Genetic Control of Leaf Shape

Ciera C Martinez, University of California, Davis, California, USA
Neelima R Sinha, University of California, Davis, California, USA

Published online: September 2013

DOI: 10.1002/9780470015902.a0020101.pub2

Abstract

The variability in leaf morphology is vast; therefore, an understanding of how leaves achieve this diversity has captured the attention of many developmental biologists. Genetic mechanisms that regulate leaf shape are repeated throughout both development and between species. Leaves initiate off the shoot apical meristem and development proceeds from cell division to cell elongation. Leaf initiation and the establishment of the three main axes of a leaf are largely directed by the plant hormone auxin. Work across species reveals that adjustments to the repeated interaction of auxin, gene expression changes and small ribonucleic acid (RNA) regulation allowed species‐specific leaf shape differences to emerge. Further, genetic interactions leading to patterning in simple leaf development are reiterated during establishment of leaf complexity. To understand leaf development in an evolutionary context, future research must take advantage of the ever‐expanding genomic tools in nonmodel organisms that exhibit leaf shape diversity.

Key Concepts:

  • Leaves originate from clusters of stem cells called meristems.

  • The development of leaves occurs along three main axes: (1) adaxial/abaxial, (2) proximal/distal and (3) medial/lateral.

  • The development of both meristems and leaves involve morphogenetic activity in zones which are defined by distinct gene expression and cell division/elongation patterns.

  • The transport and concentration of the hormone auxin largely directs many aspects of leaf morphogenesis.

  • Leaf and leaflet initiation first begin with the formation of auxin maxima.

  • Recycling of genetic mechanisms is a theme that occurs throughout leaf development.

Keywords: abaxial; adaxial; HDZIPIII ; KANADI ; leaf; marginal blastozone; miRNA; polarity; PIN‐FORMED ; YABBY

Figure 1.

Leaf development zones and cell division patterns. (a) Schematic of a shoot displaying the three major leaf axes and location of meristems (grey). (b) Three domains of the meristem: central zone (CZ, pink), peripheral zone (PZ, green) and rib zone (RZ, orange). Schematic of meristem domains, L1 (grey), L2 (blue), L3 (yellow). The first leaf to initiate is Primordia 1(P1), second is P2 and the site of the next leaf initiation is I1 (dotted circle). (c) Only anticlinal cell divisions (red dotted line) occur on the L1 and L2 layers, both types anticlinal and periclinal (purple dotted line) occur in L3. (d) Gradients of cell division to differentiation from primary morphogenesis (1° Morph) (dark blue) to 2° Morph (white) on a dicot leaf (simple and complex) and on a monocot leaf (maize); * indicates leaflets on a complex leaf.
Figure 2.

Gene expression and auxin patterning on apices of a species making complex leaves. (a) and (b) Schematic of the gene expression of KNOX1 (yellow hatched) and CUC/NAM (red). Auxin concentration and auxin transport pathways (blue), darker shade shows higher auxin concentration and lighter lower auxin concentration. (c) and (d) Auxin localisation patterns from auxin‐responsive reporter, DR5::Venus (Heisler et al., ) in tomato on the (c) adaxial side of a P4 leaf and an (d) apex containing I1, P1 and P2.
Figure 3.

Adaxial and abaxial identity at the cellular level in most species and on radialised leaf structures. (a) Schematic of a cross‐section through a mature dicot leaf. Adaxial tissues, adaxial epidermis (dE) and palisade mesophyll (PM), are light blue and xylem (Xy, blue) is present on the adaxial side of a vascular bundle. Abaxial tissue structures, abaxial epidermis (bE) and spongy mesophyll (SM), are pink and the abaxial side of the vascular bundle is the phloem (Ph, red). (b) In many dicot species, the defining characteristic of the central vascular bundle in a leaf is Xy in the adaxial position and Ph in the abaxial position. Leaves that have completely lost abaxial identity are radial (no blade outgrowth) and have a central vascular bundle consisting of only Xy surrounded by adaxial tissue. Leaves with complete loss of adaxial identity are radial and only Ph surrounded by abaxial tissue.
Figure 4.

Genetic regulation of abaxial and adaxial cell fate determination and maintenance. (a) Adaxially localised HD‐ZIPIIIs (REV, PHV and PHB) have an indirect (dotted lines) antagonistic relationship with abaxial localised KANDI genes. REV, PHV, PHB are further downregulated by the abaxial localised miR165/6. KANADI gene also has a direct (solid line) antagonistic relationship with AS2 which interacts with AS1 to form a protein complex. (b) miR390, along with AGO7, TAS3 and SGS3, is required for ta‐siARF biogenesis. ta‐siARFs directly repress ARF3 (an abaxial determinant) in the adaxial domain. (c) ta‐siARFs biogenesis is localised to the adaxial side by adaxial localisation of ta‐siARF biogenesis components TAS3 (orange) and AGO7 (red) in Arabidopsis and miR390 in maize.
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References

Aida M , Ishida T and Tasaka M (1999) Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP‐SHAPED COTYLEDON and SHOOT MERISTEMLESS genes. Development 126: 1563–1570.

Aida M , Vernoux T , Furutani M , Traas J and Tasaka M (2002) Roles of PIN‐FORMED1 and MONOPTEROS in pattern formation of the apical region of the Arabidopsis embryo. Development 129: 3965–3974.

Allen E , Xie Z , Gustafson AM and Carrington JC (2005) microRNA‐directed phasing during trans‐acting siRNA biogenesis in plants. Cell 121: 207–221.

Barkoulas M , Hay A , Kougioumoutzi E and Tsiantis M (2008) A developmental framework for dissected leaf formation in the Arabidopsis relative Cardamine hirsuta. Nature Genetics 40: 1136–1141.

Barton MK and Poethig RS (1993) Formation of the shoot apical meristem in Arabidopsis thaliana: an analysis of development in the wild type and in the shoot meristemless mutant. Development 119: 823–831.

Beerling DJ and Fleming AJ (2007) Zimmermann's telome theory of megaphyll leaf evolution: a molecular and cellular critique. Current Opinion in Plant Biology 10: 4–12.

Benková E , Michniewicz M , Sauer M et al. (2003) Local, efflux‐dependent auxin gradients as a common module for plant organ formation. Cell 115: 591–602.

Blein T , Pulido A , Vialette‐Guiraud A et al. (2008) A conserved molecular framework for compound leaf development. Science 322: 1835–1839.

Byrne ME , Barley R , Curtis M et al. (2000) Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis . Nature 408: 967–971.

Chapman EJ and Carrington JC (2007) Specialization and evolution of endogenous small RNA pathways. Nature Reviews Genetics 8: 884–896.

Chitwood DH , Headland LR , Ranjan A et al. (2012) Leaf asymmetry as a developmental constraint imposed by auxin‐dependent phyllotactic patterning. Plant Cell 24: 2318–2327.

Chitwood DH , Nogueira FT , Howell MD et al. (2009) Pattern formation via small RNA mobility. Genes and Development 23: 549–554.

Emery JF , Floyd SK , Alvarez J et al. (2003) Radial patterning of Arabidopsis shoots by Class III HD‐ZIP and KANADI genes. Current Biology 13: 1768–1774.

Eshed Y , Izhaki A , Baum SF , Floyd SK and Bowman JL (2004) Asymmetric leaf development and blade expansion in Arabidopsis are mediated by KANADI and YABBY activities. Development 131: 2997–3006.

Floyd SK and Bowman JL (2010) Gene expression patterns in seed plant shoot meristems and leaves: homoplasy or homology? Journal of Plant Research 123: 43–55.

Friml J , Vieten A , Sauer M et al. (2003) Efflux‐dependent auxin gradients establish the apical–basal axis of Arabidopsis . Nature 426: 147–153.

Guilfoyle TJ and Hagen G (2007) Auxin response factors. Current Opinion in Plant Biology 10: 453–460.

Guo M , Thomas J , Collins G and Timmermans MC (2008) Direct repression of KNOX loci by the ASYMMETRIC LEAVES1 complex of Arabidopsis . Plant Cell 20: 48–58.

Hagemann W and Gleissberg S (1996) Organogenetic capacity of leaves: the significance of marginal blastozones in angiosperms. Plant Systematics and Evolution 199: 121–152.

Hay A and Tsiantis M (2006) The genetic basis for differences in leaf form between Arabidopsis thaliana and its wild relative Cardamine hirsuta . Nature Genetics 38: 942–947.

Heisler MG , Ohno C , Das P et al. (2005) Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Current Biology 15: 1899–1911.

Itoh J , Hibara K , Sato Y and Nagato Y (2008) Developmental role and auxin responsiveness of Class III homeodomain leucine zipper gene family members in rice. Plant Physiology 147: 1960–1975.

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 102: 405–413.

Juarez M , Twigg R and Timmermans M (2004) Specification of adaxial fate during maize leaf development. Development 131: 4533–4544.

Kerstetter RA , Bollman K , Taylor RA , Bomblies K and Poethig S (2001) KANADI regulates organ polarity in Arabidopsis . Nature 411: 706–709.

Kim M , McCormick S , Timmermans M and Sinha N (2003) The expression domain of PHANTASTICA determines leaflet placement in compound leaves. Nature 424: 438–443.

Koenig D , Bayer E , Kang J , Kuhlemeier C and Sinha N (2009) Auxin patterns Solanum lycopersicum leaf morphogenesis. Development 136: 2997–3006.

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

Lodha M , Marco CF and Timmermans MC (2013) The ASYMMETRIC LEAVES complex maintains repression of KNOX homeobox genes via direct recruitment of Polycomb‐repressive complex2. Genes and Development 27: 596–601.

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

Mallory AC , Reinhart BJ , Jones‐Rhoades MW et al. (2004) MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5′ region. EMBO Journal 23: 3356–3364.

McConnell JR , Emery J , Eshed Y et al. (2001) Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411: 709–713.

Moon J and Hake S (2011) How a leaf gets its shape. Current Opinion in Plant Biology 14: 24–30.

Nicotra AB , Leigh A , Boyce CK et al. (2011) The evolution and functional significance of leaf shape in the angiosperms. Functional Plant Biology 38: 535.

Nogueira FT , Chitwood DH , Madi S et al. (2009) Regulation of small RNA accumulation in the maize shoot apex. PLoS Genetics 5: e1000320.

Nogueira FT , Madi S , Chitwood DH , Juarez MT and Timmermans MC (2007) Two small regulatory RNAs establish opposing fates of a developmental axis. Genes and Development 21: 750–755.

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

Pekker I , Alvarez JP and Eshed Y (2005) Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 17: 2899–2910.

Reinhardt D , Frenz M , Mandel T and Kuhlemeier C (2005) Microsurgical and laser ablation analysis of leaf positioning and dorsoventral patterning in tomato. Development 132: 15–26.

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

Reinhardt D , Pesce E‐R , Stieger P et al. (2003) Regulation of phyllotaxis by polar auxin transport. Nature 426: 255–260.

Scarpella E , Marcos D , Friml J and Bereth T (2006) Control of leaf vascular patterning by polar auxin transport. Genes and Development 20: 1015–1027.

Steeves TA and Sussex IM (1989) Patterns in Plant Development. Cambridge: Cambridge University Press.

Sussex IM (1951) Experiments on the cause of dorsiventrality in leaves. Nature 167: 651–652.

Timmermans MCP (1999) ROUGH SHEATH2: a Myb protein that represses knox homeobox genes in maize lateral organ primordia. Science 284: 151–153.

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

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

Williams L , Grigg SP , Xie M , Christensen S and Fletcher JC (2005) Regulation of Arabidopsis shoot apical meristem and lateral organ formation by microRNA miR166g and its AtHD‐ZIP target genes. Development 132: 3657–3668.

Xu L , Xu Y , Dong A et al. (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.

Xu L , Yang L , Pi L et al. (2006) Genetic interaction between the AS1‐AS2 and RDR6‐SGS3‐AGO7 pathways for leaf morphogenesis. Plant and Cell Physiology 47: 853–863.

Yadav RK , Girke T , Pasala S , Xie M and Reddy GV (2009) Gene expression map of the Arabidopsis shoot apical meristem stem cell niche. Proceedings of the National Academy of Sciences of the USA 106: 4941–4946.

Further Reading

Husbands AY , Chitwood DH , Plavskin Y and Timmermans MCP (2009) Signals and prepatterns: new insights into organ polarity in plants. Genes and Development 23: 1986–1997.

Koenig D and Sinha N (2010) Evolution of leaf shape: a pattern emerges. Current Topics in Developmental Biology 91: 169–183.

Moon J and Hake S (2011) How a leaf gets its shape. Current Opinion in Plant Biology 14: 24–30.

Scarpella E and Berleth T (2013) Auxin transport and signaling in leaf vascular patterning. In: Chen R and Baluska F (eds) Polar Auxin Transport, pp 129–154. Berlin, Heidelberg: Springer.

Related Sub-Topics:

Leaves | Genes, Molecules and Cellular Processes | Plant Development | Plant Evolution | Plant Genetics and Molecular Biology
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Article Title: Genetic Control of Leaf Shape
 
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Martinez, Ciera C, and Sinha, Neelima R(Sep 2013) Genetic Control of Leaf Shape. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020101.pub2]