plant is hypersensitive to KCl, but no difference in sensitivity to MgCl2 or high osmoticum is observed. This mutant plant is also Ca2+ deficient (Yamaguchi et al. 2006). The overall phenotypes of ion sensitivity and Ca2+ deficiency were similar to those of transgenic plants overexpressing AtGluR2 and CAX1, which encode a Ca2+ influx channel at the plasma membrane and a vacuolar Ca2+/H+ exchanger, respectively (Hirschi 1999; Kim et al. 2001). The acl5/spms plant also loses more water compared to control plants, due to a failure of stomatal closure upon onset of drought (Yamaguchi et al. 2007). It is known that changes in free Ca2+ concentrations in the cytoplasm of guard cells are involved in stomatal aperture/closure (Ward and Schroeder 1994; Allen and Sanders 1996; Rob et al. 2005). Taken together, these results suggest that the absence of spermine may cause deregulation of Ca2+ trafficking, resulting in a lack of proper adaptation to high NaCl or drought stresses (Kusano et al. 2007a, b). As mentioned above, it is proven that ACL5 encodes thermospermine synthase (Knott et al. 2007). Therefore, the experiments using the spms single mutant plant are currently underway.
Consistent with the above data, it has been reported that polyamines including spermine inhibit stomatal opening and induce closure by regulating KAT1-like voltage-dependent inward K+ channels of Vicia faba guard cells (Liu et al. 2000). Recently, Shabala et al. (2007) reported that polyamines prevent NaCl-induced K+ efflux from pea leaf mesophyll cells by the inhibition of non-selective cation channels. Zhao et al. (2007) showed that polyamines improve barley root K+/Na+ homeostasis by regulating ion channel activities. It is plausible that one of the tasks of stress-induced polyamines is to modulate the activity of a certain set of ion channels to adapt ionic fluxes in response to environmental changes. To substantiate the above hypothesis, concerted research that includes many areas of science, including electrophysiology, genetics, and molecular biology, will be required.
Plant polyamines are also proposed to play a defensive role during biotic stress responses (Walters 2003a, b). One defense mechanism, the hypersensitive response (HR), which consists of rapid cell death at the sight of pathogen entry, typically develops in the interaction between tobacco mosaic virus (TMV) and N resistance gene carrying Nicotiana tabacum. Enhanced polyamine synthesis and accumulation was reported in this interaction (Torrigiani et al. 1997; Marini et al. 2001). Using a similar experimental system, it was discovered that apoplast-accumulated spermine is an endogenous inducer of the expression of the pathogenesis-related (PR) protein-genes (Yamakawa et al. 1998). Exogenous application of spermine to tobacco leaves, which mimics a situation of apoplastic accumulation upon incompatible pathogen attacks, induces a pathway involving mitochondrial dysfunction, activation of mitogen-activated protein kinases, increased expression of HR marker genes (including transcription factors), and caused defense responses and HR-like cell death (Takahashi et al. 2003, 2004a, b; Uehara et al. 2005; Mitsuya et al. 2007). It is likely, therefore, that spermine transmits a signal to activate defense pathways against pathogens (Takahashi et al. 2003). This pathway has been designated the “spermine-signaling pathway”.
To lead to mitochondrial malfunction, at least two events, activation of Ca2+ influx and the production of reactive oxygen species, are prerequisite (Takahashi et al. 2003) (Fig. 5). Mitochondrial involvement in biotic stress responses and programmed cell death has been reviewed (Amirsadeghi et al. 2007). Apolastic spermine may directly affect cation channel(s) and/or be catabolized by polyamine oxidase. These combined reactions would result in changes in K+/Ca2+ trafficking and in generation of H2O2, both of which may trigger the downstream reaction of the spermine-signaling pathway (Kusano et al. 2007a). Polyamine catabolism in plants is associated with cell survival and cell growth, such as cell wall stiffening and lignification (Šebela et al. 2001; Cona et al. 2006). Yoda et al. (2003, 2006) demonstrated that HR cell death caused by TMV infection or cryptogein, an oomycete-originated elicitor, is partly mediated by H2O2 production through polyamine catabolism. These authors suggest that the polyamine substrate for H2O2 production is spermidine, since during HR elicitation spermidine but not spermine accumulates in the apoplasts. The idea that plants employ polyamine-catabolized H2O2 as a defensive tool upon exposure to biotic stresses has been reviewed by other groups (Cona et al. 2006; Walters 2003a, b).
A hypothetical role for spermine in plant survival against pathogens
Tobacco ZFT1 is a spermine-responsive gene encoding a zinc-finger type transcriptional repressor, and is positioned in the spermine-signaling pathway (Uehara et al. 2005). Tobacco plants overexpressing ZFT1 are more resistant to TMV compared with control plants (Uehara et al. 2005). Transgenic pine plants overexpressing the gene CaPF1, which encodes the ERF (ethylene responsive factor)/AP2-type transcription factor, have dramatically increased tolerances to drought, freezing, and salt stress (Tang et al. 2005). Curiously, in control pine plants, the levels of polyamines decrease upon exposure to stresses, whereas in the transgenics plants the polyamine levels remain constant. This result suggests that enhanced stress tolerance in transgenic pines expressing CaPF1 is associated with polyamine biosynthesis (Tang et al. 2007). These studies suggest that the expressional modulation of key factors which are positioned upstream of polyamine biosynthesis or the polyamine-induced signaling pathway could make the host organisms resistant to abiotic and biotic stresses.
Tun et al. (2006) reported that spermine and spermidine are potent inducers of nitric oxide (NO) in Arabidopsis, but putrescine and its biosynthetic precursor arginine are not. NO has the potential to inhibit oxidative phosphorylation in plant mitochondria (Yamasaki et al. 2001) and plays an important signaling role in plant–pathogen interactions (Romero-Puertas et al. 2004); therefore, further research on the role of polyamine-mediated NO production is justified (Yamasaki and Cohen 2006).
Rhee et al. (2007) mentioned that the basic principle underlying polyamine adaptive responses appears to be shared by the prokaryotic stringent response and the eukaryotic unfolded protein response (UPR). UPR is triggered when unfolded proteins and uncharged tRNAs accumulate in the endoplasmic reticulum (ER) due to ER stress or nutrient starvation. Cap-dependent translation of many mRNAs is suppressed and the expression of a certain set of genes including the luminal binding protein gene BiP is induced. The underlying mechanisms of UPR in yeasts and mammals have been well researched (Rutkowski and Kaufman 2004), although those in plants have not (Kamauchi et al. 2005; Urade 2007).
Recently, Iwata and Koizumi (2005) reported that AtbZIP60, which belongs to a basic leucine zipper protein family, is a key transcription factor involved in Arabidopsis UPR. In relation to this, we have identified NtbZIP60, an orthologue of AtbZIP60, via screening of the spermine-responsive genes in tobacco (Tateda et al. 2008). We also confirmed that AtbZIP60 is responsive to spermine and that some of the UPR-responsive genes are modulated by spermine (Y. Takahashi, unpublished data). This indicates that the cross-talk between polyamine function in survival and the UPR/stringent response warrants further investigation.
As described in this section, polyamines are involved in the defense response during interaction of resistant NN tobacco plants and TMV. By means of this interaction another effect of polyamines has been investigated. Polyamines can affect the conformation and function of specific proteins, by forming covalent linkages mediated by the activity of transglutaminase (TGase, EC 2.3.2.13) enzymes (Griffin et al. 2002). TGases catalyze the formation of a covalent bond between a free amine group, like protein-bound lysine and the γ-carboxamide group of protein-bound glutamine resulting in protein cross-links. Polyamines also act as physiological substrates. The terminal amino group binds one or two glutamyl residues, producing either mono-(γ-glutamyl)-polyamines or bis-(γ-glutamyl)-polyamines (Folk et al. 1980). TGase activity has also been identified in plants (Della Mea et al. 2004). It has now been shown that TGase activity is enhanced during the HR in tobacco/TMV interaction and that mono- and bis-glutamyl-polyamines were formed (Del Duca et al. 2007). The authors suggest that the latter polyamine derivatives may either induce conformational changes or intra- or intermolecular cross-links of proteins. Further investigations will show what kind of role these modified polyamines play in the defense response of plants.
Perspectives
Because of the pharmaceutical interest, intense research on polyamines has been done in animal fields. In bacteria, a variety of phenomena have been reported that confirm the importance of these molecules. As these ‘mysterious’ molecules are versatile players, most plant biologists have put them aside. But currently, as summarized in this review, their importance for growth and survival has been appreciated in plants. However, the knowledge on plant polyamines is still behind compared to the one of animals and prokaryotes. For example, the molecules involved in intracellular, extracellular and intercellular transport of polyamines remain unknown. Are there any mechanisms to regulate the polyamine levels in plants except the translational control of SAMDC mRNA? The cross-talk between the spermine-signal pathway and the signaling pathways triggered by plant hormones has not been examined well. To understand the role of polyamines in growth and differentiation, a plant version of the ‘polyamine modulon’ has to be clarified. To get a deeper insight into the defensive role of polyamines in abiotic and biotic stresses, investigations on how polyamines modulate ion channels will be required.
Intensive research using many modern biological disciplines including electrophysiology, genetics, molecular biology and metabolomics on the functions of polyamines in plants will lead to fruitful results in basic and applied plant sciences.
References
Alcázar R, Marco F, Cuevas JC, Patron M, Ferrando A, Carrasco P, Tiburcio AF, Altabella T (2006) Involvement of polyamines in plant response to abiotic stress. Biotechnol Lett 28:1867–1876
Allen GJ, Sanders D (1996) Control of ionic currents guard cell vacuoles by cytosolic and luminal calcium. Plant J 10:1055–1069
Amirsadeghi S, Robson CA, Vanlerberghe GC (2007) The role of the mitochondrion in plant responses to biotic stress. Physiol Plant 129:253–266
Bagni N, Tassoni A (2001) Biosynthesis, oxidation and conjugation of aliphatic polyamines in higher plants. Amino Acids 20:301–317
Bell E, Malmberg RL (1990) Analysis of a cDNA encoding arginine decarboxylase from oat reveals similarity to the Escherichia coli arginine decarboxylase and evidence of protein processing. Mol Gen Genet 224:431–436
Belting M, Mani K, Jönsson M, Cheng F, Sandgren S, Jonsson S, Ding K, Delcros J-G, Fransson LÅ (2003) Glypican-1 is a vehicle for polyamine uptake in mammalian cells. J Biol Chem 278:47181–47189
Bolenius FN, Seiler N (1981) Acetylderivatives as intermediates in polyamine catabolism. Int J Biochem 13:287–292
Bouchereau A, Aziz A, Larher F, Martin-Tanguy J (1999) Polyamines and environmental challenges: recent development. Plant Sci 140:103–125
Brazeau BJ, Johnson BJ, Wilmot CM (2004) Copper-containing amine oxidases. Biogenesis and catalysis; a structural perspective. Arch Biochem Biophys 428:22–31
Brieger L (1885) Ueber Spaltungsprodukte der Bacterien, Zweite Mittheilung. Zeitschr Physiol Chem 9:1–7
Brüggemann L, Pottosin I, Schönknecht G (1998) Cytoplasmic polyamines block the fast-activating vacuolar cation channel. Plant J 16:101–105
Brüggemann L, Pottosin I, Schönknecht G (1999) Selectivity of the fast activating vacuolar cation channel. J Exp Bot 50:873–876
Canellakis ES, Paterakis AA, Huang S-C, Panagiotidis CA, Kyriakidis DA (1993) Identification, cloning, and nucleotide sequencing of the ornithine decarboxylase antizyme gene of Escherichia coli. Proc Natl Acad Sci USA 90:7129–7133
Capell T, Bassie L, Christou P (2004) Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc Natl Aca Sci USA 101:9909–9914
Casero RA Jr, Marton LJ (2007) Targeting polyamine metabolism and function in cancer and other hyperproliferative diseases. Nat Rev Drug Discov 6:373–390
Casero RA Jr, Pegg AE (1993) Spermidine/spermine N1-acetyltransferase—the turning point in polyamine metabolism. FASEB J 7:653–661
Cason AL, Ikeguchi Y, Skinner C, Wood TC, Holden KR, Lubs HA, Martinez F, Simensen RJ, Stevenson RE, Pegg AE, Schwartz CE (2003) X-linked spermine synthase gene (SMS) defect: the first polyamine deficiency syndrome. Eur J Hum Genet 11:937–944
Cervelli M, Cona A, Angelini R, Polticelli F, Federico R, Mariottini P (2001) A barley polyamine oxidase isoform with distinct structural features and subcellular localization. Eur J Biochem 268:3816–3830
Cervelli M, Polticelli F, Federico R, Mariottini P (2003) Heterologous expression and characterization of mouse spermine oxidase. J Biol Chem 278:5271–5276
Cervelli M, Caro OD, Penta AD, Angelini R, Federico R, Vitale A, Mariottini P (2004) A novel C-terminal sequence from barley polyamine oxidase is a vacuolar sorting signal. Plant J 40:410–418
Cervelli M, Bianchi M, Cona A, Crosatti C, Stanca M, Angelini R, Federico R, Mariottini P (2006) Barley polyamine oxidase isoforms 1 and 2, a peculiar case of gene duplication. FEBS J 273:3990–4002
Chattopadhayay MK, Tiwari BS, Chattopadhayay G, Bose A, Sengupta DN, Ghosh B (2002) Protective role of exogenous polyamines on salinity-stressed rice (Oryza sativa) plants. Physiol Plant 116:192–199
Chattopadhyay MK, Tabor CW, Tabor H (2003) Polyamines protect Escherichia coli cells from the toxic effect of oxygen. Proc Natl Acad Sci USA 100:2261–2265
Chattopadhyay MK, Tabor CW, Tabor H (2006) Polyamine deficiency leads to accumulation of reactive oxygen species in a spe2Delta mutant of Saccharomyces cerevisiae. Yeast 23:751–761
Childs AC, Metha DJ, Gerner EW (2003) Polyamine-dependent gene expresssion. Cell Mol Life Sci 60:1394–1406
Clay NK, Nelson T (2005) Arabidopsis thickvein mutation affects vein thickness and organ vascularization, and resides in a provascular cell-specific spermine synthase involved in vein definition and in polar auxin transport. Plant Physiol 138:767–777
Cohen SS (1998) A guide to the polyamines. Oxford University Press, New York
Cona A, Rea G, Angelini R, Federico R, Tavladoraki P (2006) Functions of amine oxidases in plant development and defence. Trends Plant Sci 11:80–88
Culhane JC, Cole PA (2007) LSD1 and the chemistry of histone demethylation. Curr Opin Chem Biol 11:561–568
Davenport R (2002) Glutamate receptors in plants. Ann Bot 90:549–557
Del Duca S, Betti L, Trebbi G, Serafini-Fracassini D, Torrigiani P (2007) Transglutaminase activity changes during the hypersensitive reaction, a typical defense response of tobacco NN plants to TMV. Physiol Plant 131:241–250
Della Mea M, Caparro`s-Ruiz D, Claparols I, Serafini-Fracassini D, Rigau J (2004) AtPng1p. The first plant transglutaminase. Plant Physiol 135:2046–2054
DiTomaso JM, Hart JJ, Kochian LV (1992) Transport kinetics and metabolism of exogenously applied putrescine in roots of intact maize seedlings. Plant Physiol 98:611–620
Dobrovinskaya OR, Muñiz J, Pottosin I (1999a) Inhibition of vacuolar ion channels by polyamines. J Membr Biol 167:127–140
Dobrovinskaya OR, Muñiz J, Pottosin I (1999b) Asymmetric block of the plant vacuolar Ca2+-permeable channel by organic cations. Eur Biophys J 28:552–563
Dudley HW, Rosenheim O, Starling WW (1926) The chemical constitution of spermine. III. Structure and synthesis. Biochem J 20:1082–1094
Dudley HW, Rosenheim O, Starling WW (1927) The constitution and synthesis of spermidine, a newly discovered base isolated from animal tissues. Biochem J 21:97–103
Dufe VT, Lürsen K, Eschbach ML, Haider N, Karlberg T, Walter RD, Al-Karadaghi S (2005) Cloning, expression, characterization and three-dimensional structure determination of Caenorhabditis elegans spermidine synthase. FEBS Lett 579:6037–6043
Federico R, Cona A, Angelini R, Schininà ME, Giartosio A (1990) Characterization of maize polyamine oxidase. Phytochemistry 29:2411–2414
Ficker E, Taglialatela M, Wible BA, Henly CM, Brown AM (1994) Spermine and spermidine as gating molecules for inward rectifier K+ channels. Science 266:1068–1072
Folk JE, Park MH, Chung SI, Schrode J, Lester EP, Cooper HL (1980) Polyamines as physiological substrates for transglutaminases. J Biol Chem 255:3695–3700
Franceschetti M, Hanfrey C, Scaramagli S, Torrigiani P, Bagni N, Burtin D, Michael AJ (2001) Characterization of monocot and dicot plant S-adenosyl-l-methionine decarboxylase gene families including identification in the mRNA of a highly conserved pair of upstream overlapping open reading frames. Biochem J 353:403–409
Garufi A, Visconti S, Camoni L, Aducci P (2007) Polyamines as physiological regulators of 14-3-3 interaction with the plant plasma membrane H+-ATPase. Plant Cell Physiol 48:434–440
Ge C, Cui X, Wang Y, Hu Y, Fu Z, Zhang D, Cheng Z, Li J (2006) BUD2, encoding an S-adenosylmethionine decarboxylase, is required for Arabidopsis growth and development. Cell Res 16:446–456
Griffin M, Casadio R, Bergamini CM (2002) Transglutaminases: nature’s biological glues. Biochem J 368:377–396
Groppa MD, Benavides MP (2007) Polyamines and abiotic stress: recent advances. Amino Acids 34:35–45
Ha HC, Sirosoma NS, Kuppusamy P, Zweiler JL, Woster PM, Casero RA (1998) The natural polyamine spermine functions directly as a free radical scavenger. Proc Natl Acad Sci USA 95:11140–11145
Hamana K, Niitsu M, Samejima K, Itoh T, Hamana H, Shinozawa T (1998) Polyamines of thermophilic eubacteria belonging to the genera Thermotoga, Thermodesulfovibrio, Thermoleophilum, Thermus, Rhodothermus and Meiothermus, and the thermophilic archaebacteria belonging to the genera Aeropyrum, Picrophilus, Methanobacterium and Methanococcus. Microbios 94:7–21
Hamasaki-Katagiri N, Katagiri Y, Tabor CW, Tabor H (1998) Spermine is not essential for growth of Saccharomyces cerevisiae: identification of the SPE4 gene (spermine synthase) and characterization of a spe4 deletion mutant. Gene 210:195–201
Hanfrey C, Sommer S, Mayer MJ, Burtin D, Michael AJ (2001) Arabidopsis polyamine biosynthesis: absence of ornithine decarboxylase and the mechanism of arginine decarboxylase activity. Plant J 27:551–560
Hanfrey C, Franceschetti M, Mayer MJ, Illingworth C, Michael AJ (2002) Abrogation of upstream open reading frame-mediated translational control of a plant S-adenosylmethionine decarboxylase results in polyamine disruption and growth perturbations. J Biol Chem 277:44131–44139
Hanfrey C, Franceschetti M, Mayer MJ, Illingworth C, Elliot K, Collier M, Thompson B, Perry B, Michael AJ (2003) Translational regulation of the plant S-adenosylmethionine decarboxylase. Biochem Soc Trans 31:424–427
Hanfrey C, Elliot KA, Franceschetti M, Mayer MJ, Illingworth C, Michael AJ (2005) A dual upstream open reading frame-based autoregulatory circuit controlling polyamine-responsive translation. J Biol Chem 280:39229–39237
Hanzawa Y, Takahashi T, Komeda Y (1997) ACL5: an Arabidopsis gene required for internodal elongation after flowering. Plant J 12:863–874
Hanzawa Y, Takahashi T, Michael AJ, Burtin D, Long D, Pineiro M, Coupland G, Komeda Y (2000) ACAULIS5, an Arabidopsis gene required for stem elongation, encodes a spermine synthase. EMBO J 19:4248–4256
Hanzawa Y, Imai A, Michael AJ, Komeda Y, Takahashi T (2002) Characterization of the spermidine synthase-related gene family in Arabidopsis thaliana. FEBS Lett 527:176–180
Hayashi S, Murakami Y, Matsufuji S (1996) Ornithine decarboxylase antizyme: a novel type of regulatory protein. Trends Biochem Sci 21:27–30
He Y, Suzuki T, Kashiwagi K, Igarashi K (1994) Antizyme delays the restoration by spermine of growth of polyamine-deficient cells through its negative regulation of polyamine transport. Biochem Biophys Res Commun 203:608–614
Heim WG, Sykes KA, Hildreth SB, Sun J, Lu R-H, Jelesko JG (2007) Cloning and characterization of a Nicotiana tabacum methylputrescine oxidase transcript. Phytochemistry 68:454–463
Hibi N, Higashiguchi S, Hashimoto T, Yamada Y (1994) Gene expression in tobacco low-nicotine mutants. Plant Cell 6:723–735
Hirschi KD (1999) Expression of Arabidopsis CAX1 in tobacco: altered calcium homeostasis and increased stress sensitivity. Plant Cell 11:2113–2122
Igarashi K (2006) Physiological functions of polyamines and regulation of polyamine contents in cells. Yakugaku Zasshi 126:455–471 in Japanese
Igarashi K, Kashiwagi K (1999) Polyamine transport in bacteria and yeast. Biochem J 344:633–642
Igarashi K, Kashiwagi K (2000) Polyamines: mysterious modulators of cellular functions. Biochem Biophys Res Commun 271:559–564
Igarashi K, Kashiwagi K (2006) Polyamine modulon in Escherichia coli: genes involved in the stimulation of cell growth by polyamines. J Biochem (Tokyo) 139:11–16
Imai A, Akiyama T, Kato T, Sato S, Tabata S, Yamamoto KT, Takahashi T (2004a) Spermine is not essential for survival of Arabidopsis. FEBS Lett 556:148–152
Imai A, Matsuyama T, Hanzawa Y, Akiyama T, Tamaoki M, Saji H, Shirano Y, Kato T, Hayashi H, Shibata D, Tabata S, Komeda Y, Takahashi T (2004b) Spermidine synthase genes are essential for survival of Arabidopsis. Plant Physiol 135:1565–1573
Imai A, Hanzawa Y, Komura M, Yamamoto KT, Komeda Y, Takahashi T (2006) The dwarf phenotype of the Arabidopsis acl5 mutant is suppressed by a mutation in an upstream ORF of a bHLH gene. Development 133:3575–3585
Ivanov IP, Matsufuji S, Murakami Y, Gesteland RF, Atkins JF (2000) Conservation of polyamine regulation by translational frameshifting from yeast to mammals. EMBO J 19:1907–1917
Iwata Y, Koizumi N (2005) An Arabidopsis transcription factor, AtbZIP60, regulates the endoplasmic reticulum stress response in a manner unique to plants. Proc Natl Acad Sci USA 102:5280–5285
Janowitz T, Kneifel H, Piotrowski M (2003) Identification and characterization of plant agmatine iminohydrolase, the last missing link in polyamine biosynthesis of plants. FEBS Lett 544:258–261
Jiang D, Yang W, He Y, Amasino RA (2007) Arabidopsis relatives of the human lysine-specific demethylase1 repress the expression of FWA and Flowering Locus C and thus promote the floral transition. Plant Cell 19:2975–2987
Johnson TD (1996) Modulation of channel function by polyamines. Trends Pharmacol Sci 17:22–27
Jung IL, Oh TJ, Kim IG (2003) Abnormal growth of polyamine-deficient Escherichia coli mutant is partially caused by oxidative stress-induced damage. Arch Biochem Biophys 418:125–132
Kamauchi S, Nakatani H, Nakano C, Urade R (2005) Gene expression in response to endoplasmic reticulum stress in Arabidopsis thaliana. FEBS J 272:3461–3476
Kameji T, Pegg AE (1987) Effect of putrescine on the synthesis of S-adenosylmethionine decarboxylase. Biochem J 243:285–288
Kamio Y, Itoh Y, Terawaki Y, Kusano T (1981) Cadaverine is covalently linked to peptidoglycan in Selenomonas ruminantium. J Bacteriol 145:122–128
Kashiwagi K, Taneja SK, Liu TY, Tabor CW, Tabor H (1990) Spermidine biosynthesis in Saccharomyces cerevisiae. J Biol Chem 265:22321–22328
Kasukabe Y, He L, Nada K, Misawa S, Ihara I, Tachibana S (2004) Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol 45:712–722
Kasukabe Y, He L, Watakabe Y, Otani M, Shimada T, Tachibana S (2006) Improvement of environmental stress tolerance of sweet potato by introduction of genes for spermidine synthase. Plant Biotechnol 23:75–83
Katoh A, Shoji T, Hashimoto T (2007) Molecular cloning of N-methylputrescine oxidase from tobacco. Plant Cell Physiol 48:550–554
Kim SA, Kwak JM, Jae SK, Wang MH, Nam HG (2001) Overexpression of the AtGluR2 gene encoding an Arabidopsis homolog of mammalian glutamate receptors impairs calcium utilization and sensitivity to ionic stress in transgenic plants. Plant Cell Physiol 42:74–84
Kitashiba H, Hao Y-J, Honda C, Moriguchi T (2005) Two types of spermine synthase gene: MdACL5 and MdSPMS are differentially involved in apple fruit development and cell growth. Gene 361:101–111
Knott JM, Römer P, Sumper M (2007) Putative spermine synthases from Thalassiosira pseudonana and Arabidopsis thaliana synthesize thermospermine rather than spermine. FEBS Lett 581:3081–3086
Korolev S, Ikeguchi Y, Skarina T, Beasley S, Arrowsmith C, Edwards A, Joachimiak A, Pegg AE, Savchenko A (2002) The crystal structure of spermidine synthase with a multisubstrate adduct inhibitor. Nat Struct Biol 9:27–31
Kumar A, Altabella T, Taylor M, Tiburcio AF (1997) Recent advances in polyamine research. Trends Plant Sci 2:124–130
Kurihara S, Oda S, Kato K, Kim HG, Koyanagi T, Kumagai H, Suzuki H (2005) A novel putrescine utilization pathway involves γ-glutamylated intermediates of Escherichia coli K-12. J Biol Chem 280:4602–4608
Kusano T, Yamaguchi K, Berberich T, Takahashi Y (2007a) Advances in polyamine research in 2007. J Plant Res 120:345–350
Kusano T, Yamaguchi K, Berberich T, Takahashi Y (2007b) The polyamine spermine rescues Arabidopsis from salinity and drought stresses. Plant Signal Behav 2:250–251
Kusunoki S, Yasumasu I (1978) Inhibitory effect of α-hydrazinoornithine on egg cleavage in sea urchin eggs. Dev Biol 67:336–345
Ladenburg A (1886) Über die Identität des Cadaverin mit dem Pentamethyldiamin. Ber Dtsch Chem Ges 19:2585–2586
Ladenburg A, Abel J (1888) Über das Aethylenimin (Spermin?). Ber Dtsch Chem Ges 21:758–766
Landry J, Sternglanz R (2003) Yeast Fms1 is a FAD-utilizing polyamine oxidase. Biochem Biophys Res Commun 303:771–776
Leete E (1980) The alkaloids. In: Bell EA, Charwood BV (eds) Encyclopedia of plant physiology. New series, vol 8. Springer, Berlin, pp 65–91
Li Y-F, Hess S, Pannell LK, Tabor CW, Tabor H (2001) In vivo mechanism-based inactivation of S-adenosylmethionine decarboxylases from Escherichia coli, Salmonella typhimurium, and Saccharomyces cerevisiae. Proc Natl Acad Sci USA 98:10578–10583
Li J, Doyle KM, Tatlisumak T (2007) Polyamines in the brain: distribution, biological interactions, and their potential therapeutic role in brain ischaemia. Curr Med Chem 14:1804–1813
Lioliou EE, Kyriakidis DA (2004) The role of bacterial antizyme: from an inhibitory protein to AtoC transcriptional regulator. Microb Cell Fact 3:8–16
Liu K, Fu H, Bei Q, Luan S (2000) Inward potassium channel in guard cells as a target for polyamine regulation of stomatal movements. Plant Physiol 124:1315–1326
Liu J-H, Kitashiba H, Wang J, Ban Y, Moriguchi T (2007) Polyamines and their ability to provide environmental stress tolerance to plants. Plant Biotechnol 24:117–126
Lopatin AN, Makhina EN, Nichols CG (1994) Potassium channel block by cytoplasmic polyamines as the mechanism of intrinsic rectification. Nature 372:366–369
Lorenz B, Francis F, Gempel K, Boddrich A, Josten M, Schmahl W, Schmidt J, Lehrach H, Meitinger T, Strom TM (1998) Spermine deficiency in Gy mice caused by deletion of the spermine synthase gene. Hum Mol Genet 7:541–547
Lu Z, Ding L (1999) Blockage of a retinal cGMP-gated channel by polyamines. J Gen Physiol 113:35–43
Mackintosh CA, Pegg AE (2000) Effect of spermine synthase deficiency on polyamine biosynthesis and content in mice and embryonic fibroblasts, and the sensitivity of fibroblasts to 1,3-bis-(2-chloroethyl)-N-nitrosourea. Biochem J 351:439–447
Malmberg RL, Watson MB, Galloway GL, Yu W (1998) Molecular genetic analyses of plant polyamines. Crit Rev Plant Sci 17:199–224
Mangold U (2005) The antizyme family: polyamines and beyond. IUBMB Life 57:671–676
Marini F, Betti L, Scaramagli S, Biodi S, Torrigiani P (2001) Polyamine metabolism is upregulated in response to tobacco mosaic virus in hypersensitive, but not in susceptible, tobacco. New Phytol 149:301–309
Matsufuji S, Matsufuji T, Miyazaki Y, Murakami Y, Atkins JF, Gesteland RF, Hayashi S (1995) Autoregulatory frameshifting in decoding mammalian ornithine decarboxylase antizyme. Cell 80:51–60
Matto AK, Sobolev AP, Neelam A, Goyal RK, Handa AK, Segre AL (2006) Nuclear magnetic resonance spectroscopy-based metabolite profiling of transgenic tomato fruit engineered to accumulate spermidine and spermine reveals enhanced anabolic and nitrogen–carbon interactions. Plant Physiol 142:1759–1770
Mehta RA, Cassol T, Li N, Ali N, Handa AK, Matto AK (2002) Engineered polyamine accumulation in tomato enhances phytonutrient content, juice quality, and vine life. Nat Biotechnol 20:613–618
Michael AJ, Furze JM, Rhodes MJ, Burtin D (1996) Molecular cloning and functional identification of a plant ornithine decarboxylase cDNA. Biochem J 314:241–248
Mitchell JL, Judd GG, Bareyal-Leyser A, Ling SY (1994) Feedback repression of polyamine transport is mediated by antizyme in mammalian tissue-culture cells. Biochem J 299:19–22
Mitsuya Y, Takahashi Y, Uehara Y, Berberich T, Miyazaki A, Takahashi H, Kusano T (2007) Identification of a novel Cys2/His2-type zinc finger protein as a component of a spermine-signaling pathway in tobacco. J Plant Physiol 164:785–793
Møller SG, McPherson MJ (1998) Developmental expression and biochemical analysis of the Arabidopsis atao1 gene encoding an H2O2-generating diamine oxidase. Plant J 13:781–791
Oliver D, Baukrowitz T, Fakler B (2000) Polyamines as gating molecules of inward-rectifier K+ channels. Eur J Biochem 267:5824–5829
Oshima T (2007) Unique polyamines produced by an extreme thermophile, Thermus thermophilus. Amino Acids 33:367–372
Panicot M, Minguet EG, Ferrando A, Alcazar R, Blazquez MA, Carbonell J, Altabella T, Koncz C, Tiburcio AF (2002) A polyamine metabolon involving aminopropyl transferase complexes in Arabidopsis. Plant Cell 14:2539–2551
Park MH (2006) The post-translational synthesis of a polyamine-derived amino acid, hypusine, in the eukaryotic translation initiation factor 5A (eIF5A). J Biochem (Tokyo) 139:161–169
Pegg AE (1986) Recent advances in the biochemistry of polyamines in eukaryotes. Biochem J 234:249–262
Pegg AE (2006) Regulation of ornithine decarboxylase. J Biol Chem 281:14529–14532
Piotrowski M, Janowitz T, Kneifel H (2003) Plant C–N hydrolase and the identification of plant N-carbamoylputrescine amidohydrolase involved in polyamine biosynthesis. J Biol Chem 278:1708–1712
Pistocchi R, Bagni N, Creus JA (1987) Polyamine uptake in carrot cell cultures. Plant Physiol 84:374–380
Rhee HJ, Kim E-J, Lee JK (2007) Physiological polyamines: simple primordial stress molecules. J Cell Mol Med 11:685–703
Rider JE, Hacker A, Mackintosh CA, Pegg AE, Woster PM, Casero RA Jr (2007) Spermine and spermidine mediate protection against oxidative damage caused by hydrogen peroxide. Amino Acids 33:231–240
Rob M, Roelfsema G, Hedrich R (2005) In the light of stomatal opening: new insights into ‘the Watergate’. New Phytol 167:665–691
Romero-Puertas MC, Perazzolli M, Zago ED, Delledonne M (2004) Nitric oxide signalling functions in plant–pathogen interactions. Cell Microbiol 6:795–803
Ruan H, Shantz LM, Pegg AE, Morris DR (1996) The upstream open reading frame of the mRNA encoding S-adenosylmethionine decarboxylase is a polyamine-responsive translational control element. J Biol Chem 271:29576–29582
Rutkowski DT, Kaufman RJ (2004) A trip to the ER: coping with stress. Trends Cell Biol 14:20–28
Saunder FR, Wallace HM (2007) Polyamine metabolism and cancer prevention. Biochem Soc Trans 35:364–368
Šebela M, Radová A, Angelini R, Tavladoraki P, Frébort I, Peč P (2001) FAD-containing polyamine oxidases: a timely challenge for researchers in biochemistry and physiology of plants. Plant Sci 160:197–207
Seiler N (2004) Catabolism of polyamines. Amino Acids 26:217–233
Seiler N, Raul F (2005) Polyamines and apoptosis. J Cell Mol Med 9:623–642
Seiler N, Raul F (2007) Polyamines and the intestinal tract. Crit Rev Clin Lab Sci 44:365–411
Seiler N, Duranton B, Raul F (2002) The polyamine oxidase inactivator MDL 72527. Prog Drug Res 59:1–40
Shabala S, Cuin TA, Pottosin I (2007) Polyamines prevent NaCl-induced K+ efflux from pea mesophyll by blocking non-selective cation channels. FEBS Lett 581:1993–1999
Shi Y, Lan F, Matson C, Mulligan P, Whetstine JR, Cole PA, Casero RA, Shi Y (2004) Histone demethylase mediated by the nuclear amine oxidase homolog LSD1. Cell 119:941–953
Soulet D, Gagnon B, Rivest S, Audette M, Poulin R (2004) A fluorescent probe of polyamine transport accumulates into intracellular acidic vesicles via a two-step mechanism. J Biol Chem 279:49355–49366
Tabor CW, Tabor H (1984) Polyamines. Annu Rev Biochem 53:749–790
Takahashi Y, Berberich T, Miyazaki A, Seo S, Ohashi Y, Kusano T (2003) Spermine signalling in tobacco: activation of mitogen-activated protein kinases by spermine is mediated through mitochondrial dysfunction. Plant J 36:820–829
Takahashi Y, Berberich T, Yamashita K, Uehara Y, Miyazaki A, Kusano T (2004a) Identification of tobacco HIN1 and two closely related genes as spermine-responsive genes and their differential expression during the Tobacco mosaic virus-induced hypersensitive response and during leaf- and flower-senescence. Plant Mol Biol 54:613–622
Takahashi Y, Uehara Y, Berberich T, Ito A, Saitoh H, Miyazaki A, Terauchi R, Kusano T (2004b) A subset of the hypersensitive response marker genes including HSR203J is downstream target of a spermine-signal transduction pathway in tobacco. Plant J 40:586–595
Tang W, Charles TM, Newton RJ (2005) Overexpression of the pepper transcription factor CaPF1 in transgenic Virginia pine (Pinus virginiana Mill.) confers multiple stress tolerance and enhances organ growth. Plant Mol Biol 59:603–617
Tang W, Newton RJ, Li C, Charles TM (2007) Enhanced stress tolerance in transgenic pine expressing the pepper CaPF1 gene is associated with the polyamine biosynthesis. Plant Cell Rep 26:115–124
Tateda C, Ozaki R, Onodera Y, Takahashi Y, Yamaguchi K, Berberich T, Koizumi N, Kusano T (2008) NtbZIP60, an endoplasmic reticulum-localized transcription factor, plays a role in defense response against bacterial pathogen in tobacco. J Plant Res (in press)
Tavladoraki P, Schininà ME, Cecconi F, Di Agostino S, Manera F, Rea G, Mariottini P, Federico R, Angelini R (1998) Maize polyamine oxidase: primary structure from protein and cDNA sequencing. FEBS Lett 426:62–66
Tavladoraki P, Rossi MN, Saccuti G, Perez-Amador MA, Polticelli F, Angelini R, Ferderico R (2006) Heterologous expression and biochemical characterization of a polyamine oxidase from Arabidopsis involved in polyamine back conversion. Plant Physiol 141:1519–1532
Terui Y, Higashi K, Taniguchi S, Shigemasa A, Nishimura K, Yamamoto K, Kashiwagi K, Ishihama A, Igarashi K (2004) Enhancement of the synthesis of RpoN, Cra, and H-NS by polyamines at the level of translation in Escherichia coli cultured with glucose and glutamate. J Bacteriol 189:2359–2368
Thomas T, Thomas TJ (2001) Polyamines in cell growth and cell death: molecular mechanisms and therapeutic applications. Cell Mol Life Sci 58:244–258
Thomas T, Thomas TJ (2003) Polyamine metabolism and cancer. J Cell Mol Med 7:113–126
Tipping AJ, McPherson MJ (1995) Cloning and molecular analysis of the pea seedling copper amine oxidase. J Biol Chem 270:16939–16946
Torrigiani P, Rabiti AL, Bortolotti C, Betti L, Marani F, Canova A, Bagni N (1997) Polyamine synthesis and accumulation in the hypersensitive response to TMV in Nicotiana tabacum. New Phytol 135:467–473
Tun NN, Santa-Catarina C, Begum T, Silveira V, Handro W, Floh EI, Scherer GF (2006) Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol 47:346–354
Uehara Y, Takahashi Y, Berberich T, Miyazak A, Takahashi H, Matsui K, Ohme-Takagi M, Saitoh H, Terauchi R, Kusano T (2005) Tobacco ZFT1, a transcriptional repressor with a Cys2/His2 type zinc finger motif that functions in spermine-signaling pathway. Plant Mol Biol 59:435–448
Umekage S, Ueda T (2006) Spermidine inhibits transient and stable ribosome subunit dissociation. FEBS Lett 580:1222–1226
Urade R (2007) Cellular response to unfolded proteins in the endoplasmic reticulum of plants. FEBS J 274:1152–1171
Urano K, Yoshiba Y, Nanjo T, Igarashi Y, Seki M, Sekiguchi F, Yamaguchi-Shinozaki K, Shinozaki K (2003) Characterization of Arabidopsis genes involved in biosynthesis of polyamines in abiotic stress responses and developmental stages. Plant Cell Environ 26:1917–1926
Urano K, Yoshiba Y, Nanjo T, Ito T, Yamaguchi-Shinozaki K, Shinozaki K (2004) Arabidopsis stress-inducible gene for arginine decarboxylase AtADC2 is required for accumulation of putrescine in salt tolerance. Biochem Biophys Res Commun 313:369–375
Urano K, Hobo T, Shinozaki K (2005) Arabidopsis ADC genes involved in polyamine biosynthesis are essential for seed development. FEBS Lett 579:1557–1564
van Leeuwenhoek A (1678) Observationes D. Anthonii Leeuwenhoek, de natis e semine genitali animalculis. Philos Trans R Soc Lond 12:1040–1043
von Udransky L, Baumann E (1888) Über die Identität des Putrescins und des Tetramethylendiamins. Ber Dtsch Chem Ges 21:2938–2941
Vujcic S, Diegelmann P, Bacchi CJ, Kramer DL, Porter CW (2002) Identification and characterization of a novel flavin-containing spermine oxidase of mammalian cell origin. Biochem J 367:665–675
Walden R, Cordeiro A, Tiburcio AF (1997) Polyamines: small molecules triggering pathways in growth and development. Plant Physiol 113:1009–1013
Wallace HM, Fraser AV, Hughes A (2003) A perspective of polyamine metabolism. Biochem J 376:1–14
Walters DR (2003a) Resistance to plant pathogens: possible roles for free polyamines and polyamine catabolism. New Phytol 159:109–115
Walters DR (2003b) Polyamines and plant disease. Phytochemistry 64:97–107
Wang Y, Devereux W, Woster PM, Stewart TM, Hacker A, Casero RA Jr (2001) Cloning and characterization of a human polyamine oxidase that is inducible by polyamine analogue exposure. Cancer Res 61:5370–5373
Wang X, Ikeguchi Y, McCloskey DE, Nelson P, Pegg AE (2004) Spermine synthesis is required for normal viability, growth, and fertility in the mouse. J Biol Chem 279:51370–51375
Ward JM, Schroeder JI (1994) Calcium-activated K+ channels and calcium-induced calcium release by slow vacuolar ion channels in guard cell vacuoles implicated in the control of stomatal closure. Plant Cell 6:669–683
Watson MW, Malmberg RL (1996) Regulation of Arabidopsis thaliana (L.) Heynh arginine decarboxylase by potassium deficiency stress. Plant Physiol 111:1077–1083
Watson MW, Yu W, Galloway GL, Malmberg RL (1997) Isolation and characterization of a second arginine decarboxylase cDNA from Arabidopsis (PGR97–114). Plant Physiol 114:1569
Wen XP, Pang XM, Matsuda N, Kita M, Inoue H, Hao Y-J, Honda C, Moriguchi T (2007) Over-expression of the apple spermidine synthase gene in pear confers multiple abiotic stress tolerance by altering polyamine titers. Transgenic Res 17:251–263
William K (1997a) Interactions of polyamines with ion channels. Biochem J 325:289–297
Williams K (1997b) Modulation and block of ion channels: a new biology of polyamines. Cell Signal 9:1–13
Wortham BW, Patel CN, Oliveira MA (2007) Polyamines in bacteria: pleiotropic effects yet specific mechanisms. Adv Exp Med Biol 603:106–115
Wrede F (1925) Über die aus menschlichem Sperma isolierte Base Spermin. Dtsch Med Wochenschr 51:24
Wu G, Bazer FW, Hu J, Hohnson GA, Spencer TE (2005) Polyamine synthesis from proline in the developing porcine placenta. Biol Reprod 72:842–850
Xiong H, Stanly BA, Tekwani BL, Pegg AE (1997) Processing of mammalian and plant S-adenosylmethionine decarboxylase proenzymes. J Biol Chem 272:28342–28348
Yamaguchi Y, Takatsuka Y, Kamio Y (2002) Identification of a 22-kDa protein required for the degradation of Selenomonas ruminantium lysine decarboxylase by ATP-dependent protease. Biosci Biotechnol Biochem 66:1431–1434
Yamaguchi K, Takahashi Y, Berberich T, Imai A, Miyazaki A, Takahashi T, Michael A, Kusano T (2006) The polyamine spermine protects against high salt stress in Arabidopsis thaliana. FEBS Lett 580:783–6788
Yamaguchi K, Takahashi Y, Berberich T, Imai A, Takahashi T, Michael A, Kusano T (2007) A protective role for the polyamine spermine against drought stress in Arabidopsis. Biochem Biophys Res Commun 352:86–490
Yamakawa H, Kamada H, Satoh M, Ohashi Y (1998) Spermine is a salicylate-independent endogenous inducer for both tobacco acidic pathogenesis-related proteins and resistance against Tobacco mosaic virus infection. Plant Physiol 118:213–1222
Yamasaki H, Cohen MF (2006) NO signal at the crossroads: polyamine-induced nitric oxide synthesis in plants? Trends Plant Sci 11:522–524
Yamasaki H, Shimoji H, Ohshiro Y, Sakihama Y (2001) Inhibitory effects of nitric oxide on oxidative phosphorylation in plant mitochondria. Nitric Oxide 5:261–270
Yoda H, Yamaguchi Y, Sano H (2003) Induction of hypersensitive response by hydrogen peroxide produced through polyamine degradation in tobacco plants. Plant Physiol 132:1973–1981
Yoda H, Hiroi Y, Sano H (2006) Polyamine oxidase is one of the key elements for oxidative burst to induce programmed cell death in tobacco cultured cells. Plant Physiol 142:193–206
Yoshida M, Kashiwagi K, Shigemasa A, Taniguchi S, Yamamoto K, Makinoshima H, Ishihama A, Igarashi K (2004) A unifying model for the role of polyamines in bacterial cell growth, the polyamine modulon. J Biol Chem 279:46008–46013
Zeller EA (1938) Zur Kenntnis der Diamin-oxydase. 3. Mitteilung über den enzymatischen Abbau von Poly-aminen. Helv Chim Acta 21:1645–1665
Zhao F, Song C-P, He J, Zhu H (2007) Polyamines improve K+/Na+ homeostasis in barley seedlings by regulating root ion channel activities. Plant Physiol 145:1061–1072
Acknowledgments
We apologize to the researchers whose works are not cited in this review due to space limitation. We are grateful to our past and present colleagues, especially Y. Uehara, Y. Mitsuya and K. Yamaguchi. Drs. A. Mator and T. Moriguchi are appreciated for providing their preprints. Dr. Matthew R. Shenton is acknowledged for critically reading the manuscript. Our research was partly supported by Grants-in-Aid from the Japan Society for the Promotion of Science to TK (19658039) and to YT (19780002), and grants from Saito Gratitude Foundation to CT and the Sumitomo Foundation to YT. We deeply acknowledge the remarks of Dr. D. Scheel and the anonymous reviewers who contributed to improving this review.
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Kusano, T., Berberich, T., Tateda, C. et al. Polyamines: essential factors for growth and survival. Planta 228, 367–381 (2008). https://doi.org/10.1007/s00425-008-0772-7
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DOI: https://doi.org/10.1007/s00425-008-0772-7