Skip to main content
SpringerLink
Log in

MKRN expression pattern during embryonic and post-embryonic organogenesis in rice (Oryza sativa L. var. Nipponbare)

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

Abstract

Rice MKRN is a member of the makorin RING finger protein gene (MKRN) family, which encodes a protein with a characteristic array of zinc-finger motifs conserved in various eukaryotes. Using non-radioactive in situ hybridization, we investigated the spatio-temporal gene expression pattern of rice MKRN during embryogenesis, imbibition, seminal and lateral root development of Oryza sativa L. var. Nipponbare. MKRN expression was ubiquitous during early organogenesis in the embryo along the apical–basal and radial axes. The expression of MKRN decreased during embryonic organ elongation and maturation compared to early embryogenesis, but increased again during imbibition. Tissue-specific and position-dependent MKRN expression was found during embryonic and post-embryonic root and shoot development. Meristematic cells ubiquitously expressed MKRN transcripts, while differentiating cells showed a gradual reduction and termination of MKRN expression. Interestingly, during post-germination MKRN expression was prominent and continued in the metabolically active, differentiated companion cells of the phloem. The differential expression pattern was observed both in the differentiating and differentiated cells. Also, MKRN was expressed in the various developmental stages of the lateral root primordia and the cells surrounding them. Expression of MKRN was also observed after periclinal division of the presumptive pericycle founder cells. The MKRN expression pattern during development of various growth stages suggests an important role of makorin RING finger protein gene (MKRN) in embryonic and post-embryonic organogenesis in both apical–basal and radial developmental axes of rice.

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

DAP:

Days after pollination

hTERT:

Human telomere reverse transcriptase enzyme

LRP:

Lateral root primordia

MKRN:

Makorin RING finger protein

PFC:

Pericycle founder cells

RAM:

Root apical meristem

SAM:

Shoot apical meristem

References

  • Abe S, Chiba S, Mishra N, Minamino Y, Nakasuji H, Doi M, Gray TA (2004) Origin and evolution of the genomic region encoding RAF1, MKRN2, PPARG, and SYN2 in human chromosomes 3p25. Proceedings of the Marine Biotechnology Conference, Chiba, Japan, 2003. Mar Biotechnol 6: S404–S412

  • Abe S, Nakasuji H, Arumugam TU, Gray TA, Weidner SM (2007) Genomic organization and expression profile of a gene encoding makorin RING zinc finger protein in germinating pea (Pisum sativum L. var. Alaska) seeds. Acta Physiol Plant 29:81–94

    Article  CAS  Google Scholar 

  • Arumugam TU, Davies E, Morita EH, Abe S (2007) Sequence, expression and tissue localization of a gene encoding a makorin RING zinc-finger protein in germinating rice (Oryza sativa L. ssp. Japonica) seeds. Plant Physiol Biochem 45:767–780

    Article  PubMed  CAS  Google Scholar 

  • Bhat SP, Padayatty JD (1975) Transcriptional events during early phase of germination of rice embryos. Nature 256:227–228

    Article  PubMed  CAS  Google Scholar 

  • Böhne A, Darras A, D’Cotta H, Baroiller JF, Galiana-Arnoux D, Volff JN (2010) The vertebrate makorin ubiquitin ligase gene family has been shaped by large-scale duplication and retroposition from an ancestral gonad-specific, maternal-effect gene. Genomics 11:721–733

    Article  PubMed  Google Scholar 

  • Botha FC, Potgieter GP, Botha AM (1992) Respiratory metabolism and gene expression during seed germination. Plant Growth Regul 11:211–224

    Article  CAS  Google Scholar 

  • Chamnan C, Abe S, Doi M, Chiba S, Gray TA (2003) The genomic organization of MKRN1, and expression of MKRN1, MKRN2, and RAF1 in yellowtail fish (Seriola quinqueradiata). J Egypt Germ Soc Zool C: Histol Histochem 42:57–75

    Google Scholar 

  • Comai L, Harada J (1990) Transcriptional activities in dry seed nuclei indicate the timing of the transition from embryogeny to germination. Proc Natl Acad Sci USA 87:2671–2674

    Article  PubMed  CAS  Google Scholar 

  • De Smet I, Tetsumura T, De Rybel B et al (2007) Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development 134:681–690

    Article  PubMed  Google Scholar 

  • Du Z, Cong H, Yao Z (2001) Identification of putative downstream genes of Oct-4 by suppression-subtractive hybridization. Biochem Biophys Res Comm 282:701–706

    Article  PubMed  CAS  Google Scholar 

  • Dubrovsky JG, Doerner P, Colo′n-Carmona A, Rost TL (2000) Pericycle cell proliferation and lateral root initiation in Arabidopsis. Plant Physiol 124:1648–1657

    Article  PubMed  CAS  Google Scholar 

  • Dubrovsky JG, Sauer M, Napsucialy-Mendivil S et al (2008) Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proc Natl Acad Sci USA 105:8790–8794

    Article  PubMed  CAS  Google Scholar 

  • Ebenezer GAI, Amirthalingam M, Ponsamuel J, Dayanandan P (1990) Role of palea and lemma in the development of rice caryopsis. J Indian Bot Soc 69:245–250

    Google Scholar 

  • Ellis JR, Chaffey N (1987) Structural differentiation of the nucellar epidermis in the caryopsis of rice (Oryza sativa L.). Ann Bot 60:671–675

    Google Scholar 

  • Esau K (1977) Anatomy of seed plants, 2nd edn. Wiley, New York

    Google Scholar 

  • Friml J (2003) Auxin transport-shaping the plant. Curr Opin Plant Biol 6:7–12

    Article  PubMed  CAS  Google Scholar 

  • Gray TA, Hernandez L, Carey AH et al (2000) The ancient source of a distinct gene family encoding proteins featuring RING and C(3)H zinc-finger motifs with abundant expression in developing brain and nervous system. Genomics 66:76–86

    Article  PubMed  CAS  Google Scholar 

  • Gray TA, Azama K, Whitmore K, Min A, Abe S, Nicholls RD (2001) Phylogenetic conservation of the makorin-2 gene, encoding a multiple zinc-finger protein, antisense to the RAF1 proto-oncogene. Genomics 77:119–126

    Article  PubMed  CAS  Google Scholar 

  • Gray TA, Wilson A, Fortin PJ, Nicholls RD (2006) The putatively functional Mkrn1-p1 pseudogene is neither expressed nor imprinted, nor does it regulate its source gene in trans. Proc Natl Acad Sci USA 103:12039–12044

    Article  PubMed  CAS  Google Scholar 

  • Itoh J, Nonomura K, Ikeda K, Yamaki S, Inukai Y, Yamagishi H, Kitano H, Nagato Y (2005) Rice plant development: from zygote to spikelet. Plant Cell Physiol 46:23–47

    Article  PubMed  CAS  Google Scholar 

  • Kim JH, Park SM, Kang MR, Oh SY, Lee TH, Muller MT, Chung IK (2005) Ubiquitin ligase MKRN1 modulates telomere length homeostasis through a proteolysis of hTERT. Gene Dev 19:776–781

    Article  PubMed  CAS  Google Scholar 

  • Kitano H, Tamura Y, Satoh H, Nagato Y (1993) Hierarchical regulation of organ differentiation during embryogenesis in rice. Plant J 3:607–610

    Article  Google Scholar 

  • Krauss L (1933) Entwicklungsgeschichte der Früchte von Hordeum, Triticum, Bromus und Poa mit besonderer Berücksichtigung ihrer Samenschalen. Jahrbücher für Wissenschaftliche Botanik 77:733–808

    Google Scholar 

  • Krishnan S, Dayanandan P (2003) Structural and histochemical studies on grain-filling in the caryopsis of rice (Oryza sativa L.). J Biosci 28:455–469

    Article  PubMed  CAS  Google Scholar 

  • Laskowski M, Biller S, Stanley K, Kajstura T, Prusty R (2006) Expression profiling of auxin-treated Arabidopsis roots: toward a molecular analysis of lateral root emergence. Plant Cell Physiol 47:788–792

    Article  PubMed  CAS  Google Scholar 

  • Lee EW, Lee MS, Camus S, Ghim J, Yang MR, Oh W, Ha NC, Lane DP, Song J (2009) Differential regulation of p53 and p21 by MKRN1 E3 ligase controls cell cycle arrest and apoptosis. EMBO J 28:2100–2113

    Article  PubMed  CAS  Google Scholar 

  • Malamy JE, Benefy P (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124:33–44

    PubMed  CAS  Google Scholar 

  • Mayer U, Ruiz RAT, Berleth T, Miseera S, Jürgens G (1991) Mutations affecting body organization in the Arabidopsis embryo. Nature 353:402–407

    Article  Google Scholar 

  • Miroci H, Schob C, Kindler S et al (2012) Makorin ring zinc finger protein 1 (MKRN1), a novel poly(A)-binding protein-interacting protein, stimulates translation in nerve cells. J Biol Chem 287:1322–1334

    Article  PubMed  CAS  Google Scholar 

  • Mogensen HL (1973) Some histochemical, ultrastructural and nutritional aspects of the ovule of Quercus gambelii. Am J Bot 60:48–54

    Article  Google Scholar 

  • Moon J, Parry G, Estelle M (2004) The ubiquitin-proteasome pathway and plant development. Plant Cell 16:3181–3195

    Article  PubMed  CAS  Google Scholar 

  • Neuteboom LW, Veth-Tello LM, Clijdesdale OR, Hooykaas PJJ, van der Zaal BJ (1999) A novel subtilisin-like protease gene from Arabidopsis thaliana is expressed at sites of lateral root emergence. DNA Res 6:13–19

    Article  PubMed  CAS  Google Scholar 

  • Nishimura S, Maeda E (1982) Cytological studies on differentiation and dedifferentiation in pericycle cells of excised rice roots. Jpn J Crop Sci 51:553–560

    Article  Google Scholar 

  • Omwancha J, Zhou XF, Chen SY, Baslan T, Fisher CJ, Zheng Z, Cai C, Shemshedini L (2006) Makorin RING finger protein 1 (MKRN1) has negative and positive effects on RNA polymerase II-dependent transcription. Endocrine 29:363–373

    Article  PubMed  CAS  Google Scholar 

  • Péret B, Larrieu A, Bennett MJ (2009) Lateral root emergence: a difficult birth. J Exp Bot 60:3637–3643

    Article  PubMed  Google Scholar 

  • Rebouillat J, Dievart A, Verdeil JL et al (2009) Molecular genetics of rice root development. Rice 2:15–34

    Article  Google Scholar 

  • Saha B (1956) Studies on the development of the embryo of Oryza sativa L. and the homologies of its parts. Proc Nat Inst Sci India 22:86–101

    Google Scholar 

  • Sahi VP, Arumugam TU, Morita EH, Abe S (2011) Expression of a gene encoding a MKRN RING zinc finger protein in early germination stages of pea (Pisum sativum L. var. Alaska) and its possible role in differentiation. Acta Physiol Plant 33:1759–1767

    Article  CAS  Google Scholar 

  • Sahi VP, Wadekar HB, Nagganatha Suganthan R, Arumugam TU, Morita EH, Abe S (2012) A molecular insight into Darwin’s ‘plant brain hypothesis’ through expression pattern study of the MKRN gene in plant embryo compared with mouse embryo. Plant Signal Behav 7:1–7

    Article  Google Scholar 

  • Salvatico J, Kim JH, Chung IK, Muller MT (2010) Differentiation linked regulation of telomerase activity by Makorin-1. Mol Cell Biochem 342:241–250

    Article  PubMed  CAS  Google Scholar 

  • Steeves TA, Sussex I (1989) Patterns in plant development. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Swarup K, Benkova E, Swarup R et al (2008) The auxin influx carrier LAX3 promotes lateral root emergence. Nat Cell Biol 10:946–954

    Article  PubMed  CAS  Google Scholar 

  • Yang PH, Cheung WK, Peng Y et al (2008) Makorin-2 is a neurogenesis inhibitor downstream of phosphatidylinositol 3-kinase/Akt (PI3 K/Akt) signal. J Biol Chem 283:8486–8495

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Molecular Cell Physiology, Faculty of Agriculture, Ehime University, 3-5-7 Tarumi, Matsuyama, 790-8566, Japan

    Hanumant Baburao Wadekar, Vaidurya Pratap Sahi, Eugene Hayato Morita & Shunnosuke Abe

Authors
  1. Hanumant Baburao Wadekar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vaidurya Pratap Sahi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eugene Hayato Morita
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shunnosuke Abe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shunnosuke Abe.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wadekar, H.B., Sahi, V.P., Morita, E.H. et al. MKRN expression pattern during embryonic and post-embryonic organogenesis in rice (Oryza sativa L. var. Nipponbare). Planta 237, 1083–1095 (2013). https://doi.org/10.1007/s00425-012-1828-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-012-1828-2

Keywords

Search

Navigation