Polyamines in response to abiotic stress tolerance through transgenic approaches.

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Polyamines in response to abiotic stress tolerance through transgenic approaches a

b

c

Malabika Roy Pathak , Jaime A Teixeira da Silva & Shabir H Wani a

Desert and Arid Zone Sciences Program; College of Graduate Studies; Arabian Gulf University; Manama, Kingdom of Bahrain

b

Miki-cho post office; Ikenobe, Kagawa-ken Japan

c

Division of Genetics and Plant Breeding; SKUAST-K; Shalimar, Srinagar, Kashmir, India Published online: 07 Apr 2014.

Click for updates To cite this article: Malabika Roy Pathak, Jaime A Teixeira da Silva & Shabir H Wani (2014) Polyamines in response to abiotic stress tolerance through transgenic approaches, GM Crops & Food: Biotechnology in Agriculture and the Food Chain, 5:2, 87-96, DOI: 10.4161/gmcr.28774 To link to this article: http://dx.doi.org/10.4161/gmcr.28774

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GM Crops & Food: Biotechnology in Agriculture and the Food Chain 5:2, 87–96; April/May/June 2014; © 2014 Landes Bioscience

Polyamines in response to abiotic stress tolerance through transgenic approaches Malabika Roy Pathak1,*, Jaime A Teixeira da Silva2, and Shabir H Wani3,* Desert and Arid Zone Sciences Program; College of Graduate Studies; Arabian Gulf University; Manama, Kingdom of Bahrain; 2Miki-cho post office; Ikenobe, Kagawa-ken Japan; 3Division of Genetics and Plant Breeding; SKUAST-K; Shalimar, Srinagar, Kashmir, India

1

Abbreviations: ACC, 1-aminocyclopropane-1-carboxylic acid; ADC, arginine decarboxylase; Cad, cadaverine; DAO, diaminooxidase; Dap, 1,3-diaminopropane; Nor-Spd, norspermidine; Nor-Spm, norspermine; ODC, ornithine decarboxylase; PA, polyamine; PAO, polyamineoxidase; Put, putrecine; SAM, S-adenosylmethionine; SAMDC, S-adenosylmethionine decarboxylase; Spd, spermidine; Spm, spermine; SPDS, spermidine synthase; SPMS, spermine synthase

Introduction The distribution, growth, development and productivity of crop plants are greatly affected by various abiotic stresses. Worldwide, sustainable crop productivity is facing major challenges caused by abiotic stresses by reducing the potential yield in crop plants by as much as 70%. Plants can generally adapt to one or more environmental stresses to some extent. Physiological and molecular studies at transcriptional, translational, and transgenic plant levels have shown the pronounced involvement of naturally occurring plant polyamines (PAs), in controlling, conferring, and modulating abiotic stress tolerance in plants. PAs are small, low molecular weight, non-protein polycations at physiological pH, that are present in all living organisms, and that have strong binding capacity to negatively charged DNA, RNA, and different protein molecules. They play an important role in plant growth and development by controlling the cell cycle, acting as cell signaling molecules in modulating plant tolerance to a variety of abiotic stresses. The commonly known PAs, putrescine, spermidine, and spermine tend to accumulate together accompanied by an increase in the activities of their biosynthetic enzymes under a range of environmental stresses. PAs help plants to combat stresses either directly or by mediating a signal transduction pathway, as shown by molecular cloning and expression studies of PA biosynthesis-related genes, knowledge of the functions of PAs, as demonstrated by developmental studies, and through the analysis of transgenic plants carrying PA genes. This review highlights how PAs in higher plants act during environmental stress and how transgenic strategies have improved our understanding of the molecular mechanisms at play.

*Correspondence to: Malabika Roy Pathak; Email: [email protected]; Shabir H Wani; Email: [email protected] Submitted: 15/01/2014; Revised: 30/03/2014; Accepted: 03/04/2014; Published Online: 07/04/2014 http://dx.doi.org/10.4161/gmcr.28774

www.landesbioscience.com

Plant development and productivity are negatively affected by environmental stresses. The major abiotic stress factors limiting crop productivity and plant growth are soil salinity, exposure to high and low temperatures, and drought. In the past decade, the average yields of major crops have been reduced up to 70% due to abiotic stresses.1 On the other hand, the increasing world population has added more pressure on the demand for increased crop yields, creating an urgent need to cultivate stress-tolerant crops with increased productivity.2 Agriculture around the globe is facing great challenges due to climate change with more erratic climate and with it, an increasing effect of abiotic stress factors. Plants are able to sense environmental changes, to respond to them, adapt and survive. Such changes under stress occur at cellular, physiological, biochemical, and molecular levels. The expression of a variety of genes is induced by different stresses in a wide diversity of plants.3 However, the stress-tolerant plants can alter their cellular mechanism and metabolic pathways to counteract the created imbalance under environmental stresses.4 The ability to survive of stress-tolerant plants depends on the proper maintenance of the structural and functional integrity of cells.5 Due to the complex nature of stresses, multiple sensors, rather than a single sensor, are responsible for a plant’s response to stress. In general, various nitrogen-containing compounds accumulate in plants in response to environmental stress such as amino acids (arginine, proline), amino acid-derived compounds, amides (glutamine, asparagine), ammonium, quaternary ammonium (glycinebetain), and polyamines (PAs).6-9 In addition to the maintenance of cellular functions and osmotic balance, these amino acids and their derivatives, including PAs, protecting cellular components, such as membrane protein complexes, by acting as molecular chaperons or regulators.10-12 Diverse stress conditions activate both acclimatization and adaptation techniques of plants to deal with abiotic stresses by using general and conserved stress response mechanisms. This is exemplified by Arabidopsis thaliana, which uses a common signal transduction pathway that involves the use of PAs as secondary messengers.13

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Keywords: abiotic stress, genetic engineering, polyamine, putrescine, spermidine, stress tolerance, transgenic plants

and intricate hormonal cross-talks to elucidate the proposed model of environmental stress tolerance capacity of PAs.

The biosynthesis and degradation pathway of PAs in plants is well documented in Figure 1. Put is synthesized either directly from decarboxylation of the amino acid L-ornithine by ornithine decarboxylase (ODC; EC 4.1.1.17) or indirectly, by the decarboxylation of l-arginine by ADC (EC 4.1.1.19) via agmatine.28 The product of ADC is agmatine, which is converted into Put through an intermediate N-carbamoylputrescine. Conversion of agmatin into Put requires two distinct enzymes: agmatin iminohydrolase (EC 3.5.3.12) and Figure 1. Polyamine biosynthetic and main catabolic pathways in Plants. ACC, N-carbamoylputrescine aminohydrolase (EC 1-aminocyclopropane-1-carboxylic acid; ADC, Arginine decarboxylase; DAO, 3.5.1.53). The increased synthesis of PAs under Diaminoxidase; ODC, Ornithine decarboxylic acid; PAO, polyamineoxidase; SAM, S-adenosylmethionine; SAMDC, S-adenosylmethionine decarboxylase; SPDS, different stresses is activated by the ADC pathway.18,29 Spermidine synthase; SPMS, Spermine synthase (ref. 18, after modification). The ODC pathway is more active in the early stages of plant growth, development, organ differentiation PAs are low molecular weight, non-protein polycations at and reproductive stage. A few plant species, including Arabidopsis physiological pH with a strong binding capacity to negatively thaliana, lack the ODC pathway.14,30 charged DNA, RNA, and different protein molecules, and Spd and Spm are synthesized by the successive attachment the ability to stabilize membrane structures.10,14 They regulate of aminopropyl with Put first to synthesize Spd and then Spd many physiological, growth, and developmental processes in to synthesize spermine (Spm).28,31 These reactions are catalyzed organogenesis, embryogenesis, flower initiation and development, by aminopropyltransferases such as Spd synthase (SPDS, EC leaf senescence, fruit development and ripening, and abiotic and 2.5.1.16) and Spm synthase (SPMS, EC 2.5.1.22). Aminopropyl biotic plant stress responses.15-18 The induced accumulation of is formed due to the decarboxylation of S-adenosylmethionine putrescine (Put) in response to potassium deficiency was among (SAM) by S-adenosylmethionine decarboxylase (SAMDC; EC the first reports to demonstrate a link between PAs and abiotic 4.1.1.50). SAM is produced from the amino acid l-methionine stress.19 Since then, a large number of reports have shown the and ATP by S-adenosylmethionine synthetase (SAMS, EC relationship between PA accumulation and the activities of their 2.5.1.6). Aminopropyl transferases belong to a group of widely biosynthetic enzymes during and after stresses.11,13,18,20 In addition distributed enzymes and their genomic organization has been to common PAs, several uncommon PAs also accumulate under studied in maize (Zea mays).31,32 Activation of the ADC pathway different stresses.21-23 and accumulation of higher PAs, Spd and Spm, was hypothesized The availability of cloned PA biosynthetic genes from various under different environmental stresses.23,33-36 A halophytic plant, sources and subsequent transfer of arginine decarboxylase Mesembryanthemum crystalinum, and A. thaliana showed a (ADC), S-adenosylmethionine decarboxylase (SAMDC), similar response under high salinity stress.36,37 Recent reviews and spermidine (Spd) synthase (SPDS) showed improved concluded the positive role of PAs in abiotic stress tolerance.2,9,38,39 environmental stress tolerance in various transgenic plants. PA catabolism efficiently regulates the level of free PA in the cell Transgenic plants overexpressing different PA biosynthetic which can perform an important physiological role under normal genes showed that the accumulation of different PAs allowed and stress situations.40,41 Diamine oxidase (DAO; EC 1.4.3.6) these plants to develop multiple stress tolerance.12,24-27 This and PA oxidase (PAO; EC 1.5.3.3) are responsible for oxidizing review summarizes the relation of PA biosynthesis in abiotic the diamine Put and PA Spd and Spm, respectively.22,42 stress responses, their pathways during stress, modulation of PA metabolic pathways by transgenic technology and finally transcriptomic and metabolomic approaches to unravel the key Polyamines in Response functions of different PAs in the regulation of abiotic stress to Different Abiotic Stresses tolerance. Nevertheless, the precise molecular mechanism(s) by which PAs control plant responses to stress stimuli remain Metal stress largely unknown. Recent studies indicate that PA signaling is Potassium (K) is an important macronutrient and common involved in direct interactions with different metabolic routes stress-related factor carrying vital functions in plant metabolism,

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GM Crops & Food: Biotechnology in Agriculture and the Food Chain Volume 5 Issue 2



Polyamine Biosynthetic Pathway under Abiotic Stresses

Abiotic stress

Plant species

Accumulated PA(s)

Enzyme activated

Ref. #

Aluminum

Catharanthus roseus

Cadmium

Avena sativa Helianthus annuus Phaseolus vulgaris

Put

-

65

Put Put, Spd, Spm Put

ADC ADC, ODC ADC

44 45 44

Chromium

Raphanus sativus

Put

-

76

Cold

Cicer arietinum

Put, Spd

-

82

Copper

Helianthus annuus Raphanus sativus

Put, Spd, Spm Put, Spd

ADC, ODC -

45 46

Heat

Arabidopsis thaliana Gossypium hirsutum

Put, Spd NorSpd, NorSpm

ADC, SAMDC -

71 68

Lead

Potamogeton cripus

Put

ADC, PAO

75

Mercury

Chlorogonium elongatum

Put

-

74

Osmotic

Cicer arietinum Lupinus luteus Sorghum bicolor Zea mays

Put, Spd Put, Spd Spd, Spm Spd, Spm

ADC -

79 58 78 78

Potassium

Arabidopsis thaliana Hordeum vulgaris

Put Put

ADC -

43 19

Salt

Aeluropus littoralis Arabidopsis thaliana Brassica campestris Helianthus annuus Lupinus luteus Malus domestica Oryza sativa Oryza sativa Oryza sativa Zea mays

Spd Spd, Spm Put, Spd Put, Spd Put, Spd Put Put Put Spd, Spm Spd, Spm

ADC ADC, ODC ADC ADC ADC -

61 37 62 80 58 59 50 81 51 60

ADC, Arginine decarboxylase; NorSpd, Norspermidine; NorSpm, Norspermine; ODC, Ornithine decarboxylase; PAO, Polyamine oxidase; Put, Putrescine; SAMDC, S-adenosylmethionine decarboxylase; Spd, Spermidine; Spm, Spermine.

growth and stress adaptation. However, studies related to this type of stress are often performed on leaves and/or seedlings, as the external symptoms of deficiency become acute. The accumulation of Put in the leaves of K-deficient barley (Hordeum vulgaris) plants,19 and the subsequent studies, established the specific role of Put in maintaining a cation-anion balance in plant tissues.18 The accumulation of different PAs and activated enzymes under different stress conditions are listed in Table 1. Watson and Malmberg43 investigated the regulation of ADC activity in relation to Put content during K+ deficiency stress in A. thaliana. The effects of cadmium (Cd) on Put accumulation by the activation of ADC was confirmed in bean (Phaseolus vulgaris) seedlings by using ADC enzyme inhibitor (L-αdifluromethylarginine, i.e., DFMA) and ODC enzyme inhibitor (L-α-difluromethylornithine, i.e., DFMO).44 Later on, different studies on the exposure of heavy metals such as Cd, copper (Cu), nickel (Ni), and zinc (Zn) also demonstrated the accumulation of different PAs and increased ADC activity.7,45 PA metabolism and the antioxidant property of Spm was proposed as a heavy metal stress-protecting mechanism. Different studies suggested the function of Spm as an antioxidant in protecting tissues from metal-induced oxidative damage to a certain extent.45 Heavy metal stress, Cu- and chromium (Cr)-induced Put and


Spd accumulation in plants afforded them protection against oxidative damage.46 Salinity, osmotic, heat, and/or cold stress The first report of the accumulation of Put and Spd in oats (Avena sativa) cells and protoplasts by exposure to various osmotica (sorbitol, mannitol, proline, betaine, sucrose, etc.), initiated PA research in response to osmotic stress.47 Osmotic stress induced an increase in ADC transcript level, supporting the ADC activation pathway during stress.48 Osmotic stress induced an increase in the level of Put and diaminopropane (Dap) with a decrease in the level of Spm in rape (Brassica napus) plants, explained by the role of Spm in post-translational regulation of ADC.49 The accumulation of PAs in response to saline stress49-51 and their exogenous application help to overcome the harmful effects of NaCl stress was reported in rice (Oryza sativa) seedlings.52-54 Several other studies showed that exogenous application of different PAs helped to overcome the stress effect to some extent.55,56 The effect of salinity stress on the activation of ADC, as well as its increased transcript level was observed in NaCltolerant rice cultivars exposed to 150 mM NaCl for 12 h.57 Salt and osmotic stress induced the accumulation of Put and Spd and increased ADC activity in the roots and leaves of lupine (Lupinus luteus) seedlings and in apple (Malus domestica).58,59 Increased


89



Table 1. Abiotic stress-induced polyamine (PA) accumulation and biosynthetic enzyme activation in plants

90

Molecular Cloning and Expression of Polyamine Biosynthetic Genes Induced under Abiotic Stress A large number of genes encoding key enzymes for the PA biosynthesis pathway have been cloned and characterized from various plant species following the cloning of oats (Avena sativa) ADC.83 The cDNA of ADC, ODC, SAMDC, SPDS, and SPMS cloned from different plants are listed in Table 2. Differential expression of two genes encoding ADC (ADC1 and ADC2) was observed in A. thaliana in response to environmental stresses. The expression of ADC2, SPDS1, and SPMS was strongly induced by several abiotic stresses (dehydration, high salinity, K+ deficiency) while ADC1 was mainly induced by cold.84-87 However, no changes in SPDS2 expression were detected in response to any stress. SAMDC2 expression was induced mainly by cold and salt stress whereas SAMDC1 was induced by cold stress in A. thaliana cell suspensions.88 Three cDNAs (MdSPMS-1, MdSPMS-2, and MdSPMS) with high homology to SPMS of A. thaliana were isolated and characterized from apple.89DAO cDNA has been isolated, sequenced and compared from pea (Pisum sativum) 90 whereas PAO cDNA was isolated and compared from maize.91 Database searches within the A. thaliana genome sequences showed the presence of a gene (AtPAO1) encoding a putative PAO with 45% amino acid sequence identity with maize PAO. The correlation of physiological and biochemical responses of abiotic stress tolerance with increased PA biosynthesis at its transcriptional level is well documented.13,32,57,92,93 The expression of these genes under different abiotic stresses was induced and showed a differential response in terms of mRNA induction and accumulation depending on the type, duration and intensity of the stress, the plant species, and other factors. Moreover, transcriptomic, metabolomics, and genetic approaches have implicated the key functions of different PAs in the regulation of abiotic stress tolerance at the global level while cross-talking between different stress hormones and metabolic pathways.10,13,94 Previously, it was suggested that PAs can act by stabilizing membranes, scavenging free radicals, affecting nucleic acids and protein synthesis, RNase, protease and other enzyme activities, and interacting with hormones, phytochromes, and ethylene biosynthesis.95,96 However, recent studies focused on the molecular mechanism of PA signaling and their integration with other metabolic pathways during abiotic stress tolerance. The expression of several genes involved in PA biosynthesis was strongly induced by one or more abiotic stresses as well as by abscisic acid (ABA)-induced stress in A. thaliana.85 The dehydration stress induced expression of ADC2, SPDS1, and SPMS as ABA-dependent response was observed in a mutant study of A. thaliana.86 However, the accumulation of Put and the induction of genes involved in Spd and Spm biosynthesis did not affect the content of both PAs. This could be due to the translational and post translational regulation of SAMDC, a key enzyme in PA biosynthesis.86 PA degradation by PAOs and generation of hydrogen peroxide (H2O2) under stress is important for protecting stressed cells by lignification and cross-linking extensions in response to stress and wounding.97,98




accumulation of Spd and Spm with increase tolerance to salt stress was observed in maize seedlings and in flowers and flower stocks of A. thaliana while growing constantly in 200 mM NaCl.37,60 Increased levels of Spd and Spm, as well as increased ADC and SPDS expression levels, were detected in A. thaliana by reverse transcriptase polymerase chain reaction (RT-PCR). In most of the studies concerning salt stress, induced PA accumulation was due to the activation of ADC. NaCl stress induced a reduction in the level of Spm in the shoots of Mediterranean salt grass (Aeluropus littoralis), caused by the degradation of Spm to higher PAs.61 A study of ADC and ODC inhibitors shed light on the induction of the ADC pathway and on the accumulation of Put and Spd under stress: although the activation of both ADC and ODC in dicotyledonous plant, turnip (Brassica campestris) was reported, but there was no inhibitor study or mutant analysis to confirm the observations.62 A study of the PA level and PA enzyme activity during salt stress in PA-deficient mutants of A. thaliana demonstrated the decreased formation of Put due to lower ADC activity, which ultimately led to reduced salt tolerance.63 Drought stress in rice also increased bound and free Put with increased resistance.64 PAs improve K/sodium (Na) homeostasis in barley seedlings by regulating ion channel activities and thus improving stress tolerance.65 The translocation and accumulation of Put and other PAs in an organ-specific manner after external application during salt stress afforded protection to rice.66 Put imparted protection to salt stress by improving water relations and nutrient imbalance in cucumber (Cucumis sativus).67 Under heat stress, heat-tolerant plants showed increased levels of higher PA (Spd and Spm) pools.22,23 Moreover, long chain uncommon PAs (norspermidine, norspermine, and caldopentamine) were also noticed during exposure to heat stress, similar to a thermophilic bacterium, Thermus thermophilus.23,68 Only heat-tolerant rice cv “N22” accumulated norspermidine and norspermine after heat stress. ADC and PAO activities increased to a large extent in heat-tolerant ‘N22’ than in the heat-sensitive cultivar ‘IR8’. Exogenous application of 1 mM Spd and 1 mM Spm helped to recover the heat shock (50 °C for 2 h) in mung bean (Vigna radiata) seedlings.69 Spd and Spm content and SAMDC activity increased after rice seedlings were chilled at 5 °C for 3 d.70 Put, Spd, and Spm content increased and SAMDC2, SPMS, and ADC2 genes were induced during 35 °C heat shook for 1 h in A. thaliana. It was also reported that the SPMS transgenic plants were protected from heat shock damage similar to exogenously applied Spm effect by the expression of heat shock protein genes (HPS101, HPS90, and HPS70).71 The effect of drought stress at supraoptimal temperatures on free proline and PA levels were compared in wild and proline-overproducing transgenic soybean (Glycine max).72 Similarly, the relationship of PA and proline in drought and heat stress tolerance responses in proline overproducing transgenic tobacco (Nicotiana tabacum) plants was explained: increased Spm level was one factor that imparted stress tolerance.73 These studies indicate that manipulation of proline synthesis also affects the level of PA by developing stress tolerance and adaptation. Stress induced accumulation of proline and different PAs were known to improve osmotic stress tolerance and maintaining ionic balances in cellular environment.77

PA biosynthetic genes

Source plants

Accession number

PubMed No. or Ref. No.

Arginine decarboxylase (ADC)

Arabidopsis thaliana

U52851

8756495

Avena sativa

X56802

2266946

Brassica juncea

AF22009 / AF220098

12060267 21282323

Ornithine decarboxylase (ODC)

S-Adenosylmethionine decarboxylase (SAMDC)

Spermidine synthase (SPDS)

Spermine synthase (SPMS)

Citrus trifoliata

HQ008237

Dianthus caryophyllus

U63832

99*

Glycine max

U35367

100* 15723827

Malus domestica

AB181854

Nicotiana tabacum

AF321137

15032880

Oryza sativa

NM001063230 / NM001058553 / AY604047

18089549 18089549 16769152

Pisum sativum

Z37540

7548836

Pringleaantis corbutica

AY337606 / AY337607

15527979

Prunus persica

AB379849

18996450

Solanum lycopersicon

L16582

8022938

Vitis vinifera

X96791

1042065

Capsicum annuum

AF480882

14972797

Datura stramonium

X 87847

8660289

Glycine max

AJ563382

15763662 15723827

Malus domestica

AB181855

Nicotiana tabacum

D89984

9869416

Nicotiana glutinosa

AF323910

11736657

Oryza sativa

NM001070362 NM001053389

18089549 17210932 16510395

Prunus persica

AB194103


AF030292

9733552

Triticum aestivum

HM770451

21192794

Zea mays

NM001148682

19936069


Y07765

11139406 9390449

Brassica juncea

U80916 / X95729

Catharanthus roseus

U12573

101*


U94786

9289746

Hordeum chilense x Triticum turgidum

X83881

8639739

Ipomoea batatas

AF188998

12060284

Ipomoea nil

U64927

102*

Malus domestica

AB077441/AB077442

15781000

Oryza sativa

Y07766 AB122089

11139406 15215597

Phaseolus lunatus

AB062360

12060229

Pisum sativum

U60592

11925048

Solanum tuberosum

Z11680 S74514

1450379 7948879

Triticum aestivum

AF117660

92*

Vicia faba

AJ250026

103*

Vitis vinifera

AJ567368

16982115


AB062360

9517003

Coffea arabica

AB015599

104*

Cucumis sativus

AY646352

106*

Hyoscyamus nigra

AB006691

9517003

Malus domestica

AB072915/AB072915

12655406

Nicotiana sylvestris

AB006692

95170

Oryza sativa

AB098063

15310079 10344199

Pisum sativum

AF043108/AF043109


AJ006414

105*

Arabis gemmifera

AB076744

12655134

Malus sylvestis

AB204521

16182474

*PubMed number of the published article is not available in NCBI site, but papers are available as in text reference.





Table 2. List of plant-cloned PA biosynthetic genes

91

Name of PA genes

Source Organisms

Transgenic plants

Accumulated PA

Tolerance developed

Ref. No

ADC

Avena sativa

Oryza sativa

Put

Salinity

24

ADC

Datura stramonium

Oryza sativa

Put, Spd, Spm

Drought

26

Avena sativa

Solanum meloangena

Put, Spd, Spm

Salinity, drought, low and high temperature, heavy metal

108


ADC ADC

Avena sativa

Triticum aestivum

Put, Spd, Spm

Drought

109

ADC-2



Put

Drought

10

ADC

Avena sativa


Put

Drought, freezing

110

ADC

Poncirus trifoliata


Put

Osmotic, drought, cold, oxidative

111

Anti ACC


Nicotiana tabacum

Spd, Spm

Oxidative

114

ODC

Mus musculus

Nicotiana tabacum

Put

Salt

121

SAMDC

Hordeum chilense x Triticum turgidum

Oryza sativa

Spd, Spm

Salt

25

SAMDC

Homo sapiens

Nicotiana tabacum

Put, Spd

Salt, drought, fungal wilt

113

SAMDC


Nicotiana tabacum

Spd

Salt, cold, acidic, oxidative

112

SAMDC

Dianthus stramonium

Oryza sativa

Spd, Spm

Drought

122

SAMDC

Saccharomyces cerevisiae


Spd,Spm

Heat, oxidative

27

SAMDC

Malus domestica

Nicotiana tabacum

Spd

Chilling, salt, osmotic

123

SPDS-1

Cucurbita ficifolia

A. Arabidopsis B. thaliana

Spd

Chilling, salt, drought

116

SPDS-1

Cucurbita ficifolia

Ipomoea batatas

Spd

Salt, drought

117

SPDS-1

Malus domestica

Pyrus communis

Spd, Spm

Salt, osmotic

118

SPDS-1

Malus domestica

Pyrus communis

Spd

Heavy metals, oxidative

119

ACC, Aminocyclopropane carboxylate; ADC, Arginine decarboxylase; ODC, Ornithine decarboxylase; Put, Putrescine; SAMDC, S-adenosylmethionine decarboxylase; SPDS, Spermidine synthase; Spd, Spermidine; Spm, Spermine.

Polyamine Accumulating Transgenic Plants with Improved Abiotic Stress Tolerance Modification of the PA level by transgenic approach and study of the role of PA in response to several stresses has been analyzed. Manipulation of the PA level in several plants may lead to improved plant tolerance against multiple environmental stresses are listed in Table 3. Different levels of mRNA accumulation of oat ADC, increased ADC activity and accumulation of PAs at different levels were observed in tobacco, rice, eggplant (Solanum melongena), and wheat (Triticum aestivum).23,57,107,109,124 Transgenic plants were generated by expressing the ADC gene of oats and datura (Datura stramoniun) under the control of different constitutive (maize ubiquitin 1) and inducible (tetracycline and ABA) promoters, and transgenic plants showed tolerance to salt and drought with an increased accumulation of Put, Spd, and Spm.24,26,109 The accumulation of Put as well as enhanced tolerance to dehydration, freezing and salt stress was observed in transgenic A. thaliana.110 Overexpression of ADC of Poncirus trifoliata (PtADC) in A. thaliana showed increased synthesis of Put and enhanced tolerance to high osmotic, drought and cold stress.111 As SAMDC is one of the key regulatory enzymes in the biosynthesis of PAs, in order to better understand the effect of

92

regulation of PA biosynthesis on the tolerance of different types of stress such as salt, drought, and low and high-temperature stress in rice, tobacco, and tomato (Lycopersicon esculentum), the SAMDC gene of different sources were introduced by Agrobacterium tumefaciens and transgenic plants showed increased environmental stress tolerance and accumulation of higher PAs than non-transgenic plants.25,27,112 Different SAMDC transgenes of tritordeum (Hordeum chilense × Triticum turgidum), carnation (Dianthus caryophyllus), and yeast (Saccharomyces cerevisiae) showed an inducible and constitutive type of expression under different stresses. Transgenic rice plants containing a tritordeum SAMDC and induced with 50 µM ABA produced a 3- to 4-fold increase of Spd and Spm than unstressed control plants under salt stress and afforded protection to transgenic plants after 150 mM NaCl stress in a re growth recovery study.25 Transgenic tomato plants constitutively expressing the SAMDC gene of yeast accumulated 1.7- to 2.4-fold higher levels of Spd and Spm than wild-type plants under temperature stress (38 °C for 1 h) and showed tolerance to this stress, enhanced antioxidant enzyme activity and low membrane lipid peroxidation.27 Constitutive overexpression of human SAMDC in tobacco gave rise to an increment in Put and Spd levels that led to tolerance to salt and osmotic stress.113



Table 3. List of transgenic plants encoding PA biosynthetic genes

References 1.

Gosal SS, Wani HS, Kang MS. Biotechnology and drought tolerance. J Crop Improv 2009; 23:19-54; http://dx.doi.org/10.1080/15427520802418251 2. Gill SS, Tuteja N. Polyamines and abiotic stress tolerance in plants. Plant Signal Behav 2010; 5:2633; PMID:20592804; http://dx.doi.org/10.4161/ psb.5.1.10291 3. Sanghera GS, Wani SH, Hussain W, Singh NB. Engineering cold stress tolerance in crop plants. Curr Genomics 2011; 12:30-43; PMID:21886453; http:// dx.doi.org/10.2174/138920211794520178


the control of several metabolic pathways in which PAs mediate signal transduction.42,73,75,131 All these studies support the view that increasing PA biosynthesis could be a good strategy in transgenic research in response to plant stress and to improve the tolerance of stresssensitive plants against adverse environmental conditions. It is clear that PAs play a central role in enhanced tolerance to adverse abiotic stresses. However, overexpression of heterologous genes only provides limited information about the importance of endogenous PA synthesis and the function of endogenous enzymes during salt and drought stresses. Studies using endogenous genes and mutants with reduced enzyme activity might help to understand the mechanism of action of PA metabolism in different stress responses.

Conclusions and Future Perspectives Genetic manipulation leading to increased PA biosynthesis is a potential strategy to study the roles of PAs in a plant’s responses to abiotic stress and to improve their tolerance against adverse environmental conditions. Abiotic stresses are the primary cause of plant losses worldwide, and thus approaches employing genetic modification aimed at overcoming severe environmental stresses need to be quickly implemented in association with molecular-assisted traditional breeding and metabolomics.132 A large amount of research data indicates that overexpression of PA biosynthetic genes play an important role in environmental stress tolerance and could be exploited in biotechnological programs to produce stress-tolerant plants. Future strategies should be based on a detailed knowledge-based framework of PA metabolism using PA biosynthetic genes and their regulation by employing different types of stress-inducible promoters and transcription factors. A concrete understanding of the genetic engineering of PA biosynthetic genes, a biotechnological strategy, may be of great importance in solving future problems related to environmental stress-resistant plants using transgenic strategies.133 Disclosure of Potential Conflicts of Interest

No potential conflict of interest was disclosed. Acknowledgments

Malabika Roy Pathak wishes to thank Prof Bharati Ghosh for developing research interest on polyamines and the Desert and Arid Zone Sciences Program, Arabian Gulf University, Kingdom of Bahrain.

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On the other hand, tobacco plants transformed with antisense ACC synthase or ACC oxidase from carnation showed higher SAMDC activity as well as higher Put and Spd levels, tolerance to oxidative stress, high salinity, and low pH.114 In tobacco, constitutive overexpression of carnation SAMDC resulted in the accumulation of total PAs and generated broad spectrum tolerance to abiotic stresses.112 A. thaliana plants constitutively overexpressing a mustard SAMDC exhibited an increased level of Spd and Spm and tolerance to salt, drought, and oxidative stresses.115 Overexpression of the SPDS gene in A. thaliana, sweet potato (Ipomoea batatus), and pear (Pyrus communis) transgenic cell lines showed an increased titer of Spd as well as increased tolerance to different abiotic stresses compared with non-transgenic plants.116-118 A. thaliana plants overexpressing the SPDS cDNA from melon (Cucurbita ficifolia) exhibited a significant increase in SPDS activity as well as Put, Spd, Spm concentration, and tolerance to chilling, freezing, salinity, hyper-osmosis, and drought.116 Moreover, overexpressed SPDS transgenic plants of A. thaliana showed high level expression of various stressresponsive transcription factors such as DREB1A, DREB1B, DREB2B, and stress protective proteins rd29A.116 Overexpression of the apple SPDS gene in pear showed altered PA levels as well as increased tolerance to multiple abiotic stresses.119 Functional analyses of stress tolerance genes identified PAs and proline as molecular chaperones and key protective elements in drought, salinity, and temperature stress tolerance.42,120 Knowledge of the molecular mechanisms governing plant responses to abiotic stresses has increased considerably during the last decade and it is clear that protective mechanisms and metabolic networks connected with several upstream and downstream processes involved in stress tolerance are interconnected. Different abiotic stresses in plant is commonly known to alter osmotic potential and in accumulation of reactive oxygen species (ROS), while PAs may act as osmotic regulators and scavengers of ROS by overexpressing ADC in transgenic A. thaliana.125 Exogenous application of PAs (Put, Spd, Spm) in A. thaliana induced nitric oxide (NO) production and transgenic A. thaliana overexpressing rat nitric oxide synthase (NOS) showed enhanced tolerance to dehydration stress (10 d) and 200 mM NaCl stress (2 d) compared with nontransgenic plants.126 Genetic engineering of several metabolic pathways of several compatible solutes such as proline or glyceinbetaine for abiotic stress tolerance is also important.127-130 Abiotic stress tolerance is a complex phenomenon involving the adaptation, perpetuation, and responsive attitude of stress tolerance in a cyclic crosstalk by

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