Impact Factor 4.402 | CiteScore 7.8
More on impact ›

REVIEW article

Front. Plant Sci., 10 January 2019 | https://doi.org/10.3389/fpls.2018.01945

Polyamine Function in Plants: Metabolism, Regulation on Development, and Roles in Abiotic Stress Responses

Dandan Chen1,2, Qingsong Shao1,2*, Lianghong Yin1,2, Adnan Younis3 and Bingsong Zheng1
  • 1State Key Laboratory of Subtropical Silviculture, Zhejiang A&F University, Hangzhou, China
  • 2Department of Traditional Chinese Medicine, Zhejiang A&F University, Hangzhou, China
  • 3Institute of Horticultural Sciences, University of Agriculture, Faisalabad, Pakistan

Polyamines (PAs) are low molecular weight aliphatic nitrogenous bases containing two or more amino groups. They are produced by organisms during metabolism and are present in almost all cells. Because they play important roles in diverse plant growth and developmental processes and in environmental stress responses, they are considered as a new kind of plant biostimulant. With the development of molecular biotechnology techniques, there is increasing evidence that PAs, whether applied exogenously or produced endogenously via genetic engineering, can positively affect plant growth, productivity, and stress tolerance. However, it is still not fully understood how PAs regulate plant growth and stress responses. In this review, we attempt to cover these information gaps and provide a comprehensive and critical assessment of the published literature on the relationships between PAs and plant flowering, embryo development, senescence, and responses to several (mainly abiotic) stresses. The aim of this review is to summarize how PAs improve plants' productivity, and to provide a basis for future research on the mechanism of action of PAs in plant growth and development. Future perspectives for PA research are also suggested.

Introduction

Polyamines (PAs) are low molecular weight aliphatic nitrogenous bases containing two or more amino groups, and they have potent biological activity (Xu et al., 2009; Vuosku et al., 2018). They are widely distributed in eukaryotic and prokaryotic cells (Liu et al., 2017; Mustafavi et al., 2018). In living organisms, PAs mainly exist in free (F-PAs), covalently conjugated (CC-PAs) or non-covalently conjugated (NCC-PAs) forms (Gholami et al., 2013). The CC-PAs can be divided into perchloric acid-soluble covalently conjugated polyamines (PSCC-PAs) and perchloric acid-insoluble covalently conjugated polyamines (PISCC-PAs).

In higher plants, PAs are mainly present in their free form. Putrescine (Put), spermidine (Spd), and spermine (Spm) are the main PAs in plants, and they are involved in the regulation of diverse physiological processes (Xu et al., 2014b; Mustafavi et al., 2018), such as flower development, embryogenesis, organogenesis (Xu, 2015), senescence, and fruit maturation and development. They are also involved in responses to biotic and abiotic stresses (Vuosku et al., 2012; de Oliveira et al., 2016; Reis et al., 2016; Mustafavi et al., 2018).

Free polyamines covalently combine with a small molecular substance, such as a phenolic compound and a derivative thereof in the amide bond to form a binding PA, which is also known as a PSCC-PA. The phenolic compound may be hydroxy cinnamic acid, coumaric acid, caffeic acid, or ferulic acid (Luo et al., 2009; Martin-Tanguy, 2010). This kind of PA forms the largest pools of PAs in plants (Kusano et al., 2008; Bassard et al., 2010). Many studies have confirmed that PSCC-PAs act as secondary metabolites, and participate not only in the local allergic reaction of plants against external infestation (Kumar et al., 1997), but also in plant morphogenesis (de Oliveira et al., 2016; De Oliveira et al., 2018; Mustafavi et al., 2018).

Free polyamines covalently bind to biomacromolecules, such as proteins, nucleic acids, uronic acids, or lignin by ionic and hydrogen bonds to form bound PAs, also known as PISCC-PAs. In the physiological pH range, F-PAs are fully protonated and positively charged, and can electrostatically combine with negatively charged biomacromolecules, such as acidic proteins, membrane phospholipids, and nucleic acids in the organism to become NCC-PAs (Igarashi and Kashiwagi, 2015). The NCC-PAs are associated with the regulation of enzyme activity, DNA replication, gene transcription, cell division and membrane stability, and have a wide range of biological functions in plant growth and development. Generally, the more the amino groups, the stronger the physiological activity.

Recent studies using exogenous PAs, PA synthesis inhibitors, and transgenic methods have intensively investigated the role of PAs in plant development and their mechanism of action. Such studies have shown that PAs are closely associated with plant growth, the stability of nucleic acids and membrane structure, stress resistance, and even plant survival (Agudelo-Romero et al., 2013; Pál et al., 2015; Sequeramutiozabal et al., 2016).

In this review, we provide a comprehensive and critical assessment of the published literature on the relationship between plant PAs and plant growth and development. We summarize recent research on the effects of PAs on the development of plants from flowering to embryonic development to senescence, and explore their roles in the responses to several stresses. The aim of this paper is to reveal the roles that PAs play in plant growth and development and provide a basis for future research on the mechanism of action of PAs in plant growth and development. We also discuss the ways in which exogenous PAs can be used regulate and promote plant growth and development in production.

Distribution and Metabolism of PAs in Plants

PAs Distribution

Polyamines are ubiquitous in eukaryotic and prokaryotic cells (Liu et al., 2016, 2017), and are found even in plant RNA viruses and plant tumors. They have potent biological activities. There are numerous forms of PAs. In higher plants, PAs are predominantly present in their free form. The most common PAs in higher plants are Put, Spd, Spm, thermospermine (Tspm) (Kim et al., 2014; Sobieszczuk-Nowicka, 2017; Takahashi et al., 2017b), and cadaverine (Cad) (Regla-Márquez et al., 2015; Nahar et al., 2016) (Table 1). Other PAs are found only in certain plants or under special conditions.

TABLE 1
www.frontiersin.org

Table 1. Polyamine structure and distribution.

Polyamines show tissue- and organ-specific distribution patterns in plants. For example, the most abundant PA in leaves was found to be Put, and its levels were three times higher than those of Spd and Spm, whereas Spd was found to be the most abundant PA in other organs (Takahashi et al., 2017b). Different types of PAs also show different localization patterns within cells. In carrot cells, Put was found to accumulate in the cytoplasm, and Spm in the cell wall (Cai et al., 2006). The distribution patterns of PAs may be related to their unique functions. In general, more vigorous plant growth and metabolism is associated with greater PA biosynthesis and higher PA contents (Zhao et al., 2004; Cai et al., 2006).

Polyamine Biosynthesis

Putrescine is the central product of the common PA biosynthetic pathway. It contains two amino groups and is a synthetic precursor of Spd and Spm (Xu et al., 2009). There are three different routes of Put biosynthesis in plants (Figure 1). In the first route, the No. 8 carbon atom is removed from arginine (Arg) by arginine decarboxylase (ADC) to form agmatine (Agm) and CO2; the No. 2 nitrogen atom is removed from Agm to form N-carbamoyl Put (NCPA) and NH3; and then NCPA is hydrolyzed by N-carbamoylputreseine amidohydrolase (NCPAH) and its carbamoyl group is removed to form Put, CO2, and NH3. This is the main Put synthesis pathway in plants (Docimo et al., 2012; Pegg, 2016). In the second route, ornithine (Orn) is produced from Arg by arginase; and then ornithine decarboxylase (ODC) removes the carboxyl group of the no.1 carbon atom of Orn to form Put and CO2 (Docimo et al., 2012; Pegg, 2016). The ODC gene has been lost from Arabidopsis thaliana and many members of the Brassicaceae (Hanfrey et al., 2010), indicating that the ornithine pathway is not essential for normal growth. In the third route, Arg is first converted into citrulline (Cit), which is then decarboxylated by citrulline decarboxylase (CDC) to form Put (Han, 2016; Ouyang et al., 2017; De Oliveira et al., 2018). To date, the Cit pathway has only been found in sesame, and so the first two pathways are more common in plants. The activities of ADC and ODC can be inhibited by the irreversible competitive inhibitors difluoromethylarginine (DFMA) and difluoromethylornithine (DFMO), respectively (Grossi et al., 2016; Yamamoto et al., 2016). Spermidine and Spm are produced from Put and aminopropyl residues, which are gradually provided by methionine (Vuosku et al., 2018) (Figure 1).

FIGURE 1
www.frontiersin.org

Figure 1. The pathway of PAs biosynthesis in plant. The orange part is the ethylene synthesis pathway, and the green part is the polyamine synthesis pathway (There are three routes of putrescine synthesis, route 1, route 2, and route 3), and the blue part is the corresponding enzyme inhibitor.

Polyamine Catabolism

The catabolism of PAs in plants is mainly dependent on the action of amine oxidases. The known amine oxidases include diamine oxidase (DAO) and PA oxidase (PAO) (Figure 2). Diamine oxidase, which relies on Cu2+ and pyridoxal phosphate as its cofactors, catalyzes the formation of H2O2, ammonia, and 4-aminobutanal from Put. Then, 4-aminobutanal undergoes cyclization to form pyrroline (PYRR), which is converted into γ-aminobutyric acid (GABA) by the action of pyrroline dehydrogenase (PYRR-DH). Then, GABA is further converted into succinate, which enters the Krebs cycle. Dicots contain high contents of DAO, but its encoding gene has been found in only a few species (Cona et al., 2006). Unlike DAO, PAO is linked to flavin adenine dinucleotide (FAD) by non-covalent bonds and is found at high levels in monocots (Takahashi et al., 2017a; Hao et al., 2018). Its substrates are advanced PAs, such as Spd, Spm, and Tspm. There are multiple PAO families in many plants (Liu et al., 2014; Takahashi et al., 2017a). Some PAOs catalyze the production of metabolic end-products of PAs; for example, the wheat PAO oxidizes Spd and Spm to form 4-aminobutanal,3-aminopropyl-4-aminobutanal,1,3-diaminopropane (Dap) and H2O2 (Cona et al., 2006; Liu et al., 2014). Some PAOs catalyze the reverse reaction of PA synthesis in the PA back-conversion pathway (PBCP) (Liu et al., 2014; Takahashi et al., 2017a). Del Duca and Tassoni et al. found that exogenous Spd applied to Helianthus tuberosis and A. thaliana was transformed into Put (Tassoni et al., 2000). In Arabidopsis, PAO1 and PAO4 were able to convert Spm to Spd; and PAO2 and PAO3 catalyzed the production of Spd from Spm and then produced Put (Moschou et al., 2008). The PAO2 of Brachypodium distachyon catalyzed the conversion of Spm or Tspm to Spd, and Spd to Put, with Spd as the preferred substrate. In contrast, BdPAO3 preferentially utilized Spm as the substrate and catalyzed the conversion of tetraamines to Spd (Takahashi et al., 2017a) (Figure 2).

FIGURE 2
www.frontiersin.org

Figure 2. The pathway of polyamine catabolism in plant.

The metabolism of PAs in plants is closely connected to many other metabolic pathways. The H2O2 produced by PA oxidation functions in the signal transduction process of plants during biotic and abiotic stress responses (Freitas et al., 2017; Mellidou et al., 2017), and affects stomatal closure induced by abscisic acid (ABA) (Cona et al., 2006; Tun et al., 2006; An et al., 2008). S-adenosylmethionine (SAM) in the PA biosynthetic pathway is also a precursor for ethylene synthesis (Figure 1), and studies have demonstrated that PAs synthesis competes with ethylene synthesis (Lasanajak et al., 2014). In addition, the metabolism of PAs is related to the production of NO (Pál et al., 2015), which is an essential signaling component for plant growth (Agurla et al., 2017). Therefore, the roles of PAs in plant growth and development and the mechanisms underlying their function can be explored by studying the relationship between PA metabolism and plant hormones, and the effects of PA metabolism on plant signaling substances.

Polyamines and Plant Development

Polyamines and Flowering

After a period of vegetative growth, higher plants enter a period of reproductive growth; that is, leaf bud tissue changes its physiological state to become flower bud tissue, and then develops into a floral organ. This process is called flower bud differentiation (Guo et al., 2015). Flower bud differentiation is a complex process of morphogenesis. It is triggered by various factors, such as photoperiod, vernalization, nutrition, and water status, and is accomplished by the interaction and coordination of hormones and PAs (Xu, 2015).

Polyamines are considered to be a class of growth regulators in plants (Xu et al., 2014b). Many studies have shown that exogenous PAs and PA synthesis inhibitors can affect flower bud differentiation. Exogenous PAs were shown to accelerate the process of flower bud differentiation, and high PA contents in apical buds were beneficial for the initiation and maintenance of flower bud differentiation in Chrysanthemum (Xu, 2015) (Table 3). In Arabidopsis, PAs were found to be more abundant in flowers than in any other organ, and the addition of exogenous PAs to poorly flowering plants significantly promoted their flowering response (Applewhite et al., 2010) (Table 3). The application of Spm (10 ppm) improved flower quality and extended vase life by 3 days in cut rose flowers (Tatte et al., 2015). Lower contents of PAs (mainly Put and Spd) in rapeseed were found to be conducive to the initiation of flower bud differentiation, and an increased PAs content was beneficial for flower bud development. Earlier peaking of PA contents in tissues led to earlier bolting time (Ai et al., 2011). Similar results were observed in Dendrobium nobile, where plants with higher levels of Put and Spd in the leaves had more flower buds, more flowers, and a larger mean floral diameter (Li et al., 2014). The recombinant proteins of GtSPDS and GtSPMS from Gentiana triflora (homologs of two Arabidopsis PA biosynthetic enzymes) had SPDS and SPMS activity, respectively. The expression levels of GtSPDS and GTSPMS transiently increased from the vegetative to the reproductive growth phase, and overexpression of these genes hastened flowering (Applewhite et al., 2010; Imamura et al., 2015) (Table 2).

TABLE 2
www.frontiersin.org

Table 2. Genes related to polyamines on regulating plant growth.

TABLE 3
www.frontiersin.org

Table 3. Effects of polyamines on plant growth and development.

Applying polyamine synthase inhibitors to the growth medium reduced the Spd content in Arabidopsis, and almost completely inhibited bolting and flowering. When the plants were transferred to medium without inhibitors, bolting and flowering were restored (Applewhite et al., 2010; Xu et al., 2014b; Xu, 2015) (Table 3). However, feeding Spd via the roots under permissive flowering conditions resulted in delayed flowering in Arabidopsis (Applewhite et al., 2010; Ahmed et al., 2017). Overexpression of ADC resulted in Put accumulation in the leaves, and plants showed a dwarf and delayed-flowering phenotype (Ahmed et al., 2017). Endogenous Put was found to be closely related to IAA and gibberellin (GA) contents, and high levels of Put and Spd were not conducive to the accumulation of IAA and GA (Xu, 2015). The effects of exogenous PAs and PA synthesis inhibitors on GA were mainly observed at the inflorescence differentiation and floret differentiation stages (Xu, 2015). Both the dwarf and delayed-flowering phenotypes were alleviated by spraying leaves with GA. Under short-day conditions, exogenous Spd significantly promoted PAO activity and lignin synthesis during flower bud differentiation. D-arginine inhibits flower bud differentiation, and reduces PAO activity and lignin synthesis (Xu et al., 2014a). Lignin is a secondary metabolite in plant growth and development, and it is of great significance in the growth, differentiation, and resistance of plant cells (Smita and Upendranath, 2008).

Polyamines and Embryo Development

Polyamines have typical polycation characteristics. They bind to negatively charged nucleic acids, proteins, and phospholipids by ionic and hydrogen bonds through their amino and imino groups, and participate in zygote polarity establishment, apical axis formation, cell layer differentiation, and establishment of the meristem (Cangahuala-Inocente et al., 2014; Tiburcio et al., 2014). Polyamines are generally regarded as regulators in the process of embryogenesis in both angiosperms and gymnosperms (de Oliveira et al., 2016), and an increase in PAs content is required for embryogenesis. Studies have shown that the normal development of plant embryos requires a well-maintained dynamic balance of PAs in vivo. The types and abundance of PAs vary among different stages of embryonic development, from the multi-cell proembryo, globular, heart-shaped, and torpedo stages to the cotyledon stage (Krasuska et al., 2013). It is possible to regulate nucleic acid synthesis and protein translation in both directions by applying exogenous PAs and PA synthesis inhibitors. This can affect the development of organelles, such as endoplasmic reticulum, plastids, and mitochondria, and the structures of microtubules (Vondráková et al., 2015).

Generally, efficient somatic embryogenesis and the growth of embryos into complete plantlets are closely related to the levels of endogenous hormones, such as IAA, cytokinins (Cyt), ethylene, ABA, and PAs. Many studies have shown that PAs play a vital role in inducing cell division and promoting regeneration in plant tissues and cell cultures (Minocha and Minocha, 1995; Yadav and Rajam, 1997; Vondráková et al., 2015). In general, PAs are more abundant in embryogenic callus and somatic and zygotic immature embryos than in mature and germinating embryos. Putrescine stimulates somatic embryogenesis, and reduced concentrations of Put and Spd result in fewer somatic embryos. In cultured Panax ginseng somatic embryos, the addition of PAs at different concentrations (10–1,000 μm) to induction or regeneration media affected the formation of embryogenic structures. A 5- and 4-fold increase in the number of embryogenic structures was obtained by adding Spd (1,000 μm) to induction and regeneration medium, respectively (Kevers et al., 2000). In the embryogenic suspensor mass (ESM) of Norway spruce, the Put and Spd contents were approximately equal at the early stage of proliferation, but after 4 weeks, the Spd level was significantly higher than the Put level (Vondráková et al., 2015). In a range of hybrid combinations of seedless grapevine, the addition of 3 mM Put, 0.5 mM Spd, or 0.3 mM Spm to the culture medium significantly promoted plantlet development or the embryo germination rate. This indicated that addition of appropriate amounts of PAs to the culture medium could significantly increase the efficiency of in vitro embryo rescue for seedless grapevine (Jiao et al., 2017) (Table 3). A study on embryo development in litchi showed that the contents of Put, Spd, and Spm were higher in normal ovules than in abortive ovules during embryonic development (Chen and Lv, 2000).

Other studies have used PA synthesis inhibitors to explore the roles of PAs in plant embryogenesis. The addition of PA biosynthesis inhibitors (DFMO and DFMA) to induction and regeneration media at all tested concentrations (10–1,000 μm) significantly reduced the number of P. ginseng somatic embryos (Kevers et al., 2000). The concentrations of Spm and Spd were 11 times and 3 times higher, respectively, in embryogenic callus than in non-embryogenic callus of Coffea canephora, but the Put content did not differ significantly between embryogenic callus and non-embryogenic callus. Exogenous PAs resulted in a 58% explant response for embryogenesis, compared with a 42% response in the control. The PA biosynthesis inhibitors DFMO and DFMA caused an 83% decrease in the embryogenic response (Kumar et al., 2008). These results were consistent with those of other studies (Bais and Sudha Gravishankar, 2001).

With the development of molecular biology techniques, genes encoding key enzymes in PA biosynthesis have been successfully isolated and cloned from plants, such as rice, tobacco, and Arabidopsis, and the corresponding mutants have been obtained by T-DNA insertion mutation (Su et al., 2012; Miller-Fleming et al., 2015). Analyses of these genes and signal transduction regulators in wild-type and mutant Arabidopsis revealed that one mutant had a blocked PA signal transduction pathway, which in turn affected cell division and differentiation (Gallois et al., 2013; Molesini et al., 2015).

Polyamines and Plant Senescence

The activities of PA metabolic enzymes and PAs contents change throughout the stages of plant growth. In whole plants, endogenous PAs and PA synthetase activity were found to be highest in the meristem and growing cells, and lowest in senescent tissues. As leaves senescence, the chlorophyll content gradually decreases, and the activities of ADC and ODC decrease, while the activities of PAO and hydrolases, such as ribonuclease and protease increase rapidly. All of these changes can be inhibited by the application of exogenous PAs (Duan, 2000; Cai, 2009) A reduction in PA levels seems to be a significant prelude to senescence signals, or it may be that a decrease in PAs content is the senescence signal (Duan et al., 2006).

Exogenous Spd and Spm treatments can increase the PAs content in cut flowers, and delay their senescence and improve quality (Yang and He, 2001; Cao, 2010). In Anthurium andraeanum, the application of GA3 + Spm by spraying delayed the senescence of cut flowers stored at 20°C, and improved the quality of the inflorescences (Simões et al., 2018). Delayed leaf senescence was found to be associated with a higher Spm level, reduced reactive oxygen species (ROS) production, and increased NO levels (Sobieszczuk-Nowicka, 2017). Polyamines appeared to delay senescence by inhibiting ethylene biosynthesis (Woo et al., 2013; Anwar et al., 2015).

Gerbera flowers sprayed with 0.1 mM Spd or treated with 10 mM Spd in vase water showed delayed senescence, while those sprayed with 1 mM Spd, 10 mM Spd, 0.1 mM Spm, 1 mM Spm, or mixed solution of 0.1 mM each of Put, Spd, Spm showed accelerated senescence, with brown spots and yellowing of the petal rims starting from day 2 of treatment (Bagni and Tassoni, 2006). Legocka and Serafni-Fracassini et al. found that chlorophyll rapidly degraded and Put accumulated during senescence, while the exogenous addition of Spd or Spm inhibited protein degradation and reduced chlorophyll losses (Serafini-Fracassini et al., 2010; Cai et al., 2015). In peony, a PA synthesis inhibitor (0.1 Mm) extended the lifespan and delayed the senescence of cut flowers, while PAs shortened the lifespan and accelerated flower senescence (Han, 2016).

Polyamines and Abiotic Stress Responses

Polyamines and Temperature Stress

There are two major categories of temperature stress; low and high temperature stress. Low temperature stress can be further divided into cold stress and freezing stress. To date, few studies have focused on the physiological functions of PAs in plants under high temperature stress. High temperature stress significantly affected PA synthesis in the leaves of Chinese kale; after 6 days of high temperature treatment, the total PAs and Put contents had increased, but the increases were not sustained over longer treatment times (Yang and Yang, 2002). Under high temperature stress, PAs can promote photosynthesis, and increase the antioxidant capacity and osmotic adjustment ability of plants (Tian, 2012). Antioxidant enzymes can scavenge ROS to prevent membrane lipid peroxidation and stabilize membrane structure (Ouyang et al., 2017). Shao et al. reported that the heat tolerance of alfalfa was related to higher Spd contents and lower Put and Spm contents (Shao et al., 2015). The PAs have many different functions in plants, and the main physiological mechanisms of high temperature tolerance differ among plant species. This explains why the various PAs show different patterns of change in different plant species under high temperature stress (Shao et al., 2015).

Polyamines can bind to the phospholipid site of the cell membrane to prevent cytolysis and improve cold resistance (Li and He, 2012) (Table 2). However, there are several different viewpoints on the relationship between Put and plant chilling stress (Wu and Yuan, 2008). When sweet pepper and zucchini fruits were stored at chilling temperature, the Put content increased exponentially, accompanied by chilling damage. Storage under CO2 modified atmosphere reduced the extent of cold damage and inhibited the accumulation of Put, suggesting that Put accumulated as a result of chilling stress (Serrano et al., 1997, 1998). In contrast, Roy et al. proposed that Put accumulation caused chilling damage, and increased Spm may be a defense response to cold damage. They found that the Put, Spm, and Spd contents gradually increased in loquat fruit stored at low temperatures. The application of exogenous Spm maintained high levels of endogenous Spm and Spd, inhibiting Put accumulation and reducing chilling damage (Zhen et al., 2000; Roy and Wu, 2001). Another opinion was that Put may accumulate as a defense response of plants to chilling damage, because Put accumulation was found to be positively correlated with the cold resistance of plants (Wang et al., 2003b).

Sun et al. studied the effect of Put and D-Arg at different concentrations (0.5, 1.0, 1.5, and 2.0 mmol/L) on the physiological and biochemical indexes of Anthurium andraeanum under chilling stress at 6°C in winter. They found that Put application resulted in increased antioxidant enzyme activities, root activity, nitrogen metabolism, chlorophyll content, and proline content, and a decrease in malondialdehyde content. Treatment with 1.0 mmol/L Put had the strongest effect, and chilling damage was reduced by treatment with D-Arg (Sun et al., 2018b). Similar results were obtained for stevia plants, where PA supplementation increased their tolerance to cold conditions (Peynevandi et al., 2018). When an SPDS cDNA from Cucurbita ficifolia was introduced into Arabidopsis (Kasukabe et al., 2004), the transgenic plants exhibited a significant increase in SPDS activity and Spd content in leaves together with enhanced tolerance to various stresses including chilling and freezing (Groppa and Benavides, 2008). Recent studies have suggested that abiotic stress tolerance is mainly affected by the role of PAs in signal transduction rather than their accumulation (Pál et al., 2015).

PAs and Water Stress

Most studies on the relationship between PAs and water stress have focused on drought resistance (Ebeed et al., 2017), and few have focused on waterlogging resistance. Polyamines (Spm, Spd, and Put) can regulate the size of the potassium channel and the size of pores in the plasma membrane of guard cells, thereby strongly regulating pore opening and closing. In this way, PAs can control water loss in plants (Liu et al., 2000). Many studies have shown that foliar application of Put at an appropriate level can trigger physiological processes and induce the biosynthesis of osmotic adjustment substances, such as free amino acids, soluble sugars, and proline. This may compensate for the negative impacts of drought stress on plant biomass and increase the quality and quantity of certain bioactive substances (Sánchezrodríguez et al., 2016; Mohammadi et al., 2018). In alfalfa, a Put treatment was shown to improve seed germination and increase all growth indexes (hypocotyl length, root and shoot fresh and dry mass) under drought stress caused by different concentrations of polyethylene glycol (PEG 4000), both in vitro and in a pot experiment (Zeid and Shedeed, 2006) (Table 4).

TABLE 4
www.frontiersin.org

Table 4. Effects of polyamines on plant abiotic stress.

The Arabidopsis mutant acl5/Spms, which cannot produce Spm, is hypersensitive to high salt and drought. This phenotype was cured by a Spm pretreatment but not by pretreatments with Put and Spd, suggesting that the drought-hypersensitivity of the mutant is due to Spm deficiency (Yamaguchi et al., 2007). A high Spm content and a high ratio of (Spd+Spm)/Put were associated with the drought resistance of mycorrhizal masson pine (Xu et al., 2009). Among the three main endogenous PAs, Spm was most strongly related to drought resistance apple (Liu et al., 2010). Similar results were obtained for cherry tomato (Montesinos-Pereira et al., 2015). However, Yang et al. found that Spd and Spm relieved the inhibitory effects of drought stress and promoted grain filling and drought resistance in wheat, while Put had the opposite effect (Yang et al., 2016) (Table 4).

The above results indicate that the function of PAs can differ among different plants and even different parts of the same plant, whether under osmotic stress or water stress (Sen et al., 2018). Therefore, the response of plants to exogenous PAs under osmotic stress and water stress will depend on the plant species.

PAs and Salt Stress

Salt and drought stress are the two major abiotic stresses in agriculture, and both of them lead to reduced water potential in plants. Salinity is a complex environmental constraint. A high salt concentration reduces membrane integrity, decreases the activity of various enzymes, and impairs the function of the photosynthetic apparatus. Plants adapt to such unfavorable environmental conditions by accumulating low molecular-weight osmolytes, such as proline and PAs. The application of different types and concentrations of exogenous PAs has been shown to alleviate the effects of NaCl stress on various plants, and reduce damage (Verma and Mishra, 2005; Li et al., 2008) (Table 4). Plants rich in PAs usually show strong salt tolerance.

It has been suggested that the level of Spm in plants is an important indicator of salt tolerance (Li and He, 2012). The free, acid-soluble bound, and total Spm contents in leaf tissues of sunflower plants increased under 50, 100, or 150 mM NaCl treatments (Mutlu and Bozcuk, 2005). Exogenous PAs, especially Spm and Spd, resulted in increased reactive oxygen metabolism and photosynthesis, which improved plant growth and reduced the inhibitory effects of salt stress (Meng et al., 2015; Baniasadi et al., 2018). Similar results were obtained in a study on soybean seedlings (Wang and Bo, 2014). Li et al. produced a cucumber line with up-regulated SAMDC expression and down-regulated ADC and ODC expression, resulting in increased accumulation of Spd and Spm and decreased accumulation of Put under salt stress. As a result, the inhibition of plant growth under salt stress was alleviated in the transgenic seedlings (Li et al., 2011; Takahashi et al., 2017b). Several metabolic pathways are affected by Spm and Spd (Paul and Roychoudhury, 2017). Sun et al. showed that PAs and ABA together alleviated salt stress in grape seedlings (Sun et al., 2018a).

Recent studies have explored the relationship between PAs and plant drought resistance by using genetic engineering techniques. Malabika et al. transformed the oat ADC gene into rice, and found that the ADC activity, biological yield, and Put contents were higher in the transgenic rice and its progeny than in non-transgenic rice under NaCl stress (Roy and Wu, 2001). Later, they introduced the SAMDC gene of the durum wheat × barley hybrid Tritordeum into rice. A Southern blot analysis showed that the SAMDC gene was stably integrated. Under NaCl stress, the growth potential of transgenic rice seedlings was better than that of non-transgenic rice, and the contents of Spd and Spm were 3–4 times higher in transgenic lines than in non-transgenic lines (Roy and Wu, 2002). Similarly, micropropagated transgenic Lotus tenuis plants expressing ADC were healthier than wild-type plants under salinity stress and showed better osmotic adjustment (5.8-fold) (Espasandin et al., 2018). An ADC2 deletion mutant of Arabidopsis showed extreme sensitivity to salt stress, which was alleviated by applying exogenous Put (Naka et al., 2010).

PAs and Oxidative Stress

Polyamines play a complex role in plant oxidative stress (Minocha et al., 2014). On one hand, polyamines can increase the activity of various antioxidant enzymes in plants, so that it can effectively regulate oxidative stress in plants caused by various environmental factors. Maize leaves pretreated with Spm and Put showed increased tolerance to oxidative stress induced by paraquat (Durmu and Kadioglu, 2005). Exogenous Spd significantly increased the contents of Spd and Spm and reduced the content of Put in the roots of cucumber seedlings under hypoxia stress. These changes were related to increased antioxidant enzyme activity, enhanced ROS scavenging ability, and less membrane lipid peroxidation, which ultimately led to enhanced hypoxia stress tolerance (Jia et al., 2008; Wu et al., 2018). Under cadmium- and copper-induced oxidative stress, lipid peroxidation in sunflower leaf discs increased, while the activities of glutathione reductase (GR) and superoxide dismutase (SOD) decreased (Groppa et al., 2001). When plants were treated with exogenous PAs (1 mM), Spm treatment reduced the effects of Cd2+ and Cu2+ on lipid peroxidation almost to control values (Tajti et al., 2018). In addition, GR activity was completely restored by Spm or Spd treatments, and SOD activity under Cu2+ treatment was restored by Spm treatment (Table 3).

On the other hand, PAs are a source of reactive oxygen species. Because their catabolism produces the strong oxidizers H2O2 and acrolein, PAs can potentially be the cause of cellular harm under stress conditions (Minocha et al., 2014). However, H2O2 is also a signaling molecule that can enter the stress signal transduction chain and activate an antioxidant defense response (Groppa and Benavides, 2008). Thus, it seems that PAs are regulators of redox homeostasis that play a dual role in plant oxidative stress (Saha et al., 2015).

Other

Plants can also be affected by other stresses, such as acid stress, radiation stress, wounding, heavy metals (Tajti et al., 2018), and diseases and pests (Khajuria and Ohri, 2018). Few studies have focused on these topics, but current data indicate that PAs are important in the responses to these stresses. Exogenous Put was shown to regulate the balance of active oxygen metabolism under acid stress and stabilize membrane system structure, thereby protecting plants from acid stress and improving their acid resistance (Li et al., 1995). Arabidopsis plants subjected to mechanical injury showed increased expression of ADC2 (Perezamador et al., 2002). Similarly, mechanical wounding of the first leaves of oilseed rape led to a significant increase in free Put content in the wounded first leaf and the unwounded second leaf (Cowley and Walters, 2010). Treatment with the heavy metals Hg2+ and Cr6+ led to reduced contents of Spd and Spm and decreased activities of SOD, catalase, and peroxidase in amaranth leaves, leading to excessive accumulation of membrane lipid peroxides (malondialdehyde) and a significant decrease in chlorophyll and soluble protein contents. Exogenous Spd ameliorated these negative effects of Hg2+ and Cr6+ (Wang et al., 2003a; Wang and Shi, 2004).

As well as being involved in abiotic stress responses, PAs are also closely related to biotic stress responses in plants. Plant tissues infected with pathogens accumulate large amounts of PAs, which inhibit the growth of bacteria and viruses and inactivate viruses. When pathogens invade plant cells, they induce PA accumulation and PA oxidase activity; this leads to increased H2O2 content, which prevents pathogens from infecting cells (Yordanova et al., 2003). Overexpression of the ADC gene from trifoliate orange significantly increased resistance to ulcer disease in citrus (Wang, 2009). Similarly, a higher Put content was found to be associated with greater insect resistance in Chinese cabbage (Wang, 2007).

Conclusions and Future Prospects

This paper represents a comprehensive review of the published literature on the relationship between PAs and plant growth, development and stress tolerance. We explored the role of PAs in plant developmental processes ranging from flowering to senescence, and discussed the effects of PAs on plant growth and development. This information provides a reference for the future research on the regulation mechanism of PAs and the use of exogenous PAs to regulate plant growth in production. In recent years, many studies have focused on the relationship between PAs and plant growth and development, but most of them have been relatively simple and similar. Almost all of them have focused the effects of exogenous PAs on the growth and development of fruit or vegetable crops or model plants. However, it is becoming increasingly popular to increase endogenous PA production via genetic manipulation to regulate plant growth. There are still many questions to answer regarding the roles of PAs in regulating plant growth and development. It is still largely unknown how the biosynthetic and catabolic pathways are regulated at the transcriptional, translational, and post-transcriptional levels. Further research is required to uncover the exact mechanism of PA accumulation to improve plant stress resistance. Similarly, there is still much to learn about the metabolic relationship between PAs and other hormones during the growth and development of higher plants, especially the relationship between PAs and ethylene. With the advancement of molecular biology techniques, research is now focusing on events at the molecular level. The contents of intracellular PAs have been modulated by altering the expression of ADC, ODC, and SAMDC. The use of transgenic methods to manipulate PA metabolism has become an effective tool to study the physiological functions of PAs in higher plants. Illuminating the regulation mechanism of PAs at the molecular level should be a major research direction in the future.

Author Contributions

DC read a lot of literatures and wrote the paper. QS provided the writing direction and revised the paper. LY provided some suggestions for the paper. AY and BZ helped in polish the language of this article.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

This work was supported by the National Natural Science Foundation of China (81673531), Major Science and Technology Projects of Breeding New Varieties of Agriculture in Zhejiang Province (2016C02058). We thank Jennifer Smith, Ph.D., from Liwen Bianji, Edanz Group China (www.liwenbianji.cn/ac), for polishing the English text of this manuscript, and we thank the reviewers for carefully reviewing our manuscript and making many valuable suggestions.

Abbreviations

PAs, polyamines; F-PAs, free polyamines; CC-PAs, covalently conjugated polyamines; NCC-PAs, non-covalently conjugated polyamines; PSCC-PAs, perchloric acid-soluble covalently conjugated polyamines; PISCC-PAs, perchloric acid-insoluble covalently conjugated polyamines; Put, putrescine; Spd, spermidine; Spm, spermine; Tspm, thermospermine; Cad, cadaverine; Arg, arginine; ADC, arginine decarboxylase; Agm, agmatine; NCPA, N-carbamoylputrescine; NCPAH, N-carbamoylputreseine amidohydrolase; Orn, ornithine; ODC, ornithine decarboxylase; Cit, citrulline; CDC, citrulline decarboxylase; DFMA, difluoromethylarginine; DFMO, difluoromethylornithine; AIH, agmatine iminohydrolase; SPDS, spermidine synthase; CHA, clohexylamine, the inhibitor of SPDS; SPMS, spermine synthase; ACL5, thermospermine synthase; SAM, s-adenosylmethionine; SAMDC, S-adenosylmethionine decarboxylase; SAMS, S-adenosylmethionine synthase; ACC, 1-amino-1-carboxycyclopropane; ACS, 1-aminocyclopropane-1-carboxylate synthase; ACO, 1-aminocyclopropane-1-carboxylate oxidase; MGBG, methylglyoxal bis (guanylhy-drazone), the inhibitor of SAMDC; DeSAM, decarboxylated SAM; MTA, 5′-methyl-thioadenosine; DAO, diamine oxidase; PAO, polyamine oxidase; PYRR, pyrroline; GABA, γ-aminobutyric acid; PYRR-DH, pyrroline dehydrogenase; FAD, flavin adenine dinucleotide; Dap, 1, 3-diaminopropane; PBCP, polyamines back-conversion pathway; ABA, abscisic acid; IAA, auxin; ETH, ethylene; GA, gibberellic acid; Cyt, cytokinins; ESM, embryogenic suspensor mass; ROS, reactive oxygen species; PEG, polyethylene glycol; CAT, catalase; SOD, superoxide dismutase; GR, glutathione reductase.

References

Agudelo-Romero, P., Bortolloti, C., Pais, M. S., and Al, E. (2013). Study of polyamines during grape ripening indicate an important role of polyamine catabolism. Plant Physiol. Biochem. 67, 105–119. doi: 10.1016/j.plaphy.2013.02.024

PubMed Abstract | CrossRef Full Text | Google Scholar

Agurla, S., Gayatri, G., and Raghavendra, A. S. (2017). Polyamines increase nitric oxide and reactive oxygen species in guard cells of Arabidopsis thaliana during stomatal closure. Protoplasma 255, 153–162. doi: 10.1007/s00709-017-1139-3

PubMed Abstract | CrossRef Full Text | Google Scholar

Ahmed, S., Ariyaratne, M., Patel, J., and Al, E. (2017). Altered expression of polyamine transporters reveals a role for spermidine in the timing of flowering and other developmental response pathways. Plant Sci. 258, 146–155. doi: 10.1016/j.plantsci.2016.12.002

PubMed Abstract | CrossRef Full Text | Google Scholar

Ai, Y., Chen, G., and Zhou, Y. (2011). The study on polyamine metabolism in leaves during flower formation in the early-maturing mutant of Brassica Napus L. Chin. Agric. Sci. Bull. 27, 101–105.

Google Scholar

An, Z., Jing, W., Liu, Y., and Zhang, W. (2008). Hydrogen peroxide generated by copper amine oxidase is involved in abscisic acid-induced stomatal closure in Vicia faba. J. Exp. Bot. 59, 815–825. doi: 10.1093/jxb/erm370

PubMed Abstract | CrossRef Full Text | Google Scholar

Anwar, R., Mattoo, A. K., and Handa, A. K. (2015). Polyamine interactions with plant hormones: crosstalk at several levels. Int. J. Hydrogen Energy 38, 1039–1051. doi: 10.1007/978-4-431-55212-3_22

CrossRef Full Text | Google Scholar

Applewhite, P. B., Kaur-Sawhney, R., and Galston, A. W. (2010). A role for spermidine in the bolting and flowering of Arabidopsis. Physiol. Plant 108, 314–320. doi: 10.1034/j.1399-3054.2000.108003314.x

CrossRef Full Text | Google Scholar

Bagni, N., and Tassoni, A. (2006). The role of polyamines in relation to flower senescence. Floricult. Ornament. Plant Biotechnol. 1536, 855–856.

Google Scholar

Bais, H. P., and Sudha Gravishankar, G. A. (2001). Influence of putrescine, silver nitrate and polyamine inhibitors on the morphogenetic response in untransformed and transformed tissues of Cichorium intybus and their regenerants. Plant Cell Rep. 20, 547–555. doi: 10.1007/s002990100367

CrossRef Full Text | Google Scholar

Baniasadi, F., Saffari, V. R., and Moud, A. A. M. (2018). Physiological and growth responses of Calendula officinalis L. plants to the interaction effects of polyamines and salt stress. Sci. Horticult. 234, 312–317. doi: 10.1016/j.scienta.2018.02.069

CrossRef Full Text | Google Scholar

Bassard, J. E., Ullmann, P., Bernier, F., and Al, E. (2010). Phenolamides: bridging polyamines to the phenolic metabolism. Phytochemistry 71, 1808–1824. doi: 10.1016/j.phytochem.2010.08.003

PubMed Abstract | CrossRef Full Text | Google Scholar

Benavides, M. P., Groppa, M. D., Recalde, L., and Verstraeten, S. V. (2018). Effects of polyamines on cadmium- and copper-mediated alterations in wheat (Triticum aestivum L) and sunflower (Helianthus annuus L) seedling membrane fluidity. Arch. Biochem. Biophys. 654, 27–39. doi: 10.1016/j.abb.2018.07.008

PubMed Abstract | CrossRef Full Text | Google Scholar

Cai, G., Sobieszczuknowicka, E., Aloisi, I., and Al, E. (2015). Polyamines are common players in different facets of plant programmed cell death. Amino Acids 47, 27–44. doi: 10.1007/s00726-014-1865-1

PubMed Abstract | CrossRef Full Text | Google Scholar

Cai, Q. (2009). Progress in physiology of plant polyamines. Fujian Sci. Technol. Rice Wheat 27, 37–40. doi: 10.3969/j.issn.1008-9799.2009.01.020

CrossRef Full Text | Google Scholar

Cai, Q., Zhang, J., Guo, C., and Al, E. (2006). Reviews of the physiological roles and molecular biology of polyamines in higher plants. J. Fujian Educ. Coll. 7, 118–124. doi: 10.3969/j.issn.1673-9884.2006.10.039

CrossRef Full Text | Google Scholar

Cangahuala-Inocente, G. C., Silveira, V., Caprestano, C. A., and Al, E. (2014). Dynamics of physiological and biochemical changes during somatic embryogenesis of Acca sellowiana. Vitro Cell. Deve. Biol. 50, 166–175. doi: 10.1007/s11627-013-9563-3

CrossRef Full Text | Google Scholar

Cao, D. (2010). Effects of Polyamines on Seed Quality and Germination of Super Sweet Corn Seeds during Development. Hangzhou: Zhejiang University.

Google Scholar

Chen, M., Chen, J., Fang, J., and Al, E. (2014). Down-regulation of S -adenosylmethionine decarboxylase genes results in reduced plant length, pollen viability, and abiotic stress tolerance. Plant Cell Tissue Organ Cult. 116, 311–322. doi: 10.1007/s11240-013-0405-0

CrossRef Full Text | Google Scholar

Chen, W., and Lv, L. (2000). Changes in polyamine content in relation to embryo development in Litchi Ovules. J. Trop. Subtrop. Bot. 8, 229–234. doi: 10.3969/j.issn.1005-3395.2000.03.008

CrossRef Full Text | Google Scholar

Cheng, X. Q., Zhu, X. F., Tian, W. G., and Al, E. (2017). Genome-wide identification and expression analysis of polyamine oxidase genes in upland cotton (Gossypium hirsutum L.). Plant Cell Tissue Organ Cult. 129, 237–249. doi: 10.1007/s11240-017-1172-0

CrossRef Full Text | Google Scholar

Cona, A., Rea, G., Angelini, R., and Al, E. (2006). Functions of amine oxidases in plant development and defence. Trends Plant Sci. 11, 80–88. doi: 10.1016/j.tplants.2005.12.009

PubMed Abstract | CrossRef Full Text | Google Scholar

Cowley, T., and Walters, D. R. (2010). Local and systemic changes in arginine decarboxylase activity, putrescine levels and putrescine catabolism in wounded oilseed rape. N. Phytol. 165, 807–811. doi: 10.1111/j.1469-8137.2004.01280.x

PubMed Abstract | CrossRef Full Text | Google Scholar

de Oliveira, L. F., Elbl, P., Navarro, B. V., and Al, E. (2016). Elucidation of the polyamine biosynthesis pathway during Brazilian pine (Araucaria angustifolia) seed development. Tree Physiol. 37, 116–130. doi: 10.1093/treephys/tpw107

PubMed Abstract | CrossRef Full Text | Google Scholar

De Oliveira, L. F., Navarro, B. V., Cerruti, G., and Al, E. (2018). Polyamines and amino acid related metabolism: the roles of arginine and ornithine are associated with the embryogenic potential. Plant Cell Physiol. 59, 1084–1098. doi: 10.1093/pcp/pcy049

CrossRef Full Text | Google Scholar

Docimo, T., Reichelt, M., Schneider, B., and Al, E. (2012). The first step in the biosynthesis of cocaine in Erythroxylum coca: the characterization of arginine and ornithine decarboxylases. Plant Mol. Biol. 78, 599–615. doi: 10.1007/s11103-012-9886-1

PubMed Abstract | CrossRef Full Text | Google Scholar

Duan, G. (2000). Effect of speridine on protein contents and protease during senescence of fxicsed wheat leaves. J. Sichuan Teach. Coll. 21, 44–47. doi: 10.3969/j.issn.1673-5072.2000.01.009

CrossRef Full Text | Google Scholar

Duan, G., Huang, Z., and Lin, H. (2006). The role of polyamines in the ontogeny of higher plants. Acta Agric. Boreali Occidentalis Sinica 15, 190–194. doi: 10.7606/j.issn.1004-1389.2006.02.050

CrossRef Full Text | Google Scholar

Durmu, N., and Kadioglu, A. (2005). Spermine and putrescine enhance oxidative stress tolerance in maize leaves. Acta Physiol. Plant. 27, 515–522. doi: 10.1007/s11738-005-0057-8

CrossRef Full Text | Google Scholar

Ebeed, H. T., Hassan, N. M., and Aljarani, A. M. (2017). Exogenous applications of Polyamines modulate drought responses in wheat through osmolytes accumulation, increasing free polyamine levels and regulation of polyamine biosynthetic genes. Plant Physiol. Biochem. 118, 438–448. doi: 10.1016/j.plaphy.2017.07.014

PubMed Abstract | CrossRef Full Text | Google Scholar

Espasandin, F. D., Calzadilla, P. I., Maiale, S. J., and Al, E. (2018). Overexpression of the arginine decarboxylase gene improves tolerance to salt stress in Lotus tenuis plants. J. Plant Growth Regul. 37, 156–165. doi: 10.1007/s00344-017-9713-7

CrossRef Full Text | Google Scholar

Freitas, V. S., Miranda, R. D. S., Costa, J. H., and Al, E. (2017). Ethylene triggers salt tolerance in maize genotypes by modulating polyamine catabolism enzymes associated with H2O2 production. Environ. Exp. Bot. 145, 75–86. doi: 10.1016/j.envexpbot.2017.10.022

CrossRef Full Text | Google Scholar

Gallois, J. L., Drouaud, J., Lécureuil, A., and Al, E. (2013). Functional characterization of the plant ubiquitin regulatory X (UBX) domain-containing protein AtPUX7 in Arabidopsis thaliana. Gene 526, 299–308. doi: 10.1016/j.gene.2013.05.056

PubMed Abstract | CrossRef Full Text | Google Scholar

Gholami, M., Fakhari, A. R., and Ghanati, F. (2013). Selective regulation of nicotine and polyamines biosynthesis in tobacco cells by enantiomers of ornithine. Chirality 25, 22–27. doi: 10.1002/chir.22107

PubMed Abstract | CrossRef Full Text | Google Scholar

Groppa, M. D., and Benavides, M. P. (2008). Polyamines and abiotic stress: recent advances. Amino Acids 34, 35–45. doi: 10.1007/s00726-007-0501-8

PubMed Abstract | CrossRef Full Text | Google Scholar

Groppa, M. D., Tomaro, M. L., and Benavides, M. P. (2001). Polyamines as protectors against cadmium or copper-induced oxidative damage in sunflower leaf discs. Plant Sci. 161, 481–488. doi: 10.1016/S0168-9452(01)00432-0

CrossRef Full Text | Google Scholar

Grossi, M., Phanstiel, O., Rippe, C., and Al, E. (2016). Inhibition of polyamine uptake potentiates the anti-proliferative effect of polyamine synthesis inhibition and preserves the contractile phenotype of vascular smooth muscle cells. J. Cell. Physiol. 231, 1334–1342. doi: 10.1002/jcp.25236

PubMed Abstract | CrossRef Full Text | Google Scholar

Guo, J., Tian, L., Sun, X. Z., and Al, E. (2015). Relationship between endogenous polyamines and floral bud differentiation in Chrysanthemum morifolium under short-day conditions. Wonye kwahak kisulchi 33, 31–38. doi: 10.7235/hort.2015.14043

CrossRef Full Text | Google Scholar

Han, L. (2016). Studies on Mechanism of Low Temperature Storage and Polyamine Impact in Cut Flowers of Herbaceous Peony Postharvest Senescence. Shandong: Shandong Agricultural University.

Google Scholar

Hanfrey, C., Sommer, S., Mayer, M. J., and Al, E. (2010). Arabidopsis polyamine biosynthesis: absence of ornithine decarboxylase and the mechanism of arginine decarboxylase activity. Plant J. 27, 551–560. doi: 10.1046/j.1365-313X.2001.01100.x

PubMed Abstract | CrossRef Full Text | Google Scholar

Hao, Y., Huang, B., Jia, D., and Al, E. (2018). Identification of seven polyamine oxidase genes in tomato (Solanum lycopersicum L.) and their expression profiles under physiological and various stress conditions. J. Plant Physiol. 228, 1–11. doi: 10.1016/j.jplph.2018.05.004

PubMed Abstract | CrossRef Full Text | Google Scholar

Hu, X., Xu, Z., Xu, W., and Al, E. (2015). Application of γ-aminobutyric acid demonstrates a protective role of polyamine and GABA metabolism in muskmelon seedlings under Ca(NO3)2 stress. Plant Physiol. Biochem. 92, 1–10. doi: 10.1016/j.plaphy.2015.04.006

PubMed Abstract | CrossRef Full Text | Google Scholar

Igarashi, K., and Kashiwagi, K. (2015). Modulation of protein synthesis by polyamines. Iubmb Life 67, 160–169. doi: 10.1002/iub.1363

PubMed Abstract | CrossRef Full Text | Google Scholar

Imamura, T., Fujita, K., Tasaki, K., and Al, E. (2015). Characterization of spermidine synthase and spermine synthase–The polyamine-synthetic enzymes that induce early flowering in Gentiana triflora. Biochem. Biophys. Res. Commun. 463, 781–786. doi: 10.1016/j.bbrc.2015.06.013

PubMed Abstract | CrossRef Full Text | Google Scholar

Jia, Y., Guo, S., and Li, J. (2008). Effects of exogenous putrescine on polyamines and antioxidant system in cucumber seedlings under root-zone hypoxia Stress. Acta Bot. Boreali Occidentalia Sinica 28, 1654–1662.

Google Scholar

Jiao, Y., Li, Z., Xu, K., and Al, E. (2017). Study on improving plantlet development and embryo germination rates in in vitro embryo rescue of seedless grapevine. N. Z. J. Crop Horticult. Sci. 46, 39–53. doi: 10.1080/01140671.2017.1338301

CrossRef Full Text | Google Scholar

Kasukabe, Y., He, L., Nada, K., and Al, E. (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. doi: 10.1093/pcp/pch083

PubMed Abstract | CrossRef Full Text | Google Scholar

Kevers, C., Gal, N. L., Monteiro, M., and Al, E. (2000). Somatic embryogenesis of Panax ginseng in liquid cultures: a role for polyamines and their metabolic pathways. Plant Growth Regul. 31, 209–214. doi: 10.1023/A:1006344316683

CrossRef Full Text | Google Scholar

Khajuria, A., and Ohri, P. (2018). Exogenously applied putrescine improves the physiological responses of tomato plant during nematode pathogenesis. Sci. Hortic. 230, 35–42. doi: 10.1016/j.scienta.2017.11.021

CrossRef Full Text | Google Scholar

Khoshbakht, D., Asghari, M. R., and Haghighi, M. (2017). Influence of foliar application of polyamines on growth, gas exchange characteristics, and chlorophyll fluorescence in Bakraii citrus under saline conditions. Photosynthetica 56, 731–742. doi: 10.1007/s11099-017-0723-2

CrossRef Full Text | Google Scholar

Kim, D. W., Watanabe, K., Murayama, C., and Al, E. (2014). Polyamine oxidase5 regulates Arabidopsis growth through thermospermine oxidase activity. Plant Physiol. 165, 1575–1590. doi: 10.1104/pp.114.242610

PubMed Abstract | CrossRef Full Text | Google Scholar

Krasuska, U., Ciacka, K., Bogatek, R., and Al, E. (2013). Polyamines and nitric oxide link in regulation of dormancy removal and germination of Apple (Malus domestica Borkh.) embryos. J. Plant Growth Regul. 33, 590–601. doi: 10.1007/s00344-013-9408-7

CrossRef Full Text | Google Scholar

Krishnan, S., and Merewitz, E. B. (2017). Polyamine Application effects on gibberellic acid content in creeping bentgrass during drought stress. J. Am. Soc. Horticult. Sci. 142, 135–142. doi: 10.21273/JASHS03991-16

CrossRef Full Text | Google Scholar

Kumar, A., Taylor, M., Altabella, T., and Al, E. (1997). Recent advances in polyamine research. Trends Plant Sci. 2, 124–130. doi: 10.1016/S1360-1385(97)01013-3

CrossRef Full Text | Google Scholar

Kumar, V., Giridhar, P., Chandrashekar, A., and Al, E. (2008). Polyamines influence morphogenesis and caffeine biosynthesis in vitro cultures of Coffea canephora P. Acta Physiol. Plant. 30, 217–223. doi: 10.1007/s11738-007-0110-x

CrossRef Full Text | Google Scholar

Kusano, T., Berberich, T., Tateda, C., and Al, E. (2008). Polyamines: essential factors for growth and survival. Planta 228, 367–381. doi: 10.1007/s00425-008-0772-7

PubMed Abstract | CrossRef Full Text | Google Scholar

Lasanajak, Y., Minocha, R., Minocha, S. C., and Al, E. (2014). Enhanced flux of substrates into polyamine biosynthesis but not ethylene in tomato fruit engineered with yeast S-adenosylmethionine decarboxylase gene. Amino Acids 46, 729–742. doi: 10.1007/s00726-013-1624-8

CrossRef Full Text | Google Scholar

Li, B., Guo, S., Sun, J., and Al, E. (2011). Effects of exogenous spermidine on free polyamine content and polyamine biosynthesis gene expression in cucumber seedlings under salt Stress. Plant Sci. J. 29, 480–485.

Google Scholar

Li, C., Pei, Z., and Gan, L. (2014). Effects of photoperiod on flowering and polyamine contents of nobile-type Dendrobium. Plant Physiol. J. 1167–1170. doi: 10.13592/j.cnki.ppj.2012.0435

CrossRef Full Text | Google Scholar

Li, K., Xing, C., Yao, Z., and Al, E. (2017). PbrMYB21, a novel MYB protein of Pyrus betulaefolia, functions in drought tolerance and modulates polyamine levels by regulating arginine decarboxylase gene. Plant Biotechnol. J. 15, 1186–1203. doi: 10.1111/pbi.12708

PubMed Abstract | CrossRef Full Text | Google Scholar

Li, Q., Ge, H., and Hu, S. (2008). Effects of exogenous putrescine and calciumon ion uptake of strawberry seedling under NaCI stress. J. Plant Nutr. Fertil. 14, 540–545. doi: 10.3724/SP.J.1005.2008.01083

CrossRef Full Text | Google Scholar

Li, R., Shen, H., and Li, M. (1995). Effects of acid stress on the contents of proline and putrescine in several forest trees. J. Nanjing Forestry Univ. 9, 88–93.

Google Scholar

Li, S., Jin, H., and Zhang, Q. (2016). The effect of exogenous spermidine concentration on polyamine metabolism and salt tolerance inzoysiagrass (Zoysia japonica Steud) subjected to short-term salinity stress. Front. Plant Sci. 7:1221. doi: 10.3389/fpls.2016.01221

PubMed Abstract | CrossRef Full Text | Google Scholar

Li, Y., and He, J. (2012). Advance in metabolism and response to stress of polyamines in plant. Acta Agric. Boreali Sinica 27, 240–245. doi: 10.3969/j.issn.1000-7091.2012.z1.048

CrossRef Full Text | Google Scholar

Liu, K., Fu, H., Bei, Q., and Al, E. (2000). Inward potassium channel in guard cells as a target for polyamine regulation of stomatal movements. Plant Physiol. 124, 1315–1325. doi: 10.1104/pp.124.3.1315

PubMed Abstract | CrossRef Full Text | Google Scholar

Liu, Q., Nishibori, N., Imai, I., and Al, E. (2016). Response of polyamine pools in marine phytoplankton to nutrient limitation and variation in temperature and salinity. Mar. Ecol. Prog. 544, 93–105. doi: 10.3354/meps11583

CrossRef Full Text | Google Scholar

Liu, T., Kim, D. W., Niitsu, M., and Al, E. (2014). Polyamine oxidase 7 is a terminal catabolism-type enzyme in Oryza sativa and is specifically expressed in anthers. Plant Cell Physiol. 55, 1110–1122. doi: 10.1093/pcp/pcu047

PubMed Abstract | CrossRef Full Text | Google Scholar

Liu, W., Tan, M., Zhang, C., and Al, E. (2017). Functional characterization of murB-potABCD operon for polyamine uptake and peptidoglycan synthesis in Streptococcus suis. Microbiol. Res. 207, 177–187. doi: 10.1016/j.micres.2017.11.008

PubMed Abstract | CrossRef Full Text | Google Scholar

Liu, Y., Gu, D., Wu, W., and Al, E. (2013). The relationship between polyamines and hormones in the regulation of wheat grain. Filling 8:e78196. doi: 10.1371/journal.pone.0078196

PubMed Abstract | CrossRef Full Text | Google Scholar

Liu, Y., Zuo, Z., and Hu, J. (2010). Effects of exogenous polyamines on growth and drought resistance of Apple seedlings. J. Northwest Forestry Univ. 25, 000039–000042.

Google Scholar

Luo, J., Fuell, C., Parr, A., and Al, E. (2009). A novel polyamine acyltransferase responsible for the accumulation of spermidine conjugates in Arabidopsis seed. Plant Cell 21, 318–333. doi: 10.1105/tpc.108.063511

PubMed Abstract | CrossRef Full Text | Google Scholar

Martin-Tanguy, J. (2010). Conjugated polyamines and reproductive development: biochemical, molecular and physiological approaches. Physiol. Plant 100, 675–688. doi: 10.1111/j.1399-3054.1997.tb03074.x

CrossRef Full Text | Google Scholar

Mellidou, I., Karamanoli, K., Beris, D., and Al, E. (2017). Underexpression of apoplastic polyamine oxidase improves thermotolerance in Nicotiana tabacum. J. Plant Physiol. 218, 171–174. doi: 10.1016/j.jplph.2017.08.006

PubMed Abstract | CrossRef Full Text | Google Scholar

Meng, D., Hou, L., and Yang, S. (2015). Exogenous polyamines alleviating salt stress on peanuts (Arachis hypogaea) grown in pots. Chin. J. Plant Ecol. 39, 1209–1215. doi: 10.17521/cjpe.2015.0117

CrossRef Full Text | Google Scholar

Miller-Fleming, L., Olin-Sandoval, V., Campbell, K., and Al, E. (2015). Remaining mysteries of molecular biology: the role of polyamines in the cell. J. Mol. Biol. 427, 3389–3406. doi: 10.1016/j.jmb.2015.06.020

PubMed Abstract | CrossRef Full Text | Google Scholar

Minocha, R., Majumdar, R., and Minocha, S. C. (2014). Polyamines and abiotic stress in plants: a complex relationship. Front. Plant Sci. 5:175. doi: 10.3389/fpls.2014.00175

PubMed Abstract | CrossRef Full Text | Google Scholar

Minocha, S. C., and Minocha, R. (1995). Role of Polyamines in Somatic Embryogenesis. Berlin; Heidelberg: Springer. doi: 10.1007/978-3-662-03091-2_5

CrossRef Full Text | Google Scholar

Mohammadi, H., Ghorbanpour, M., and Brestic, M. (2018). Exogenous putrescine changes redox regulations and essential oil constituents in field-grown Thymus vulgaris L. under well-watered and drought stress conditions. Ind. Crops Prod. 122, 119–132. doi: 10.1016/j.indcrop.2018.05.064

CrossRef Full Text | Google Scholar

Molesini, B., Mennella, G., Martini, F., and Al, E. (2015). Involvement of the putative N-acetylornithine deacetylase from Arabidopsis thaliana in flowering and fruit development. Plant Cell Physiol. 56, 1084–1096. doi: 10.1093/pcp/pcv030

PubMed Abstract | CrossRef Full Text | Google Scholar

Montesinos-Pereira, D., Barrameda-Medina, Y., Romero, L., Ruiz, J., and M, Sánchez-Rodríguez, E. (2015). Genotype differences in the metabolism of proline and polyamines under moderate drought in tomato plants. Plant Biol. 16, 1050–1057. doi: 10.1111/plb.12178

PubMed Abstract | CrossRef Full Text | Google Scholar

Moschou, P. N., Paschalidis, K. A., and Roubelakis-Angelakis, K. A. (2008). Plant polyamine catabolism. Plant Signal. Behav. 3, 1061–1066. doi: 10.4161/psb.3.12.7172

PubMed Abstract | CrossRef Full Text | Google Scholar

Mustafavi, S. H., Badi, H. N., Sekara, A., and Al, E. (2018). Polyamines and their possible mechanisms involved in plant physiological processes and elicitation of secondary metabolites. Acta Physiol. Plant. 40, 102. doi: 10.1007/s11738-018-2671-2

CrossRef Full Text | Google Scholar

Mutlu, F., and Bozcuk, S. (2005). Effects of salinity on the contents of polyamines and some other compounds in sunflower plants differing in salt tolerance. Russian J. Plant Physiol. 52, 29–34. doi: 10.1007/s11183-005-0005-x

CrossRef Full Text | Google Scholar

Nahar, K., Hasanuzzaman, M., Rahman, A., and Al, E. (2016). Polyamines confer salt tolerance in Mung Bean (Vigna radiata L.) by reducing sodium uptake, improving nutrient homeostasis, antioxidant defense, and methylglyoxal detoxification systems. Front. Plant Sci. 7:1104. doi: 10.3389/fpls.2016.01104

PubMed Abstract | CrossRef Full Text | Google Scholar

Naka, Y., Watanabe, K., Sagor, G. H. M., and Al, E. (2010). Quantitative analysis of plant polyamines including thermospermine during growth and salinity stress. Plant Physiol. Biochem. 48, 527–533. doi: 10.1016/j.plaphy.2010.01.013

PubMed Abstract | CrossRef Full Text | Google Scholar

Ouyang, J., Song, C., and Chen, D. (2017). Research progress on heat-tolerance mechanism and transports of polyamfines in plant. Mol. Plant Breed. 15, 3286–3294. doi: 10.13271/j.mpb.015.003286

CrossRef Full Text | Google Scholar

Pál, M., Szalai, G., and Janda, T. (2015). Speculation: polyamines are important in abiotic stress signaling. Plant Sci. 237, 16–23. doi: 10.1016/j.plantsci.2015.05.003

PubMed Abstract | CrossRef Full Text | Google Scholar

Pandey, R., Gupta, A., Chowdhary, A., and Al, E. (2015). Over-expression of mouse ornithine decarboxylase gene under the control of fruit-specific promoter enhances fruit quality in tomato. Plant Mol. Biol. 87, 249–260. doi: 10.1007/s11103-014-0273-y

PubMed Abstract | CrossRef Full Text | Google Scholar

Parvin, S., Lee, O. R., Sathiyaraj, G., and Al, E. (2014). Spermidine alleviates the growth of saline-stressed ginseng seedlings through antioxidative defense system. Gene 537, 70–78. doi: 10.1016/j.gene.2013.12.021

PubMed Abstract | CrossRef Full Text | Google Scholar

Paul, S., and Roychoudhury, A. (2017). Seed priming with spermine and spermidine regulates the expression of diverse groups of abiotic stress-responsive genes during salinity stress in the seedlings of indica rice varieties. Plant Gene 11, 124–132. doi: 10.1016/j.plgene.2017.04.004

CrossRef Full Text | Google Scholar

Pegg, A. E. (2016). Functions of polyamines in mammals. J. Biol. Chem. 291, 14904–14912. doi: 10.1074/jbc.R116.731661

PubMed Abstract | CrossRef Full Text | Google Scholar

Perezamador, M. A., Leon, J., Green, P. J., and Al, E. (2002). Induction of the arginine decarboxylase ADC2 gene provides evidence for the involvement of polyamines in the wound response in Arabidopsis. Plant Physiol. 130, 1454–1463. doi: 10.1104/pp.009951

CrossRef Full Text | Google Scholar

Peynevandi, K. M., Razavi, S. M., and Zahri, S. (2018). The ameliorating effects of polyamine supplement on physiological and biochemical parameters of Stevia rebaudiana Bertoni under cold stress. Plant Prod. Sci. 21, 123–131. doi: 10.1080/1343943X.2018.1437756

CrossRef Full Text | Google Scholar

Regla-Márquez, C. F., Canto-Flick, A., Avilés-Viñas, S. A., and Al, E. (2015). Cadaverine: a common polyamine in zygotic embryos and somatic embryos of the species Capsicum chinense Jacq. PCTOC 124, 253–264. doi: 10.1007/s11240-015-0889-x

CrossRef Full Text | Google Scholar

Reis, R. S., Vale, E. M., Heringer, A. S., and Al, E. (2016). Putrescine induces somatic embryo development and proteomic changes in embryogenic callus of sugarcane. J. Proteomics 130, 170–179. doi: 10.1016/j.jprot.2015.09.029

PubMed Abstract | CrossRef Full Text | Google Scholar

Roy, M., and Wu, R. (2001). Arginine decarboxylase transgene expression and analysis of environmental stress tolerance in transgenic rice. Plant Sci. 160, 869–875. doi: 10.1016/S0168-9452(01)00337-5

PubMed Abstract | CrossRef Full Text | Google Scholar

Roy, M., and Wu, R. (2002). Overexpression of S-adenosylmethionine decarboxylase gene in rice increases polyamine level and enhances sodium chloride-stress tolerance. Plant Sci. 163, 987–992. doi: 10.1016/S0168-9452(02)00272-8

CrossRef Full Text | Google Scholar

Saha, J., Brauer, E. K., Sengupta, A., and Al, E. (2015). Polyamines as redox homeostasis regulators during salt stress in plants. Front. Environ. Sci. 3:21. doi: 10.3389/fenvs.2015.00021

CrossRef Full Text | Google Scholar

Sánchezrodríguez, E., Romero, L., and Ruiz, J. M. (2016). Accumulation of free polyamines enhances the antioxidant response in fruits of grafted tomato plants under water stress. J. Plant Physiol. 190, 72–78. doi: 10.1016/j.jplph.2015.10.010

CrossRef Full Text | Google Scholar

Sen, S., Ghosh, D., and Mohapatra, S. (2018). Modulation of polyamine biosynthesis in Arabidopsis thaliana by a drought mitigating Pseudomonas putida strain. Plant Physiol. Biochem. 129, 180–188. doi: 10.1016/j.plaphy.2018.05.034

PubMed Abstract | CrossRef Full Text | Google Scholar

Sequeramutiozabal, M. I., Erban, A., Kopka, J., and Al, E. (2016). Global metabolic profiling of Arabidopsis polyamine oxidase 4 (AtPAO4) loss-of-function mutants exhibiting delayed dark-induced senescence. Front. Plant Sci. 7:173. doi: 10.3389/fpls.2016.00173

CrossRef Full Text | Google Scholar

Serafini-Fracassini, D., Sandro, A. D., and Duca, S. D. (2010). Spermine delays leaf senescence in Lactuca sativa and prevents the decay of chloroplast photosystems. Plant Physiol. Biochem. 48, 602–611. doi: 10.1016/j.plaphy.2010.03.005

PubMed Abstract | CrossRef Full Text | Google Scholar

Serrano, M., Mc, M.-M., and Mt, P. (1997). Modified atmosphere packaging minimizes increases in putrescine and abscisic acid levels caused by chilling injury in pepper fruit. J. Agric. Food Chem. 45, 1668–1672. doi: 10.1021/jf960866h

CrossRef Full Text | Google Scholar

Serrano, M., Pretel, M. T., and Martinezmadrid, M. C. (1998). CO2 treatment of zucchini squash reduces chilling-induced physiological changes. J. Agric. Food Chem. 46, 2465–2468. doi: 10.1021/jf970864c

CrossRef Full Text | Google Scholar

Shao, C. G., Wang, H., and Yu-Fen, B. I. (2015). Relationship between endogenous polyamines and tolerance in Medicago sativa L.under heat stress. Acta Agrestia Sinica. 23, 1214–1219. doi: 10.11733/j.issn.1007-0435

CrossRef Full Text | Google Scholar

Simões, A. D. N., Diniz, N. B., Vieira, M. R. D. S., and Al, E. (2018). Impact of GA3 and spermine on postharvest quality of anthurium cut flowers (Anthurium andraeanum) cv. Arizona. Sci. Horticult. 241, 178–186. doi: 10.1016/j.scienta.2018.06.095

CrossRef Full Text | Google Scholar

Smita, R., and Upendranath, D. (2008). Manipulation of lignin in plants with special reference to O-methyltransferase. Plant Sci. 174, 264–277. doi: 10.1016/j.plantsci.2007.11.014

CrossRef Full Text | Google Scholar

Sobieszczuk-Nowicka, E. (2017). Polyamine catabolism adds fuel to leaf senescence. Amino Acids 49, 49–56. doi: 10.1007/s00726-016-2377-y

PubMed Abstract | CrossRef Full Text | Google Scholar

Su, J. J., Wi, S. J., Choi, Y. J., and Al, E. (2012). Increased polyamine biosynthesis enhances stress tolerance by preventing the accumulation of reactive oxygen species: T-DNA mutational analysis of oryza sativa lysine decarboxylase-like Protein 1. Molecules Cells 34, 251–262. doi: 10.1007/s10059-012-0067-5

CrossRef Full Text | Google Scholar

Sun, L., Yu, S., and Zhao, F. (2018a). Effects of salt stress on polyamines and hormone metabolism in Grape seedlings. Xinjiang Agric. Sci. 55, 66–73. doi: 10.6048/j.issn.1001-4330

CrossRef Full Text | Google Scholar

Sun, X., Wang, Y., Tan, J., and Al, E. (2018b). Effects of exogenous putrescine and D-Arg on physiological and biochemical indices of anthurium under chilling stress. Jiangsu J. Agric. Sci. 34, 152–157 doi: 10.3969/j.issn.1000-4440.2018.01.022

CrossRef Full Text | Google Scholar

Tajti, J., Janda, T., Majláth, I., Szalai, G., and Pál, M. (2018). Comparative study on the effects of putrescine and spermidine pre-treatment on cadmium stress in wheat. Ecotoxicol. Environ. Safety 148, 546–554. doi: 10.1016/j.ecoenv.2017.10.068

PubMed Abstract | CrossRef Full Text | Google Scholar

Takahashi, Y., Ono, K., Akamine, Y., Asano, T., Ezaki, M., and Mouri, I. (2017a). Highly-expressed polyamine oxidases catalyze polyamine back conversion in Brachypodium distachyon. J. Plant Res. 131, 341–348. doi: 10.1007/s10265-017-0989-2

PubMed Abstract | CrossRef Full Text | Google Scholar

Takahashi, Y., Tahara, M., Yamada, Y., and Al, E. (2017b). Characterization of the polyamine biosynthetic pathways and salt stress response in Brachypodium distachyon. J. Plant Growth Regul.37, 625–634. doi: 10.1007/s00344-017-9761-z

CrossRef Full Text | Google Scholar

Tan, Y., Hu, W., Xu, X., and Al, E. (2017). Polyamine plays a role in subculture growth of in vitro callus of indica rice. Acta Biol. Cracoviensia S Botanica 59, 105–112. doi: 10.1515/abcsb-2017-0001

CrossRef Full Text | Google Scholar

Tassoni, A., Buuren, M. V., Franceschetti, M., and Al, E. (2000). Polyamine content and metabolism in Arabidopsis thaliana and effect of spermidine on plant development. Plant Physiol. Biochem. 38, 383–393. doi: 10.1016/S0981-9428(00)00757-9

CrossRef Full Text | Google Scholar

Tatte, S., Alka, S.ingh, and Ahlawat, T. R. (2015). Effect of PAs on postharvest quality and vaselife of rose var. Samurai The Bioscan 10, 675–678.

Google Scholar

Tian, J. (2012). Physiological regulation function and proteomics research of exogenous spermidine on alleviating high temperature stressthe of cucumber seedlings. Nanjing Agric. Unive. 7–21.

Google Scholar

Tiburcio, A. F., Altabella, T., Bitrián, M., and Alcázar, R. (2014). The roles of polyamines during the lifespan of plants: from development to stress. Planta 240, 1–18. doi: 10.1007/s00425-014-2055-9

PubMed Abstract | CrossRef Full Text | Google Scholar

Tun, N. N., Santa-Catarina, C., Begum, T., Silveira, V., Handro, W., and Floh, E. I. (2006). Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol. 47, 346–354. doi: 10.1093/pcp/pci252

PubMed Abstract | CrossRef Full Text | Google Scholar

Verma, S., and Mishra, S. N. (2005). Putrescine alleviation of growth in salt stressed Brassica juncea by inducing antioxidative defense system. J. Plant Physiol. 162, 669–677. doi: 10.1016/j.jplph.2004.08.008

PubMed Abstract | CrossRef Full Text | Google Scholar

Vondráková, Z., Eliášová, K., Vágner, M., and Al, E. (2015). Exogenous putrescine affects endogenous polyamine levels and the development of Picea abies somatic embryos. Plant Growth Regul. 75, 405–414. doi: 10.1007/s10725-014-0001-2

CrossRef Full Text | Google Scholar

Vuosku, J., Karppinen, K., Muilu-Mäkelä, R., Kusano, T., Sagor, G. H. M., and Avia, K. (2018). Scots pine aminopropyltransferases shed new light on evolution of the polyamine biosynthesis pathway in seed plants. Ann. Bot. 121, 1243–1256. doi: 10.1093/aob/mcy012

PubMed Abstract | CrossRef Full Text | Google Scholar

Vuosku, J., Suorsa, M., Ruottinen, M., Sutela, S., Muilu-Mäkelä, R., and Julkunen-Tiitto, R. (2012). Polyamine metabolism during exponential growth transition in Scots pine embryogenic cell culture. Tree Physiol. 32, 1274–1287. doi: 10.1093/treephys/tps088

PubMed Abstract | CrossRef Full Text | Google Scholar

Wang, J. (2009). Changes in polyamine contents in Citrus and its closely related species under abitic stresses and isolation, characterization of two polyamine biosynthetic genes. Huazhong Agric. Univ. 1–8 doi: 10.7666/d.y1995975

CrossRef Full Text | Google Scholar

Wang, Q., and Bo, Y. (2014). Alleviative effects of different kinds of exogenous polyamines on salt inj ury of Soybean seedlings. J. Henan Agric. Sci. 43, 48–50. doi: 10.3969/j.issn.1004-3268.2014.04.011

CrossRef Full Text | Google Scholar

Wang, W., and Liu, J. H. (2015). Genome-wide identification and expression analysis of the polyamine oxidase gene family in sweet orange (Citrus sinensis). Gene 555, 421–429. doi: 10.1016/j.gene.2014.11.042

PubMed Abstract | CrossRef Full Text | Google Scholar

Wang, X. (2007). Studies on the evaluation methods and the mechanism of resistance of Chinese Cabbage (Brassica campestris L.) to Diamondback Moth (Plutella xylostella). Chin. Acad. Agric. Sci. 24–31 doi: 10.7666/d.Y1057065

CrossRef Full Text | Google Scholar

Wang, X., and Shi, G. (2004). Effect of exogenous spermidine on anti-Hg2+ stress ability of Amaranth. J. Plant Physiol. Mol. Biol. 30, 69–74. doi: 10.3321/j.issn:1671-3877.2004.01.010

CrossRef Full Text | Google Scholar

Wang, X., Shi, G., and Xu, Q. (2003a). Toxic effects of Cr6+ on nymphoides peltatum mitigated by exogenous polyamine. Acta Sci. Circumst. 23, 689–693. doi: 10.3321/j.issn:0253-2468.2003.05.024

CrossRef Full Text | Google Scholar

Wang, Y., Lu, W., and Zhang, Z. (2003b). ABA and putrescine treatment alleviate the chilling damage of banana fruit. J. Plant Physiol. Mol. Biol. 29, 549–554. doi: 10.3321/j.issn:1671-3877.2003.06.011

CrossRef Full Text | Google Scholar

Woo, H.R, Kim, H.J, Nam, H.G, and Lim, P. O. (2013). Plant leaf senescence and death–regulation by multiple layers of control and implications for aging in general. J. Cell Sci. 126, 4823–4833. doi: 10.1242/jcs.109116

PubMed Abstract | CrossRef Full Text | Google Scholar

Wu, J., Shu, S., Li, C., Sun, J., and Guo, S. (2018). Spermidine-mediated hydrogen peroxide signaling enhances the antioxidant capacity of salt-stressed cucumber roots. Plant Physiol. Biochem. 128, 152–162. doi: 10.1016/j.plaphy.2018.05.002

PubMed Abstract | CrossRef Full Text | Google Scholar

Wu, M., and Yuan, L. (2008). Research progress in the relationship between polyamine and plant resistance. J. Anhui Agric. Sci. 36, 3516–3518. doi: 10.3969/j.issn.0517-6611.2008.09.020

CrossRef Full Text | Google Scholar

Xu, C., Wu, X., and Zhang, H. (2009). Impact of D-Arg on drought resistance and endogenous polyamines in mycorrhizal Pinus massoniana. J. Nanjing Forestry Univ. 33, 019–023. doi: 10.3969/j.issn.1000-2006.2009.04.004

CrossRef Full Text | Google Scholar

Xu, D., Guo, J., and Xu, L. (2014a). The relationship between polyamine oxidase activity and lignin deposition and chrysanthemum flower bud differentiation. Acta Agric. Boreali Sinica 29, 164-169. doi: 10.7668/hbnxb.2014.03.030

CrossRef Full Text | Google Scholar

Xu, L. (2015). The effect of polyamineon flower bud differentiation and bud germination of chrysanthemum. Shandong Agric. Univ. 31–36.

Google Scholar

Xu, L., Xing, S. T, and Sun, X. (2014b). Effects of polyamines on hormones contents and the relationship with the flower bud differentiation in chrysanthemum. Plant Physiol. J. 50, 1195–1202. doi: 10.13592/j.cnki.ppj.2014.0212

CrossRef Full Text | Google Scholar

Yadav, J. S., and Rajam, M. V. (1997). Spatial distribution of free and conjugated polyamines in leaves of Solanum melongena L. associated with differential morphogenetic capacity: efficient somatic embryogenesis with putrescine. J. Exp. Bot. 48, 1537–1545. doi: 10.1093/jxb/48.8.1537

CrossRef Full Text | Google Scholar

Yamaguchi, K., Takahashi, Y., Berberich, T., and Al, E. (2007). A protective role for the polyamine spermine against drought stress in Arabidopsis. Biochem. Biophys. Res. Commun. 352, 486–490. doi: 10.1016/j.bbrc.2006.11.041

PubMed Abstract | CrossRef Full Text | Google Scholar

Yamamoto, A., Shim, I. S., and Fujihara, S. (2016). Inhibition of putrescine biosynthesis enhanced salt stress sensitivity and decreased spermidine content in rice seedlings. Biol. Plant. 61, 385–388. doi: 10.1007/s10535-016-0676-5

CrossRef Full Text | Google Scholar

Yang, C., and He, S. (2001). The relationship between polyamine and membrane lipid peroxidase during the senescence of cut rose flowers. Acta Botanica Boreali Occidentalia Sinica 21, 1157–1161. doi: 10.1109/8.244640

CrossRef Full Text | Google Scholar

Yang, L., Liang, H., Lv, X., Liu, D., Wen, X., and Liao, Y. (2016). Effect of polyamines on the grain filling of wheat under drought stress. Plant Physiol. Biochem. 100, 113–129. doi: 10.1016/j.plaphy.2016.01.003

CrossRef Full Text | Google Scholar

Yang, Y., and Yang, X. (2002). Effect of temperature on endogenous polyamine content in leaves of Chinese Kale Seedlings. J. South China Agric. Univ. 23, 9–12. doi: 10.3969/j.issn.1001-411X.2002.03.003

CrossRef Full Text | Google Scholar

Yin, Z. P., Li, S., Ren, J., and Al, E. (2014). Role of spermidine and spermine in alleviation of drought-induced oxidative stress and photosynthetic inhibition in Chinese dwarf cherry (Cerasus humilis) seedlings. Plant Growth Regul. 74, 209–218. doi: 10.1007/s10725-014-9912-1

CrossRef Full Text | Google Scholar

Yordanova, R. Y., Alexieva, V. S., and Popova, L. P. (2003). Influence of root oxygen deficiency on photosynthesis and antioxidant status in barley plants1. Russian J. Plant Physiol. 50, 163–167. doi: 10.1023/A:1022908811211

CrossRef Full Text | Google Scholar

Zeid, I. M., and Shedeed, Z. A. (2006). Response of alfalfa to putrescine treatment under drought stress. Biol. Plant. 50, 635–640. doi: 10.1007/s10535-006-0099-9

CrossRef Full Text | Google Scholar

Zhao, W., Sun, G., and Li, S. (2004). Polyamines and plant stress resistance. J. Southern Agric. 35, 443–447. doi: 10.3969/j.issn.2095-1191.2004.06.003

CrossRef Full Text | Google Scholar

Zhen, Y., Li, S., and Su, X. (2000). Polvamine changes and chilling injury in cold-stored Loquat fruits. J. Integr. Plant Biol. 42, 824–827. doi: 10.3321/j.issn:1672-9072.2000.08.007

CrossRef Full Text | Google Scholar

Zhuo, C., Liang, L., Zhao, Y., Guo, Z, and Lu, S. (2018). A cold responsive ethylene responsive factor from Medicago falcata confers cold tolerance by up-regulation of polyamine turnover, antioxidant protection, and proline accumulation. Plant Cell Environ. 41, 2021–2032. doi: 10.1111/pce.13114

PubMed Abstract | CrossRef Full Text | Google Scholar

Keywords: polyamines, flowering, embryonic development, senescence, abiotic stress

Citation: Chen D, Shao Q, Yin L, Younis A and Zheng B (2019) Polyamine Function in Plants: Metabolism, Regulation on Development, and Roles in Abiotic Stress Responses. Front. Plant Sci. 9:1945. doi: 10.3389/fpls.2018.01945

Received: 06 October 2018; Accepted: 13 December 2018;
Published: 10 January 2019.

Edited by:

Vasileios Fotopoulos, Cyprus University of Technology, Cyprus

Reviewed by:

Toshihiro Obata, University of Nebraska-Lincoln, United States
Caiji Gao, South China Normal University, China

Copyright © 2019 Chen, Shao, Yin, Younis and Zheng. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Qingsong Shao, sqszjfc@126.com