Skip to main content
SpringerLink
Log in

Down-regulation of S-adenosylmethionine decarboxylase genes results in reduced plant length, pollen viability, and abiotic stress tolerance

  • Original Paper
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

Abstract

S-adenosylmethionine decarboxylase (SAMDC) is a key enzyme for synthesis of polyamines, regulating plant growth and development as well as plant stress responses. Transgenic rice plants down-regulating OsSAMDC2 were generated by RNA interference. Transcript levels of OsSAMDC2, OsSAMDC1 and OsSAMDC4 were all reduced in transgenic rice, along with decreased levels of sperimidine (Spd) and spermin (Spm) and polyamine oxidase activity. The transgenic lines showed a reduced apical dominance phenotype with lower plant length, higher tiller numbers, reduced and delayed seed germination rate, and decreased pollen viability, seed setting rate and grain yield per plant. Tolerance to multiple abiotic stresses (drought, salinity, and chilling) was also reduced in transgenic plants in association with inhibition of antioxidant enzyme activities under stressed conditions. Our results suggest that Spd and Spm are essential for maintenance of normal plant growth, pollen viability, seed setting rate, grain yield and stress tolerance in rice.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249

    Article  PubMed  Google Scholar 

  • Alcázar R, Cuevas JC, Planas J, Zarza X, Bortolotti C, Carrascoc P, Salinas J, Tiburcio AF, Altabell T (2011) Integration of polyamines in the cold acclimation response. Plant Sci 180:31–38

    Article  PubMed  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts: Polyphenol oxidase in Beta vulgaris. Plant Physiol 24:1–15

    Google Scholar 

  • Capell T, Bassie L, Christou P (2004) Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc Natl Acad Sci USA 101:9909–9914

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Guo Z, Fang J, Lu S (2013) Physiological responses of a centipedegrass mutant to chilling stress. Agron J 105:1814–1820

    Article  CAS  Google Scholar 

  • Cheng L, Zou YJ, Ding SL, Zhang JJ, Yu XL, Cao JS, Lu G (2009) Polyamine accumulation in transgenic tomato enhances the tolerance to high temperature stress. J Integr Plant Biol 51:489–499

    Article  CAS  PubMed  Google Scholar 

  • Chu CC, Wang CC, Sun C, Hsu C, Yin KC, Chu CY, Bi FY (1975) Establishment of an efficient experiments on the nitrogen sources. Sci Sin 18:659–668

    Google Scholar 

  • Cuevas JC, López-Cobollo R, Alcázar P, Zarza X, Koncz C, Altabella T, Salinas J, Tiburcio AF, Ferrando A (2008) Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant Physiol 148:1094–1105

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Do PT, Degenkolbe T, Erban A, Heyer AG, Kopka J, Köhl KI, Hincha DK, Zuther E (2013) Dissecting rice polyamine metabolism under controlled long-term drought stress. PLoS One 8:e60325

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Falasca G, Franceschetti M, Bagni N, Altamura MM, Biasi R (2010) Polyamine biosynthesis and control of the development of functional pollen in kiwifruit. Plant Physiol Biochem 48:565–573

    Article  CAS  PubMed  Google Scholar 

  • Filippou P, Antoniou C, Fotopoulos V (2013) The nitric oxide donor sodium nitroprusside regulates polyamine and proline metabolism in leaves of Medicago truncatula plants. Free Radic Biol Med 56:172–183

    Article  CAS  PubMed  Google Scholar 

  • Flores E, Galston AW (1982) Analysis of polyamines in higher plants by high performance liquid chromatography. Plant Physiol 69:701–706

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirement suspension cultures of soybean root cells. Exp Cell Res 50:151–158

    Article  CAS  PubMed  Google Scholar 

  • Ge C, Cui X, Wang Y, Hu Y, Fu Z, Zhang D, Cheng Z, Li J (2006) BUD2, encoding an S-adenosylmethionine decarboxylase, is required for Arabidopsis growth and development. Cell Res 16:446–456

    Article  CAS  PubMed  Google Scholar 

  • Gill SS, Tuteja N (2010) Polyamines and abiotic stress tolerance in plants. Plant Signal Behav 5:26–33

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Grossmann K, Häuser C, Sauerbrey E, Fritsch H, Schmidt O, Jung J (1989) Plant growth retardants as inhibitors of ethylene production. J Plant Physiol 134:538–543

    Article  CAS  Google Scholar 

  • Guo DP, Sun YZ, Chen ZJ (2003) Involvement of polyamines in cytoplasmic male sterility of stem mustard (Brassica juncea var. tsatsai). Plant Growth Regul 41:33–40

    Article  CAS  Google Scholar 

  • Guo Z, Ou W, Lu S, Zhong Q (2006) Differential responses of antioxidative system to chilling and drought in four rice cultivars differing in sensitivity. Plant Physiol Biochem 44:828–836

    Article  CAS  PubMed  Google Scholar 

  • Gupta K, Dey A, Gupta B (2013) Plant polyamines in abiotic stress responses. Acta Physiol Plant 35:2015–2036

    Google Scholar 

  • Hao YJ, Zhang Z, Kitashiba H, Honda C, Ubi B, Kita M, Moriguchi T (2005) Molecular cloning and functional characterization of two apple S-adenosylmethionine decarboxylase genes and their different expression in fruit development, cell growth and stress responses. Gene 350:41–50

    Article  CAS  PubMed  Google Scholar 

  • He L, Ban Y, Inoue H, Matsuda N, Liu J, Moriguchi T (2008) Enhancement of spermidine content and antioxidant capacity in transgenic pear shoots overexpressing apple spermidine synthase in response to salinity and hyperosmosis. Phytochemistry 69:2133–2141

    Article  CAS  PubMed  Google Scholar 

  • Hu X, Liu Y (2006) The construction of RNAi vectors and the use for gene silencing in rice. Mol Plant Breed 4:621–626

    CAS  Google Scholar 

  • Huang HT, Villanueva VR (1992) Inhibition of polyamine biosynthesis and seed germination in Picea abies. Phytochemistry 31:3353–3356

    Article  Google Scholar 

  • Huang CK, Chang BS, Wang KC, Her SJ, Chen TW, Chen YA, Cho CL, Liao LJ, Huang KL, Chen WS, Liu ZH (2004) Changes in polyamine pattern are involved in floral initiation and development in Polianthes tuberosa. J Plant Physiol 161:709–713

    Article  CAS  PubMed  Google Scholar 

  • Hussain SS, Ali M, Ahmad M, Siddique KH (2011) Polyamines: natural and engineered abiotic and biotic stress tolerance in plants. Biotechnol Adv 29:300–311

    Article  CAS  PubMed  Google Scholar 

  • Imai A, Matsuyama T, Hanzawa Y, Akiyama T, Tamaoki M, Saji H, Shirano Y, Kato T, Hayashi H, Shibata D, Tabata S, Komeda Y, Takahashi T (2004) Spermidine synthase genes are essential for survival of Arabidopsis. Plant Physiol 135:1565–1573

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kasinathan V, Wingler A (2004) Effect of reduced arginine decarboxylase activity on salt tolerance and on polyamine formation during salt stress in Arabidopsis thaliana. Physiol Plant 121:101–107

    Article  CAS  PubMed  Google Scholar 

  • Kasukabe Y, He L, Nada K, Misawa S, Ihara I, Tachibana S (2004) Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress regulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol 45:712–722

    Article  CAS  PubMed  Google Scholar 

  • Kasukabe Y, He L, Watakabe Y, Otani M, Shimada T, Tachibana S (2006) Improvement of environmental stress tolerance of sweet potato by introduction of genes for spermidine synthase. Plant Biotechnol 23:75–83

    Article  CAS  Google Scholar 

  • Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kawai K, Galbraith D, Bohnert HJ (2001) Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13:889–905

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kovács Z, Simon-Sarkadi L, Szúucs A, Kocsy G (2010) Differential effects of cold, osmotic stress and abscisic acid on polyamine accumulation in wheat. Amino Acids 38:623–631

    Article  PubMed  Google Scholar 

  • Kumar A, Taylor MA, Arif SA, Davies HV (1996) Potato plants expressing antisense and sense S-adenosylmethionine decarboxylase (SAMDC) transgenes show altered levels of polyamines and ethylene: antisense plants display abnormal phenotypes. Plant J 9:147–158

    Article  CAS  Google Scholar 

  • Kumria R, Rajam MV (2002) Ornithine decarboxylase transgene in tobacco affects polyamines, in vitro-morphogenesis and response to salt stress. J Plant Physiol 159:983–990

    Article  CAS  Google Scholar 

  • Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228:367–381

    Article  CAS  PubMed  Google Scholar 

  • Li SC, Yang L, Deng QM, Wang SQ, Wu FQ, Li P (2006) Phenotypic characterization of a female sterile mutant in rice. J Intergr Plant Biol 48:307–314

    Article  Google Scholar 

  • Liu JH, Nada K, Honda C, Kitashiba H, Wen XP, Pang XM, Moriguchi T (2006) Polyamine biosynthesis of apple callus under salt stress: importance of the arginine decarboxylase pathway in stress response. J Exp Bot 57:2589–2599

    Article  CAS  PubMed  Google Scholar 

  • Lu S, Wang Z, Peng X, Guo Z, Zhang G, Han L (2006) An efficient callus suspension culture system for triploid bermudagrass (Cynodon transvaalensis × C. dactylon) and somaclonal variations. Plant Cell Tiss Org Cult 87:77–84

    Article  Google Scholar 

  • Ma W, Wang J, Hu J, Guan Y, Li Y, Zheng Y (2012) Relation between changes in polyamine, protective enzyme activity and pollen vigor of tobacco in different flowering stages. Afr J Agric Res 7:5491–5497

    Google Scholar 

  • Moschou PN, Paschalidis KA, Delis ID, Andriopoulou AH, Lagiotis GD, Yakoumakis DI, Roubelakis-Angelakis KA (2008) Spermidine exodus and oxidation in the apoplast induced by abiotic stress is responsible for H2O2 signatures that direct tolerance responses in tobacco. Plant Cell 20:1708–1724

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nayyar H, Chander S (2004) Protective effects of polyamines against oxidative stress induced by water and cold stress in chickpea. J Agron Crop Sci 190:355–365

    Article  CAS  Google Scholar 

  • Prabhavathi VR, Rajam MV (2007) Polyamine accumulation in transgenic eggplant enhances tolerance to multiple abiotic stresses and fungal resistance. Plant Biotechnol 24:273–282

    Article  CAS  Google Scholar 

  • Rodríguez AA, Maiale SJ, Menéndez AB, Ruiz OA (2009) Polyamine oxidase activity contributes to sustain maize leaf elongation under saline stress. J Exp Bot 60:4249–4262

    Article  PubMed  Google Scholar 

  • Roy M, Wu R (2001) Arginine decarboxylase transgene expression and analysis of environmental stress tolerance in transgenic rice. Plant Sci 160:869–875

    Article  CAS  PubMed  Google Scholar 

  • Roy M, Wu R (2002) Overexpression of S-adenosyl methionine dearboxylase gene in rice increases polyamine level and enhances sodium chloride-stress tolerance. Plant Sci 163:987–992

    Article  CAS  Google Scholar 

  • Roy P, Niyogi K, SenGupta DN, Ghosh B (2005) Spermidine treatment to rice seedlings recovers salinity stress-induced damage of plasma membrane and PM-bound H1-ATPAe in salt-tolerant and salt-sensitive rice cultivars. Plant Sci 168:583–591

    Article  CAS  Google Scholar 

  • Roychoudhury A, Basu S, Sengupta DN (2011) Amelioration of salinity stress by exogenously applied spermidine or spermine in three varieties of indica rice differing in their level of salt tolerance. J Plant Physiol 168:317–328

    Article  CAS  PubMed  Google Scholar 

  • Shen W, Nada K, Tachibana S (2000) Involvement of polyamines in the chilling tolerance of cucumber cultivars. Plant Physiol 124:431–439

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shi J, Fu XZ, Peng T, Huang XS, Fan QJ, Liu JH (2010) Spermine pretreatment confers dehydration tolerance of citrus in vitro plants via modulation of antioxidative capacity and stomatal response. Tree Physiol 30:914–922

    Article  CAS  PubMed  Google Scholar 

  • Shimizu-Sato S, Mori H (2001) Control of outgrowth and dormancy in axillary buds. Plant Physiol 127:1405–1413

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sinha R, Rajam MV (2013) RNAi silencing of three homologues of S-adenosylmethionine decarboxylase gene in tapetal tissue of tomato results in male sterility. Plant Mol Biol 82:169–180

    Article  CAS  PubMed  Google Scholar 

  • Slocum RD, Flores HE, Gaiston AW, Weinstein LH (1989) Improved method for HPLC analysis of polyamines, agmatine and aromatic monoamines in plant tissue. Plant Physiol 89:512–517

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Song J, Nada K, Tachibana S (2001) The early increase of S-adenosylmethionine decarboxylase activity is essential for the normal germination and tube growth in tomato (Lycopersicon esculentum Mill.) pollen. Plant Sci 161:507–515

    Article  CAS  Google Scholar 

  • Tassoni A, Franceschetti M, Bagni N (2008) Polyamines and salt stress response and tolerance in Arabidopsis thaliana flowers. Plant Physiol Biochem 46:607–613

    Article  CAS  PubMed  Google Scholar 

  • Urano K, Hobo T, Shinozaki K (2005) Arabidopsis ADC genes involved in polyamine biosynthesis are essential for seed development. FEBS Lett 579:1557–1564

    Article  CAS  PubMed  Google Scholar 

  • Verma S, Mishra SN (2005) Putrescine alleviation of growth in salt stressed Brassica juncea by inducing antioxidative defense system. J Plant Physiol 162:669–677

    Article  CAS  PubMed  Google Scholar 

  • Waie B, Rajam MV (2003) Effect of increased polyamine biosynthesis on stress responses in transgenic tobacco by introduction of human S-adenosylmethionine gene. Plant Sci 164:727–734

    Article  CAS  Google Scholar 

  • Wan X, Tan J, Lu S, Lin C, Hu Y, Guo Z (2009) The increased tolerance to oxidative stress in transgenic tobaccos expressing a wheat oxalate oxidase gene via induction of antioxidant enzymes is mediated by H2O2. Physiol Plant 136:30–44

    Article  CAS  PubMed  Google Scholar 

  • Wen XP, Pang XM, Matsuda N, Kita M, Inoue H, Hao YJ, Honda C, Moriguchi T (2008) Overexpression of the apple spermidine synthase gene in pear confers multiple abiotic stress tolerance by altering polyamine titers. Transgenic Res 17:251–263

    Article  CAS  PubMed  Google Scholar 

  • Wi SJ, Kim WT, Park KY (2006) Overexpression of carnation S-adenosylmethionine decarboxylase gene generates a broad-spectrum tolerance to abiotic stresses in transgenic tobacco plants. Plant Cell Rep 25:1111–1121

    Article  CAS  PubMed  Google Scholar 

  • Wu J, Shang Z, Wu J, Jiang X, Moschou PN, Sun W, Roubelakis-Angelakis KA, Zhang S (2010) Spermidine oxidase-derived H2O2 regulates pollen plasma membrane hyperpolarization-activated Ca2+-permeable channels and pollen tube growth. Plant J 63:1042–1053

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi T, Nakayama K, Hayashi T, Yazaki J, Kishimoto N, Kikuchi S, Koike S (2004) cDNA microarray analysis of rice anther genes under chilling stress at the microsporogenesis stage revealed two genes with DNA transposon Castaway in the 5′-flanking region. Biosci Biotechnol Biochem 68:1315–1323

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi K, Takahashi Y, Berberich T, Imai A, Miyazaki A, Takahashi T, Michael A, Kusano T (2006) The polyamine spermine protects against high salt stress in Arabidopsis thaliana. FEBS Lett 580:6783–6788

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi K, Takahashi Y, Berberich T, Imai A, Takahashi T, Michael AJ, Kusano T (2007) A protective role for the polyamine spermine against drought stress in Arabidopsis. Biochem Biophys Res Commun 352:486–490

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Zhang J, Liu K, Wang Z, Liu L (2007) Involvement of polyamines in the drought resistance of rice. J Exp Bot 58:1545–1555

    Article  CAS  PubMed  Google Scholar 

  • Zhuo C, Wang T, Lu S, Zhao Y, Li X, Guo Z (2013) A cold responsive galactinol synthase gene from Medicago falcata (MfGolS1) is induced by myo-inositol and confers multiple tolerances to abiotic stresses. Physiol Plant 149:67–78. doi:10.1111/ppl.12019

    Google Scholar 

Download references

Acknowledgments

This work was funded by grants from the Natural Science Foundation of China (30972027, 31172253) and Research Fund for the Doctoral Program of Higher Education of China (20114404110009).

Author information

Author notes

  1. Jingjing Chen

    Present address: South Subtropical Crop Research Institute, Chinese Academy of Tropical Agricultural Science, Zhanjiang, 524091, China

Authors and Affiliations

  1. State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, South China Agricultural University, Guangzhou, 510642, China

    Miao Chen, Jingjing Chen, Junyang Fang, Zhenfei Guo & Shaoyun Lu

  2. Guangdong Key Laboratory for Innovative Development and Utilization of Forest Plant Germplasm, South China Agricultural University, Guangzhou, 510642, China

    Miao Chen, Jingjing Chen, Junyang Fang, Zhenfei Guo & Shaoyun Lu

Authors
  1. Miao Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jingjing Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Junyang Fang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhenfei Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shaoyun Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Zhenfei Guo or Shaoyun Lu.

Additional information

Miao Chen and Jingjing Chen have equally contribute to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 275 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-013-0405-0

Keywords

Search

Navigation