Skip to main content
Log in

Functional Divergence of the Glutamine Phosphoribosyl Pyrophosphate Amidotransferase (ASE) Gene Family in Arabidopsis

  • Experimental Papers
  • Published:
Journal of Evolutionary Biochemistry and Physiology Aims and scope Submit manuscript

Abstract

Background: Functional divergence occurs widely among duplicated genes in plants. The divergence of functional genes may result from changes in gene regulation or protein-coding regions, or both. These changes contributing to the functional divergence of plants require further elucidation. Glutamine phosphoribosyl pyrophosphate amidotransferase (ASE) is a key enzyme in de novo purine biosynthesis and plays important roles in plant growth and development.

Results: In our research, three ASE genes were identified in the Arabidopsis thaliana genome, and they were designated AtASE1, AtASE2 and AtASE3. Gene expression profiles revealed that the three genes exhibit very different expression, and gene regulation plays a pivotal role in the divergence of the ASE gene family. Subcellular localization analysis indicated that the three proteins were all localized in chloroplasts. Protein biochemical analysis revealed that the catalytic abilities of ASE proteins show differentiation, but further transgenic overexpression experiments proved that this was not the main reason for physiological functional divergence.

Conclusions: Our results indicate that the functional divergence of the ASE gene family members might result from changes in their promoters, but not protein-coding region.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

Abbreviations

ASE:

glutamine phosphoribosyl pyrophosphate amidotransferase

GST:

glutathione S-transferase

PRA:

5-phosphoribosyl-(β) 1-amine

PRPP:

phosporibosyl pyrophosphate

PRX:

class III peroxidase

References

  1. Nei M, Rooney AP (2005) Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39:121-152. https://doi.org/10.1146/annurev.genet.39.073003.112240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Conant GC, Wolfe KH (2008) Turning a hobby into a job: how duplicated genes find new functions. Nat Rev Genet 9:938-950. https://doi.org/10.1038/nrg2482

    Article  CAS  PubMed  Google Scholar 

  3. Panchy N, Lehti-Shiu M, Shiu SH (2016) Evolution of Gene Duplication in Plants. Plant Physiol 171:2294-2316. https://doi.org/10.1104/pp.16.00523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Zhang J (2003) Evolution by gene duplication: an update. Trends in Ecology & Evolution 18:292-298. https://doi.org/10.1016/S0169-5347(03)00033-8

    Article  Google Scholar 

  5. Rutter MT, Cross KV, Van Woert PA (2012) Birth, death and subfunctionalization in the Arabidopsis genome. Trends Plant Sci 17:204-212. https://doi.org/10.1016/j.tplants.2012.01.006

    Article  CAS  PubMed  Google Scholar 

  6. Birchler JA, Veitia RA (2014) The Gene Balance Hypothesis: dosage effects in plants. Methods Mol Biol 1112:25-32. https://doi.org/10.1007/978-1-62703-773-0_2

    Article  PubMed  Google Scholar 

  7. Birchler JA, Veitia RA (2012) Gene balance hypothesis: connecting issues of dosage sensitivity across biological disciplines. Proc Natl Acad Sci U S A 109:14746-14753. https://doi.org/10.1073/pnas.1207726109

    Article  PubMed  PubMed Central  Google Scholar 

  8. Lan T, Yang ZL, Yang X, Liu YJ, Wang XR, Zeng QY (2009) Extensive functional diversification of the Populus glutathione S-transferase supergene family. Plant Cell 21:3749-3766. https://doi.org/10.1105/tpc.109.070219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Liu HJ, Tang ZX, Han XM, Yang ZL, Zhang FM, Yang HL, Liu YJ, Zeng QY (2015) Divergence in Enzymatic Activities in the Soybean GST Supergene Family Provides New Insight into the Evolutionary Dynamics of Whole-Genome Duplicates. Mol Biol Evol 32:2844-2859. https://doi.org/10.1093/molbev/msv156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Ganko EW, Meyers BC, Vision TJ (2007) Divergence in expression between duplicated genes in Arabidopsis. Mol Biol Evol 24:2298-2309. https://doi.org/10.1093/molbev/msm158

    Article  CAS  PubMed  Google Scholar 

  11. Renny-Byfield S, Gallagher JP, Grover CE, Szadkowski E, Page JT, Udall JA, Wang X, Paterson AH, Wendel JF (2014) Ancient gene duplicates in Gossypium (cotton) exhibit near-complete expression divergence. Genome Biol Evol 6:559-571. https://doi.org/10.1093/gbe/evu037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Ren LL, Liu YJ, Liu HJ, Qian TT, Qi LW, Wang XR, Zeng QY (2014) Subcellular Relocalization and Positive Selection Play Key Roles in the Retention of Duplicate Genes of Populus Class III Peroxidase Family. Plant Cell 26:2404-2419. https://doi.org/10.1105/tpc.114.124750

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Smith JL, Zaluzec EJ, Wery JP, Niu L, Switzer RL, Zalkin H, Satow Y (1994) Structure of the allosteric regulatory enzyme of purine biosynthesis. Science 264:1427-1433. https://doi.org/10.1126/science.8197456

    Article  CAS  PubMed  Google Scholar 

  14. Smith PM, Atkins CA (2002) Purine biosynthesis. Big in cell division, even bigger in nitrogen assimilation. Plant Physiol 128:793-802. https://doi.org/10.1104/pp.010912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Coleto I, Trenas AT, Erban A, Kopka J, Pineda M, Alamillo JM (2016) Functional specialization of one copy of glutamine phosphoribosyl pyrophosphate amidotransferase in ureide production from symbiotically fixed nitrogen in Phaseolus vulgaris. Plant Cell Environ 39:1767-1779. https://doi.org/10.1111/pce.12743

    Article  CAS  PubMed  Google Scholar 

  16. Tso JY, Zalkin H, van Cleemput M, Yanofsky C, Smith JM (1982) Nucleotide sequence of Escherichia coli purF and deduced amino acid sequence of glutamine phosphoribosylpyrophosphate amidotransferase. J Biol Chem 257:3525-3531. https://doi.org/10.1016/S0021-9258(18)34810-5

    Article  CAS  PubMed  Google Scholar 

  17. Mäntsälä P, Zalkin H (1984) Glutamine nucleotide sequence of Saccharomyces cerevisiae ADE4 encoding phosphoribosylpyrophosphate amidotransferase. J Biol Chem 259:8478-8484. https://doi.org/10.1016/S0021-9258(17)39755-7

    Article  PubMed  Google Scholar 

  18. Muchmore CR, Krahn JM, Kim JH, Zalkin H, Smith JL (1998) Crystal structure of glutamine phosphoribosylpyrophosphate amidotransferase from Escherichia coli. Protein Sci 7:39-51. https://doi.org/10.1002/pro.5560070104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Qin L, Gong X, Xie J, Jiang D, Cheng J, Li G, Huang J, Fu Y (2011) Phosphoribosylamidotransferase, the first enzyme for purine de novo synthesis, is required for conidiation in the sclerotial mycoparasite Coniothyrium minitans. Fungal Genet Biol 48:956-965. https://doi.org/10.1016/j.fgb.2011.06.007

    Article  CAS  PubMed  Google Scholar 

  20. Cao X, Du B, Han F, Zhou Y, Ren J, Wang W, Chen Z, Zhang Y (2020) Crystal Structure of the Chloroplastic Glutamine Phosphoribosylpyrophosphate Amidotransferase GPRAT2 From Arabidopsis thaliana. Front Plant Sci 11:157. https://doi.org/10.3389/fpls.2020.00157

    Article  PubMed  PubMed Central  Google Scholar 

  21. Makaroff CA, Zalkin H, Switzer RL, Vollmer SJ (1983) Cloning of the Bacillus subtilis glutamine phosphoribosylpyrophosphate amidotransferase gene in Escherichia coli. Nucleotide sequence determination and properties of the plasmid-encoded enzyme. J Biol Chem 258:10586-10593. https://doi.org/10.1016/S0021-9258(17)44497-8

    Article  CAS  PubMed  Google Scholar 

  22. Zhou GC, Dixon JE, Zalkin H (1990) Cloning and expression of avian glutamine phosphoribosylpyrophosphate amidotransferase. Conservation of a bacterial propeptide sequence supports a role for posttranslational processing. J Biol Chem 265:21152-21159. https://doi.org/10.1016/S0021-9258(17)45339-7

    Article  CAS  PubMed  Google Scholar 

  23. Iwahana H, Oka J, Mizusawa N, Kudo E, Ii S, Yoshimoto K, Holmes EW, Itakura M (1993) Molecular cloning of human amidophosphoribosyltransferase. Biochem Biophys Res Commun 190:192-200. https://doi.org/10.1006/bbrc.1993.1030

    Article  CAS  PubMed  Google Scholar 

  24. Brayton KA, Chen Z, Zhou G, Nagy PL, Gavalas A, Trent JM, Deaven LL, Dixon JE, Zalkin H (1994) Two genes for de novo purine nucleotide synthesis on human chromosome 4 are closely linked and divergently transcribed. J Biol Chem 269:5313-5321. https://doi.org/10.1016/S0021-9258(17)37689-5

    Article  CAS  PubMed  Google Scholar 

  25. Walsh TA, Bauer T, Neal R, Merlo AO, Schmitzer PR, Hicks GR, Honma M, Matsumura W, Wolff K, Davies JP (2007) Chemical genetic identification of glutamine phosphoribosylpyrophosphate amidotransferase as the target for a novel bleaching herbicide in Arabidopsis. Plant Physiol 144:1292-1304. https://doi.org/10.1104/pp.107.099705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Ito T, Shiraishi H, Okada K, Shimura Y (1994) Two amidophosphoribosyltransferase genes of Arabidopsis thaliana expressed in different organs. Plant Mol Biol 26:529-533. https://doi.org/10.1007/bf00039565

    Article  CAS  PubMed  Google Scholar 

  27. Hung WF, Chen LJ, Boldt R, Sun CW, Li HM (2004) Characterization of Arabidopsis glutamine phosphoribosyl pyrophosphate amidotransferase-deficient mutants. Plant Physiol 135:1314-1323. https://doi.org/10.1104/pp.104.040956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools: An Integrative Toolkit Developed for Interactive Analyses of Big Biological Data. Mol Plant 13:1194-1202. https://doi.org/10.1016/j.molp.2020.06.009

    Article  CAS  PubMed  Google Scholar 

  29. Liu YJ, Han XM, Ren LL, Yang HL, Zeng QY (2013) Functional divergence of the glutathione S-transferase supergene family in Physcomitrella patens reveals complex patterns of large gene family evolution in land plants. Plant Physiol 161:773-786. https://doi.org/10.1104/pp.112.205815

    Article  CAS  PubMed  Google Scholar 

  30. Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2:1565-1572. https://doi.org/10.1038/nprot.2007.199

    Article  CAS  PubMed  Google Scholar 

  31. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735-743. https://doi.org/10.1046/j.1365-313x.1998.00343.x

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This study was supported by grants from the National Natural Science Foundation of China, (Grant No. 31400574), and High-Level Talent Research Program of Inner Mongolia University (21400-5175163). The funding bodies were not involved in the design of the study, collection, analysis, and interpretation of data or writing of the manuscript.

Author information

Authors and Affiliations

Authors

Contributions

QTT and YZL designed the research. QTT performed the experiments. LHJ, WX, WYM and QTT analyzed the data and prepared the figures. LHJ and QTT wrote the paper. YZL and RLL commented on the paper. QTT led the whole project. All the authors read and approved the final manuscript.

Corresponding authors

Correspondence to Hai-Jing Liu or Ting-Ting Qian.

Ethics declarations

Conflict of Interest

The authors declare that they have no competing interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, HJ., Yang, ZL., Ren, LL. et al. Functional Divergence of the Glutamine Phosphoribosyl Pyrophosphate Amidotransferase (ASE) Gene Family in Arabidopsis. J Evol Biochem Phys 57, 1310–1321 (2021). https://doi.org/10.1134/S0022093021060119

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0022093021060119

Keywords:

Navigation