Editorial: Physiological Aspects of Non-proteinogenic Amino Acids in Plants (2024)

editorial

. 2020 Dec 17;11:519464. doi: 10.3389/fpls.2020.519464

In addition to the canonical 20 amino acids that constitute the essential building blocks of proteins, plants produce a wide variety of non-proteinogenic amino acids (NPAAs; Fowden, 1981, Rosenthal, 1982, Barrett, 1985, Bell, 2003). Some of these plant metabolites are components of central metabolism, serving as intermediates in biosynthetic pathways or as signaling molecules during plant stress responses. NPAAs such as ornithine, citrulline, arginosuccinate, homoserine, homocysteine, and cystathionine, are well-studied metabolic intermediates and are likely to be present in all plant species. Other commonly encountered plant NPAAs, for instance pipecolic acid with its derivatives, can function as signaling molecules that influence plant development, physiology, and defense responses (Huang et al., 2020).

A particularly noteworthy NPAA, γ-aminobutyric acid (GABA), is essential for many physiological and developmental processes in plants, including energy dissipation, maintenance of carbon/nitrogen balance, pollen tube growth, and fruit development (Kinnersley and Turano, 2000, Palanivelu et al., 2003, Fait et al., 2008, Snowden et al., 2015, Amir et al., 2018). Functioning as both signaling molecule and a regulator of plant metabolism, GABA can modulate plant immune responses (Kim et al., 2013, Wang et al., 2019, Deng et al., 2020, Tarkowski et al., 2020). Numerous studies have shown a role for GABA accumulation in protecting plants against abiotic stresses such as drought and salinity (Bor et al., 2009, Akcay et al., 2012, Vijayakumari and Puthur, 2015, Mekonnen, 2017, Carillo, 2018, Rezaei-Chiyaneh et al., 2018, Jin et al., 2019, Podlesakova et al., 2019).

NPAAs that are not part of primary metabolism are often defense-related, providing protection against pests and pathogens, and typically have a more sporadic distribution in the plant kingdom (Bell, 1976). For instance, many legumes accumulate large amounts of canavanine or other NPAAs that not only function as defensive metabolites but also serve for nitrogen storage in the seeds (Huang et al., 2011). Canavanine is a structural analog of arginine and exerts its toxicity in animals by interfering with arginine-related metabolism, including nitric oxide synthase and incorporation of arginine into proteins (Bence and Crooks, 2003). In new research on the toxicity of canavanine in plants, Staszek et al. show that the canavanine-mediated inhibition of nitric oxide biosynthesis leads to formation of differentially nitrated proteins and a disruption of the antioxidant system in tomato roots.

Another NPAA, 1-aminocyclopropane carboxylate (ACC), is the direct precursor of ethylene, a gaseous hormone regulating a wide ranges of developmental and stress-related processes in plants (e.g., Lee et al., 2019, Seo and Yoon, 2019). However, as discussed by Polko and Kieber, ACC itself also functions as a plant signaling molecule. Physiological processes in plants that are influenced directly by ACC include stomatal development, cell wall biosynthesis, stress responses, and pathogen interactions (Xu et al., 2008, Tsuchisaka et al., 2009, Tsang et al., 2011, Yin et al., 2019). The levels of ACC in plants are critical for ethylene production and seem to be influenced by another group of NPAAs, the D-Amino acids. D-Amino acid isomers of the proteinogenic L-amino acids are produced by soil microbes and are taken up by plant roots, but can also be produced by plants themselves (Genchi, 2017). Although some D-amino acids are toxic to Arabidopsis thaliana (Arabidopsis) at low concentrations (Erikson et al., 2004), the metabolism of D-amino acids strongly varies between different Arabidopsis ecotypes (Gordes et al., 2013). Suarez et al. used natural accessions and transgenic mutant lines to identify and investigate AtDAT1, a major D-amino acid transaminase in Arabidopsis. Decreased activity of this enzyme leads to enhanced susceptibility to D-methionine and increased D-amino acid abundance stimulated accumulation of ethylene. In this study it was demonstrated, that the regulation of D-methionine and ACC derivatives in plants are interlinked. However, the detailed mechanisms by which D-amino acids induce ethylene production remain to be investigated.

β-Amino acids, which have the amino group attached to the β-carbon rather than the adjacent α-carbon, have been reported in many plant species (Kudo et al., 2014). Whereas, some β-amino acids, for instance β-tyrosine, have likely defensive functions in plants (Yan et al., 2015), others are essential components of primary metabolism. Parthasarathy et al. review the biosynthesis and function of β-alanine, which is not only a component of vitamin B5 and thereby is essential for Coenzyme A function, but also contributes to plant responses to both biotic and abiotic stresses. Although the β-alanine biosynthetic pathways are not yet completely elucidated in plants, spermine, spermidine, propionate, and uracil are known metabolic precursors.

The biosynthetic pathways of proteinogenic amino acids, and by extension the biosynthesis of NPAAs that serve as intermediates in these pathways, have been elucidated in Arabidopsis and other plant species (Jander and Joshi, 2010). However, the biosynthetic pathways and/or metabolic functions have been unraveled for only a few of the hundreds of other plant NPAAs, including D-amino acids, β-amino acids, other isomers, and structural mimics. Thus, there are many opportunities for novel discoveries in this research area. In particular, with the development of new research methods for studying non-model plant species at the molecular level, it will be possible to study the biosynthesis pathways, as well as structural, defensive, and signaling functions, of NPAAs that are not present in Arabidopsis.

Author Contributions

GJ wrote the first draft. All authors contributed revisions and approved the published version of the manuscript.

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Footnotes

Funding. This work was supported by and award from the Triad Foundation to GJ and US National Science Foundation award MCB-1817286 to GY.

References

  1. Akcay N., Bor M., Karabudak T., Ozdemir F., Turkan I. (2012). Contribution of Gamma amino butyric acid (GABA) to salt stress responses of Nicotiana sylvestris CMSII mutant and wild type plants. J. Plant Physiol. 169, 452–458. 10.1016/j.jplph.2011.11.006 [DOI] [PubMed] [Google Scholar]
  2. Amir R., Galili G., Cohen H. (2018). The metabolic roles of free amino acids during seed development. Plant Sci. 275, 11–18. 10.1016/j.plantsci.2018.06.011 [DOI] [PubMed] [Google Scholar]
  3. Barrett G. C. (1985). Chemistry and Biochemistry of the Amino Acids. London; NY: Chapman and Hall. [Google Scholar]
  4. Bell E. A. (1976). Uncommon amino acids in plants. FEBS Lett. 64, 29–35. 10.1016/0014-5793(76)80241-4 [DOI] [PubMed] [Google Scholar]
  5. Bell E. A. (2003). Nonprotein amino acids of plants: significance in medicine, nutrition, and agriculture. J. Agric Food Chem. 51, 2854–2865. 10.1021/jf020880w [DOI] [PubMed] [Google Scholar]
  6. Bence A. K., Crooks P. A. (2003). The mechanism of L-canavanine cytotoxicity: arginyl tRNA synthetase as a novel target for anticancer drug discovery. J. Enzyme Inhib. Med. Chem. 18, 383–394. 10.1080/1475636031000152277 [DOI] [PubMed] [Google Scholar]
  7. Bor M., Seckin B., Ozgur R., Yilmaz O., Ozdemir F., Turkan I. (2009). Comparative effects of drought, salt, heavy metal and heat stresses on gamma-aminobutryric acid levels of sesame (Sesamum indicum L.). Acta Phys. Plant. 31, 655–659. 10.1007/s11738-008-0255-2 [DOI] [Google Scholar]
  8. Carillo P. (2018). GABA shunt in durum wheat. Front. Plant Sci. 9:100. 10.3389/fpls.2018.00100 [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Deng X., Xu X., Liu Y., Zhang Y., Yang L., Zhang S., et al. (2020). Induction of gamma-aminobutyric acid plays a positive role to Arabidopsis resistance against Pseudomonas syringae. J. Integr. Plant Biol. 62, 1797–1812. 10.1111/jipb.12974 [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Erikson O., Hertzberg M., Nasholm T. (2004). A conditional marker gene allowing both positive and negative selection in plants. Nat. Biotechnol. 22, 455–458. 10.1038/nbt946 [DOI] [PubMed] [Google Scholar]
  11. Fait A., Fromm H., Walter D., Galili G., Fernie A. R. (2008). Highway or byway: the metabolic role of the GABA shunt in plants. Trends Plant Sci. 13, 14–19. 10.1016/j.tplants.2007.10.005 [DOI] [PubMed] [Google Scholar]
  12. Fowden L. (1981). Non-protein amino acids of plants. Food Chem. 6, 201–211. 10.1016/0308-8146(81)90009-1 [DOI] [Google Scholar]
  13. Genchi (2017). An overview on D-amino acids. Amino Acids. 49, 1521–1533. 10.1007/s00726-017-2459-5 [DOI] [PubMed] [Google Scholar]
  14. Gordes D., Koch G., Thurow K., Kolukisaoglu U. (2013). Analyses of Arabidopsis ecotypes reveal metabolic diversity to convert D-amino acids. Springerplus. 2:559. 10.1186/2193-1801-2-559 [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Huang T., Jander G., De Vos M. (2011). Non-protein amino acids in plant defense against insect herbivores: representative cases and opportunities for further functional analysis. Phytochemistry72, 1531–1537. 10.1016/j.phytochem.2011.03.019 [DOI] [PubMed] [Google Scholar]
  16. Huang W., Wang Y., Li X., Zhang Y. (2020). Biosynthesis and regulation of salicylic acid and N-hydroxypipecolic acid in plant immunity. Mol Plant. 13, 31–41. 10.1016/j.molp.2019.12.008 [DOI] [PubMed] [Google Scholar]
  17. Jander G., Joshi V. (2010). Recent progress in deciphering the biosynthesis of aspartate-derived amino acids in plants. Mol Plant. 3, 54–65. 10.1093/mp/ssp104 [DOI] [PubMed] [Google Scholar]
  18. Jin X., Liu T., Xu J., Gao Z., Hu X. (2019). Exogenous GABA enhances muskmelon tolerance to salinity-alkalinity stress by regulating redox balance and chlorophyll biosynthesis. BMC Plant Biol. 19:48. 10.1186/s12870-019-1660-y [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kim N. H., Kim B. S., Hwang B. K. (2013). Pepper arginine decarboxylase is required for polyamine and gamma-aminobutyric acid signaling in cell death and defense response. Plant Physiol. 162, 2067–2083. 10.1104/pp.113.217372 [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kinnersley A. M., Turano F. J. (2000). Gamma aminobutyric acid (GABA) and plant responses to stress. Crit. Rev. Plant Sci. 19, 479–509. [Google Scholar]
  21. Kudo F., Miyanaga A., Eguchi T. (2014). Biosynthesis of natural products containing beta-amino acids. Nat Prod Rep. 31, 1056–1073. 10.1039/c4np00007b [DOI] [PubMed] [Google Scholar]
  22. Lee H. Y., Chen Z., Zhang C., Yoon G. M. (2019). Editing of the OsACS locus alters phosphate deficiency-induced adaptive responses in rice seedlings. J. Exp. Bot. 70, 1927–1940. 10.1093/jxb/erz074 [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mekonnen D. W. (2017). Oversensitivity of Arabidopsis gad1/2 mutant to NaCl treatment reveals the importance of GABA in salt stress responses. African J. Plant Sci. 11, 252–263. 10.5897/AJPS2017.1551 [DOI] [Google Scholar]
  24. Palanivelu R., Brass L., Edlund A. F., Preuss D. (2003). Pollen tube growth and guidance is regulated by POP2, an Arabidopsis gene that controls GABA levels. Cell114, 47–59. 10.1016/s0092-8674(03)00479-3 [DOI] [PubMed] [Google Scholar]
  25. Podlesakova K., Ugena L., Spichal L., Dolezal K., De Diego N. (2019). Phytohormones and polyamines regulate plant stress responses by altering GABA pathway. N. Biotechnol. 48, 53–65. 10.1016/j.nbt.2018.07.003 [DOI] [PubMed] [Google Scholar]
  26. Rezaei-Chiyaneh E., Seyyedi S. M., Ebrahimian E., Moghaddam S. S., Damalas C. A. (2018). Exogenous application of gamma-aminobutyric acid (GABA) alleviates the effect of water deficit stress in black cumin (Nigella sativa L.). Ind. Crop. Prod. 112, 741–748. 10.1016/j.indcrop.2017.12.067 [DOI] [Google Scholar]
  27. Rosenthal G. A. (1982). Plant Nonprotein Amino and Imino Acids: Biological, Biochemical, and Toxicological Properties. New York, N.Y.: Academic Press. [Google Scholar]
  28. Seo D. H., Yoon G. M. (2019). Light-induced stabilization of ACS contributes to hypocotyl elongation during the dark-to-light transition in Arabidopsis seedlings. Plant J. 98, 898–911. 10.1111/tpj.14289 [DOI] [PubMed] [Google Scholar]
  29. Snowden C. J., Thomas B., Baxter C. J., Smith J. A., Sweetlove L. J. (2015). A tonoplast Glu/Asp/GABA exchanger that affects tomato fruit amino acid composition. Plant J. 81, 651–660. 10.1111/tpj.12766 [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Tarkowski L. P., Signorelli S., Höfte M. (2020). gamma-Aminobutyric acid and related amino acids in plant immune responses: Emerging mechanisms of action. Plant Cell Environ. 43, 1103–1116. 10.1111/pce.13734 [DOI] [PubMed] [Google Scholar]
  31. Tsang D. L., Edmond C., Harrington J. L., Nuhse T. S. (2011). Cell wall integrity controls root elongation via a general 1-aminocyclopropane-1-carboxylic acid-dependent, ethylene-independent pathway. Plant Physiol. 156, 596–604. 10.1104/pp.111.175372 [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Tsuchisaka A., Yu G., Jin H., Alonso J. M., Ecker J. R., Zhang X., et al. (2009). A combinatorial interplay among the 1-aminocyclopropane-1-carboxylate isoforms regulates ethylene biosynthesis in Arabidopsis thaliana. Genetics183, 979–1003. 10.1534/genetics.109.107102 [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Vijayakumari K., Puthur J. T. (2015). Gamma-aminobutyric acid (GABA) priming enhances the osmotic stress tolerance in Piper nigrum Linn. plants subjected to PEG-induced stress. Plant Growth Reg. 78, 57–67. 10.1007/s10725-015-0074-6 [DOI] [Google Scholar]
  34. Wang G., Kong J., Cui D., Zhao H., Niu Y., Xu M., et al. (2019). Resistance against Ralstonia solanacearum in tomato depends on the methionine cycle and the gamma-aminobutyric acid metabolic pathway. Plant J. 97, 1032–1047. 10.1111/tpj.14175 [DOI] [PubMed] [Google Scholar]
  35. Xu S. L., Rahman A., Baskin T. I., Kieber J. J. (2008). Two leucine-rich repeat receptor kinases mediate signaling, linking cell wall biosynthesis and ACC synthase in Arabidopsis. Plant Cell. 20, 3065–3079. 10.1105/tpc.108.063354 [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Yan J., Aboshi T., Teraishi M., Strickler S. R., Spindel J. E., Tung C. W., et al. (2015). The rice tyrosine aminomutase TAM1 is required for beta-tyrosine biosynthesis. Plant Cell. 27, 1265–1278. 10.1105/tpc.15.00058 [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Yin J., Zhang X., Zhang G., Wen Y., Liang G., Chen X. (2019). Aminocyclopropane-1-carboxylic acid is a key regulator of guard mother cell terminal division in Arabidopsis thaliana. J. Exp. Bot. 70, 897–908. 10.1093/jxb/ery413 [DOI] [PMC free article] [PubMed] [Google Scholar]
Editorial: Physiological Aspects of Non-proteinogenic Amino Acids in Plants (2024)
Top Articles
Latest Posts
Recommended Articles
Article information

Author: Aracelis Kilback

Last Updated:

Views: 5924

Rating: 4.3 / 5 (44 voted)

Reviews: 83% of readers found this page helpful

Author information

Name: Aracelis Kilback

Birthday: 1994-11-22

Address: Apt. 895 30151 Green Plain, Lake Mariela, RI 98141

Phone: +5992291857476

Job: Legal Officer

Hobby: LARPing, role-playing games, Slacklining, Reading, Inline skating, Brazilian jiu-jitsu, Dance

Introduction: My name is Aracelis Kilback, I am a nice, gentle, agreeable, joyous, attractive, combative, gifted person who loves writing and wants to share my knowledge and understanding with you.