Skip to main content
Springer Nature Link
Log in

DRM1 and DRM2 expression regulation: potential role of splice variants in response to stress and environmental factors in Arabidopsis

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

The DRM1/ARP gene family is increasingly exhibiting associations with stress conditions at the transcript level. Traditionally correlated with dormancy, increases in transcript levels in response to various treatments have also been reported in various species. As alternative transcript splicing is common in stress conditions, the splice variants of AtDRM1 and AtDRM2 were assessed further in this study. A previously undescribed splice variant of AtDRM1 (AtDRM1.6) is introduced in this work. In silico analyses of predicted protein sequence of all splice variants showed that all variants retain the predicted intrinsically disordered nature. Transcriptional studies of AtDRM1 and AtDRM2 in response to a wide range of abiotic, physical and hormonal treatments showed that AtDRM1.6 is differentially regulated at the transcriptional level compared with other splice variants. Promoter analyses demonstrated AtDRM1 light regulation via the upstream promoter sequence.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Abbreviations

RT qPCR:

Reverse transcriptase quantitative polymerase chain reaction

IDP:

Intrinsically disordered protein

DRM1 :

Dormancy-associated gene-1

ARP :

Auxin-repressed protein

WT:

Wild type

bp:

Base pairs

aa:

Amino acid

h:

Hour

min:

Minutes

References

  • Arber A (1920) Water plants: a study of aquatic angiosperms. Cambridge University Press, Cambridge

    Google Scholar 

  • Barbazuk WB, Fu Y, McGinnis KM (2008) Genome-wide analyses of alternative splicing in plants: opportunities and challenges. Genome Res 18(9):1381–1392. doi:10.1101/gr.053678.106

    Article  CAS  PubMed  Google Scholar 

  • Campbell MA, Haas BJ, Hamilton JP, Mount SM, Buell CR (2006) Comprehensive analysis of alternative splicing in rice and comparative analyses with Arabidopsis. BMC Genomics 7 (327) doi:10.1186/1471-2164-7-327

  • Cheng Y, Oldfield CJ, Meng J, Romero P, Uversky VN, Dunker AK (2007) Mining α-helix-forming molecular recognition features with cross species sequence alignments. Biochemistry 46(47):13468–13477. doi:10.1021/bi7012273

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743. doi:10.1046/j.1365-313x.1998.00343.x

    Article  CAS  PubMed  Google Scholar 

  • Dosztányi Z, Chen J, Dunker AK, Simon I, Tompa P (2006) Disorder and sequence repeats in hub proteins and their implications for network evolution. J Proteome Res 5(11):2985–2995

    Article  PubMed  Google Scholar 

  • Dunker AK, Lawson JD, Brown CJ, Williams RM, Romero P, Oh JS, Oldfield CJ, Campen AM, Ratliff CM, Hipps KW, Ausio J, Nissen MS, Reeves R, Kang C, Kissinger CR, Bailey RW, Griswold MD, Chiu W, Garner EC, Obradovic Z (2001) Intrinsically disordered protein. J Mol Gr Model 19(1):26–59

    Article  CAS  Google Scholar 

  • Dunker AK, Cortese MS, Romero P, Iakoucheva LM, Uversky VN (2005) Flexible nets: the roles of intrinsic disorder in protein interaction networks. FEBS J 272(20):5129–5148

    Article  CAS  PubMed  Google Scholar 

  • Durek P, Schmidt R, Heazlewood JL, Jones A, MacLean D, Nagel A, Kersten B, Schulze WX (2010) PhosPhAt: the Arabidopsis thaliana phosphorylation site database. An update. Nucleic Acids Res 38 (Database issue):D828–D834

  • Ekman D, Light S, Björklund ÅK, Elofsson A (2006) What properties characterize the hub proteins of the protein–protein interaction network of Saccharomyces cerevisiae? Genome Biology 7 (6) doi:10.1186/gb-2006-7-6-r45

  • Finlayson SA, Krishnareddy SR, Kebrom TH, Casal JJ (2010) Phytochrome regulation of branching in Arabidopsis. Plant Physiol 152(4):1914–1927. doi:10.1104/pp.109.148833

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Franklin KA, Whitelam GC (2005) Phytochromes and shade-avoidance responses in plants. Ann Bot 96(2):169–175

    Article  CAS  PubMed  Google Scholar 

  • Garay-Arroyo A, Colmenero-Flores JM, Garciarrubio A, Covarrubias AA (2000) Highly hydrophilic proteins in prokaryotes and eukaryotes are common during conditions of water deficit. J Biol Chem 275(8):5668–5674

    Article  CAS  PubMed  Google Scholar 

  • Gebauer F, Merendino L, Hentze MW, Valcarcel J (1998) The Drosophila splicing regulator sex-lethal directly inhibits translation of male-specific-lethal 2 mRNA. RNA 4(2):142–150

    CAS  PubMed Central  PubMed  Google Scholar 

  • Giuliano G, Pichersky E, Malik VS, Timko MP, Scolnik PA, Cashmore AR (1988) An evolutionarily conserved protein binding sequence upstream of a plant light-regulated gene. Proc Nat Acad Sci USA 85(19):7089–7093

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Govind G, Vokkaliga ThammeGowda H, Jayaker Kalaiarasi P, Iyer D, Muthappa S, Nese S, Makarla U (2009) Identification and functional validation of a unique set of drought induced genes preferentially expressed in response to gradual water stress in peanut. Mol Genet Genomics 281(6):591–605. doi:10.1007/s00438-009-0432-z

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Haynes C, Oldfield CJ, Ji F, Klitgord N, Cusick ME, Radivojac P, Uversky VN, Vidal M, Iakoucheva LM (2006) Intrinsic disorder is a common feature of hub proteins from four eukaryotic interactomes. PLoS Comp Biol 2(8):0890–0901

    Article  CAS  Google Scholar 

  • Heazlewood JL, Durek P, Hummel J, Selbig J, Weckwerth W, Walther D, Schulze WX (2007) PhosPhAt: a database of phosphorylation sites in Arabidopsis thaliana and a plant-specific phosphorylation site predictor. Nucleic Acids Res 36(Database issue):D1015–D1021

    Google Scholar 

  • Hellens R, Allan A, Friel E, Bolitho K, Grafton K, Templeton M, Karunairetnam S, Gleave A, Laing W (2005) Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods 18 (1) doi:10.1186/1746-4811-1-13

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27(1):297–300. doi:10.1093/nar/27.1.297

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hsu WL, Oldfield CJ, Xue B, Meng J, Huang F, Romero P, Uversky VN, Dunker AK (2013) Exploring the binding diversity of intrinsically disordered proteins involved in one-to-many binding. Protein Sci 22(3):258–273

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Huang F, Oldfield C, Meng J, Hsu WL, Xue B, Uversky VN, Romero P, Dunker AK (2012) Subclassifying disordered proteins by the CH-CDF plot method. Pac Symp Biocomputing pp 128–139

  • Hwang EW, Kim KA, Park SC, Jeong MJ, Byun MO, Kwon HB (2005) Expression profiles of hot pepper (Capsicum annuum) genes under cold stress conditions. J Biosci 30(5):657–667

    Article  CAS  PubMed  Google Scholar 

  • Kazan K (2003) Alternative splicing and proteome diversity in plants: the tip of the iceberg has just emerged. Trends Plant Sci 8 (10):468–471. doi:10.1016/j.tplants.2003.09.001

  • Kebrom TH, Burson BL, Finlayson SA (2006) Phytochrome B represses Teosinte Branched1 expression and induces sorghum axillary bud outgrowth in response to light signals. Plant Physiol 140(3):1109–1117. doi:10.1104/pp.105.074856

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kebrom TH, Brutnell TP, Finlayson SA (2010) Suppression of sorghum axillary bud outgrowth by shade, phyb and defoliation signalling pathways. Plant Cell Environ 33(1):48–58. doi:10.1111/j.1365-3040.2009.02050.x

    CAS  PubMed  Google Scholar 

  • Lang GA, Early JD, Martin GC, Darnell RL (1987) Endo-, para-, and ecodormancy: physiological terminology and classification for dormancy research. Hortscience 22(3):371–377

    Google Scholar 

  • Lee J, Han C-T, Hur Y (2013) Molecular characterization of the Brassica rapa auxin-repressed, superfamily genes, BrARP1 and BrDRM1. Mol Biol Rep 40(1):197–209. doi:10.1007/s11033-012-2050-9

    Article  CAS  PubMed  Google Scholar 

  • Mastrangelo AM, Marone D, Laidò G, De Leonardis AM, De Vita P (2012) Alternative splicing: enhancing ability to cope with stress via transcriptome plasticity. Plant Sci 185–186:40–49. doi:10.1016/j.plantsci.2011.09.006

    Article  PubMed  Google Scholar 

  • Mohan A, Oldfield CJ, Radivojac P, Vacic V, Cortese MS, Dunker AK, Uversky VN (2006) Analysis of molecular recognition features (MoRFs). J Mol Biol 362(5):1043–1059. doi:10.1016/j.jmb.2006.07.087

    Article  CAS  PubMed  Google Scholar 

  • Mohan A, Sullivan WJ Jr, Radivojac P, Dunker AK, Uversky VN (2008) Intrinsic disorder in pathogenic and non-pathogenic microbes: discovering and analyzing the unfoldomes of early-branching eukaryotes. Mol Bio Syst 4(4):328–340

    CAS  Google Scholar 

  • Mouillon JM, Gustafsson P, Harryson P (2006) Structural investigation of disordered stress proteins. Comparison of full-length dehydrins with isolated peptides of their conserved segments. Plant Physiol 141(2):638–650

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ner-Gaon H, Halachmi R, Savaldi-Goldstein S, Rubin E, Ophir R, Fluhr R (2004) Intron retention is a major phenomenon in alternative splicing in Arabidopsis. Plant J 39(6):877–885. doi:10.1111/j.1365-313X.2004.02172.x

    Article  CAS  PubMed  Google Scholar 

  • Oldfield CJ, Cheng Y, Cortese MS, Brown CJ, Uversky VN, Dunker AK (2005) Comparing and combining predictors of mostly disordered proteins. Biochemistry 44(6):1989–2000. doi:10.1021/bi047993o

    Article  CAS  PubMed  Google Scholar 

  • Park S, Han KH (2003) An auxin-repressed gene (RpARP) from black locust (Robinia pseudoacacia) is posttranscriptionally regulated and negatively associated with shoot elongation. Tree Physiol 23:815–823

    Google Scholar 

  • Patil A, Nakamura H (2006) Disordered domains and high surface charge confer hubs with the ability to interact with multiple proteins in interaction networks. FEBS Lett 580(8):2041–2045. doi:10.1016/j.febslet.2006.03.003

    Article  CAS  PubMed  Google Scholar 

  • Pietrosemoli N, García-Martín JA, Solano R, Pazos F (2013) Genome-wide analysis of protein disorder in Arabidopsis thaliana: implications for plant environmental adaptation. PLoS One 8(2):e55524. doi:10.1371/journal.pone.0055524

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rae GM, David KM, Wood M (2013) The dormancy marker DRM1/ARP: associated with dormancy but a broader role in planta. Dev Biol J 2013 (Article ID 632524):12 pages. doi:10.1155/2013/632524

  • Rechsteiner M, Rogers SW (1996) PEST sequences and regulation by proteolysis. Trends Biochem Sci 21(7):267–271

    Article  CAS  PubMed  Google Scholar 

  • Rohde A, Van Montagu M, Boerjan W (1999) The Abscisic acid-insensitive 3 (ABI3) gene is expressed during vegetative quiescence processes in Arabidopsis. Plant Cell Environ 22(3):261–270. doi:10.1046/j.1365-3040.1999.00428.x

    Article  CAS  Google Scholar 

  • Romero PR, Zaidi S, Fang YY, Uversky VN, Radivojac P, Oldfield CJ, Cortese MS, Sickmeier M, LeGall T, Obradovic Z, Dunker AK (2006) Alternative splicing in concert with protein intrinsic disorder enables increased functional diversity in multicellular organisms. Proc Natl Acad Sci USA 103(22):8390–8395

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386

    CAS  PubMed  Google Scholar 

  • Schaffer R, Landgraf J, Accerbi M, Simon V, Larson M, Wisman E (2001) Microarray analysis of diurnal and circadian-regulated genes in Arabidopsis. Plant Cell 13(1):113–123

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Singh GP, Dash D (2007) Intrinsic disorder in yeast transcriptional regulatory network. Proteins Struct Funct Genet 68(3):602–605

    Article  CAS  PubMed  Google Scholar 

  • Singh GP, Ganapathi M, Dash D (2007) Role of intrinsic disorder in transient interactions of hub proteins. Proteins Struct Funct Genet 66(4):761–765

    Article  CAS  PubMed  Google Scholar 

  • Stafstrom JP (2000) Regulation of growth and dormancy in pea axillary buds. In: JDVAJ Crabbé (ed) Dormancy in Plants. CAB International, Wallingford, pp 331–346

    Google Scholar 

  • Stafstrom JP, Ripley BD, Devitt ML, Drake B (1998) Dormancy-associated gene expression in pea axillary buds. Cloning and expression of PsDRM1 and PsDRM2. Planta 205(4):547–552. doi:10.1007/s004250050354

    Article  CAS  PubMed  Google Scholar 

  • Sun X, Jones WT, Harvey D, Edwards PJB, Pascal SM, Kirk C, Considine T, Sheerin DJ, Rakonjac J, Oldfield CJ, Xue B, Dunker AK, Uversky VN (2010) N-terminal domains of DELLA proteins are intrinsically unstructured in the absence of interaction with GID1/Gibberellic acid receptors. J Biol Chem 285(15):11557–11571. doi:10.1074/jbc.M109.027011

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sun X, Xue B, Jones W, Rikkerink E, Dunker A, Uversky V (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. doi:10.1007/s11103-011-9803-z

    Article  CAS  PubMed  Google Scholar 

  • Tatematsu K, Ward S, Leyser O, Kamiya Y, Nambara E (2005) Identification of cis-elements that regulate gene expression during initiation of axillary bud outgrowth in Arabidopsis. Plant Physiol 138(2):757–766. doi:10.1104/pp.104.057984

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tompa P, Csermely P (2004) The role of structural disorder in the function of RNA and protein chaperones. FASEB J 18(11):1169–1175. doi:10.1096/fj.04-1584rev

    Article  CAS  PubMed  Google Scholar 

  • Uversky VN (2011) Multitude of binding modes attainable by intrinsically disordered proteins: a portrait gallery of disorder-based complexes. Chem Soc Rev 40(3):1623–1634

    Article  CAS  PubMed  Google Scholar 

  • Uversky VN (2013) Intrinsic disorder-based protein interactions and their modulators. Curr Pharm Des 19(23):4191–4213

    Article  CAS  PubMed  Google Scholar 

  • Uversky VN, Dunker AK (2010) Understanding protein non-folding. Biochimica et Biophysica Acta Proteins Proteomics 1804(6):1231–1264. doi:10.1016/j.bbapap.2010.01.017

    Article  CAS  Google Scholar 

  • Uversky VN, Oldfield CJ, Dunker AK (2005) Showing your ID: intrinsic disorder as an ID for recognition, regulation and cell signaling. J Mol Recognit 18(5):343–384

    Article  CAS  PubMed  Google Scholar 

  • Vacic V, Oldfield CJ, Mohan A, Radivojac P, Cortese MS, Uversky VN, Dunker AK (2007) Characterization of molecular recognition features, MoRFs, and their binding partners. J Proteome Res 6(6):2351–2366

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang BB, Brendel V (2006) Genomewide comparative analysis of alternative splicing in plants. Proc Natl Acad Sci 103(18):7175–7180

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9(5):244–252. doi:10.1016/j.tplants.2004.03.006

    Article  CAS  PubMed  Google Scholar 

  • Wilkins O, Nahal H, Foong J, Provart NJ, Campbell MM (2009) Expansion and diversification of the populus R2R3-MYB family of transcription factors. Plant Physiol 149(2):981–993. doi:10.1104/pp.108.132795

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wood M, Rae GM, Wu R-M, Walton EF, Xue B, Hellens RP, Uversky VN (2013) Actinidia DRM1: an intrinsically disordered protein whose mRNA expression is inversely correlated with spring budbreak in kiwifruit. PLoS One 8(3):e57354. doi:10.1371/journal.pone.0057354

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xue B, Dunbrack RL, Williams RW, Dunker AK, Uversky VN (2010) PONDR-FIT: A meta-predictor of intrinsically disordered amino acids. Biochimica et Biophysica Acta (BBA) Proteins Proteomics 1804(4):996–1010. doi:10.1016/j.bbapap.2010.01.011

Download references

Acknowledgments

Thank you to Tim Homes for photographic assistance. Thank you to Rebecca Kirk and Kim Snowden for critical reading of the manuscript.

Author information

Authors and Affiliations

  1. The New Zealand Institute for Plant and Food Research Limited, Mt Albert, Private Bag 92169, Auckland Mail Centre, Auckland, 1142, New Zealand

    Georgina M. Rae & Marion Wood

  2. Plant Molecular Sciences, School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland, New Zealand

    Georgina M. Rae & Karine David

  3. Department of Molecular Medicine, Morsani College of Medicine, University of South Florida, Tampa, FL, 33612, USA

    Vladimir N. Uversky

  4. USF Health Byrd Alzheimer’s Research Institute, Morsani College of Medicine, University of South Florida, Tampa, FL, 33612, USA

    Vladimir N. Uversky

  5. Institute for Biological Instrumentation, Russian Academy of Sciences, 142290 Pushchino, Moscow Region, Russia

    Vladimir N. Uversky

Authors
  1. Georgina M. Rae
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Vladimir N. Uversky
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Karine David
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Marion Wood
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to Marion Wood.

Additional information

Communicated by A. K. Tyagi.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rae, G.M., Uversky, V.N., David, K. et al. DRM1 and DRM2 expression regulation: potential role of splice variants in response to stress and environmental factors in Arabidopsis . Mol Genet Genomics 289, 317–332 (2014). https://doi.org/10.1007/s00438-013-0804-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-013-0804-2

Keywords