Cadaverine’s functional role in plant development and environmental response

Frontiers in Plant Science

Volumn 7, Issue , 2016, Pages

  Jancewicz, Amy L ^a   Gibbs, Nicole M ^a   Masson, Patrick H ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Cadaverine; Metabolism; Phyllosphere; Plant development; Polyamine; Rhizosphere; Root architecture; Stress response

Indexed keywords

EID: 84976484751     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2016.00870     Document Type: Review

References (62)

1. Alcázar, R., Altabella, T., Marco, F., Bortolotti, C., Reymond, M., Koncz, C., et al. (2010). Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231, 1237-1249. doi: 10. 1007/s00425-010-1130-0
2. Andronis, E. A., Moschou, P. N., Toumi, I., and Roubelakis-Angelakis, K. A. (2014). Peroxisomal polyamine oxidase and NADPH-oxidase cross-talk for ROS homeostasis which affects respiration rate in Arabidopsis thaliana. Front. Plant Sci. 5: 132. doi: 10. 3389/fpls. 2014. 00132
3. Aziz, A., Martin-Tanguy, J., and Larher, F. (1998). Stress-induced changes in polyamine and tyramine levels can regulate proline accumulation in tomato leaf discs treated with sodium chloride. Physiol. Plant. 104, 195-202. doi: 10. 1034/j. 1399-3054. 1998. 1040207. x
4. Bagni, N., and Tassoni, A. (2001). Biosynthesis, oxidation and conjugation of aliphatic polyamines in higher plants. Amino Acids 20, 301-317. doi: 10. 1007/s007260170046
5. Bai, D. L., Tang, X. C., and He, X. C. (2000). Huperzine A, a potential therapeutic agent for treatment of Alzheimer's disease. Curr. Med. Chem. 7, 355-374. doi: 10. 2174/0929867003375281
6. Bunsupa, S., Katayama, K., Ikeura, E., Oikawa, A., Toyooka, K., Saito, K., et al. (2012a). Lysine decarboxylase catalyzes the first step of quinolizidine alkaloid biosynthesis and coevolved with alkaloid production in leguminosae. Plant Cell 24, 1202-1216. doi: 10. 1105/tpc. 112. 095885
7. Bunsupa, S., Yamazaki, M., and Saito, K. (2012b). Quinolizidine alkaloid biosynthesis: recent advances and future prospects. Front. Plant Sci. 3: 239. doi: 10. 3389/fpls. 2012. 00239
8. Campestre, M. P., Bordenave, C. D., Origone, A. C., Menéndez, A. B., Ruiz, O. A., Rodríguez, A. A., et al. (2011). Polyamine catabolism is involved in response to salt stress in soybean hypocotyls. J. Plant Physiol. 168, 1234-1240. doi: 10. 1016/j. jplph. 2011. 01. 007
9. Cassán, F., Maiale, S., Masciarelli, O., Vidal, A., Luna, V., and Ruiz, O. (2009). Cadaverine production by Azospirillum brasilense and its possible role in plant growth promotion and osmotic stress mitigation. Eur. J. Soil Biol. 45, 12-19. doi: 10. 1016/j. ejsobi. 2008. 08. 003
10. Çavuşoǧlu, K., Kılıç, S., and Kabar, K. (2007). Some morphological and anatomical observations during alleviation of salinity (NaCI) stress on seed germination and seedling growth of barley by polyamines. Acta Physiol. Plant 29, 551-557. doi: 10. 1007/s11738-007-0066-x
11. Cona, A., Rea, G., Angelini, R., Federico, R., and Tavladoraki, P. (2006). Functions of amine oxidases in plant development and defence. Trends Plant Sci. 11, 80-88. doi: 10. 1016/j. tplants. 2005. 12. 009
12. de Vrieze, J. (2015). The littlest farmhands. Science 349, 680-683. doi: 10. 1126/science. 349. 6249. 680
13. Di Martino, M. L., Campilongo, R., Casalino, M., Micheli, G., Colonna, B., and Prosseda, G. (2013). Polyamines: emerging players in bacteria-host interactions. Int. J. Med. Microbiol. 303, 484-491. doi: 10. 1016/j. ijmm. 2013. 06. 008
14. Dunand, C., Crèvecoeur, M., and Penel, C. (2007). Distribution of superoxide and hydrogen peroxide in Arabidopsis root and their influence on root development: possible interaction with peroxidases. New Phytol. 174, 332-341. doi: 10. 1111/j. 1469-8137. 2007. 01995. x
15. Dwoskin, L. P., and Crooks, P. A. (2002). A novel mechanism of action and potential use for lobeline as a treatment for psychostimulant abuse. Biochem. Pharmacol. 63, 89-98. doi: 10. 1016/S0006-2952(01)00899-1
16. Felix, H., and Harr, J. (1987). Association of polyamines to different parts of various plant species. Physiol. Plant. 71, 245-250. doi: 10. 1111/j. 1399-3054. 1987. tb04337. x
17. Fujita, M., Fujita, Y., Iuchi, S., Yamada, K., Kobayashi, Y., Urano, K., et al. (2012). Natural variation in a polyamine transporter determines paraquat tolerance in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 109, 6343-6347. doi: 10. 1073/pnas. 1121406109
18. Gamarnik, A. A., and Frydman, R. B. R. (1991). Cadaverine, an essential diamine for the normal root development of germinating soybean (Glycine max) seeds. Annu. Rev. Plant Physiol. 97, 778-785. doi: 10. 1104/pp. 97. 2. 778
19. Haneburger, I., Fritz, G., Jurkschat, N., Tetsch, L., Eichinger, A., Skerra, A., et al. (2012). Deactivation of the E. coli pH stress sensor CadC by cadaverine. J. Mol. Biol. 424, 15-27. doi: 10. 1016/j. jmb. 2012. 08. 023
20. Hart, J. J., Ditomaso, J. M., Linscott, D. L., and Kochian, L. V. (1992). Transport interactions between paraquat and polyamines in roots of intact maize seedlings. Plant Physiol. 99, 1400-1405. doi: 10. 1104/pp. 99. 4. 1400
21. Huang, C.-K., Chang, B.-S., Wang, K.-C., Her, S.-J., Chen, T.-W., Chen, Y.-A., et al. (2004). Changes in polyamine pattern are involved in floral initiation and development in Polianthes tuberosa. J. Plant Physiol. 161, 709-713. doi: 10. 1078/0176-1617-01256
22. Hussain, A., Saraiva, L. R., Ferrero, D. M., Ahuja, G., Krishna, V. S., Liberles, S. D., et al. (2013). High-affinity olfactory receptor for the death-associated odor cadaverine. Proc. Natl. Acad. Sci. U. S. A. 110, 19579-19584. doi: 10. 1073/pnas. 1318596110
23. Igarashi, K., Hamasaki, H., Miura, A., Kakegawa, T., Hirose, S., Matsuzaki, S., et al. (1986). Formation of a compensatory polyamine by Escherichia coli polyaminerequiring mutants during growth in the absence of polyamines. J. Bacteriol. 166, 128-134.
24. Kaniakova, M., Skrenkova, K., Adamek, S., Vyskocil, F., and Krusek, J. (2014). Different effects of lobeline on neuronal and muscle nicotinic receptors. Eur. J. Pharmacol. 738, 352-359. doi: 10. 1016/j. ejphar. 2014. 05. 057
25. Kuiper, I., Bloemberg, G. V., and Noreen, S. (2001). Increased uptake of putrescine in the rhizosphere inhibits competitive root colonization by Pseudomonas fluorescens strain WCS365. Mol. Plant 14, 1096-1104. doi: 10. 1094/MPMI. 2001. 14. 9. 1096
26. Kurakawa, T., Ueda, N., Maekawa, M., Kobayashi, K., Kojima, M., Nagato, Y., et al. (2007). Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature 445, 652-655. doi: 10. 1038/nature05504
27. Kuznetsov, V., Shorina, M., Aronova, E., Stetsenko, L., Rakitin, V., and Shevyakova, N. (2007). NaCl-and ethylene-dependent cadaverine accumulation and its possible protective role in the adaptation of the common ice plant to salt stress. Plant Sci. 172, 363-370. doi: 10. 1016/j. plantsci. 2006. 09. 012
28. Lavenus, J., Goh, T., Roberts, I., Guyomarc'h, S., Lucas, M., De Smet, I., et al. (2013). Lateral root development in Arabidopsis: fifty shades of auxin. Trends Plant Sci. 18, 450-458. doi: 10. 1016/j. tplants. 2013. 04. 006
29. Lavizzari, T., Breccia, M., Bover-Cid, S., Vidal-Carou, M. C., and Veciana-Nogués, M. T. (2010). Histamine, cadaverine, and putrescine produced in vitro by enterobacteriaceae and pseudomonadaceae isolated from spinach. J. Food Prot. 73, 385-389. doi: 10. 1007/s00217-006-0530-7
30. Lebeis, S. L., Paredes, S. H., Lundberg, D. S., Breakfield, N., Gehring, J., McDonald, M., et al. (2015). Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 349, 860-864. doi: 10. 1126/science. aaa8764
31. Lelandais-Brière, C., Jovanovic, M., Torres, G. A. M., Perrin, Y., Lemoine, R., Corre-Menguy, F., et al. (2007). Disruption of AtOCT1, an organic cation transporter gene, affects root development and carnitine-related responses in Arabidopsis. Plant J. 51, 154-164. doi: 10. 1111/j. 1365-313X. 2007. 03131. x
32. Liu, K., Fu, H., Bei, Q., and Luan, S. (2000). Inward potassium channel in guard cells as a target for polyamine regulation of stomatal movements. Annu. Rev. Plant Physiol. 124, 1315-1326. doi: 10. 1104/pp. 124. 3. 1315
33. Liu, T., Dobashi, H., Kim, D. W., Sagor, G. H. M., Niitsu, M., Berberich, T., et al. (2014). Arabidopsis mutant plants with diverse defects in polyamine metabolism show unequal sensitivity to exogenous cadaverine probably based on their spermine content. Physiol. Mol. Biol. Plants 20, 151-159. doi: 10. 1007/s12298-014-0227-5
34. Lundberg, D. S., Lebeis, S. L., Paredes, S. H., Yourstone, S., Gehring, J., Malfatti, S., et al. (2012). Defining the core Arabidopsis thaliana root microbiome. Nature 488, 86-90. doi: 10. 1038/nature11237
35. Meng, S., Su, L., Li, Y., Wang, Y., Zhang, C., and Zhao, Z. (2016). Nitrate and ammonium contribute to the distinct nitrogen metabolism of Populus simonii during moderate salt stress. PLoS ONE 11: e0150354. doi: 10. 1371/journal. pone. 0150354
36. Mulangi, V., Phuntumart, V., Aouida, M., Ramotar, D., and Morris, P. (2011). Functional analysis of OsPUT1, a rice polyamine uptake transporter. Planta 235, 1-11. doi: 10. 1007/s00425-011-1486-9
37. Negrel, J., Paynot, M., and Javelle, F. (1992). Purification and properties of putrescine hydroxycinnamoyl transferase from tobacco (Nicotiana tabacum) cell suspensions. Plant Physiol. 98, 1264-1269. doi: 10. 1104/pp. 98. 4. 1264
38. Neill, S. J., Desikan, R., Clarke, A., Hurst, R. D., and Hancock, J. T. (2002). Hydrogen peroxide and nitric oxide as signalling molecules in plants. J. Exp. Bot. 53, 1237-1247. doi: 10. 1093/jexbot/53. 372. 1237
39. Niemi, K., Häggman, H., and Sarjala, T. (2002). Effects of exogenous diamines on the interaction between ectomycorrhizal fungi and adventitious root formation in Scots pine in vitro. Tree Physiol. 22, 373-381. doi: 10. 1093/treephys/22. 6. 373
40. Ohe, M., Sasaki, H., Niitsu, M., Bagni, N., Tassoni, A., and Matsuzaki, S. (2010). Cadaverine turnover in soybean seedlings using 15N-labelled lysine and cadaverine. Plant Physiol. Biochem. 48, 591-595. doi: 10. 1016/j. plaphy. 2010. 01. 018
41. Ozawa, R., Bertea, C. M., Foti, M., Narayana, R., Arimura, G. I., Muroi, A., et al. (2009). Exogenous polyamines elicit herbivore-induced volatiles in Lima bean leaves: involvement of calcium. H2O2 and jasmonic acid. Plant Cell Physiol. 50, 2183-2199. doi: 10. 1093/pcp/pcp153
42. Pangesti, N., Pineda, A., Pieterse, C. M. J., Dicke, M., and van Loon, J. J. A. (2013). Two-way plant-mediated interactions between root-associated microbes and insects: from ecology to mechanisms. Front. Plant Sci. 4: 414. doi: 10. 3389/fpls. 2013. 00414
43. Planas-Portell, J., Gallart, M., Tiburcio, A. F., and Altabella, T. (2013). Coppercontaining amine oxidases contribute to terminal polyamine oxidation in peroxisomes and apoplast of Arabidopsis thaliana. BMC Plant Biol. 13: 109. doi: 10. 1186/1471-2229-13-109
44. Rolen, S. H., Sorensen, P. W., Mattson, D., and Caprio, J. (2003). Polyamines as olfactory stimuli in the goldfish Carassius auratus. J. Exp. Biol. 206, 1683-1696. doi: 10. 1242/jeb. 00338
45. Sagor, G. H. M., Berberich, T., Kojima, S., Niitsu, M., and Kusano, T. (2016). Spermine modulates the expression of two probable polyamine transporter genes and determines growth responses to cadaverine in Arabidopsis. Plant Cell Rep. 35, 1247-1257. doi: 10. 1007/s00299-016-1957-3
46. Schlaeppi, K., and Bulgarelli, D. (2015). The plant microbiome at work. Mol. Plant Microbe Interact. 28, 212-217. doi: 10. 1094/MPMI-10-14-0334-FI
47. Schoofs, G., Teichmann, S., Hartmann, T., and Wink, M. (1983). Lysine decarboxylase in plants and its integration in quinolizidine alkaloid biosynthesis. Phytochemistry 22, 65-69. doi: 10. 1016/S0031-9422(00)80 059-X
48. Shevyakova, N. I., Rakitin, V. Y., Duong, D. B., Sadomov, N. G., and Kuznetsov, V. V. (2001). Heat shock-induced cadaverine accumulation and translocation throughout the plant. Plant Sci. 161, 1125-1133. doi: 10. 1016/S0168-9452(01)00515-5
49. Simon-Sarkadi, L., Ludidi, N., and Kocsy, G. (2014). Modification of cadaverine content by NO in salt-stressed maize. Plant Signal. Behav. 9: e27598. doi: 10. 4161/psb. 27598
50. Strohm, A. K., Vaughn, L. M., and Masson, P. H. (2015). Natural variation in the expression of ORGANIC CATION TRANSPORTER 1 affects root length responses to cadaverine in Arabidopsis. J. Exp. Bot. 66, 853-862. doi: 10. 1093/jxb/eru444
51. Sziderics, A. H., Oufir, M., Trognitz, F., Kopecky, D., Matušíková, I., Hausman, J.-F., et al. (2010). Organ-specific defence strategies of pepper (Capsicum annuum L.) during early phase of water deficit. Plant Cell Rep. 29, 295-305. doi: 10. 1007/s00299-010-0822-z
52. Tokunaga, H., Kojima, M., Kuroha, T., Ishida, T., Sugimoto, K., Kiba, T., et al. (2011). Arabidopsis lonely guy (LOG) multiple mutants reveal a central role of the LOG-dependent pathway in cytokinin activation. Plant J. 69, 355-365. doi: 10. 1111/j. 1365-313X. 2011. 04795. x
53. Tomar, P. C., Lakra, N., and Mishra, S. (2013a). Cadaverine: a lysine catabolite involved in plant growth and development. Plant Signal Behav. 8: e25850. doi: 10. 4161/psb. 25850
54. Tomar, P. C., Lakra, N., and Mishra, S. N. (2013b). Effect of cadaverine on Brassica juncea (L.) under multiple stresses. Indian J. Exp. Biol. 51, 758-763.
55. Torrigiani, P., and Scoccianti, V. (1995). Regulation of cadaverine and putrescine levels in different organs of chick-pea seed and seedlings during germination. Physiol. Plant. 93, 512-518. doi: 10. 1111/j. 1399-3054. 1995. tb0 6851. x
56. Torrigiani, P., Serafini-Fracassini, D., and Bagni, N. (1987). Polyamine biosynthesis and effect of dicyclohexylamine during the cell cycle of Helianthus tuberosus tuber. Plant Physiol. 84, 148-152.
57. Vaz, F. M., and Wanders, R. J. A. (2002). Carnitine biosynthesis in mammals. Biochem. J. 361, 417-429. doi: 10. 1042/bj3 610417
58. Voigt, J., Deinert, B., and Bohley, P. (2000). Subcellular localization and light-dark control of ornithine decarboxylase in the unicellular green alga Chlamydomonas reinhardtii. Physiol. Plant. 108, 353-360. doi: 10. 1034/j. 1399-3054. 2000. t01-1-100403. x
59. Wink, M. (1992). "The role of quinolizidine alkaloids in plant-insect interactions, " in Insect-Plant Interactions, ed. E. A. Bernays (Boca Raton, FL: CRC-Press), 133-169.
60. Wink, M. (2010). "Molecular modes of action of cytotoxic alkaloids: from DNA intercalation, spindle poisoning, topoisomerase inhibition to apoptosis and multiple drug resistance, " in The Alkaloids, Vol. 64, ed. G. A. Cordell (Amsterdam: Elsevier), 1-47. doi: 10. 1016/S1099-4831(07)64001-2
61. Yamaguchi, K., Takahashi, Y., Berberich, T., Imai, A., Miyazaki, A., Takahashi, T., et al. (2006). The polyamine spermine protects against high salt stress in Arabidopsis thaliana. FEBS Lett. 580, 6783-6788. doi: 10. 1016/j. febslet. 2006. 10. 078
62. Yokota Hirai, M., Suzuki, H., Yamazaki, M., and Saito, K. (2000). Biochemical and partial molecular characterization of bitter and sweet forms of Lupinus angustifolius, an experimental model for study of molecular regulation of quinolizidine alkaloid biosynthesis. Chem. Pharm. Bull. 48, 1458-1461. doi: 10. 1248/cpb. 48. 1458