Skip to main content
SpringerLink
Log in

Evolution and diversity of PAPhy_a phytase in the genepool of wheat (Triticum aestivum L., Poaceae)

  • Research Article
  • Published:
Genetic Resources and Crop Evolution Aims and scope Submit manuscript

Abstract

Higher phytase activity in food and feedstuffs is desirable in order to counter the antinutritional effects of phytate. The most promising platform where this might be achieved through plant breeding is wheat and its Triticeae relatives. They already accumulate notable amounts of phytase in the grains and higher expression of the responsible PAPhy_a gene can increase the activity further. Here we provide a survey of the genetic diversity of PAPhy_a in wild and extant relatives of wheat. Fifty sequences of the structural gene were obtained from 34 samples representing 21 species or subspecies. A phylogenetic tree is presented, demonstrating that the three gene copies in hexaploid wheat have been inherited from its diploid ancestors. This finding is not only relevant for applied research, it also provides further evidence regarding the origin of the genomes in polyploid wheat. T. urartu Tumanian ex Gandilyan and Ae. tauschii Coss. are confirmed as donors of the A and D genomes, respectively, and the hypothesis of a common origin (Ae. speltoides Tausch) of the B and G genomes is supported. The survey suggests that the allele variation available for breeding is increased by the inclusion of the closest relatives of wheat. This effort should benefit greatly from molecular methods because specimens of the same species may have either novel- or alleles-identical to those of wheat.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Baum BR, Bailey LG (2004) The origin of the A genome donor of wheats (Triticum: Poaceae)—a perspective based on the sequence variation of the 5S DNA gene units. Genet Resour Crop Evol 51:183–196

    Article  CAS  Google Scholar 

  • Brinch-Pedersen H, Sorensen LD, Holm PB (2002) Engineering crop plants: getting a handle on phosphate. Trends Plant Sci 7:118–125

    Article  CAS  PubMed  Google Scholar 

  • Brinch-Pedersen H, Madsen CK, Holme IB, Dionisio G (2013) Increased understanding of the cereal phytase complement for better mineral bio-availability and resource management. J Cereal Sci 59:373–381

    Article  Google Scholar 

  • CLCbio (2007) White paper on alignment speed and quality. http://www.clcbio.com/files/whitepapers/wp_alignmentspeed_A4.pdf. Accessed 7 March 2016

  • Dionisio G et al (2011) Cloning and characterization of purple acid phosphatase phytases from wheat (Triticum aestivum L.), barley (Hordeum vulgare L.), maize (Zea maize L.) and rice (Oryza sativa L.). Plant Physiol 156:1087–1100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dreisigacker S, Kishii M, Lage J, Warburton M (2008) Use of synthetic hexaploid wheat to increase diversity for CIMMYT bread wheat improvement. Aust J Agric Res 59:413–420

    Article  Google Scholar 

  • Dvorak J, Terlizzi P, Zhang HB, Resta P (1993) The evolution of polyploid wheats: identification of the A genome donor species. Genome 36:21–31

    Article  CAS  PubMed  Google Scholar 

  • Eeckhout W, De Paepe M (1994) Total phosphorus, phytate-phosphorus and phytase activity in plant feedstuffs. Anim Feed Sci Technol 47:19–29

    Article  CAS  Google Scholar 

  • El Baidouri M et al (2017) Reconciling the evolutionary origin of bread wheat (Triticum aestivum). New Phytol 213:1477–1486

    Article  PubMed  Google Scholar 

  • Feng D-F, Doolittle RF (1987) Progressive sequence alignment as a prerequisite to correct phylogenetic trees. J Mol Evol 25(4):351–360

    Article  CAS  PubMed  Google Scholar 

  • Fernández-Calvín B, Orellana J (1994) Metaphase I-bound arms frequency and genome analysis in wheat-Aegilops hybrids. 3. Similar relationships between the B genome of wheat and S or S l genomes of Ae. speltoides, Ae. longissima and Ae. sharonensis. Theor Appl Genet 88:1043–1049

    Article  PubMed  Google Scholar 

  • Friebe B, Tuleen NA, Gill BS (1995) Standard karyotype of Triticum searsii and its relationship with other S-genome species and common wheat. Theor Appl Genet 91:248–254

    Article  CAS  PubMed  Google Scholar 

  • Golovnina K, Glushkov S, Blinov A, Mayorov V, Adkison L, Goncharov N (2007) Molecular phylogeny of the genus Triticum L. Plant Syst Evol 264:195–216

    Article  CAS  Google Scholar 

  • Graybosch RA (2001) Mini review: uneasy unions: quality effects of rye chromatin transfers to wheat. J Cereal Sci 33:3–16

    Article  CAS  Google Scholar 

  • Haider N (2013) The origin of the B-genome of bread wheat (Triticum aestivum L.). Russ J Genet 49:263–274

    Article  CAS  Google Scholar 

  • Holme IB, Dionisio G, Brinch-Pedersen H, Wendt T, Madsen CK, Vincze E, Holm PB (2012) Cisgenic barley with improved phytase activity. Plant Biotechnol J 10:237–247

    Article  CAS  PubMed  Google Scholar 

  • Huang S, Sirikhachornkit A, Su X, Faris J, Gill B, Haselkorn R, Gornicki P (2002) Genes encoding plastid acetyl-CoA carboxylase and 3-phosphoglycerate kinase of the Triticum/Aegilops complex and the evolutionary history of polyploid wheat. Proc Natl Acad Sci USA 99:8133–8138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kearse M et al (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    Article  PubMed  PubMed Central  Google Scholar 

  • Kihara H (1944) Discovery of the DD-analyser, one of the ancestors of Triticum vulgare. Agric Hortic 19:13–14

    Google Scholar 

  • Kilian B et al (2007) Independent wheat B and G genome origins in outcrossing Aegilops progenitor haplotypes. Mol Biol Evol 24:217–227

    Article  CAS  PubMed  Google Scholar 

  • Li L-F, Liu B, Olsen KM, Wendel JF (2015a) Multiple rounds of ancient and recent hybridizations have occurred within the Aegilops–Triticum complex. New Phytol 208:11–12

    Article  PubMed  Google Scholar 

  • Li L-F, Liu B, Olsen KM, Wendel JF (2015b) A re-evaluation of the homoploid hybrid origin of Aegilops tauschii, the donor of the wheat D-subgenome. New Phytol 208:4–8

    Article  PubMed  Google Scholar 

  • Madsen CK, Dionisio G, Holme IB, Holm PB, Brinch-Pedersen H (2013) High mature grain phytase activity in the Triticeae has evolved by duplication followed by neofunctionalization of the purple acid phosphatase phytase (PAPhy) gene. J Exp Bot 64:3111–3123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marcussen T et al (2014) Ancient hybridizations among the ancestral genomes of bread wheat. Science 345(6194):1250092. doi:10.1126/science.1250092

  • McFadden ES, Sears ER (1944) The artificial synthesis of Triticum spelta. Rec Genet Soc Am 13:26–27

    Google Scholar 

  • McFadden ES, Sears ER (1946) The origin of Triticum spelta and its free-threshing hexaploid relatives. J Hered 37:81–107

    Article  PubMed  Google Scholar 

  • Møller MG, Taylor C, Rasmussen SK, Holm PB (2003) Molecular cloning and characterisation of two genes encoding asparagine synthetase in barley (Hordeum vulgare L.). Biochim Biophys Acta 1628:123–132

    Article  PubMed  Google Scholar 

  • Oettler G (2005) The fortune of a botanical curiosity—triticale: past, present and future. J Agric Sci 143:329–346

    Article  Google Scholar 

  • Peng J, Sun D, Nevo E (2011) Domestication evolution, genetics and genomics in wheat. Mol Breed 28:281–301

    Article  CAS  Google Scholar 

  • Perugini LD, Murphy JP, Marshall D, Brown-Guedira G (2008) Pm37, a new broadly effective powdery mildew resistance gene from Triticum timopheevii. Theor Appl Genet 116:417–425

    Article  CAS  PubMed  Google Scholar 

  • Petersen G, Seberg O, Yde M, Berthelsen K (2006) Phylogenetic relationships of Triticum and Aegilops and evidence for the origin of the A, B, and D genomes of common wheat (Triticum aestivum). Mol Phylogenet Evol 39:70–82

    Article  CAS  PubMed  Google Scholar 

  • Rabinovich SV (1998) Importance of wheat-rye translocations for breeding modern cultivar of Triticum aestivum L. Euphytica 100:323–340

    Article  Google Scholar 

  • Salamini F, Ozkan H, Brandolini A, Schäfer-Pregl R, Martin W (2002) Genetics and geography of wild cereal domestication in the near east. Nat Rev Genet 3:429–441

    CAS  PubMed  Google Scholar 

  • Salse J et al (2008) New insights into the origin of the B genome of hexaploid wheat: evolutionary relationships at the SPA genomic region with the S genome of the diploid relative Aegilops speltoides. BMC Genom 9:1–12

    Article  Google Scholar 

  • Sarkar P, Stebbins GL (1956) Morphological evidence concerning the origin of the B genome in wheat. Am J Bot 43:297–304

    Article  Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    Article  CAS  PubMed  Google Scholar 

  • Steiner T, Mosenthin R, Zimmermann B, Greiner R, Roth S (2007) Distribution of phytase activity, total phosphorus and phytate phosphorus in legume seeds, cereals and cereal by-products as influenced by harvest year and cultivar. Anim Feed Sci Technol 133:320–334

    Article  CAS  Google Scholar 

  • van Slageren MW (1994) Wild wheats: a monograph of Aegilops L. and Amblyopyrum (Jaub. & Spach) Eig (Poaceae): a revision of all taxa closely related to wheat, excluding wild Triticum species, with notes on other genera in the tribe Triticeae, especially Triticum. Wageningen Agricultural University papers; 94-7. ISBN-9067543772

  • Viveros A, Centeno C, Brenes A, Canales R, Lozano A (2000) Phytase and acid phosphatase activities in plant feedstuffs. J Agric Food Chem 48:4009–4013

    Article  CAS  PubMed  Google Scholar 

  • Wagenaar EB (1966) Studies on the genome constitution of Triticum timopheevi Zhuk. II. The T. timopheevi complex and its origin. Evolution 20:150–164

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the Danish Ministry of Food, Agriculture and Fisheries (Grant No. 3304-FVFP-08-M-07-01).

Author information

Authors and Affiliations

  1. Department of Molecular Biology and Genetics, Section for Crop Genetics and Biotechnology, Aarhus University, Forsøgsvej, 1, 4200, Slagelse, Denmark

    Claus Krogh Madsen & Henrik Brinch-Pedersen

  2. Faculty of Science, Natural History Museum of Denmark, University of Copenhagen, Sølvgade 83, 1307, Copenhagen K, Denmark

    Gitte Petersen & Ole Seberg

Authors
  1. Claus Krogh Madsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gitte Petersen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ole Seberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Henrik Brinch-Pedersen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Claus Krogh Madsen.

Ethics declarations

Conflict of interest

The authors declare they have no conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Madsen, C.K., Petersen, G., Seberg, O. et al. Evolution and diversity of PAPhy_a phytase in the genepool of wheat (Triticum aestivum L., Poaceae). Genet Resour Crop Evol 64, 2115–2126 (2017). https://doi.org/10.1007/s10722-017-0501-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10722-017-0501-9

Keywords

Search

Navigation