Skip to main content
SpringerLink
Log in

Genome-wide identification, structural analysis and expression profiles of GRAS gene family in orchardgrass

  • Original Article
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

The GRAS gene family is a family of transcription factors that regulates plant growth and development. Despite being well-studied in many plant species, little is known about this gene family in orchardgrass (Dactylis glomerata L.), one of the top four economically important perennial forage grasses cultivated worldwide. We identified 46 GRAS genes in orchardgrass and analyzed their characteristics by phylogenetic, gene structural, motifs and expression patterns analysis. The phylogenetic analysis of eight species revealed that DgGRAS family had the evolutional conservation and closer homology relationship with the GRAS family of rice, barley and Brachypodium distachyon. Moreover, 46 DgGRAS proteins were divided into eight subfamilies based on the tree topology and rice or Arabidopsis classification, and LISCL subfamily was the largest one. Besides, we found that the motif 15 may be unique to the orchardgrass LISCL subfamily, and the motif 6 and motif 17 had indispensable functions in the orchardgrass LISCL subfamily. We further analyzed the expression profiles of DgGRAS genes at mature and seeding stage. And we found that DgGRAS17 played an important role in the growth and development no matter what stage it was at. DgGRAS5, DgGRAS28, DgGRAS31, DgGRAS42 and DgGRAS44 got involved in processes of the growth and development at seeding stage instead of mature stage. These results indicated that the major expression patterns and detailed functions of the DgGRAS genes varied with developmental stages. Taken together, this is the first systematic analysis of the GRAS gene family in the orchardgrass genome and the results provide insights into the potential functions of GRAS genes.

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
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Bolle C (2004) The role of GRAS proteins in plant signal transduction and development. Planta 218(5):683–692

    CAS  PubMed  Google Scholar 

  2. Yuyu G, Hongyu W, Xiang L, Qi L, Xinyan Z, Xueqing D, Yanrong A, Wei L, Hailong A (2017) Identification and expression of GRAS family genes in maize (Zea mays L.). Plos ONE 12(9):e0185418

    Google Scholar 

  3. Wei X, Zexi C, Naeem A, Bing H, Qinghua C, Aizhong L (2016) Genome-wide identification, evolutionary analysis, and stress responses of the GRAS gene family in castor beans. Int J Mol Sci 17(7):1004

    Google Scholar 

  4. Bolle C, Koncz C, Chua NH (2000) PAT1, a new member of the GRAS family, is involved in phytochrome A signal transduction. Genes Dev 14(10):1269–1278

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Xiaolin S, Bin X, Jones WT, Erik R, Keith A, Uversky D VN (2011) A functionally required unfoldome from the plant kingdom: intrinsically disordered N-terminal domains of GRAS proteins are involved in molecular recognition during plant development. Plant Mol Biol 77(3):205–223

    Google Scholar 

  6. Chaoguang T, Ping W, Shouhong S, Jiayang L, Mingsheng C (2004) Genome-wide analysis of the GRAS gene family in rice and Arabidopsis. Plant Mol Biol 54(4):519–532

    Google Scholar 

  7. Hua Z, Limin M, Long X, Changxiu Y, Chen L, Chunli C (2019) Genome-wide identification, characterization, interaction network and expression profile of GRAS gene family in sweet orange (Citrus sinensis). Sci Rep 9(1):2156

    Google Scholar 

  8. Lili S, Tao L, Huiping C, Ling L, Changhong G (2017) Genome-wide identification and expression analysis of the GRAS family proteins in Medicago truncatula. Acta Physiol Plant 39(4):93

    Google Scholar 

  9. Kengo M, Masayoshi M, Hisabumi T, Yasuo H, Kazuyuki H (2003) Isolation and characterization of a novel GRAS gene that regulates meiosis-associated gene expression. J Biol Chem 278(23):20865–20873

    Google Scholar 

  10. Jung Ok H, Kwang Suk C, Kim IA, Mi Hyun L, Shin Ae L, Sang Kee S, Myeong Min L, Jun L (2011) Funneling of gibberellin signaling by the GRAS transcription regulator scarecrow-like 3 in the Arabidopsis root. Proc Natl Acad Sci USA 108(5):2166–2171

    Google Scholar 

  11. Sabrina S, Renze H, Marjolein W, Ben S (2003) SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes Dev 17(3):354

    Google Scholar 

  12. Di LL, Wysockadiller J, Malamy JE, Pysh L, Helariutta Y, Freshour G, Hahn MG, Feldmann KA, Benfey PN (1996) The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86(3):423

    Google Scholar 

  13. Schumacher K, Schmitt T, Rossberg M, Schmitz G, Theres K (1999) The Lateral suppressor (Ls) gene of tomato encodes a new member of the VHIID protein family. Proc Natl Acad Sci USA 96(1):290–295

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Zhong Lin Z, Mikihiro O, Fleet CM, Rodolfo Z, Jianhong H, Jung Ok H, Jun L, Yuji K, Shinjiro Y, Tai Ping S (2011) Scarecrow-like 3 promotes gibberellin signaling by antagonizing master growth repressor DELLA in Arabidopsis. Proc Natl Acad Sci USA 108(5):2160–2165

    Google Scholar 

  15. Dill A, Sun T (2001) Synergistic derepression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana. Genetics 159(2):777–785

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Xiangdong F, Richards DE, Tahar AA, Hynes LW, Helen O, Jinrong P, Harberd NP (2002) Gibberellin-mediated proteasome-dependent degradation of the barley DELLA protein SLN1 repressor. Plant Cell 14(12):3191–3200

    Google Scholar 

  17. Xingliang H, Li Yen Candy L, Kuaifei X, Yuanyuan Y, Hao Y (2010) DELLAs modulate jasmonate signaling via competitive binding to JAZs. Developmental Cell 19(6):884–894

    Google Scholar 

  18. Silke S, Barbara Nicole SF, Eneida Abreu P, Olivier V, Klaus T (2010) LOST MERISTEMS genes regulate cell differentiation of central zone descendants in Arabidopsis shoot meristems. Plant J 64(4):668–678

    Google Scholar 

  19. Jeroen S, Fabienne JG, Cris K (2002) Shoot meristem maintenance is controlled by a GRAS-gene mediated signal from differentiating cells. Genes Dev 16(17):2213–2218

    Google Scholar 

  20. Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, Sena G, Hauser MT, Benfey PN (2000) The SHORT-ROOT gene controls radial patterning of the arabidopsis root through radial signaling. Cell 101(5):555–567

    CAS  PubMed  Google Scholar 

  21. Xueyong L, Qian Q, Zhiming F, Yonghong W, Guosheng X, Dali Z, Xiaoqun W, Xinfang L, Sheng T, Fujimoto H (2003) Control of tillering in rice. Nature 422(6932):618

    Google Scholar 

  22. Thomas G, Oliver C, Elisabeth S, Dorte M, Ruben H, Gregor S, Klaus T (2003) Molecular analysis of the LATERAL SUPPRESSOR gene in Arabidopsis reveals a conserved control mechanism for axillary meristem formation. Genes Dev 17(9):1175–1187

    Google Scholar 

  23. Xiao Ming S, Tong Kun L, Wei Ke D, Qing Hua M, Jun R, Zhen W, Ying L, Xi Lin H (2013) Genome-wide analysis of the GRAS gene family in Chinese cabbage (Brassica rapa ssp. pekinensis). BMC Genomics 14(1):573–573

    Google Scholar 

  24. Jiuxing L, Tao W, Zongda X, Lidan S, Qixiang Z (2015) Genome-wide analysis of the GRAS gene family in Prunus mume. Mol Genet Genomics 290(1):303–317

    Google Scholar 

  25. Wei H, Zhiqiang X, Xia K, Ning T, Zhengguo L (2015) Genome-wide identification, phylogeny and expression analysis of GRAS gene family in tomato. BMC Plant Biol 15:209

    Google Scholar 

  26. Mengyao L, Bo S, Fangjie X, Ronggao G, Ya L, Fen Z, Zesheng Y, Haoru T (2019) Identification of the GRAS gene family in the Brassica juncea genome provides insight into its role in stem swelling in stem mustard. PeerJ 7:e6682

    Google Scholar 

  27. Guangyan F, Linkai H, Ji L, Jianping W, Lei X, Ling P, Xinxin Z, Xia W, Ting H, Xinquan Z (2017) Comprehensive transcriptome analysis reveals distinct regulatory programs during vernalization and floral bud development of orchardgrass (Dactylis glomerata L.). BMC Plant Biol 17(1):216

    Google Scholar 

  28. Casler MD, Fales SLUndersander DJ, Mcelroy AR (2001) Genetic progress from 40 years of orchardgrass breeding in North America measured under management-intensive rotational grazing. Can J Plant Sci 81(4):713–721

    Google Scholar 

  29. Wilkins P, Humphreys M (2003) Progress in breeding perennial forage grasses for temperate agriculture. J Agric Sci 140(2):129–150

    CAS  Google Scholar 

  30. Hirata M, Yuyama N, Cai H (2011) Isolation and characterization of simple sequence repeat markers for the tetraploid forage grass Dactylis glomerata. Plant Breed 130(4):503–506

    CAS  Google Scholar 

  31. Volaire F (2003) Seedling survival under drought differs between an annual (Hordeum vulgare) and a perennial grass (Dactylis glomerata). New Phytol 160(3):501–510

    PubMed  Google Scholar 

  32. Volaire F, Conéjero G, Lelièvre F (2001) Drought survival and dehydration tolerance in Dactylis glomerata and Poa bulbosa. Funct Plant Biol 28(8):743–754

    Google Scholar 

  33. Tronsmo AM (1993) Resistance to winter stress factors in half-sib families of Dactylis glomerata, tested in a controlled environment. Acta Agric Scand B 43(2):89–96

    Google Scholar 

  34. Guangyan F, Lei X, Jianping W, Gang N, Bradley Shaun B, Wengang X, Haidong Y, Zhongfu Y, Hao G, Linkai H (2018) Integration of small RNAs and transcriptome sequencing uncovers a complex regulatory network during vernalization and heading stages of orchardgrass (Dactylis glomerata L.). BMC Genomics 19(1):727

    Google Scholar 

  35. Yang J, Peilin C, Jing C, Kayla P, Xiaoyu L, Haidong Y, Sifan Z, Guangyan F, Chengran W, Guohua Y (2018) Combinations of small RNA, RNA, and degradome sequencing uncovers the expression pattern of microRNA–mRNA pairs adapting to drought stress in leaf and root of Dactylis glomerata L. Int J Mol Sci 19(10):3114

    Google Scholar 

  36. Linkai H, Haidong Y, Xinxin Z, Xinquan Z, Wang J, Frazier T, Yin G, Huang X, Yan D, Zang W (2015) Identifying differentially expressed genes under heat stress and developing molecular markers in orchardgrass (Dactylis glomerata L.) through transcriptome analysis. Mol Ecol Resour 15(6):1497–1509

    Google Scholar 

  37. Huang L, Feng G, Yan H, Zhang Z, Bushman BS, Wang J, Bombarely A, Li M, Yang Z, Nie G (2019) Genome assembly provides insights into the genome evolution and flowering regulation of orchardgrass. Plant Biotechnol J 18(2):373–388

    PubMed  PubMed Central  Google Scholar 

  38. Eddy SR (2011) Accelerated profile HMM searches. PLoS Comput Biol 7(10):e1002195

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Finn R, Mistry J, Tate J, Coggill P, Heger A (2014) Pfam: the protein families database. Nucleic Acids Res 42(D1):D222–D230

    CAS  PubMed  Google Scholar 

  40. Wilm A, Higgins DG, Valentin F, Blackshields G, McWilliam H, Wallace IM, Thompson JD, Larkin MA, Brown NP, McGettigan PA, Chenna R, Lopez R, Gibson TJ (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947–2948

    PubMed  Google Scholar 

  41. Tamura K, Peterson D, Stecher G, Peterson N, Kumar S, Nei M (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739. https://doi.org/10.1093/molbev/msr121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Hu B, Jin J, Guo A-Y, Zhang H, Luo J, Gao G (2014) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31(8):1296–1297

    PubMed  PubMed Central  Google Scholar 

  43. Bailey TL, Johnson J, Grant CE, Noble WS (2015) The MEME suite. Nucleic Acids Res 43:W39–W49

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Conesa A, Götz S (2008) Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics 2008:1–12

    Google Scholar 

  45. Xiong L, Yuansheng W, Boqun L, Wenqi H, Yonghong Y, Yongping Y (2018) Genome-wide identification and expression analysis of the cation diffusion facilitator gene family in turnip under diverse metal ion stresses. Front Genetics 9:103

    Google Scholar 

  46. Linkai H, Haidong Y, Xiaomei J, Yu Z, Xinquan Z, Yang J, Bing Z, Bin X, Guohua Y, Samantha L (2014) Reference gene selection for quantitative real-time reverse-transcriptase PCR in orchardgrass subjected to various abiotic stresses. Gene 553(2):158–165

    Google Scholar 

  47. Pysh LD, Wysocka-Diller JW, Camilleri C, Bouchez D, Benfey PN (1999) The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J 18(1):9

    Google Scholar 

  48. Gallagher KL, Benfey PN (2008) Both the conserved GRAS domain and nuclear localization are required for SHORT-ROOT movement. Plant J 57(5):785–797

    PubMed  PubMed Central  Google Scholar 

  49. Fuxreiter M, Simon I, Bondos S (2011) Dynamic protein–DNA recognition: beyond what can be seen. Trends Biochem Sci 36(8):415–423

    CAS  PubMed  Google Scholar 

  50. Patthy L (1987) Intron-dependent evolution: preferred types of exons and introns. FEBS Lett 214(1):1–7

    CAS  PubMed  Google Scholar 

  51. Xiaolin S, Jones WT, Rikkerink EHA (2012) GRAS proteins: the versatile roles of intrinsically disordered proteins in plant signalling. Biochem J 442(1):1–12

    Google Scholar 

  52. Amasino R (2010) Seasonal and developmental timing of flowering. Plant J 61(6):1001–1013

    CAS  PubMed  Google Scholar 

  53. Mouradov A, Cremer F, Coupland G (2002) Control of flowering time: interacting pathways as a basis for diversity. Plant Cell 14(suppl 1):S111–S130

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Hazebroek JP, Metzger JD (1990) Thermoinductive regulation of gibberellin metabolism in Thlaspi arvense L.: I. Metabolism of [2H]-ent-Kaurenoic Acid and [14C] Gibberellin A12-Aldehyde. Plant Physiol 94(1):157–165

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Levy YY, Mesnage S, Mylne JS, Gendall AR, Dean C (2002) Multiple roles of Arabidopsis VRN1 in vernalization and flowering time control. Science 297(5579):243–246

    CAS  PubMed  Google Scholar 

  56. Englbrecht CC, Schoof H, Böhm S (2004) Conservation, diversification and expansion of C2H2 zinc finger proteins in the Arabidopsis thaliana genome. BMC Genomics 5(1):39

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research work was funded by the earmarked fund for Modern Agro-industry Technology Research System (No. CARS-34), and the National Natural Science Foundation of China (NSFC 31872997).

Author information

Author notes

  1. Xiaoheng Xu and Guangyan Feng have contributed equally to this work.

Authors and Affiliations

  1. Department of Grassland Science, Sichuan Agricultural University, Chengdu, Sichuan, China

    Xiaoheng Xu, Guangyan Feng, Linkai Huang, Zhongfu Yang, Qiuxu Liu, Yang Shuai & Xinquan Zhang

Authors
  1. Xiaoheng Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guangyan Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Linkai Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhongfu Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qiuxu Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yang Shuai
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xinquan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

LH and XZ planned and designed the study. XX and GF wrote the manuscript and performed the experiments. ZY provided partial data basis. And all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Xinquan Zhang.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Research involving human and animal participants

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher's Note

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

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, X., Feng, G., Huang, L. et al. Genome-wide identification, structural analysis and expression profiles of GRAS gene family in orchardgrass. Mol Biol Rep 47, 1845–1857 (2020). https://doi.org/10.1007/s11033-020-05279-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-020-05279-9

Keywords

Search

Navigation