Skip to main content
SpringerLink
Log in

A putative AGAMOUS ortholog is a candidate for the gene determining ease of dehulling in Tartary buckwheat (Fagopyrum tataricum)

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Tartary buckwheat rice-type cultivars, which allow easy dehulling, lacked periclinal cell divisions that proceed underneath the epidermis in the proximity of ovary midribs in non-rice-type cultivars. The easy dehulling in these cultivars was associated with a G→A substitution in an AGAMOUS ortholog.

Abstract

Ease of dehulling in Tartary buckwheat (Fagopyrum tataricum) can affect the quality of its products. Tartary buckwheat cultivars that allow easy dehulling are called rice-type cultivars. The rice and non-rice hull types are determined by a single gene, but this gene is unclear. Here, we show that cells underneath the epidermis in the proximity of ovary midribs undergo periclinal cell divisions in non-rice-type cultivars but do not in a rice-type cultivar. The cells that arose from the periclinal cell divisions later underwent lignification, which should increase mechanical strength of hulls. In RNA sequencing, a partial mRNA of an AGAMOUS ortholog in Tartary buckwheat (FtAG) was found to be absent in the rice-type cultivar. Cloning of this gene revealed that this is a 42-bp deletion due to a G→A substitution at a splice acceptor site in the FtAG genomic region. In F2 progeny derived from a cross between non-rice-type and rice-type cultivars, all the rice-type plants exhibited the homozygous A/A allele at this site, whereas all the Tartary-type plants exhibited either the homozygous G/G allele or the heterozygous A/G allele. These results suggest that FtAG is a candidate for the gene that determines ease of dehulling in Tartary buckwheat. The DNA marker that we developed to distinguish the FtAG alleles can be useful in breeding Tartary buckwheat cultivars.

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
Fig. 5

Similar content being viewed by others

Abbreviations

AG:

AGAMOUS

CDS:

Coding sequence

NT:

Non-rice type

RT:

Rice type

SHP:

SHATTERPROOF

References

  • Anders S, Pyl PT, Huber W (2015) HTSeq—a python framework to work with high-throughput sequencing data. Bioinformatics 31:166–169

    Article  CAS  Google Scholar 

  • Awatsuhara R, Harada K, Maeda T, Nomura T, Nagao K (2010) Antioxidative activity of the buckwheat polyphenol rutin in combination with ovalbumin. Mol Med Rep 3:121–125

    CAS  PubMed  Google Scholar 

  • Brockington SF, Rudall PJ, Frohlich MW, Oppenheimer DG, Soltis PS, Soltis DE (2012) 'Living stones' reveal alternative petal identity programs within the core eudicots. Plant J 69:193–203

    Article  CAS  Google Scholar 

  • Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST+: architecture and applications. BMC Bioinform 10:421

    Article  Google Scholar 

  • Demeke T, Ratnayaka I, Holigroski M, Phan A (2012) Assessment of DNA extraction methods for PCR testing of discontinued or unapproved biotech events in single seeds of canola, flax and soybean. Food Control 24:44–49

    Article  CAS  Google Scholar 

  • Fabjan N, Rode J, Kosir IJ, Wang Z, Zhang Z, Kreft I (2003) Tartary buckwheat (Fagopyrum tataricum Gaertn.) as a source of dietary rutin and quercitrin. J Agric Food Chem 51:6452–6455

    Article  CAS  Google Scholar 

  • Fang ZW, Qi R, Li XF, Liu ZX (2014) Ectopic expression of FaesAP3, a Fagopyrum esculentum (Polygonaceae) AP3 orthologous gene rescues stamen development in an Arabidopsis ap3 mutant. Gene 550:200–206

    Article  CAS  Google Scholar 

  • Franks RG, Wang C, Levin JZ, Liu Z (2002) SEUSS, a member of a novel family of plant regulatory proteins, represses floral homeotic gene expression with LEUNIG. Development 129:253–263

    CAS  PubMed  Google Scholar 

  • Gimenez E, Castañeda L, Pineda B, Pan IL, Moreno V, Angosto T, Lozano R (2016) TOMATO AGAMOUS1 and ARLEQUIN/TOMATO AGAMOUS-LIKE1 MADS-box genes have redundant and divergent functions required for tomato reproductive development. Plant Mol Biol 91:513–531

    Article  CAS  Google Scholar 

  • Griffith JQ Jr, Couch JF, Lindauer MA (1944) Effect of rutin on increased capillary fragility in man. Proc Soc Exp Biol Med 55:228–229

    Article  CAS  Google Scholar 

  • Ide M, Masuda K, Tsugama D, Fujino K (2019) Death of female flower microsporocytes progresses independently of meiosis-like process and can be accelerated by specific transcripts in Asparagus officinalis. Sci Rep 9:2703

    Article  Google Scholar 

  • Ikeda K, Ikeda S, Kreft I, Rufa L (2012) Utilization of Tartary buckwheat. Fagopyrum 29:27–30

    Google Scholar 

  • Jiang P, Burczynski F, Campbell C, Pierce G, Austria JA, Briggs CJ (2007) Rutin and flavonoid contents in three buckwheat species Fagopyrum esculentum, F. tataricum, and F. homotropicum and their protective effects against lipid peroxidation. Food Res Int 40:356–364

    Article  CAS  Google Scholar 

  • Khan MMAA, Jain DC, Bhakuni RS, Zaim M, Thakur RS (1991) Occurrence of some antiviral sterols in Artemisia annua. Plant Sci 75:161–165

    Article  CAS  Google Scholar 

  • Kreft I, Fabjan N, Yasumoto K (2006) Rutin content in buckwheat (Fagopyrum esculentum Moench) food materials and products. Food Chem 98:508–512

    Article  CAS  Google Scholar 

  • Krizek BA, Prost V, Macias A (2000) AINTEGUMENTA promotes petal identity and acts as a negative regulator of AGAMOUS. Plant Cell 12:1357–1366

    Article  CAS  Google Scholar 

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359

    Article  CAS  Google Scholar 

  • Lee G, Lee KI, Lee Y, Kim B, Lee D, Seo J, Jang S, Chin JH, Koh HJ (2018) Identification of a novel SPLIT-HULL (SPH) gene associated with hull splitting in rice (Oryza sativa L.). Theor Appl Genet 131:1469–1480

    Article  CAS  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079

    Article  Google Scholar 

  • Li LY, Fang ZW, Li XF, Liu ZX (2017) Isolation and characterization of the C-class MADS-box gene from the distylous pseudo-cereal Fagopyrum esculentum. J Plant Biol 60:189–198

    Article  CAS  Google Scholar 

  • Liljegren SJ, Ditta GS, Eshed Y, Savidge B, Bowman JL, Yanofsky MF (2000) SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404 (6779):766–770

    Article  CAS  Google Scholar 

  • Liu Z, Meyerowitz EM (1995) LEUNIG regulates AGAMOUS expression in Arabidopsis flowers. Development 121:975–991

    CAS  PubMed  Google Scholar 

  • Nishimura M, Ohkawara T, Sato Y, Satoh H, Suzuki T, Ishiguro K, Noda T, Morishita T, Nishihira J (2016) Effectiveness of rutin-rich Tartary buckwheat (Fagopyrum tataricum Gaertn.) ‘Manten-Kirari’ in body weight reduction related to its antioxidant properties: A randomised, double-blind, placebo-controlled study. J Func Food 26:460–469

    Article  CAS  Google Scholar 

  • Pomar F, Merino F, Ros Barceló A (2002) O-4-Linked coniferyl and sinapyl aldehydes in lignifying cell walls are the main targets of the Wiesner (phloroglucinol-HCl) reaction. Protoplasma 220:0017–0028

    Article  CAS  Google Scholar 

  • Riechmann JL, Krizek BA, Meyerowitz EM (1996a) Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. Proc Natl Acad Sci USA 93:4793–4798

    Article  CAS  Google Scholar 

  • Riechmann JL, Wang M, Meyerowitz EM (1996b) DNA-binding properties of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA and AGAMOUS. Nucleic Acids Res 24:3134–3141

    Article  CAS  Google Scholar 

  • Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP (2011) Integrative genomics viewer. Nat Biotechnol 29:24–26

    Article  CAS  Google Scholar 

  • Shanno RL (1946) Rutin: A new drug for the treatment of increased capillary fragility. Am J Med Sci 211:539–543

    Article  CAS  Google Scholar 

  • Sokal RR, Michener CD (1958) A statistical method for evaluating systematic relationships. Univ Kansas Sci Bull 38:1409–1438

    Google Scholar 

  • Taketa S, Amano S, Tsujino Y, Sato T, Saisho D, Kakeda K, Nomura M, Suzuki T, Matsumoto T, Sato K, Kanamori H, Kawasaki S, Takeda K (2008) Barley grain with adhering hulls is controlled by an ERF family transcription factor gene regulating a lipid biosynthesis pathway. Proc Natl Acad Sci USA 105:4062–4067

    Article  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  Google Scholar 

  • Wang Y, Clayton GC (2007) Tartary buckwheat breeding (Fagopyrum tataricum L. Gaertn.) through hybridization with its Rice-Tartary type. Euphytica 156:399–405

    Article  Google Scholar 

  • Wieslander G, Fabjan N, Vogrinčič M, Kreft I, Vombergar B, Norbäck D (2012) Effects of common and Tartary buckwheat consumption on mucosal symptoms, headache and tiredness: a double-blind crossover intervention study. J Food Agric Environ 10:107–110

    CAS  Google Scholar 

  • Xie Y, Wu G, Tang J, Luo R, Patterson J, Liu S, Huang W, He G, Gu S, Li S, Zhou X, Lam TW, Li Y, Xu X, Wong GK, Wang J (2014) SOAPdenovo-Trans: de novo transcriptome assembly with short RNA-Seq reads. Bioinformatics 30:1660–1666

    Article  CAS  Google Scholar 

  • Yang Y, Fanning L, Jack T (2003) The K domain mediates heterodimerization of the Arabidopsis floral organ identity proteins, APETALA3 and PISTILLATA. Plant J 33:47–59

    Article  Google Scholar 

  • Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM (1990) The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346:35–39

    Article  CAS  Google Scholar 

  • Yasui Y, Hirakawa H, Ueno M, Matsui K, Katsube-Tanaka T, Yang SJ, Aii J, Sato S, Mori M (2016) Assembly of the draft genome of buckwheat and its applications in identifying agronomically useful genes. DNA Res 23:215–224

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the JSPS (Japan Society for the Promotion of Science) KAKENHI Grant (Grant number: JP17H03754) for K.F.

Author information

Authors and Affiliations

  1. Laboratory of Crop Physiology, Research Faculty of Agriculture, Hokkaido University, Kita 9 Nishi 9 Kita-ku, Sapporo-shi, Hokkaido, 060-8589, Japan

    Yuka Fukuie, Hana Shimoyama, Daisuke Tsugama & Kaien Fujino

  2. National Agriculture and Food Research Organization (NARO) Hokkaido Agricultural Research Center, Memuro Upland Farming Research Station, Shinsei, Memuro, Kasai, Hokkaido, 082-0081, Japan

    Toshikazu Morishita

  3. Radiation Breeding Division, Institute of Crop Science, NARO, 2425 Kamimurata, Hitachiomiya, Ibaraki, 319-2293, Japan

    Toshikazu Morishita

  4. Asian Natural Environmental Science Center, The University of Tokyo, 1-1-1 Midori-cho, Nishi-tokyo-shi, Tokyo, 188-0002, Japan

    Daisuke Tsugama

  5. Division of African Area Studies, Graduate School of Asian and African Area Studies, Kyoto University, 46 Yoshida-shimo-adachi-cho, Sakyo-ku, Kyoto-shi, Kyoto, 606-8304, Japan

    Hana Shimoyama

Authors
  1. Yuka Fukuie
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hana Shimoyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Toshikazu Morishita
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Daisuke Tsugama
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kaien Fujino
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kaien Fujino.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 140 kb)

Supplementary file2 (PDF 630 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fukuie, Y., Shimoyama, H., Morishita, T. et al. A putative AGAMOUS ortholog is a candidate for the gene determining ease of dehulling in Tartary buckwheat (Fagopyrum tataricum). Planta 251, 85 (2020). https://doi.org/10.1007/s00425-020-03374-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00425-020-03374-6

Keywords

Search

Navigation