Skip to main content
SpringerLink
Log in

Ectopic expression of the Arabidopsis MINI ZINC FINGER1 and MIF3 genes induces shoot meristems on leaf margins

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

A leaf undergoes determinate growth from a primordium on flank of the shoot apical meristem. Several intrinsic pathways restrict meristematic activity in the leaf of Arabidopsis; however, other factors remain to be defined. We report here that the overexpression of MINI ZINC FINGER1 (MIF1) or MIF3 disrupted the leaf determinate growth by inducing ectopic shoot meristems on leaf margins. These ectopic meristems occurred along margins of late rosette leaves at serration sinuses in an ERECTA-dependent manner. Expression of STM was activated in these ectopic meristems but not other leaf regions. The formation of ectopic meristems was independent of the BP gene but suppressed by exogenous gibberellic acid. In addition, reduced auxin response along leaf margins and subsequent response peak in the sinus were correlated with the occurrence of ectopic meristems. Our results suggest that the sinus of leaf serration is a quiescent domain possessing the potential for meristem formation. MIF1- or MIF3-overexpressing transgenic plants may provide a new genetic system for dissecting the molecular mechanism that maintains leaf determinate growth, and for understanding the interactions between hormone actions and meristematic activity.

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

Similar content being viewed by others

References

  • Alvarez JP, Pekker I, Goldshmidt A, Blum E, Amsellem Z, Eshed Y (2006) Endogenous and synthetic microRNAs stimulate simultaneous, efficient, and localized regulation of multiple targets in diverse species. Plant Cell 18:1134–1151

    Article  PubMed  CAS  Google Scholar 

  • Benkova E, Michniewicz M, Sauer M, Teichmann T, Seifertova D, Jurgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602

    Article  PubMed  CAS  Google Scholar 

  • Bowman JL, Eshed Y (2000) Formation and maintenance of the shoot apical meristem. Trends Plant Sci 5:110–115

    Article  PubMed  CAS  Google Scholar 

  • Byrne ME, Barley R, Curtis M, Arroyo JM, Dunham M, Hudson A, Martienssen RA (2000) Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 408:967–971

    Article  PubMed  CAS  Google Scholar 

  • Byrne ME, Simorowski J, Martienssen RA (2002) ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis. Development 129:1957–1965

    PubMed  CAS  Google Scholar 

  • Chuck G, Lincoln C, Hake S (1996) KNAT1 induces lobed leaves with ectopic meristems when overexpressed in Arabidopsis. Plant Cell 8:1277–1289

    Article  PubMed  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  Google Scholar 

  • Engstrom EM, Izhaki A, Bowman JL (2004) Promoter bashing, microRNAs, and Knox genes. New insights, regulators, and targets-of-regulation in the establishment of lateral organ polarity in Arabidopsis. Plant Physiol 135:685–694

    Article  PubMed  CAS  Google Scholar 

  • Fletcher JC (2002) Coordination of cell proliferation and cell fate decisions in the angiosperm shoot apical meristem. Bioessays 24:27–37

    Article  PubMed  Google Scholar 

  • Garces HM, Champagne CE, Townsley BT, Park S, Malho R, Pedroso MC, Harada JJ, Sinha NR (2007) Evolution of asexual reproduction in leaves of the genus Kalanchoe. Proc Natl Acad Sci USA 104:15578–15583

    Article  PubMed  CAS  Google Scholar 

  • Golz JF, Hudson A (2002) Signalling in plant lateral organ development. Plant Cell 14:S277–S288

    PubMed  CAS  Google Scholar 

  • Ha CM, Kim GT, Kim BC, Jun JH, Soh MS, Ueno Y, Machida Y, Tsukaya H, Nam HG (2003) The BLADE-ON-PETIOLE 1 gene controls leaf pattern formation through the modulation of meristematic activity in Arabidopsis. Development 130:161–172

    Article  PubMed  CAS  Google Scholar 

  • Ha CM, Jun JH, Nam HG, Fletcher JC (2004) BLADE-ON-PETIOLE1 encodes a BTB/POZ domain protein required for leaf morphogenesis in Arabidopsis thaliana. Plant Cell Physiol 45:1361–1370

    Article  PubMed  CAS  Google Scholar 

  • Hake S, Char BR, Chuck G, Foster T, Long J, Jackson D (1995) Homeobox genes in the functioning of plant meristems. Philos Trans R Soc Lond B Biol Sci 350:45–51

    Article  PubMed  CAS  Google Scholar 

  • Hake S, Smith HM, Holtan H, Magnani E, Mele G, Ramirez J (2004) The role of knox genes in plant development. Annu Rev Cell Dev Biol 20:125–151

    Article  PubMed  CAS  Google Scholar 

  • Hay A, Kaur H, Phillips A, Hedden P, Hake S, Tsiantis M (2002) The gibberellin pathway mediates KNOTTED1-type homeobox function in plants with different body plans. Curr Biol 12:1557–1565

    Article  PubMed  CAS  Google Scholar 

  • Hong SY, Kim OK, Kim SG, Yang MS, Park CM (2011) Nuclear import and DNA binding of the ZHD5 transcription factor is modulated by a competitive peptide inhibitor in Arabidopsis. J Biol Chem 286:1659–1668

    Article  PubMed  CAS  Google Scholar 

  • Hu W, Ma H (2006) Characterization of a novel putative zinc finger gene MIF1: involvement in multiple hormonal regulation of Arabidopsis development. Plant J 45:399–422

    Article  PubMed  CAS  Google Scholar 

  • Hu W, Wang Y, Bowers C, Ma H (2003) Isolation, sequence analysis, and expression studies of florally expressed cDNAs in Arabidopsis. Plant Mol Biol 53:545–563

    Article  PubMed  CAS  Google Scholar 

  • Hu W, dePamphilis CW, Ma H (2008) Phylogenetic analysis of the plant-specific zinc finger-homeobox and mini zinc finger gene families. J Integr Plant Biol 50:1031–1045

    Article  PubMed  CAS  Google Scholar 

  • Janssen BJ, Lund L, Sinha N (1998) Overexpression of a homeobox gene, LeT6, reveals indeterminate features in the tomato compound leaf. Plant Physiol 117:771–786

    Article  PubMed  CAS  Google Scholar 

  • Jasinski S, Piazza P, Craft J, Hay A, Woolley L, Rieu I, Phillips A, Hedden P, Tsiantis M (2005) KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr Biol 15:1560–1565

    Article  PubMed  CAS  Google Scholar 

  • Kawamura E, Horiguchi G, Tsukaya H (2010) Mechanisms of leaf tooth formation in Arabidopsis. Plant J 62:429–441

    Article  PubMed  CAS  Google Scholar 

  • Kirch T, Simon R, Grunewald M, Werr W (2003) The DORNROSCHEN/ENHANCER OF SHOOT REGENERATION1 gene of Arabidopsis acts in the control of meristem cell fate and lateral organ development. Plant Cell 15:694–705

    Article  PubMed  CAS  Google Scholar 

  • Kumar R, Kushalappa K, Godt D, Pidkowich MS, Pastorelli S, Hepworth SR, Haughn GW (2007) The Arabidopsis BEL1-LIKE HOMEODOMAIN proteins SAW1 and SAW2 act redundantly to regulate KNOX expression spatially in leaf margins. Plant Cell 19:2719–2735

    Article  PubMed  CAS  Google Scholar 

  • Kumaran MK, Bowman JL, Sundaresan V (2002) YABBY polarity genes mediate the repression of KNOX homeobox genes in Arabidopsis. Plant Cell 14:2761–2770

    Article  PubMed  CAS  Google Scholar 

  • Kusaba S, Fukumoto M, Honda C, Yamaguchi I, Sakamoto T, Kano-Murakami Y (1998) Decreased GA1 content caused by the overexpression of OSH1 is accompanied by suppression of GA 20-oxidase gene expression. Plant Physiol 117:1179–1184

    Article  PubMed  CAS  Google Scholar 

  • Leblond J, Sicard A, Delmas FCC, Hernould M (2010) The IMA gene encodes an adapter Mini Zinc Finger protein regulating the development of floral meristem in Tomato. ASPB Plant Biology 2010. http://abstracts.aspb.org/pb2010/public/P04/P04056.html. Accessed 10 August 2010

  • Lenhard M, Jurgens G, Laux T (2002) The WUSCHEL and SHOOTMERISTEMLESS genes fulfil complementary roles in Arabidopsis shoot meristem regulation. Development 129:3195–3206

    PubMed  CAS  Google Scholar 

  • Lin WC, Shuai B, Springer PS (2003) The Arabidopsis LATERAL ORGAN BOUNDARIES-domain gene ASYMMETRIC LEAVES2 functions in the repression of KNOX gene expression and in adaxial-abaxial patterning. Plant Cell 15:2241–2252

    Article  PubMed  CAS  Google Scholar 

  • Lincoln C, Long J, Yamaguchi J, Serikawa K, Hake S (1994) A knotted1-like homeobox gene in Arabidopsis is expressed in the vegetative meristem and dramatically alters leaf morphology when overexpressed in transgenic plants. Plant Cell 6:1859–1876

    Article  PubMed  CAS  Google Scholar 

  • Long JA, Moan EI, Medford JI, Barton MK (1996) A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379:66–69

    Article  PubMed  CAS  Google Scholar 

  • McCallum CM, Comai L, Greene EA, Henikoff S (2000) Targeting induced local lesions IN genomes (TILLING) for plant functional genomics. Plant Physiol 123:439–442

    Article  PubMed  CAS  Google Scholar 

  • McConnell JR, Barton MK (1998) Leaf polarity and meristem formation in Arabidopsis. Development 125:2935–2942

    PubMed  CAS  Google Scholar 

  • Mele G, Ori N, Sato Y, Hake S (2003) The knotted1-like homeobox gene BREVIPEDICELLUS regulates cell differentiation by modulating metabolic pathways. Genes Dev 17:2088–2093

    Article  PubMed  CAS  Google Scholar 

  • Norberg M, Holmlund M, Nilsson O (2005) The BLADE ON PETIOLE genes act redundantly to control the growth and development of lateral organs. Development 132:2203–2213

    Article  PubMed  CAS  Google Scholar 

  • Ori N, Eshed Y, Chuck G, Bowman JL, Hake S (2000) Mechanisms that control knox gene expression in the Arabidopsis shoot. Development 127:5523–5532

    PubMed  CAS  Google Scholar 

  • Sakamoto T, Kamiya N, Ueguchi-Tanaka M, Iwahori S, Matsuoka M (2001) KNOX homeodomain protein directly suppresses the expression of a gibberellin biosynthetic gene in the tobacco shoot apical meristem. Genes Dev 15:581–590

    Article  PubMed  CAS  Google Scholar 

  • Schneeberger R, Tsiantis M, Freeling M, Langdale JA (1998) The rough sheath2 gene negatively regulates homeobox gene expression during maize leaf development. Development 125:2857–2865

    PubMed  CAS  Google Scholar 

  • Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18:1121–1133

    Article  PubMed  CAS  Google Scholar 

  • Semiarti E, Ueno Y, Tsukaya H, Iwakawa H, Machida C, Machida Y (2001) The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana regulates formation of a symmetric lamina, establishment of venation and repression of meristem-related homeobox genes in leaves. Development 128:1771–1783

    PubMed  CAS  Google Scholar 

  • Shpak ED, Lakeman MB, Torii KU (2003) Dominant-negative receptor uncovers redundancy in the Arabidopsis ERECTA Leucine-rich repeat receptor-like kinase signaling pathway that regulates organ shape. Plant Cell 15:1095–1110

    Article  PubMed  CAS  Google Scholar 

  • Sicard A, Petit J, Mouras A, Chevalier C, Hernould M (2008) Meristem activity during flower and ovule development in tomato is controlled by the mini zinc finger gene INHIBITOR OF MERISTEM ACTIVITY. Plant J 55:415–427

    Article  PubMed  CAS  Google Scholar 

  • Sieburth LE, Meyerowitz EM (1997) Molecular dissection of the AGAMOUS control region shows that cis elements for spatial regulation are located intragenically. Plant Cell 9:355–365

    Article  PubMed  CAS  Google Scholar 

  • Siegfried KR, Eshed Y, Baum SF, Otsuga D, Drews GN, Bowman JL (1999) Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126:4117–4128

    PubMed  CAS  Google Scholar 

  • Sinha NR, Williams RE, Hake S (1993) Overexpression of the maize homeo box gene, KNOTTED-1, causes a switch from determinate to indeterminate cell fates. Genes Dev 7:787–795

    Article  PubMed  CAS  Google Scholar 

  • Tamaoki M, Kusaba S, Kano-Murakami Y, Matsuoka M (1997) Ectopic expression of a tobacco homeobox gene, NTH15, dramatically alters leaf morphology and hormone levels in transgenic tobacco. Plant Cell Physiol 38:917–927

    PubMed  CAS  Google Scholar 

  • Tanaka-Ueguchi M, Itoh H, Oyama N, Koshioka M, Matsuoka M (1998) Over-expression of a tobacco homeobox gene, NTH15, decreases the expression of a gibberellin biosynthetic gene encoding GA 20-oxidase. Plant J 15:391–400

    Article  PubMed  CAS  Google Scholar 

  • Theodoris G, Inada N, Freeling M (2003) Conservation and molecular dissection of ROUGH SHEATH2 and ASYMMETRIC LEAVES1 function in leaf development. Proc Natl Acad Sci USA 100:6837–6842

    Article  PubMed  CAS  Google Scholar 

  • Timmermans MC, Hudson A, Becraft PW, Nelson T (1999) ROUGH SHEATH2: a Myb protein that represses knox homeobox genes in maize lateral organ primordia. Science 284:151–153

    Article  PubMed  CAS  Google Scholar 

  • Torii KU, Mitsukawa N, Oosumi T, Matsuura Y, Yokoyama R, Whittier RF, Komeda Y (1996) The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell 8:735–746

    Article  PubMed  CAS  Google Scholar 

  • Tsiantis M, Schneeberger R, Golz JF, Freeling M, Langdale JA (1999) The maize rough sheath2 gene and leaf development programs in monocot and dicot plants. Science 284:154–156

    Article  PubMed  CAS  Google Scholar 

  • Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971

    Article  PubMed  CAS  Google Scholar 

  • Waites R, Selvadurai HR, Oliver IR, Hudson A (1998) The PHANTASTICA gene encodes a MYB transcription factor involved in growth and dorsoventrality of lateral organs in Antirrhinum. Cell 93:779–789

    Article  PubMed  CAS  Google Scholar 

  • Xu L, Shen WH (2008) Polycomb silencing of KNOX genes confines shoot stem cell niches in Arabidopsis. Curr Biol 18:1966–1971

    Article  PubMed  CAS  Google Scholar 

  • Xu L, Xu Y, Dong A, Sun Y, Pi L, Huang H (2003) Novel as1 and as2 defects in leaf adaxial-abaxial polarity reveal the requirement for ASYMMETRIC LEAVES1 and 2 and ERECTA functions in specifying leaf adaxial identity. Development 130:4097–4107

    Article  PubMed  CAS  Google Scholar 

  • Yarbrough JA (1932) Anatomical and developmental studies of the foliar embryos of Bryophyllum calycinum. Am J Bot 19:443–453

    Article  Google Scholar 

  • Zhao D, Ni W, Feng B, Han T, Petrasek MG, Ma H (2003) Members of the Arabidopsis-SKP1-like gene family exhibit a variety of expression patterns and may play diverse roles in Arabidopsis. Plant Physiol 133:203–217

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Nicholas Kaplinsky for providing P STM :GUS seeds with permission from Wolfgang Werr, Lawrence Hobbie for DR5:GUS seeds, Sarah Hake for 35S:BP and bp-9 seeds and Eva Sundberg for LER+ seeds. We are grateful to Jiong Wang for plant care and anonymous reviewers for constructive comments. This work is partly supported by an NSF Plant Genome Grant for the Floral Genome Project (DBI-0115684) and by funds from the Biology Department and the Huck Institutes of the Life Sciences, the Pennsylvania State University. H.M. was also supported by funds from Fudan University.

Author information

Author notes

  1. Wei Hu

    Present address: Department of Molecular and Cellular Biology, University of California, Davis, CA, 95616, USA

  2. Baomin Feng

    Present address: Plant and Microbial Biology Department, University of California, Berkeley, CA, 94720, USA

Authors and Affiliations

  1. Department of Biology, Huck Institutes of the Life Sciences, Pennsylvania State University, 405D Life Sciences Building, University Park, PA, 16802, USA

    Wei Hu, Baomin Feng & Hong Ma

  2. State Key Laboratory of Genetic Engineering, Institute of Plant Biology, Center for Evolutionary Biology, School of Life Sciences, Fudan University, Shanghai, 200433, China

    Hong Ma

  3. Institutes of Biomedical Sciences, Fudan University, Shanghai, 200032, China

    Hong Ma

Authors
  1. Wei Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Baomin Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hong Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hong Ma.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1

35S:MIF1/bp-9 plant develops ectopic meristems along leaf margins. (A) the whole plant grown for 56 days under long-day conditions with one ectopic meristem being highlighted. (B) close-up view of the ectopic meristem from (A). Bars, A = 10 mm, B = 0.5 mm (JPEG 421 kb)

Fig. S2

A 49d-old 35S:MIF3/LER+ plant used for collecting leaf blades with visible ectopic meristems for RT-PCR. Arrows indicate ectopic meristems along leaf margins (JPEG 530 kb)

Fig. S3

Plantlet outgrowth from leaf margins of a species of Kalanchoe. (A) The whole plant. (B) Many plantlets outgrow from the sinuses of leaf margins. (C) Close-up view of leaf margin, the arrow indicates a downward-pointing protrusion from the sinus that is developing a tiny plantlet at its tip (JPEG 234 kb)

Fig. S4

Marginal serration pattern of late rosette leaves from the Col, Ler and LER+ accessions (JPEG 199 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hu, W., Feng, B. & Ma, H. Ectopic expression of the Arabidopsis MINI ZINC FINGER1 and MIF3 genes induces shoot meristems on leaf margins. Plant Mol Biol 76, 57–68 (2011). https://doi.org/10.1007/s11103-011-9768-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-011-9768-y

Keywords

Search

Navigation