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Polyamines and cellular metabolism in plants: transgenic approaches reveal different responses to diamine putrescine versus higher polyamines spermidine and spermine

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Abstract

Distribution of biogenic amines—the diamine putrescine (Put), triamine spermidine (Spd), and tetraamine spermine (Spm)—differs between species with Put and Spd being particularly abundant and Spm the least abundant in plant cells. These amines are important for cell viability and their intracellular levels are tightly regulated, which have made it difficult to characterize individual effects of Put, Spd and Spm on plant growth and developmental processes. The recent transgenic intervention and mutational genetics have made it possible to stably alter levels of naturally occurring polyamines and study their biological effects. We bring together an analysis of certain metabolic changes, particularly in amino acids, to infer the responsive regulation brought about by increased diamine or polyamine levels in actively growing poplar cell cultures (transformed with mouse ornithine decarboxylase gene to accumulate high Put levels) and ripening tomato pericarp (transformed with yeast S-adenosylmethionine decarboxylase gene to accumulate high Spd and Spm levels at the cost of Put). Our analysis indicates that increased Put has little effect on increasing the levels of Spd and Spm, while Spd and Spm levels are inter-dependent. Further, Put levels were positively associated with Ala (α and β), Ile and GABA and negatively correlated with Gln and Glu in both actively growing poplar cell cultures and non-dividing tomato pericarp tissue. Most amino acids showed positive correlations with Spd and Spm levels in actively growing cells. Collectively these results suggest that Put is a negative regulator while Spd–Spm are positive regulators of cellular amino acid metabolism.

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Abbreviations

DAO:

Diamine oxidase

eIF5A:

Eukaryotic initiation factor 5A

HP:

High putrescine

NAGS:

N-acetyl glutamate synthase

P5CS:

Δ1-Pyrroline-5-carboxylate synthase

PAO:

Polyamine oxidase

Put:

Putrescine

Spd:

Spermidine

Spm:

Spermine

ySAMDC:

Yeast S-adenosylmethionine decarboxylase

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Acknowledgments

We acknowledge the contributions of our collaborators listed in the cited references. The research presented here was funded by USDA-NRI award No. 2002-35318-12674 to SCM); the NH Agricultural Experiment Station (to SCM and RKM); the US Forest Service, Northern Research Station; US–Israel BARD grant (to AKH and AKM; Grant N0. IS-3441-03), a grant from the U.S. Department of Agriculture, IFAFS program (to AKH; Award No. 741740), and U.S. Department of Agriculture, Agricultural Research Service. This is scientific contribution number 2407 from the NH Agricultural Experiment Station. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture.

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  1. Sustainable Agriculture Systems Laboratory, The Henry A. Wallace Beltsville Agricultural Research Center, United States Department of Agriculture, Agriculture Research Service, Building 001, Beltsville, MD, 20705-2350, USA

    Autar K. Mattoo

  2. Department of Biological Sciences, University of New Hampshire, Durham, NH 03824, USA

    Subhash C. Minocha

  3. US Forest Service, Northern Research Station, Mast Road, Durham, NH, 03824, USA

    Rakesh Minocha

  4. Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN, 47907, USA

    Avtar K. Handa

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  1. Autar K. Mattoo
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Correspondence to Autar K. Mattoo.

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Mattoo, A.K., Minocha, S.C., Minocha, R. et al. Polyamines and cellular metabolism in plants: transgenic approaches reveal different responses to diamine putrescine versus higher polyamines spermidine and spermine. Amino Acids 38, 405–413 (2010). https://doi.org/10.1007/s00726-009-0399-4

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