Skip to main content
SpringerLink
Log in

Axial Patterning of the Maize Leaf

  • Chapter
Handbook of Maize: Its Biology

Abstract

The characteristic morphology and anatomy of the maize leaf reflects the outcome of developmental patterning along three axes, proximodistal, mediolateral, and adaxial-abaxial, which are specified relative to the main axis of the plant. The past decade has seen a dramatic increase in our understanding of the genetic control of leaf development. Gene regulatory networks involved in the specification of organ polarity are beginning to emerge. These are distinguished by contributions of highly conserved, often redundant transcription factor families whose expression or activity are modulated to give rise to the distinctive maize leaf. Small regulatory RNAs, hormones, as well as proteins that selectively trafficking between cells have emerged as candidate signals conveying positional information within the shoot to the newly initiated leaf. This chapter outlines findings of both classical genetic and recent molecular studies that have led to a framework for axial patterning of the maize leaf.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adenot, X., Elmayan, T., Lauressergues, D., Boutet, S., Bouche, N., Gasciolli, V., and Vaucheret, H. (2006). DRB4-dependent TAS3 trans-acting siRNAs control leaf morphology through AGO7 . Current Biology 16, 927–932.

    Article  CAS  PubMed  Google Scholar 

  • Alexander, D.L., Mellor, E.A., and Langdale, J.A. (2005). CORKSCREW1 defines a novel mechanism of domain specification in the maize shoot . Plant Physiology 138, 1396–1408.

    Article  CAS  PubMed  Google Scholar 

  • Allen, E., Xie, Z., Gustafson, A.M., and Carrington, J.C. (2005). microRNA-directed phasing during trans-acting siRNA biogenesis in plants . Cell 121, 207–221.

    Article  CAS  PubMed  Google Scholar 

  • Becraft, P., and Freeling, M. (1991). Sectors of liguleless-1 tissue interrupt an inductive signal during maize leaf develeopment . The Plant Cell 3, 801–807.

    Article  CAS  PubMed  Google Scholar 

  • Becraft, P., and Freeling, M. (1994). Genetic analysis of Rough sheath-1 developmental mutants of maize. Genetics 136, 295–311.

    CAS  PubMed  Google Scholar 

  • Becraft, P., Bongard-Pierce, D., Sylvester, A.W., Poethig, R.S., and Freeling, M. (1990). The liguleless-1 gene acts tissue specifically in maize leaf development . Developmental Biology 141, 220–232.

    Article  CAS  PubMed  Google Scholar 

  • Brink, R.A. (1933). Heritable characters in maize XLVI - Liguleless2. Journal of Heredity 24 325–326.

    Google Scholar 

  • Candela, H., Johnston, R., Gerhold, A., Foster, T., and Hake, S. (2008) . The milkweed pod1 gene encodes a KANADI protein that is required for abaxial-adaxial patterning in maize.

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Emerson, R.A. (1912). The inheritance of the ligule and auricles of corn leaves. Nebraska Agricultural Experimental Station Annual Report 25, 81–88.

    Google Scholar 

  • Emery, J., Floyd, S., Alvarez, J., Eshed, Y., Hawker, N., Izhaki, A., Baum, S., and Bowman, J. (2003). Radial patterning of Arabidopsis shoots by Class III HD-ZIP and KANADI genes. Current Biology 13, 1768–1774.

    Article  CAS  PubMed  Google Scholar 

  • Esau, K. (1965). Vascular Differentiation in Plants (New York: Holt, Rinehart and Winston).

    Google Scholar 

  • Evans, M.M.S. (2007). The indeterminate gametophyte1 gene of maize encodes a LOB domain protein required for embryo sac and leaf development . Plant Cell 19, 46–62.

    Article  CAS  PubMed  Google Scholar 

  • Foster, T., Veit, B., and Hake, S. (1999a). Mosaic analysis of the dominant mutant, Gnarley1-R, reveals distinct lateral and transverse signaling pathways during maize leaf development . Development 126, 305–313.

    CAS  Google Scholar 

  • Foster, T., Yamaguchi, J., Wong, B.C., Veit, B., and Hake, S. (1999b). Gnarley1 is a dominant mutation in the knox4 homeobox gene affecting cell shape and identity . Plant Cell 11 1239–1252.

    Article  CAS  Google Scholar 

  • Foster, T., Hay, A., Johnston, R., and Hake, S. (2004). The establishment of axial patterning in the maize leaf. Develoment 131, 3921–3929.

    CAS  Google Scholar 

  • Fowler John, E., and Freeling, M. (1996). Genetic analysis of mutations that alter cell fates in maize leaves: dominant Liguleless mutations. Developmental Genetics 18, 198–222.

    Article  Google Scholar 

  • Freeling, M. (1992). A conceptual framework for maize leaf development. Developmental Biology 153, 44–58.

    Article  CAS  PubMed  Google Scholar 

  • Hake, S., and Freeling, M. (1986). Analysis of genetic mosaics shows that the extra epidermal cell divisions in Knotted mutant maize plants are induced by adjacent mesophyll cells . Nature 320, 621–623.

    Article  Google Scholar 

  • Harper, L., and Freeling, M. (1996). Interactions of liguleless1 and liguleless2 function during ligule induction in maize . Genetics 144, 1871–1882.

    CAS  PubMed  Google Scholar 

  • Hay, A., and Hake, S. (2004). The dominant mutant Wavy auricle in blade disrupts patterning in a lateral domain of the maize leaf . Plant Physiology 135, 300–308.

    Article  CAS  PubMed  Google Scholar 

  • Henderson, D.C., Muehlbauer, G.J., and Scanlon, M.J. (2005). Radial leaves of the maize mutant ragged seedling2 retain dorsiventral anatomy . Developmental Biology 282, 455–466.

    Article  CAS  PubMed  Google Scholar 

  • Henderson, D.C., Zhang, X., Brooks III, L., and Scanlon, M.J. (2006). RAGGED SEEDLING2 is required for expression of KANADI2 and REVOLUTA homologues in the maize shoot apex . Genesis 44, 372–382.

    Article  CAS  PubMed  Google Scholar 

  • Hunter, C., Willmann, M.R., Wu, G., Yoshikawa, M., de la Luz Gutierrez-Nava, M., and Poethig, S.R. (2006). Trans-acting siRNA-mediated repression of ETTIN and ARF4 regulates heteroblasty in Arabidopsis Development 133, 2973–2981

    Article  CAS  PubMed  Google Scholar 

  • Jackson D., Veit, B., and Hake, S. (1994). Expression of maize knotted1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot . Development 120, 405–413.

    CAS  Google Scholar 

  • Jones-Rhoades, M.W., Bartel, D.P., and Bartel, B. (2006). MicroRNAs and their regulatory roles in plants. Annual Review of Plant Biology 57, 19–53.

    Article  CAS  PubMed  Google Scholar 

  • Juarez, M.T., Twigg, R.W., and Timmermans, M.C.P. (2004a). Specification of adaxial cell fate during maize leaf development . Development 131, 4533–4544.

    Article  CAS  Google Scholar 

  • Juarez, M.T., Kui, J.S., Thomas, J., Heller, B.A., and Timmermans, M.C.P. (2004b). microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity . Nature 428, 84–88.

    Article  CAS  Google Scholar 

  • Kaplan, D.R. (1973). The monocotyledons: their evolution and comparative biology. VII. The problem of leaf morphology and evolution in the monocotyledons. Quarterly Reveiw of Biology 48, 437–457.

    Article  Google Scholar 

  • Kerstetter , R.A. , Laudencia-Chingcuanco , D. , Smith , L.G. , and Hake , S. (1997) . Loss-of-function mutations in the maize homeobox gene, knotted1, are defective in shoot meristem maintenance . Development 124, 3045–3054.

    CAS  PubMed  Google Scholar 

  • Kerstetter, R., Bollman, K., Taylor, R., Bomblies, K., and Poethig, R. (2001). KANADI regulates organ polarity in Arabdopsis. Nature 411, 706–709.

    Article  CAS  PubMed  Google Scholar 

  • Kidner, C.A., and Timmermans, M.C.P. (2007). Mixing and matching pathways in leaf polarity. Current Opinion in Plant Biology 10, 13–20.

    Article  PubMed  Google Scholar 

  • Kim, J.Y., Yuan, Z., Cilia, M., Khalfan-Jagani, Z., and Jackson, D. (2002). Intercellular trafficking of a KNOTTED1 green fluorescent protein fusion in the leaf and shoot meristem of Arabidopsis. Proceedings of the National Academy of Sciences 99, 4103–4108.

    Article  CAS  Google Scholar 

  • Langdale, J., Lane, B., Freeling, M., and Nelson, T. (1989). Cell lineage analysis of maize bundle sheath and mesophyll cells . Developmental Biology 133, 128–139.

    Article  CAS  PubMed  Google Scholar 

  • Lin, W.-c., Shuai, B., and Springer, P.S. (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  CAS  PubMed  Google Scholar 

  • Long, J.A., Moan, E.I., Medford, J.I., and Barton, M.K. (1996). A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379, 66–69.

    Article  CAS  PubMed  Google Scholar 

  • Lucas, W.J., Bouchepillon, S., Jackson, D.P., Nguyen, L., Baker, L., Ding, B., and Hake, S. (1995). Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 270, 1980–1983.

    Article  CAS  PubMed  Google Scholar 

  • McConnell, J.R., Emery, J, Eshed, Y., Bao, N., Bowman, J., and Barton, K.M. (2001). Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots . Nature 411, 709 – 712 .

    Article  CAS  PubMed  Google Scholar 

  • McDaniel, C.N., and Poethig, R.S. (1988). Cell-lineage patterns in the shoot apical meristem of the germinating maize embryo . Planta 175, 13–22.

    Article  Google Scholar 

  • Moreno, M., Harper, L., Krueger, R., Dellaporta, S., and Freeling, M. (1997). liguleless1 encodes a nuclear-localized protein required for induction of ligules and auricles during maize leaf organogenesis. Genes & Development 11, 616–628.

    Article  CAS  Google Scholar 

  • Muehlbauer, G.J., Fowler, J.E., and Freeling, M. (1997). Sectors expressing the homeobox gene liguleless3 implicate a time-dependent mechanism for cell fate acquisition along the proximaldistal axis of the maize leaf . Development 124, 5097–5106.

    CAS  PubMed  Google Scholar 

  • Muehlbauer, G.J., Fowler, J.E., Girard, L., Tyers, R., Harper, L., and Freeling , M. (1999) . Ectopic expression of the maize homeobox gene Liguleless3 alters cell fates in the leaf . Plant Physiology (Rockville) 119, 651–662.

    Article  CAS  Google Scholar 

  • Nardmann, J., Ji, J., Werr, W., and Scanlon, M.J. (2004). The maize duplicate genes narrow sheath1 and narrow sheath2 encode a conserved homeobox gene function in a lateral domain of shoot apical meristems . Development 131, 2827–2839.

    Article  CAS  PubMed  Google Scholar 

  • Nelson, J., Lane, B., and Freeling, M. (2002). Expression of a mutant gene in the ventral leaf epidermis is sufficient to signal a switch of the leaf's dorsoventral axis . Development 129, 4581–4589.

    CAS  PubMed  Google Scholar 

  • Nogueira, F.T.S., Madi, S., Chitwood, D.H., Juarez, M.T., and Timmermans, M.C.P. (2007). Two small regulatory RNAs establish opposing fates of a developmental axis . Genes & Development 21, 750–755.

    Article  CAS  Google Scholar 

  • Osmont, K.S., Jesaitis, L.A., and Freeling, M. (2003). The extended auricle1 (eta1 ) gene is essential for the genetic network controlling postinitiation during maize leaf development . Genetics 165, 1507–1519.

    CAS  PubMed  Google Scholar 

  • Parkinson, S.E., Gross, S.M., and Hollick, J.B. (2007). Maize sex determination and abaxial leaf fates are canalized by a factor that maintains repressed epigenetic states . Developmental Biology 308, 462–473.

    Article  CAS  PubMed  Google Scholar 

  • Pekker, I., Alvarez, J.P., and Eshed, Y. (2005). Auxin Response Factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity . Plant Cell 17, 2899–2910.

    Article  CAS  PubMed  Google Scholar 

  • Peragine, A., Yoshikawa, M., Wu, G., Albrecht, H.L., and Poethig, R.S. (2004). SGS3 and SGS2/ SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes & Development 18, 2368–2379.

    Article  CAS  Google Scholar 

  • Phelps-Durr, T.L., Thomas, J., Vahab, P., and Timmermans, M.C.P. (2005). Maize rough sheath2 and its Arabidopsis orthologue ASYMMETRIC LEAVES1 interact with HIRA, a predicted histone chaperone, to maintain knox gene silencing and determinacy during organogenesis . The Plant Cell 17, 2886–2898.

    Article  CAS  PubMed  Google Scholar 

  • Poethig, R.S. (1984). Cellular parameters of leaf morphogenesis in maize and tobacco. In Contemporary Problems in Plant Anatomy, ed. by R.A. White and W.C. Dickison Orlando: Academic Press.

    Google Scholar 

  • Poethig, R.S. (1987). Clonal analysis of cell lineage patterns in plant development. American Journal of Botany 74, 581–594.

    Article  Google Scholar 

  • Poethig, R.S., and Szymkowiak, E.J. (1995). Clonal analysis of leaf development in maize. Maydica 40, 67–76.

    Google Scholar 

  • Pontig, C., and Aravind, L. (1999). START: a lipid-binding domain in StAR, HD-ZIP and signalling proteins. Trends in Biochemical Science 24, 130–132.

    Article  Google Scholar 

  • Reinhardt, D., Mandel, T., and Kuhlemeier, C. (2000). Auxin regulates the initiation and radial position of plant lateral organs . Plant Cell 12, 507–518.

    Article  CAS  PubMed  Google Scholar 

  • Reinhardt, D., Pesce, E.-R., Stieger, P., Mandel, T., Baltensperger, K., Bennett, M., Traas, J., Friml, J., and Kuhlemeier, C. (2003). Regulation of phyllotaxis by polar auxin transport. Nature 426, 255–260.

    Article  CAS  PubMed  Google Scholar 

  • Rhoades, M., Reinhart, B., Lim, L., Burge, C., Bartel, B., and Bartel, D. (2002). Prediction of plant microRNA targets . Cell 110, 513–520.

    Article  CAS  PubMed  Google Scholar 

  • Sachs, T. (1969). Regeneration experiments on the determination of the form of leaves. Israel Journal of Botany 18, 21–30.

    Google Scholar 

  • Scanlon, M.J. (2000). NARROW SHEATH1 functions from two meristematic foci during founder-cell recruitment in maize leaf development . Development 127, 4573–4585.

    CAS  PubMed  Google Scholar 

  • Scanlon, M.J. (2003). The polar auxin transport inhibitor N-1-Naphthylphthalamic acid disrupts leaf initiation, KNOX protein regulation, and formation of leaf margins in maize . Plant Physiology 133, 597–605.

    Article  CAS  PubMed  Google Scholar 

  • Scanlon, M.J., and Freeling, M. (1997). Clonal sectors reveal that a specific meristematic domain is not utilized in the maize mutant narrow sheath . Developmental Biology 182, 52–66.

    Article  CAS  PubMed  Google Scholar 

  • Scanlon, M.J., Schneeberger, R.G., and Freeling, M. (1996). The maize mutant narrow sheath fails to establish leaf margin identity in a meristematic domain . Development 122, 1683–1691.

    CAS  PubMed  Google Scholar 

  • Scanlon, M.J., Henderson, D.C., and Bernstein, B. (2002). SEMAPHORE1 functions during the regulation of ancestrally duplicated knox genes and polar auxin transport in maize . Development 129, 2663–2673.

    CAS  PubMed  Google Scholar 

  • Schichnes, D.E., and Freeling, M. (1998). Lax midrib1-O , a systemic, heterochronic mutant of maize. American Journal of Botany 85, 481–491.

    Article  Google Scholar 

  • Schneeberger, R.G., Becraft, P.W., Hake, S., and Freeling, M. (1995). Ectopic expression of the knox homeobox gene rough sheath1 alters cell fate in the maize leaf . Genes & Development 9 2292–2304.

    Article  CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Sessa, G., Steindler, C., Morelli, G., and Ruberti, I. (1998). The Arabidopsis Athb-8, -9 and -14 genes are members of a small gene family coding for highly related HD-ZIP 1proteins . Plant Molecular Biology 38, 609–622.

    Article  CAS  PubMed  Google Scholar 

  • Sharman, B.C. (1942). Developmental anatomy of the shoot of Zea mays L. Annals of Botany 6 245–284.

    Google Scholar 

  • Sinha, N., Williams, R., and Hake, S. (1993). Overexpression of the maize homeobox gene, KNOTTED-1 , causes a switch from determinate to indeterminate cell fates . Genes & Development 7, 787–795.

    Article  CAS  Google Scholar 

  • Sinha, N.R., and Hake, S. (1990). Mutant characters of Knotted maize leaves are determined in the innermost tissue layers . Developmental Biology 141, 203–210.

    Article  CAS  PubMed  Google Scholar 

  • Smith, L., Jackson, D., and Hake, S. (1995). Expression of knotted1 marks shoot meristem formation during maize embryogenesis . Developmental Genetics 16, 344–348.

    Article  Google Scholar 

  • Smith, L.G., Greene, B., Veit, B., and Hake, S. (1992). A dominant mutation in the maize homeobox gene, Knotted-1 , causes its ectopic expression in leaf cells with altered fates . Development 116, 21–30.

    CAS  PubMed  Google Scholar 

  • Steffensen, D.M. (1968). A reconstruction of cell development in the shoot apex of maize. American Journal of Botany 55, 354–369.

    Article  Google Scholar 

  • Sussex, I.M. (1954). Experiments on the cause of dorsiventrality in leaves. Nature 174, 351–352.

    Article  Google Scholar 

  • Sylvester, A.W., Cande, W.Z., and Freeling, M. (1990). Division and Differentiation during normal and liguleless-1 maize leaf development . Development 110, 985–1000.

    CAS  PubMed  Google Scholar 

  • Timmermans, M., Schultes, N., Jankovsky, J., and Nelson, T. (1998). Leafbladeless1 is required for dorsoventrality of lateral organs in maize . Development 125, 2813–2823.

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Troll, W. (1955). Concerning the morphological significance of the so-called vorlauferspitze of monocot leaves. Beitraege Biologie Pflanzen 31, 525–558.

    Google Scholar 

  • Tsiantis, M., Brown, M.I.N., Skibinski, G., and Langdale, J.A. (1999a). Disruption of auxin transport is associated with aberrant leaf development in maize. Plant Physiology 121, 1163–1168.

    Article  CAS  Google Scholar 

  • Tsiantis, M., Schneeberger, R., Golz John, F., Freeling, M., and Langdale Jane, A. (1999b). The maize rough sheath2 gene and leaf development programs in monocot and dicot plants . Science 284, 154–156.

    Article  CAS  Google Scholar 

  • Waites, R., and Hudson, A. (1995). phantastica : a gene required for dorsoventrality of leaves in Antirrhinum majus. Development 121, 2143–2154.

    CAS  Google Scholar 

  • Walsh, J., Waters, C., and Freeling, M. (1997). The maize gene liguleless2 encodes a basic leucine zipper protein involved in the establishment of the leaf blade-sheath boundary . Genes & Development 11, 208–218.

    Google Scholar 

  • Williams, L., Carles, C.C., Osmont, K.S., and Fletcher, J.C. (2005). A database analysis method identifies an endogenous trans-acting short-interfering RNA that targets the Arabidopsis ARF2, ARF3, and ARF4 genes. Proceedings of the National Academy of Sciences 102, 9703–9708.

    Article  CAS  Google Scholar 

  • Xie, Z., Allen, E., Wilken, A., and Carrington, J.C. (2005). DICER-LIKE 4 functions in transacting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana. Proceedings of the National Academy of Sciences 102, 12984–12989.

    Article  CAS  Google Scholar 

  • Xu, L., Xu, Y., Dong, A., Sun, Y., Pi, L., Xu, Y., and 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  CAS  PubMed  Google Scholar 

  • Yoshikawa, M., Peragine, A., Park, M.Y., and Poethig, R.S. (2005). A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes & Development 19, 2164–2175.

    Article  CAS  Google Scholar 

  • Zhang, X., Madi, S., Borsuk, L., Nettleton, D., Elshire, R., Buckner, B., Janick-Buckner, D., Beck, J., Timmermans, M., Schnable, P., and Scanlon, M. (2007). Laser microdissection of narrow sheath mutant maize uncovers novel gene expression in the shoot apical meristem . PLoS Genetics 3, 1040–1052.

    Article  CAS  Google Scholar 

Download references

Authors
  1. Toshi M. Foster
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marja C. P. Timmermans
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Genetics, University of Georgia, Athens, GA, USA

    Jeff L. Bennetzen

  2. Berkeley USDA Plant Gene Expression Center, University of California, 800 Buchanan Street, Albany, CA, USA

    Sarah C. Hake

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer Science + Business Media, LLC

About this chapter

Cite this chapter

Foster, T.M., Timmermans, M.C.P. (2009). Axial Patterning of the Maize Leaf. In: Bennetzen, J.L., Hake, S.C. (eds) Handbook of Maize: Its Biology. Springer, New York, NY. https://doi.org/10.1007/978-0-387-79418-1_9

Download citation

Publish with us

Policies and ethics

Search

Navigation