Polyamine Metabolic Canalization in Response to Drought Stress in Arabidopsis and the Resurrection Plant Craterostigma Plantagineum

Overview

Journal Plant Signal Behav

Specialty Biology

Date 2011 Feb 19

PMID 21330782

Citations 41

Authors

Ruben Alcazar

Marta Bitrian

Dorothea Bartels

Csaba Koncz

Teresa Altabella

Antonio F Tiburcio

Affiliations

Soon will be listed here.

Abstract

In this work, we have studied the transcriptional profiles of polyamine biosynthetic genes and analyzed polyamine metabolic fluxes during a gradual drought acclimation response in Arabidopsis thaliana and the resurrection plant Craterostigma plantagineum. The analysis of free putrescine, spermidine and spermine titers in Arabidopsis arginine decarboxylase (adc1-3, adc2-3), spermidine synthase (spds1-2, spds2-3) and spermine synthase (spms-2) mutants during drought stress, combined with the quantitative expression of the entire polyamine biosynthetic pathway in the wild-type, has revealed a strong metabolic canalization of putrescine to spermine induced by drought. Such canalization requires spermidine synthase 1 (SPDS1) and spermine synthase (SPMS) activities and, intriguingly, does not lead to spermine accumulation but to a progressive reduction in spermidine and spermine pools in the wild-type. Our results suggest the participation of the polyamine back-conversion pathway during the drought stress response rather than the terminal catabolism of spermine. The putrescine to spermine canalization coupled to the spermine to putrescine back-conversion confers an effective polyamine recycling-loop during drought acclimation. Putrescine to spermine canalization has also been revealed in the desiccation tolerant plant C. plantagineum, which conversely to Arabidopsis, accumulates high spermine levels which associate with drought tolerance. Our results provide a new insight to the polyamine homeostasis mechanisms during drought stress acclimation in Arabidopsis and resurrection plants.

Citing Articles

Supplemental Sodium Nitroprusside and Spermidine Regulate Water Balance and Chlorophyll Pigments to Improve Sunflower Yield under Terminal Drought.

Hussain I, Shehzad M, Akhtar G, Ahmad K, Mubeen K, Hassan W ACS Omega. 2024; 9(28):30478-30491.

PMID: 39035905 PMC: 11256320. DOI: 10.1021/acsomega.4c02061.

Transcriptional repression of under water-deficit stress promotes anthocyanin biosynthesis to enhance drought tolerance.

Mano N, Shaikh M, Widhalm J, Yoo C, Mickelbart M Plant Direct. 2024; 8(5):e594.

PMID: 38799417 PMC: 11117050. DOI: 10.1002/pld3.594.

Transcriptomic and metabolomic profiling reveals the drought tolerance mechanism of (Schisandraceae).

Zhang X, Wu C, Liu B, Liang H, Wang M, Li H Front Plant Sci. 2024; 14:1284135.

PMID: 38259923 PMC: 10800416. DOI: 10.3389/fpls.2023.1284135.

Differential Gene Expression Responses to Salt and Drought Stress in Tall Fescue (Festuca arundinacea Schreb.).

Esmailpourmoghadam E, Salehi H, Moshtaghi N Mol Biotechnol. 2023; 66(9):2481-2496.

PMID: 37742296 DOI: 10.1007/s12033-023-00888-8.

Interactions of Polyamines and Phytohormones in Plant Response to Abiotic Stress.

Napieraj N, Janicka M, Reda M Plants (Basel). 2023; 12(5).

PMID: 36904019 PMC: 10005635. DOI: 10.3390/plants12051159.

References

Bae H, Kim S, Kim M, Sicher R, Lary D, Strem M . The drought response of Theobroma cacao (cacao) and the regulation of genes involved in polyamine biosynthesis by drought and other stresses. Plant Physiol Biochem. 2007; 46(2):174-88. DOI: 10.1016/j.plaphy.2007.10.014. View

Capell T, Bassie L, Christou P . Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc Natl Acad Sci U S A. 2004; 101(26):9909-14. PMC: 470772. DOI: 10.1073/pnas.0306974101. View

Yamaguchi-Shinozaki K, Shinozaki K . Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol. 2006; 57:781-803. DOI: 10.1146/annurev.arplant.57.032905.105444. View

Alcazar R, Planas J, Saxena T, Zarza X, Bortolotti C, Cuevas J . Putrescine accumulation confers drought tolerance in transgenic Arabidopsis plants over-expressing the homologous Arginine decarboxylase 2 gene. Plant Physiol Biochem. 2010; 48(7):547-52. DOI: 10.1016/j.plaphy.2010.02.002. View

Janowitz T, Kneifel H, Piotrowski M . Identification and characterization of plant agmatine iminohydrolase, the last missing link in polyamine biosynthesis of plants. FEBS Lett. 2003; 544(1-3):258-61. DOI: 10.1016/s0014-5793(03)00515-5. View

Kakehi J, Kuwashiro Y, Niitsu M, Takahashi T . Thermospermine is required for stem elongation in Arabidopsis thaliana. Plant Cell Physiol. 2008; 49(9):1342-9. DOI: 10.1093/pcp/pcn109. View

Yamasaki H, Cohen M . NO signal at the crossroads: polyamine-induced nitric oxide synthesis in plants?. Trends Plant Sci. 2006; 11(11):522-4. DOI: 10.1016/j.tplants.2006.09.009. View

Yamaguchi K, Takahashi Y, Berberich T, Imai A, Takahashi T, Michael A . A protective role for the polyamine spermine against drought stress in Arabidopsis. Biochem Biophys Res Commun. 2006; 352(2):486-90. DOI: 10.1016/j.bbrc.2006.11.041. View

Kusano T, Yamaguchi K, Berberich T, Takahashi Y . The polyamine spermine rescues Arabidopsis from salinity and drought stresses. Plant Signal Behav. 2009; 2(4):251-2. PMC: 2634138. DOI: 10.4161/psb.2.4.3866. View

10.

Kusano T, Berberich T, Tateda C, Takahashi Y . Polyamines: essential factors for growth and survival. Planta. 2008; 228(3):367-81. DOI: 10.1007/s00425-008-0772-7. View

11.

Rios G, Lossow A, Hertel B, Breuer F, Schaefer S, Broich M . Rapid identification of Arabidopsis insertion mutants by non-radioactive detection of T-DNA tagged genes. Plant J. 2002; 32(2):243-53. DOI: 10.1046/j.1365-313x.2002.01416.x. View

12.

Chen K, Liu A . Biochemistry and function of hypusine formation on eukaryotic initiation factor 5A. Biol Signals. 1997; 6(3):105-9. DOI: 10.1159/000109115. View

13.

Sasaki K, Abid M, Miyazaki M . Deoxyhypusine synthase gene is essential for cell viability in the yeast Saccharomyces cerevisiae. FEBS Lett. 1996; 384(2):151-4. DOI: 10.1016/0014-5793(96)00310-9. View

14.

Panicot M, Minguet E, Ferrando A, Alcazar R, Blazquez M, Carbonell J . A polyamine metabolon involving aminopropyl transferase complexes in Arabidopsis. Plant Cell. 2002; 14(10):2539-51. PMC: 151234. DOI: 10.1105/tpc.004077. View

15.

Mattoo A, Minocha S, Minocha R, Handa A . Polyamines and cellular metabolism in plants: transgenic approaches reveal different responses to diamine putrescine versus higher polyamines spermidine and spermine. Amino Acids. 2009; 38(2):405-13. DOI: 10.1007/s00726-009-0399-4. View

16.

Kalamaki M, Merkouropoulos G, Kanellis A . Can ornithine accumulation modulate abiotic stress tolerance in Arabidopsis?. Plant Signal Behav. 2009; 4(11):1099-101. PMC: 2819526. DOI: 10.4161/psb.4.11.9873. View

17.

Tuteja N . Abscisic Acid and abiotic stress signaling. Plant Signal Behav. 2009; 2(3):135-8. PMC: 2634038. DOI: 10.4161/psb.2.3.4156. View

18.

Kuppusamy K, Walcher C, Nemhauser J . Cross-regulatory mechanisms in hormone signaling. Plant Mol Biol. 2008; 69(4):375-81. DOI: 10.1007/s11103-008-9389-2. View

19.

Toumi I, Moschou P, Paschalidis K, Bouamama B, Ben Salem-Fnayou A, Ghorbel A . Abscisic acid signals reorientation of polyamine metabolism to orchestrate stress responses via the polyamine exodus pathway in grapevine. J Plant Physiol. 2010; 167(7):519-25. DOI: 10.1016/j.jplph.2009.10.022. View

20.

Alcazar R, Garcia-Martinez J, Cuevas J, Tiburcio A, Altabella T . Overexpression of ADC2 in Arabidopsis induces dwarfism and late-flowering through GA deficiency. Plant J. 2005; 43(3):425-36. DOI: 10.1111/j.1365-313X.2005.02465.x. View