Polyamines: Natural and engineered abiotic and biotic stress tolerance in plants

Biotechnology Advances 29 (2011) 300–311

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Research review paper

Polyamines: Natural and engineered abiotic and biotic stress tolerance in plants

Syed Sarfraz Hussain a,⁎, Muhammad Ali b, Maqbool Ahmad c, Kadambot H.M. Siddique d,e

a Australian Centre for Plant Functional Genomics (ACPFG), University of Adelaide, PMB1, Glen Osmond SA5064, Australiab Institute of Biotechnology, Bahauddin Zakariya University, Multan 60800 Pakistanc South Australian Research and Development Institute (SARDI), GPO Box 397, Adelaide SA 5001, Australiad The UWA Institute of Agriculture, The University of Western Australia, Crawley, 6009, W.A., Australiae College of Food and Agricultural Sciences, King Saud University, P.O. Box 2460, Riyadh 11451, Saudi Arabia

⁎ Corresponding author. Tel.: +61 8 8303 7183; fax: +E-mail addresses: [email protected], syedsarf

[email protected] (K.H.M. Siddique).

0734-9750/$ – see front matter © 2011 Elsevier Inc. Aldoi:10.1016/j.biotechadv.2011.01.003

a b s t r a c t
a r t i c l e i n f o
Article history:Received 17 November 2010Received in revised form 7 January 2011Accepted 7 January 2011Available online 15 January 2011

Keywords:Compatible soluteAbiotic stressesBiotic stressesApoptosisTransgenic plantsAntioxidantsSignaling molecules

Polyamines (PAs) are ubiquitous biogenic amines that have been implicated in diverse cellular functions inwidely distributed organisms. In plants, mutant and transgenic plants with altered activity pointed to theirinvolvement with different abiotic and biotic stresses. Furthermore, microarray, transcriptomic andproteomic approaches have elucidated key functions of different PAs in signaling networks in plantssubjected to abiotic and biotic stresses, however the exact molecular mechanism remains enigmatic. Here, weargue that PAs should not be taken only as a protective molecule but rather like a double-faced molecule thatlikely serves as a major area for further research efforts. This review summarizes recent advances in plantpolyamine research ranging from transgenic and mutant characterization to potential mechanisms of actionduring environmental stresses and diseases.

61 8 8303 [email protected] (S.S. Hussain), mohammad_03ali@

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Contents

1. Polyamine: A mysterious modulator involved in plant responses to stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3012. Polyamine biosynthesis in plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 301

2.1. Polyamine-related genes in plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3013. Polyamine and plant response to abiotic stresses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 302

3.1. Polyamine metabolism under abiotic stress conditions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3023.2. Plant stress tolerance modulated by polyamine treatment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3023.3. Plant abiotic stress tolerance modulated by engineering the polyamine synthesis pathway . . . . . . . . . . . . . . . . . . . . . . 303

4. Polyamine and plant stress response: Potential mechanism of action . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3044.1. Polyamine: A compatible solute in higher plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3044.2. Polyamine and antioxidant response . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3044.3. Polyamine: A signal molecule during stress response. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3054.4. Polyamine: Regulation of ion channel and Ca2+ homeostasis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3054.5. Polyamine and programmed cell death (PCD) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 305

5. Polyamine and plant responses to biotic stresses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3065.1. Polyamine: Elicitor of the plant defense response . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3065.2. Polyamine and plant–mycorrhiza association . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3065.3. Polyamine and plant–pathogen interaction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 306

yahoo.com (M. Ali), [email protected] (M. Ahmad),

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301S.S. Hussain et al. / Biotechnology Advances 29 (2011) 300–311

6. Concluding remarks and future perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 307Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 307References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 307

1. Polyamine: A mysterious modulator involved in plant responsesto stress

Plants being sessile have to cope with continuous environmentalfluctuationswith appropriate physiological, developmental and biochem-ical changes (Mahajan and Tuteja, 2005). Abiotic stresses represent theprimary cause of crop loss worldwide with reductions of more than 50%(Alcázar et al., 2006; Hussain et al., in press-a). It is further predicted thatthese stresses will become more intense and frequent with climatechange. On the other hand, the ever increasing world population,estimated to be 10 billion by 2050, will witness serious food shortage bythat time (Bartels andHussain, 2008). To counteract these stresses, plantsare equippedwith a large set of defensemechanisms (Bartels and Sunkar,2005). The accumulation of some functional substances such ascompatible low molecular weight organic osmolites: aminoacids, sugars,sugar alcohols, and betaines (Kuznetsov and Shevyakova, 1999; Hussainet al., in press-b) and protective proteins is an integral component of thephysiological and biochemical response under stress conditions (Hussainet al., in press-c). These solutes protect cell turgor and restorewater statusof cells by maintaining cellular water potential as well as acting aschaperones to stabilize membranes or scavengers of ROS.

Among thedifferent classes of compatible solutes, polyamines standasone of the most effective against extreme environmental stress.Polyamines (PAs) are low molecular weight aliphatic nitrogen com-pounds positively charged at physiological pH (Groppa and Benavides,2008) that are found in awide range of organisms from bacteria to plantsand animals (Alcázar et al., 2006). Polyamine (tetraamine spermine) wasfirst reported more than 300 years ago in human spermatozoa (vanLeeuwenhoek, 1678). The success of PAs in nature compared to othercompatible solutes can be explained by their peculiar functions. Theseamines have been thoroughly investigated due to their role in a variety ofregulatory and cellular processes such as cell division and elongation, rootgrowth, flower and fruit development, replication, transcription, transla-tion, membrane and cell wall stabilization, chromatin organization,ribosome biogenesis and programmed cell death (Bais and Ravishankar,2002; Evans and Malmberg, 1989; Galston et al., 1997; Igarashi andKashiwagi, 2000; Kusano et al., 2007a,b; Liu et al., 2006; Paschalidis andRoubelakis-Angelakis, 2005a,b; Thomas and Thomas, 2001;Walden et al.,1997; Zhao and Yang, 2008). PAs are also implicated in a wide range ofdiverse environmental stresses (Bouchereau et al., 1999; Kasukabe et al.,2004; Kumar et al., 1997; Liu et al., 2007)which includes drought (Nayyaret al., 2005; Yamaguchi et al., 2007; Yang et al., 2007), salinity (Duan et al.,2008; Kuznetsov and Shevyakova, 2010), low temperature (Cuevas et al.,2008; Imai et al., 2004; Nayyar, 2005), oxidative stress (Rider et al., 2007)and metal toxicity (Groppa and Benavides, 2008; Groppa et al., 2003;Wang et al., 2007; Shevyakova et al., 2010).

It is well-documented that PAs are present in all compartments ofthe plant cell, including the nucleus, which indicates their role in thecontrol of diverse fundamental cellular processes (Bouchereau et al.,1999; Kaur-Sawhney et al., 2003). Plant polyamines are preferentiallydetected in actively growing tissues. However, concentration of PAsmay vary markedly depending on plant species, organ and tissue andalso on the developmental stage. Their biological activity is attributedto cationic nature therefore PAs interact with negatively chargedmacromolecules such as DNA, RNA, proteins and phospholipids. Thesereversible ionic interactions lead to the stabilization of macromole-cules. These findings have been discussed in detail in several recentarticles (Groppa and Benavides, 2008; Kaur-Sawhney et al., 2003;Kusano et al., 2008; Liu et al., 2006; Pang et al., 2007).

In the past decade, however, investigations into plant PAs at amolecular level have led to isolation of a number of genes encoding PAbiosynthetic enzymes from a variety of plant species (Bagni andTassoni, 2001; Ge et al., 2006; Hanzawa et al., 1997, 2000, 2002;Janowitz et al., 2003;Malmberg et al., 1998; Piotrowski et al., 2003). Inrecent years, molecular and genomic studies with mutants andtransgenic plants having no or altered activity of enzymes involved inthe biosynthesis of PAs have contributed to a better understanding ofbiological functions of PAs in plants. However, the precise roles of PAsremain elusive. Currently, transcriptomic and proteomic approachesare being employed to further gain an understanding in PAs functionresearch. These investigations will facilitate unraveling molecularfunctions of polyamines.

In this review, we discuss how PA metabolism is involved in plantresponses to both biotic and abiotic stresses. We also examine recentadvances in putative mechanisms whereby polyamines help plants todeal with environmental fluctuations. Finally, we discuss apparentcontradictions between some deleterious effects of polyamines onplant development and the role of PAs in response to stress.

2. Polyamine biosynthesis in plants

The PA biosynthetic pathway has been thoroughly investigated inmany organisms including plants and reviewed in detail (Alcázar et al.,2005; Bagni and Tassoni, 2001; Bortolotti et al., 2004; Hanfrey et al.,2001; Illingworth et al., 2003; Kakehi et al., 2008; Knott et al., 2007;Kusano et al., 2007b; Martin-Tanguy, 2001; Minguet et al., 2008; Panget al., 2007; Rambla et al., 2010; Teuber et al., 2007;Wallace et al., 2003).Briefly, the biosynthesis of polyamine in plants has been well-documented, covering decarboxylation of ornithine or arginine,catabolized by ornithine or arginine decarboxylases (ODC, ADC)respectively to yield diamine putrescine (Put). The resulting interme-diate agmatine synthesized from arginine is subsequently converted toPut, by agmatine iminohydrolase (AIH) and N-carbamoylputrescineamidohydrolase (CPA). Spermidine (Spd) and spermine (Spm) areformedby the sequential addition of aminopropyl groups to Put and Spdrespectively fromdecarboxylated S-adenosylmethionine (SAM)bySAMdecarboxylase (Kusano et al., 2007a; Pang et al., 2007).

2.1. Polyamine-related genes in plants

Availability of the complete genome sequence for Arabidopsis hasfacilitated the use of genomic approaches for identification and isolationof genes encoding PA biosynthetic enzymes (Liu et al., 2007). All genesin the PA biosynthesis pathway of plants have been revealed in differentplant species and Arabidopsis (Ge et al., 2006; Illingworth et al., 2003;Janowitz et al., 2003). In Arabidopsis, there are six enzymes responsiblefor PA biosynthesis encoding 10 genes: ADC-encoding genes (ADC1andADC2—Watson andMalmberg, 1996;Watson et al., 1997); SPDS (SPDS1and SPDS2—Hanzawa et al., 2002) and SAMDC (SAMDC1, SAMDC2,SAMDC3, SAMDC4—Franceschetti et al., 2001; Hashimoto et al., 1998;Urano et al., 2003, 2004). Similarly, Spm synthase, thermosperminesynthase, agmatine iminohydrolase and N-carbamoylputrescine ami-dohydrolase are represented by single genes (Hanzawa et al., 2000;Janowitz et al., 2003; Knott et al., 2007; Panicot et al., 2002; Piotrowskiet al., 2003). In contrast to ADC1, which is constitutively expressed in allplant tissues, ADC2 is responsible to abiotic stresses such as drought andwounding (Peréz-Amador et al., 2002; Soyka and Heyer, 1999).However, genes responsible for PA biosynthesis in plants except for

302 S.S. Hussain et al. / Biotechnology Advances 29 (2011) 300–311

ODC have only been characterized in Arabidopsis. Several studies foundthat the Arabidopsis genome lacks ODC (Allen, 2002; Hanfrey et al.,2001; Urano et al., 2003).

3. Polyamine and plant response to abiotic stresses

Several studies have shown that polyamine accumulation occursunder abiotic stresses including drought, salinity, extreme tempera-ture, paraquat, hypoxia, UV-B, heavy metals, mechanical woundingand herbicide treatment (Groppa and Benavides, 2008 and referencestherein; Pang et al., 2007). Hence, high cellular levels of polyaminescorrelate with plant tolerance in a wide array of environmentalstresses. However, the physiological significance of polyamineaccumulation remains elusive and must be revealed whether theseresponses are due to stress-induced injury or a protective response toabiotic stress.

3.1. Polyamine metabolism under abiotic stress conditions

The role of polyamine in abiotic stress tolerance first came underintense scrutiny after an increase in Put due to K+ deficiency wasreported decades ago. As a result, researchers extensively investigatedchanges in PA, when plants are exposed to single or combined stresses(Camacho-Cristóbal et al., 2004; Kuthanová et al., 2004; Liu et al.,2006; Mo and Pua, 2002; Shen et al., 2000; Urano et al., 2003).

Polyamine biosynthesis pathway and the principal enzymes of thispathway are under complex metabolic and developmental controland such control is necessary for efficient regulation of cellmetabolism. In Arabidopsis, differential expression of ADC (ADC1and ADC2) has been reported under stress conditions. In fact, ADC2expression is strongly induced by several abiotic stresses like drought,high salinity, mechanical injury, potassium deficiency (Alcázar et al.,2006; Armengaud et al., 2004; Hummel et al., 2004; Peréz-Amadoret al., 2002; Urano et al., 2003), while ADC1 is mainly induced by cold(Hummel et al., 2004). Similarly, the expression pattern of SPMSfollows that of ADC2 resulting in polyamine accumulation underdehydration and high salinity (Alcázar et al., 2006; Urano et al., 2003).However, SPDS2 has constitutive expression under different stressesin contrast to SPDS1 which exhibits increased expression underdehydration. On the other hand, expression of SAMDC1 and SAMDC2are positively induced by cold and SAMDC2 has slight induction inexpression under salt stress (Vergnolle et al., 2005). The expressionpatterns of CPA, AIH and ACL5 are not affected by any stress (Alcázaret al., 2006).

PA biosynthesis enzymes (ODC, ADC and SAMDC) are controlled attranscriptional, translational and post-translational levels (Hu et al.,2005); it is interesting to note that these enzymes are initiallysynthesized as an inactive precursor (proenzyme), which are latersubjected to post-translational processing resulting in matureenzymes (Xiong et al., 1997). For example, an accumulation of Puthas been detected in response to environmental fluctuationsconcomitant with ADC2 and ADC1 up-regulation. However, Putaccumulation and induction of downstream genes involved in Spdand Spm biosynthesis (SAMDC2, SPDS1, SPMS) did not affect thecontent of both polyamines. This could be due to the translational orpost-translational regulation of SAM decarboxylase, which is a keyenzyme in polyamine biosynthesis. Similarly, Hu et al. (2005) foundthat a 5′-untranslated sequence plays a central role in bothtranscriptional and post-transcriptional control of SAMDC geneexpression.

Under stress conditions, the level of PA in plant organs could alsobe regulated by its degradation. Cellular PA is controlled by catabolicpathway (Bagni and Tassoni, 2001; Cona et al., 2006), which consistsof two amine oxidases, doamine oxidase (DAO) and polyamineoxidase (PAO). The function of DAO is to convert Put into Pyrroline,ammonia and H2O2. PAO oxidizes Spd to Pyrroline, 1,3-diamine

propane (DAP), H2O2 and Spm to aminopropylpyrroline, DAP andH2O2 (Cona et al., 2003, 2006; Martin-Tanguy, 2001; Sebela et al.,2001). Capell et al. (2004) found that rice produces high levels of Spdand Spm until 3 days after drought stress but the level sharplydropped after 6 days, probably because of the action of PAO.

It is well-known that ABA contents increase under drought,salinity and other abiotic stresses (Christmann et al., 2005). ABAinduces the expression of a plethora of genes involved in defenseagainst these abiotic stresses (Yamaguchi et al., 2007). It is establishedthat genes involved in PA biosynthesis are also inducible by ABA(Alcázar et al., 2006; Kasinathan and Wingler, 2004; Urano et al.,2004). Alcázar et al. (2006) also showed that the dehydrationinducible expression of ADC2, SPDS1 and SPMS is an ABA-dependentresponse because up-regulation of these genes is not observed in ABAdeficient (aba2) and insensitive (abi1) mutants. Moreover, it is furtherrevealed that stress (DRE and LTR) and ABA responsive elements(ABRE and/or ABRE related motifs) are present in the promoters ofthese genes. Furthermore, microarray analysis has revealed that mostof the genes involved in PA metabolism in Arabidopsis respond to arange of abiotic stresses such as drought (Öztürk et al., 2002);wounding ormethyl jasmonate treatment (Peréz-Amador et al., 2002;Sasaki et al., 2001). However, the use of microarray technology forunraveling molecular mechanisms underlying PA effects on abioticstress tolerance is in its infancy.

3.2. Plant stress tolerance modulated by polyamine treatment

Stress-derived changes in cellular polyamines provide clues ontheir possible implication in stress but do not provide evidence oftheir role in counteracting stress. Classical approaches using exoge-nous PA application/mutant/use of inhibitors of enzymes involved inPA biosynthesis pathway represent an excellent model to test varioushypotheses and to answer fundamental biological questions derivedfrom pathway manipulation (Alcázar et al., 2006; Bhatnagar et al.,2002; Liu et al., 2007). Exogenous application of polyamines, which isexpected to increase levels of an endogenous polyamine, has beenattempted before or during stress (Navakouidis et al., 2003; Wanget al., 2007). There is a large body of evidence to suggest thatexogenous application of PAs could, in varying degrees, (1) preserveplant cell membrane integrity, (2) reverse growth or minimizegrowth inhibition caused by stress, (3) moderate expression ofosmotically responsive genes, (4) reduce superoxide radical and H2O2

contents, (5) reduce accumulation of NA+ and Cl− ions in differentorgans, and (6) increase activities of antioxidant enzymes (Ali, 2000;Iqbal and Ashraf, 2005; Afzal et al., 2009; Ndayiragiji and Lutts, 2006;Tang and Newton, 2005; Yiu et al., 2009; Zhang et al., 2009). However,the protective effects of individual PAs are somewhat different. Thereason for such a discrepancymay be due to differences in absorption,transport and utilization among plant species. These findings suggestthat exogenous PA application acts as an elicitor of genes involved inabiotic stress responses (Gill and Tuteja, 2010).

In another approach, treatment with PA biosynthesis inhibitors,such as x-difluoromethylarginine (DFMA), x-difluoromethylornithine(DFMO), and D-arginine, to reduce endogenous PA resulted in stress-sensitive phenotypes. However, this effect is reversed by theconcomitant application of exogenous polyamine (He et al., 2002;Navakouidis et al., 2003). The effects of these inhibitors are variable,ranging from inhibition to stimulation or no effect depending on theinhibitor stability and specificity, developmental stage, plant systemtested and existence of efficient compensatory mechanisms (Kaur-Sawhney et al., 2003).

Another genetic approach employed for analyzing biologicalfunctions of polyamine metabolism in stress response is the use ofmutants deficient in polyamine biosynthesis (Kaur-Sawhney et al.,2003; Urano et al., 2004; Watson and Malmberg, 1998). Watson et al.(1998) isolated EMS mutants of Arabidopsis with reduced ADC


activity, spe-1 and spe-2. These mutants are deficient in PAaccumulation and exhibited reduced salt tolerance compared withthe wild type (Kasinathan andWingler, 2004). On the other hand, theADC2 knockout mutant (adc2-1) showed no obvious phenotypechange under normal growth conditions and was more sensitive tosalt stress, which can be partially reversed by exogenous applicationof Put (Urano et al., 2004). These results clearly revealed that ADC2 isa key gene and Put derived from the ADC pathway was important instress response. Recently, a defective role for Spm in abiotic stressessuch as drought and salinity was established by the Arabidopsis acl5/spms mutant, defective for Spm production. This mutant exhibited asensitive phenotype under drought and salinity stresses but recoveredwhen treated with Spm (Yamaguchi et al., 2006, 2007). Takentogether, detailed characterization of mutants, defective in other PAgenes, should aid in deciphering the precise mode of action of PAgenes in response to abiotic stresses.

3.3. Plant abiotic stress tolerance modulated by engineering thepolyamine synthesis pathway

Recent advances in molecular biology with emphasis on geneticengineering and availability of PA biosynthesis genes makes itpossible to evaluate and provide a powerful strategy to identify thepossible role of PAs in stress response (Groppa and Benavides, 2008).

Table 1Abiotic stress tolerance in transgenic plants expressing polyamines.

Gene Molecular function Source Transformedplant

Performance of transgenicplant

ADC Argininedecarboxylase

Oat Rice Salinity stress tolerance

SAMDC S-adenosylmethioninedecaboxylase

Tritordeum Rice Salt tolerance

ODC Ornithinedecarboxylase

Mouse Tobacco Salinity stress tolerance

ODC Ornithinedecarboxylase

Daturastronium

Tobacco Transgenic plants nottested for abiotic stresses


Human Tobacco Drought, salinity andbiotic stress resistance

SPDS Spermidinesynthase

C. ficifolia Arabidopsis Multiple abiotic stresstolerance


D.stramonium

Rice Drought tolerance

SAMDC1 S-adenosylmethioninedecaboxylase

Arabidopsis Arabidopsis Broad spectrum stresstolerance


C. ficifolia SweetPotato

Drought and salt stresstolerance


Carnation Tobacco Multiple abiotic stresstolerance


Arabidopsis Eggplant Tolerance to multipleabiotic stresses

SAMDC2 S-adenosylmethioninedecaboxylase

Malussylvestric

Pyruscommunis

Salt tolerance

SPDS1 Spermidinesynthase

Malussylvestric

Pyruscommunis

Multiple abiotic stresstolerance

ADC1 Argininedecarboxylase

Arabidopsis Arabidopsis Freezing stress tolerance


D.stramonium

Rice Drought tolerance


Yeast Tomato High temperaturetolerance


Apple Pear Multiple abiotic stresstolerance


Arabidopsis Arabidopsis Drought tolerance

A general phenomenon observed is that PAs can alter their titres inresponse to various types of environmental stresses such as waterstress (Capell et al., 2004; Kasukabe et al., 2004; Ma et al., 2005), lowand high temperatures (Hummel et al., 2004; Imai et al., 2004; Songet al., 2002) and salinity (Liu et al., 2006; Maiale et al., 2004; Roy et al.,2005). In order to obtain fundamental information on the role of PAsduring stress, plant PAs have beenmodulated by the over-expression/down-regulation of adc/odc/samdc genes (Kakkar and Sawhney, 2002;Minocha and Sun, 1997; Thu-Hang et al., 2002). Over-expression of PAbiosynthetic genes like adc (Capell et al., 1998; 2004; Roy and Wu,2001), odc (Kumria and Rajam, 2002), samdc (Roy and Wu, 2002;Waie and Rajam, 2003) and spd syn (Franceschetti et al., 2004;Kasukabe et al., 2004, 2006) in plants like O. sativa, N. tabacum, A.thaliana and I. batatas has increased tolerance to various abioticstresses (Table 1). There are several reports on creating transgenicplants harboring polyamine biosynthetic genes in an attempt toenhance stress tolerance. Transgenic work is based on the observa-tions that AtADC2 transcripts correlates with the accumulation of freePut under different abiotic stresses in plants (Urano et al., 2004). Forexample, in a recent study, transgenic rice plants expressing theDatura stramonium adc (arginine decarboxylase) gene producedhigher levels of Put under drought stress than wild type plants,which led to higher levels of Spd and Spm and improved droughttolerance; transgenic plants exhibited less chlorophyll loss and leaf

Additional notes References

Transgenic plants exhibited higher Put with increased ADCactivity

Roy and Wu(2001)

Transgenic plants had normal growth with increased biomass Roy and Wu(2002)

Enhanced PA metabolism with higher Put Kumria andRajam (2002)

Higher ODC activity in leaves and flower buds noticed Mayer andMichael (2003)

Difficult to pinpoint whether tolerance was due to increased Putor Spd or both

Waie and Rajam(2003)

Involved in signaling pathways which led to tolerance Kasukabe et al.(2004)

Polyamine metabolism had strong connection with droughtstress

Capell et al.(2004)

Transgenic plants had overproduction of Spm Alcázar et al.(2006)

Transgenic plants with high Spd contents produced significantlyhigh storage root mass and starches

Kasukabe et al.(2006)

Normal plant development with higher photosynthetic rate &increased seed rate

Wi et al. (2006)

Increased ADC activity led to higher polyamine accumulation Prabhavathi andRajam (2007)

Stress tolerance accompanied by normal growth He et al. (2008)

Increased SPDS activity with enhanced polyamine accumulation Wen et al. (2008)

Transgenic plants had stress tolerance due to overproduction ofPut

Altabella et al.(2009)

Transgenic plants had rapid recovery from drought on re-watering

Peremarti et al.(2009)

Enhanced antioxidant activity, protection of membrane lipidperoxidation were probably responsible for tolerance

Cheng et al.(2009)

Enhanced polyamine accumulation Wen et al. (2009)

Transgenic plants exhibited reduced transpiration rate andstomatal conductance

Alcazar et al.(2010a,b)


curling than wild-type plants (Capell et al., 2004; Peremarti et al.,2009). In contrast, wild-type Datura stramonium exhibit increasedendogenous Put levels on the onset of drought stress but this Put levelis not enough to trigger the conversion of Put into Spd and Spm(Capell et al., 2004). Another example is the introduction of theTritordeum SAMDC (S-adenosylmethionine decarboxylase) gene intorice, which resulted in a three to four-fold increase in Spd and Spmlevels in transformed plants, which then had normal growth anddevelopment even under NaCl stress (Roy and Wu, 2002). In anotherexample, Waie and Rajam, 2003, observed that transgenic tobaccoplants over-expressing a human SAMDC gene had higher Spd and Putlevels and exhibited tolerance to drought and salt stress. Franceschettiet al. (2004) also showed that over-expression of Arabidopsis SAMDCin tobacco plants resulted in increased SAMDC activity, accumulationof dcSAM, perturbation of PA levels and transgenic plants exhibitedmultiple stress tolerance. Recently, Peremarti et al. (2009) generatedtransgenic rice plants constitutively expressing heterologous SAMDCgene from Datura stramonium to dissect the roles of Put from higherpolyamines Spd and Spm. Both transgenic and wild type plantsshowed identical symptoms when exposed to drought stress buttransgenic plants recovered much more quickly on re-watering.Similarly, transgenic carrot lines over-expressing mouse odc, whichconverts ornithine to diamine putrescine were able to withstand saltand osmotic stress over short period (Minocha and Sun, 1997). Inanother set of experiments, ADC expressing transgenic rice plantsproduced higher levels of Put, Spd and Spm and exhibited droughttolerance. Further, it has been proposed that Put may reflect the suboptimal growth conditions while Spd and Spm may help detoxifyingfree radicals (Larher et al., 2003). These results confirmed theinvolvement of polyamines in drought stress and further attributedindividual roles to Put, Spd and Spm. Interestingly, introduction of asingle polyamine biosynthesis gene has been shown to confertolerance to multiple stresses. Examples of these are when Kasukabeet al. (2004, 2006) and Wi et al. (2006) found broad spectrumtolerance to abiotic stresses—drought, chilling, freezing, salinity andoxidative stress—by over-expression of SPDS (Spermidine synthase)from Curcurbita ficifolia in Arabidopsis, sweet potato (Ipomoeabatatas) or tobacco. A cDNA microarray analysis between chilledleaves of a transgenic line and wild type revealed that genes encodingtranscription factors such as WRKY, B-box zinc finger proteins, NAMproteins, DREB2B and NAC domain proteins are up-regulated intransgenic plants. Wen et al. (2008) demonstrated that over-expression of an apple MdSPDS1 gene in European pear substantiallyincreased tolerance to multiple stresses by altering PA levels.Similarly, Prabhavathi and Rajam (2007) demonstrated that trans-genic eggplant harboring the oat ADC gene exhibited increasedtolerance to drought, salinity, low and high temperature and heavymetals.

These data demonstrated that a transgenic approach involving PAbiosynthetic genes may be a good strategy to improve crop toleranceto various abiotic stresses to meet the requirements of a challengingglobal environment.

4. Polyamine and plant stress response: Potential mechanismof action

4.1. Polyamine: A compatible solute in higher plants

Metabolic acclimation via the accumulation of compatible solutesis regarded as a basic strategy for the protection and survival of plantsunder abiotic stresses (Bartels and Hussain, 2008). Compatible solutesare non-toxic molecules, serve in turgor maintenance and stabilizemacromolecular structures under unfavorable conditions (Bohnertand Shen, 1999; McNeil et al., 1999). The notion of PA as a compatiblesolute is controversial in plants and needs further investigation.However, stress-induced PAs are often considered better stabilizers

than others for protecting biomolecules and preventing the mem-brane system from denaturing under stress conditions (Liu et al.,2007). PAs share many properties, for example, hydropholicity,protection of macromolecules, active oxygen scavengers, mainte-nance of cellular pH etc., which are close to those of proline and othercompatible solutes (Liu et al., 2007; Wi et al., 2006). However, theconcentration of stress-induced PAs is lower than proline and othersolutes, which suggests that PAs are not compatible solutes. On theother hand, Duhazé et al. (2002) showed that products of PAcatabolism, like β-alanine, can convert into β-alanine betaine whichis required for osmoregulation in some halophytes.

Proline is one of the most common osmolytes in stressed plants(Bartels and Hussain, 2008; Delauney and Verma, 1993; Sharma andDietz, 2006; Urano et al., 2009). Polyamine catabolism is closelyrelated to proline accumulation in response to stress conditions (Azizet al., 1998; Bouchereau et al., 1999). Öztürk and Demir (2003)showed that exogenous PA increases activity of peroxidase (POD) andcatalase (Cat), along with proline production. PA metabolism isunique in that Put, proline and GABA share a common substrate,glutamate, and these metabolites often respond similarly to abioticstresses (Seki et al., 2007; Sharma and Dietz, 2006; Simon-Sarkadiet al., 2005, 2006). There is no evidence yet about the mechanism oftheir coordinated accumulation (Radukina et al., 2007). However, it ispossible that a common signal triggers all three sub-pathways in acoordinated manner. Ornithine is a key intermediate in the biosyn-thesis of both Put and proline (Coruzzi and Last, 2000; Roosens et al.,2002; Slocum, 2005) and is a possible candidate for a regulatory rolein coordinating biosynthesis of these metabolites (Mohapatra et al.,2010). Similarly, a hierarchical accumulation of PAs in differenttransgenic tissues/organs has been observed (Lepri et al., 2001) whichsuggest that PAs might act as compatible solute in specific organs,cells or organelles.

4.2. Polyamine and antioxidant response

Reactive oxygen species (ROS) production is a common plantresponse under both abiotic and biotic stresses (Miller et al., 2008).ROS is characterized by the accumulation of toxic molecules Ō2, H2O2,and OH− in tissues which are capable of causing damage to plant cellmembranes and macromolecules (Apel and Kirt, 2004). Plants haveseveral antioxidant strategies (Rea et al., 2004) like ROS-scavengingenzymes such as superoxide dismutase (SOD) (Aronova et al., 2005),different peroxidases (POD; Hiraga et al., 2000), catalase (Cat), andglutation reductase (GR; Bartels and Hussain, 2008). PAs may berelated to their multi-faceted nature, which includes working as anantioxidant, a free radical scavenger and a membrane stabilizer(Larher et al., 2003; Velikova et al., 2000). The generation of ROS istightly linked to catabolic processes of PAs, by PAO (Cona et al., 2006)which is associated with plant defense and abiotic stress responses(Liu et al., 2005). Verma and Mishra (2005) demonstrated thatpositive effects of Put on Brassica juncea seedlings under NaCl stressare evident from reduced H2O2 and lipid peroxidation. Similarly, Putincreased activity of antioxidant enzymes and carotenoids in leaftissues of salt stressed Brassica. Based on these results, they concludedthat PAs may exhibit antioxidant properties under some conditions.Conclusive evidence regarding antioxidant roles of PAs were providedby Nayyar and Chander (2004), who observed that exogenousapplication of PAs reduced H2O2 levels and molandialdehyde (MDA)content, and raised the antioxidant level in 15-day-old chickpeaplants subjected to drought and cold stress for 4 days.

PAs are also involved in inhibition of DNA oxidative degradation byOH− as shownbyan in vitro experiment. Total DNA fromM. crystallinumis degraded, when incubated with an OH− generating system andaddition of Spm suppressed DNA damage (Kuznetsov and Shevyakova,2007). At the same time, some reports have demonstrated that PAconjugates are more efficient compared to parent compounds with


stronger protective antioxidant activities (Edreva et al., 2007). Never-theless, it can be concluded that plants not only accumulate free PAs tofunction as scavengers of free radicals but also produce their conjugateswhich are more efficient antioxidants (Edreva et al., 2007).

4.3. Polyamine: A signal molecule during stress response

In contrast to the trustworthy establishment of the role of PA inplantdefense against abiotic (Bartels and Hussain, 2008) and biotic (Walters,2003 and references therein) stresses, few reports recently indicatedthat PAs may act as cellular signals in intrinsic talk with hormonalpathways including ABA (Alcázar et al., 2010a,b; Gill and Tuteja, 2010).

It is well-known that ABA concentrations increase under waterand salt stress as well as other abiotic stresses (Christmann et al.,2005). It is also well-documented that ABA induces the expression ofmultiple genes involved in abiotic stress tolerance (Bartels andHussain, 2008; Bartels and Souer, 2003), e.g. PA biosynthesis genes inArabidopsis (Kasinathan and Wingler, 2004; Urano et al., 2004).Exogenously applied ABA helped further to identify the possible rolesof ABA in modulation of PA metabolism at the transcriptional level byup-regulating ADC2, SPDS and SPMS under stress conditions in plants(Alcázar et al., 2006; Hanfrey et al., 2001; Hanzawa et al., 2002; Peréz-Amador et al., 2002; Urano et al., 2003). Similarly, a plethora of dataon the analysis of mutant plants and transcript profiling suggest apositive feedback mechanism between Put and ABA, which permits afresh insight that both Put and ABA reciprocally promote each other'sbiosynthesis under stress to increase plant adaptive potential (Cuevaset al., 2008, 2009; Urano et al., 2003, 2009; Yamaguchi et al., 2006).

PA catabolism produces H2O2 whichwas often consideredmostly asa toxic metabolite. Only recently, our notions about H2O2 changeddramatically to a signalmolecule, capable of diffusion from the site of itsproduction to neighbouring cells and tissues, resulting in activation of adefensive response (Neill et al., 2002). Similarly, PAs like Spm and Spdare regarded as potent inducers of nitric oxide (NO) in plants (Tun et al.,2006). Reports showing NO as a signaling molecule in plants appearedas late as 1998 (Delledonne et al., 1998). These reports provoked anintensification of research on the role of NO in plants. In plant cells,several pathways coexist for NO-mediated signals including cyclicnucleotides, Ca2+ ions, protein kinases and others. Moreover, wheatplants subjected to drought had much higher ABA synthesis in roots inthe presence of NO and ROS, which suggests synergistic action of ROSand NO (Zhao et al., 2001). Also, the accumulation of NO provednecessary for ABA-induced closure of stomata in Vicia faba (Garia-Mataand Lamattina, 2002). Important clues about the functional cooperationbetweenABA, H2O2 and NO are also confirmed by a recent reportwhichfound that ABA-induced stomatal closure in Arabidopsis is dependentnot only on NO but also on H2O2 (Bright et al., 2006). Recently, An et al.(2008) reported that PAs are involved in ABA-induced stomatalregulation under abiotic stresses.

ABA, H2O2, NO and PAs aremultifunctional molecules implicated innumerous physiological and biological responses during stressresponses (Grün et al., 2006; Neill et al., 2003). Evidence obtainedso far is being compiled, showing the involvement and interaction ofABA, H2O2, NO and PAs during stress responses by a complex network.Recently, Alcázar et al. (2010a,b) suggested a synergistic interplaybetween aforesaid molecules for abiotic stress tolerance in plants.However, whether or not the unique roles of thesemolecules in plantsare attributable is still a matter of debate.

4.4. Polyamine: Regulation of ion channel and Ca2+ homeostasis

Recently, it was found that PAs could substantially affect ionchannel conductivity in plants (Kusano et al., 2007a). At physiologicalpH, PAs are positively charged molecules, which interact withnegatively charged proteins including ion channels. PAs are alsopotent blockers of fast and slow vacuolar channels, including calcium

channels (Brüggemann et al., 1999; Dobrovinskaya et al., 1999a;1999b). The effect of PAs on ion channels is proportional to its charge(Spm+4NSpd+3NPut+2) at both whole cell and single channel level,thus indicating a direct blockage of the channel by PAs (Brüggemannet al., 1998). These findings are in agreement with reports fromanimal literature, suggesting that PAs can block or modulate severaltypes of cation channels (Bowie et al., 1998; Gomez and Hellstrand,1999; Huang and Moczydlowski, 2001; Lu and Ding, 1999; Oliveret al., 2000; Williams, 1997a,b). As in the animal system, ion channelshave been identified as PA targets in plants blocking inward rectifyingK+ and Na+ channel and mediating additional aspects of ion flux-homeostasis in cell type specific manner (Liu et al., 2000; Zhao et al.,2007). Furthermore, Garufi et al. (2007) suggested that PA mayregulate the activity of numerous ion channels indirectly by affectingplasma membrane potential via activation of H+-ATPase throughenhancement of interactions with 14-3-3 proteins.

Consistent with the above data, it has been reported that PAsincluding spermine inhibit stomatal opening and induce closure byregulating KAT-1 like voltage-dependent inward K+ channel of Viciafaba guard cells. Similarly, exogenously applied PAs ameliorate thedetrimental effects of salinity by reducing NaCl-induced K+ effluxthrough non-selective cation channels, a major route of Na+ uptakeinto plant cells (Demidchik and Tester, 2002; Shabala et al., 2007).

Yamaguchi et al. (2006) showed that acl5/spms mutant plant ishypersensitive to KCl and also Ca2+ deficient. The overall phenotypeof mutant plants resembles transgenic plants over-expressing AtGluR2and CAX1, which encode a Ca2+ influx channel at the plasmamembrane and a vacuolar Ca2+/H+ exchanger, respectively (Hirschi,1999; Kim et al., 2001). Similarly, mutant plants lose more water thanwild type plants due to failed stomatal closure upon onset of drought(Yamaguchi et al., 2007). This phenomenon may again be explainedby the impairment in Ca2+ homeostasis. It is documented thatchanges of free Ca2+ in the cytoplasm of guard cells are responsible forstomatal movement (Allen and Sanders, 1996; Peiter et al., 2005; Robet al., 2005). On the other hand, spermine produced as a result ofdrought stress may modulate Ca2+ permeable channels, resulting inincreased cytoplasmic Ca2+ concentration to trigger stomatal closure.Collectively, these results indicate that the absence of spermine maycause deregulation of Ca2+ trafficking, resulting in a lack of properadaptation to high NaCl and drought stresses (Kusano et al., 2007a,b).Taken together, this data points to a possible link between PAs, Ca2+

homeostasis and stress responses which should be further explored.

4.5. Polyamine and programmed cell death (PCD)

In plants, programmed cell death (PCD) can occur following bothpathogen attack and environmental fluctuations (Reape and McCabe,2008). For example, UV-C activate PCD in Arabidopsis (Danon et al.,2004) and PCD can also be activated in tobacco by infection withPseudomonas syringae pv. phsaeolicola (del Pozo and Lam, 1998).Polyamines are considered essential for cell growth and survival(Hanfrey et al., 2001; Thomas and Thomas, 2001) and homeostasis(Mittler and Shulaev, 2003). PAs have also been involved in regulationof PCD, apoptosis (Schipper et al., 2000). There is substantial literatureavailable indicating the involvement of PAs in apoptotic cell death inplants (Desiderio et al., 1995; Ha et al., 1997; Lindsay and Wallace,1998). Furthermore, PA degradation seems to be important, leading toapoptosis in plants. In fact, Crowley and Walters (2002) observed anincrease in PA catabolism by DAO and PAO in cells undergoingapoptosis which resulted in hypersensitive response in tobacco (Yodaet al., 2003). Similarly, Yoda et al. (2003; 2006) demonstrated that celldeath caused by TMV infection is partially mediated by H2O2

production through PA catabolism. Hydrogen peroxide has longbeen considered to be a causative element for apoptotic cell death inplants (Levine et al., 1996).


Apoptosis in plants follow similar interactions between PAs andcomponents of PCD as described for animals. In numerous plantdiseases, hypersensitive response (HR) is triggered when the hostrecognizes a pathogen affecter destined to suppress immunity (Jonesand Dangl, 2006). It has been suggested that HR represents a form ofPCD in plants (Greenberg et al., 1994; Walters, 2003) and PAs havebeen implicated in a prominent role in this process. HR involvesinducing localized cell death at the point of infection, thus limiting theprogression of the pathogen. Similarly, PAs also affect conformationand function of specific proteins by forming covalent linkagesmediated by the activity of transglutamines (TGase) enzymes (Griffinet al., 2002). TGase activity has also been demonstrated in plants(Della Mea et al., 2004). TGase activity is elevated, when apoptosis isinduced in animals, and similar enhanced activity has also beenshown during HR in tobacco/TMV interactions (Del Duca et al., 2007).However, further investigations are required for conclusive evidenceof PAs involvement in PCD in plants.

5. Polyamine and plant responses to biotic stresses

Despite continued interest in polyamine metabolism in plantssubjected to abiotic stresses (Bartels and Hussain, 2008), work onpolyamine metabolism in plant-pathogen interactions relatively lagsbehind (Walters, 2000). Mostly, plant defense mechanisms againstpathogen attack are triggered by a stimulus preceding the pathogenattack that reduces disease. The stimulus can boost the concentrationof accessible defense compounds that include the assembly of newdefensive structures and chemicals (Baileya et al., 2005). PAmetabolism has long been known to distort in plant cells respondingto insightful changes in plants interacting with fungal (Asthir et al.,2004; Greenland and Lewis, 1984), viral pathogens (Torrigiani et al.,1997; Walters, 2003) and mycorrhizae (Walters, 2000). Nevertheless,much progress has been achieved regarding PA and plant diseases(Walters, 2000, 2003). For example, spermine (Spm) not only plays arole as a mediator in defense signaling against pathogen (Takahashi etal., 2003, 2004) but is also important for resistance to virus infection(Yamakawa et al., 1998).

5.1. Polyamine: Elicitor of the plant defense response

The coordination of internal processes in plants and their balancewith the environment are connected with the excitability of plantscells. Yamakawa et al. (1998) reported that Spm accumulated in theapoplast of cells after lesion formation is an endogenous inducer of theexpression of both pathogen-related (PR) proteins and resistanceagainst TMV via salicylic acid (SA)-independent signaling pathway intobacco plants. Later, it was known that Spm stimulates activity of (i)two important mitogen-activated protein kinases (MAPKs) involvedin plant defense; wound-induced protein kinase (WIPK) and SA-induced protein kinase (SIPK) and (ii) defense gene expression(Takahashi et al., 2003, 2004). Later, using a similar experimentalsystem, it was discovered that exogenously applied spermine totobacco leaves provokes a pathway involving mitochondrial dysfunc-tion, activation of MAPKs, increased expression of hypersensitiveresponse (HR) marker genes, induced defense responses and HR-likecell death (Mitsuya et al., 2007, 2009; Uehara et al., 2005). However,the mechanism of PAs as an elicitor of plant defense response requiresfurther research.

5.2. Polyamine and plant–mycorrhiza association

In soil, root development and acquisition of root architecture aswell as root functions greatly rely on interactions of root tissues withthe surrounding biotic environment, especially microorganisms.However, little is known about the interactions between plants andmycorrhizae, and the role of PAs in symbiotic relationships is less

studied (Kytoviita and Sarjala, 1997). It has been shown thatexternally applied Put in arbuscular mycorrhizae increases thecolonization frequency in pea roots (El-Ghachtouli et al., 1995,1996). A possible role of PAs in arbuscular mycorrhizal infectionwas, therefore, postulated. Later, Kytoviita and Sarjala (1997) showedthat ectomycorrhizal symbiosis result in increased free Put levels inmycorrhizal roots of Scots pine. However, they found differences in PAlevels between symbiotic and non-symbiotic roots and suggested thatPA could create a carbon sink for symbionts, resulting in attraction ofphotoassimilates (Niemi et al., 2002). Further, a high content of totalfree PAs in association with arbuscular mycorrhiza and Lotus glaberplants was detected compared to non-mycorrhizal plants (Sannazzaroet al., 2007). This relationship also increased PA levels in both plantsandmycorrhizae. The modulation of PA pools in symbionts could helpto resist host defense responses induced at the start of the association.However, the roles of PAs in the plant–mycorrhizal associationsremain elusive and await further research.

5.3. Polyamine and plant–pathogen interaction

Although long known for their pharmacology effects, there hasbeen little investigation of defense responses of polyamine duringpathogenic infection. We are now beginning to understand their rolein plant biotic stresses through molecular biology and modernbiochemical approaches (Mehta et al., 2002; Walters, 2003).

Early efforts found that in compatible interactions betweenbarley and Puccinia hordei (brown rust fungus), polyaminesparticularly spermidine accumulate in infected leaves (Greenlandand Lewis, 1984). Polyamine accumulation has also been reported inleaves of barley following infection by powdery mildew fungus(Blumeria graminis f. sp. hordei) (Walters and Wylie, 1986; Walterset al., 1985). The presence of PA in both plants and pathogenic fungimakes it difficult to identify their respective contribution to PAaccumulation in infected organs. However, themost exciting and far-reaching development in this area is the possibility of control offungal plant diseases through specific inhibition of polyaminebiosynthesis (Galston and Weinstein, 1988; Walters, 1989). Simi-larly, PA inhibitors like DFMO, MGBG and CHA resulted in completeinhibition of microcycle conidiation at 5 mM levels (Khurana et al.,1996).

In relation to biotic stress responses and in order to identifyregulatory components of the pathway involved in the hypersensitiveresponse (HR) induced by tobacco mosaic virus (TMV) in tobaccoplants, new developments are in the pipeline. Tobacco ZFT1 is aspermine-responsive gene encoding a zinc finger type transcriptionalrepressor, and is involved in spermine-signaling pathway (Ueharaet al., 2005). Interestingly, tobacco plants over-expressing ZFT1 aremore resistant to TMV compared with control plants (Mitsuya et al.,2007; Uehara et al., 2005). Another important observation regardingPA implication in the signaling pathway involved in biotic stressresponse has been postulated. Accumulation of H2O2 as a result of PAcatabolism and nitric oxide due to induction by spermine/spermidineplays an important signaling role in plant–pathogen interactions(Romero-Puertas et al., 2004; Tun et al., 2006; Walters, 2003;Yamasaki and Cohen, 2006). These studies suggest that manipulationof key factors present upstream of polyamine biosynthesis or in thepolyamine-induced signaling pathway could render the host plantresistant to biotic stresses.

Some recent studies explored another layer of complex polyamine-induced signaling pathway. Rhee et al. (2007) described that thepolyamine adaptive response appears to be shared between pathogen(prokaryote) stringent responses and host (eukaryote) unfoldedprotein responses (UPR). AtbZIP60 belongs to the basic leucine zipperprotein family and is a key transcription factor involved in ArabidopsisUPR. An orthologue of AtbZIP60 has been identified in tobacco(NtbZIP60) via screening of spermine-responsive genes (Tateda et al.,

Table 2Demonstrated and suspected effects of polyamines in plants under various abiotic and biotic stresses.

Stress/Response Status Protective effect References

Abiotic stress Demonstrated Transgenic plants over-expressing PA genes confer tolerance todifferent abiotic stresses including drought, salinity and cold

Franceschetti et al., 2004; Kasukabe et al., 2004, 2006;Peremarti et al., 2009; Wen et al. 2008; Wi et al., 2006;

Biotic stress Demonstrated PA elicits plant defense responses against different biotic stressorslike fungi and viruses

El-Ghachtouli et al., 1995, 1996; Kytoviita and Sarjala, 1997

Suspected PA could support plant-mycorrhiza association for mutualbenefits

Niemi et al., 2002; Sannazzaro et al., 2007

Antioxidant response Demonstrated PA controls damage due to enhanced antioxidant activitiesunder stress

Cona et al., 2006; Edreva et al., 2007; Nayyar and Chander, 2004

Signaling response Demonstrated PA acts as elicitor of plant defense responses under stress Mitsuya et al., 2007, 2009; Takahashi et al., 2003, 2004Antiapoptotic agent Suspected PA supports cell development and survival under stress. PA could

delay PCD in plantsCrowley and Walters, 2002; Del Duca et al., 2007;Yoda et al., 2003, 2006

Compatible solute Suspected PA could accumulate compatible solutes for osmoregulation underabiotic stresses especially when produced in certain tissues/organs

Duhazé et al., 2002; Mohapatra et al., 2010;Öztürk and Demir, 2003; Roosens et al., 2002; Slocum, 2005


2008). It is further confirmed that AtbZIP60 is responsive to spermineand is also involved in modulation of UPR-responsive genes inArabidopsis (Iwata and Koizumi, 2005). However, further researchmay highlight the cross-talk between spermine function and UPR/stringent response.

6. Concluding remarks and future perspectives

We are only just beginning to comprehend the effect of PAs, andrecent research on polyamine metabolism has built a strong case forfurther studies towards careful analysis of PA genes involved inenvironmental stresses. High throughput analysis including modernbiological disciplines like electrophysiology, microarray, transcrip-tomics, proteomics, metabolomics approaches will also be helpful tounderstand the involvement of the PA biosynthetic pathway in abioticand biotic stress tolerance. Furthermore, biotechnological improve-ment of crop abiotic and biotic stress tolerance at the molecular levelis in progress. The potential mechanisms of action of polyamines inplants that have been demonstrated or are suspected are summarizedin Table 2. Geneticmanipulation of polyaminemetabolism has alreadyprovided valuable information regarding their role in stress response.The exploitation of information revealed using plant models and thetransfer of knowledge to a wide range of crop species for breedingpurposes are current challenges for improvement of plant toleranceusing the PA pathway. However, intelligent engineering of regulatorycircuits involved in stress response requires detailed knowledge ofsignaling hierarchies and the impact of metabolic changes involved inthis response. However, it is reasonable to assume that a thoroughcomparative analysis of the expression and function of PA genes andother genes involved in stress tolerance will be useful.

Alternative approaches also include the use of PA as an externalapplication which can also be administered for increasing tolerance tovarious stresses. In the long run, PA can be exploited in the same wayas farm chemicals to mitigate stress-induced injury for cropprotection. However, evidence from field level studies is still lacking.Some striking evidences of exogenous application of PA to counteractenvironment stresses are expected to promote its extended applica-tion to other crops.

Nevertheless there are two main areas that need furtherinvestigation. Firstly, although there is a strong correlation betweenthe presence of PAs and better tolerance to environmental stresses,intensive research at the molecular level is needed on signalingfunction. Secondly, current understanding of plant resistance topathogens is that PA synthesis is stimulated by a plant–pathogeninteraction. However, the role of PA in resistance to pathogensrequires further research.

Hence, research on PA and stress tolerance is at an interestingstage and has set the stage for intensive research to understand anarray of functions of these relatively simple molecules.

Acknowledgement

S.S.H is supported by an Endeavour Research Fellowship from theDepartment of Education, Employment and Work Relation (DEEWR),Australia.

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Polyamines: Natural and engineered abiotic and biotic stress tolerance in plants