Shoot apical meristem Leaf primordia First, cells have to acquire a new identity as “leaf” rather than meristem Next the leaf has to acquire polarity:

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Shoot apical meristem Leaf primordia First, cells have to acquire a new identity as “leaf” rather than meristem Next the leaf has to acquire polarity: outer vs inner surfaces Growth involves regulated patterns of cell division and cell expansion..... and the differentiation of specialized cells Genetic control of leaf development Poethig, R.S. and Sussex,I.M. (1985) The developmental morphology and growth dynamics of the tobacco leaf. Planta 165: ; Reprinted by permission from Macmillan Publishers, Ltd: Runions, J. (2003) Cell of the Month. Nat. Rev. Mol. Cell Biol. 4: 603; Nadeau JA, Sack FD (2002) Stomatal Development in Arabidopsis: September 30, The Arabidopsis Book. Rockville, MD: ASPB ; 603Stomatal Development in Arabidopsis

Development involves positional information …. directed movement of a signal through asymmetric distribution of transport proteins (e.g. auxin movement and therefore auxin gradients are regulated by auxin transporters) … movement of a signal away from a source (e.g. signals produced by the meristem or certain differentiated cells) … selective destruction of a signal (e.g. by miRNA cleavage of mRNAs) Positional information can arise from…

Development involves boundaries A soft edge formed by a gradient can be reinforced into a hard edge by mutual antagonism If one effect of “red” is to eliminate “yellow”, and vice versa, then a hard edge or boundary forms and is maintained Shoot apical meristem Boundaries form between the shoot apical meristem and leaf primordia, and between the upper and lower surfaces of the leaf Patterning of cells in the epidermis also involves production of inhibitory signals

Development involves regulatory switches, often transcription factors Once developmental domains are established, transcription factors regulate growth and differentiation 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; Tsiantis, M., Schneeberger, R., Golz, J.F., Freeling, M. and Langdale, J.A. (1999). The maize rough sheath2 gene and leaf development programs in monocot and dicot plants. Science. 284: Reproduced with permission; Szymanski, D.B., Jilk, R.A., Pollock, S.M. and Marks, M.D. (1998). Control of GL2 expression in Arabidopsis leaves and trichomes. Development. 125: ; Ohashi-Ito, K. and Bergmann, D.C. (2006). Arabidopsis FAMA controls the final proliferation/differentiation switch during stomatal development. Plant Cell. 18: –413; Complementary expression patterns of a meristem-specific gene (left) and a leaf primordium- specific gene (right) Expression patterns of transcription factors the regulate guard cell (top) and trichome (bottom) differentiation

Genetic control of leaf identity Poethig, R.S. and Sussex,I.M. (1985) The developmental morphology and growth dynamics of the tobacco leaf. Planta 165: Figure 3 Copyright (1985) Planta. Reprinted with kind permission of Springer Science+Business Media Leaf primordium Meristem Leaf primordium How does a leaf primordium become a leaf, rather than part of the meristem?

Positional information (auxin accumulation) precedes leaf initiation Auxin accumulation precedes leaf initiation Indole-3-acetic acid (IAA) a naturally occurring auxin Poethig, R.S. and Sussex,I.M. (1985) The developmental morphology and growth dynamics of the tobacco leaf. Planta 165: Copyright (1985) Planta. Reprinted with kind permission of Springer Science+Business Media

A boundary forms by the action of mutually antagonistic genes ARP KNOX1 KNOX1 genes, expressed in the meristem, and ARP genes, expressed in the leaf primordia, are mutually repressive, and help establish a separate identity for the emerging leaf primordium

Juarez, M. T., Twigg, R.W., and Timmermans, M.C.P. (2004) Specification of adaxial cell fate during maize leaf development. Development 131: Reproduced with permission O2O2 CO 2 Most leaves have polarity – they are functionally and anatomically different on their upper and lower surfaces Abaxial surface - transpirational water loss, respiratory gas exchange Adaxial surface – light harvesting Genetic control of leaf polarity

Establishment of leaf polarity Leaf Adaxial Abaxial Information from the meristem is involved in establishing polarity Leaf primoridia have inherent polarity because one side is closer to the meristem and one side is farther away from the meristem. The meristem side is adaxial, the away side is abaxial

Waites, R., and Hudson, A. (1995) phantastica: a gene required for dorsoventrality of leaves in Antirrhinum majus. Development 121: 2143 – Reproduced with permission.2143 – 2154 The loss-of-function phantastica mutant of Antirrhinum (snapdragon) gives important clues to the basis of leaf polarity Genetic studies contributed to our understanding of leaf polarity Wild-type phan

Domain-specific transcription factor expression controls polarity KAN Adaxial fate Abaxial fate PHAN or PHB/PHV/REV Mutually antagonistic abaxial- and adaxial- expressed transcription factors are needed for proper leaf polarity and blade outgrowth phan mutant leaf Wild-type leaf Waites, R., and Hudson, A. (1995) phantastica: a gene required for dorsoventrality of leaves in Antirrhinum majus. Development 121: 2143 – Reproduced with permission.2143 – 2154 Loss of either gene function leads to the formation of radial, needle- like leaves

AAAAAAA In phb-1d plants, base changes in the PHB mRNA prevent miR166 from binding to it, allowing it to accumulate throughout the leaf primordium x PHB-1D mRNA Reprinted by permission from Macmillan Publishers, Ltd: NATURE. Kidner, C.A. and Martienssen, R.A. Nature 428: 81-84, copyright 2004.; McConnell, J.R., Emery, J., Eshed, Y., Bao, N., Bowman, J., and Barton, M.K. Nature 411: , copyright AAAAAAA AGO In wild-type plants, miR166 binds to PHB mRNA and degrades it on the abaxial side of the leaf primordium miR166PHB mRNA Domain-specific expression can be regulated by miRNAs

Meristem- derived signal Reprinted from Moon, J. and Hake, S. (2011) How a leaf gets its shape. Curr. Opin. Plant Biol. 14: 24–30 with permission from Elsevier.24–30 Summary - Establishment of polarity in leaves The adaxial domain is specified by a signal derived from the meristem Different transcription factors specify adaxial and abaxial domains In some cases domain- specific expression is maintained by miRNAs

Genetic control of leaf size and shape Size is determined by growth, shape is determined by differential growth Uniform growth Differential growth Both absolute and relative growth rates are regulated in expanding leaves

Expression of genes affecting: Primordium size b Cell expansion duration Cell size Cell division duration Cell division rate Meristemoid division Cell expansion rate Leaf growth involves cell proliferation and cell expansion Early growth is primarily through cell proliferation across the primordium, and later only in subsets of cells called meristemoids. A period of cell expansion follows and partially overlaps the division phases Reprinted from Gonzalez, N., Vanhaeren, H. and Inzé, D. (2012) Leaf size control: complex coordination of cell division and expansion. Trends Plant Sci. 17: 332–340 with permission from Elsevier.332–340

Leaf development involves cell differentiation as well as regulated growth patterns Remain undifferentiated Differentiate Genetic control of cell differentiation

Leaves have specialized cells including veins, trichomes and guard cells Upper epidermis Lower epidermis Palisade mesophyll Spongy mesophyll Trichome Guard cells Veins

Bayer, E.M, Smith, R.S., Mandel, T., Nakayama, N., Sauer, M., Prusinkiewicz, P., and Kuhlemeier, C. (2009) Integration of transport-based models for phyllotaxis and midvein formation. Genes Dev 23: The position of the midvein is specified by auxin After a leaf primordium is initiated, auxin moves basipetally and specifies the site of the midvein Auxin redistributing in a very young primordium – arrows indicate direction of auxin transport In an older primordium the future midvein is clearly demarcated. (Inset shows “top down” view)

Canalization reinforces auxin fluxes Second-order veins are formed by further auxin redistributions Adaxial surface of developing leaf Canalization is a self-generating flow of auxin via positive feedback loops

Differentiation of cells in the epidermis Image credit Louisa Howard, Dartmouth University The leaf epidermis comprises pavement cells, trichomes and guard cells Nicotiana alata

Trichome mutants have identified genes involved in many processes Reprinted from Hülskamp, M. (2004). Plant trichomes: a model for cell differentiation. Nat. Rev. Mol. Cell Biol. 5: with permission from Macmillan Publishers Ltd., and Grebe, M. (2012) The patterning of epidermal hairs in Arabidopsis — updated. Curr. Opin. Plant Biol. 15: 31–37 with permission from Elsevier. See also Yang, C. and Ye, Z. (2012) Trichomes as models for studying plant cell differentiation. Cell Mol. Life Sci. (in press) –37in press Genes affecting spacing and identity Genes affecting cell cycle regulation Genes affecting cell shape Genes affecting growth and polarity As trichomes differentiate, they endoreduplicate, causing their ploidy (DNA content) to increase from 2n to 4n to 8n to 16n. The cell cycle of endoreduplicating cells skips mitosis M G1G1 G2G2 S Endo- reduplication

In Arabidopsis, trichome spacing is controlled by an inhibitory signal A transcription complex activates expression of the trichome inducer GLABRA2 (GL2)..... and a mobile inhibitor moves into adjacent cells to inhibit GL2 expression. GL2 Transcription complex Trichome TRY CPC ETC1 Inhibitor Inactive transcription complex GL1 TTG GL3/ EGL3 No transcription, no differentiation

Guard cell differentiation in Arabidopsis In Arabidopsis, guard cells are formed through a tightly controlled series of cell divisions Asymmetric division Symmetric division Protodermal cell Meristemoid Mother Cell Guard Mother Cell Guard Cell Pair ; Reprinted from Nadeau, J.A., and Sack, F.D. (2002). Control of stomatal distribution on the Arabidopsis leaf surface. Science 296: 1697–1700 with permission from AAAS.1697–1700 SPEECHLESS, MUTE and FAMA all encode basic helix- loop-helix transcription factors SPEECHLESS MUTE FAMA

Summary – leaf development Efroni, I., Eshed, Y., and Lifschitz, E. (2010) Morphogenesis of simple and compound Leaves: A critical review. Plant Cell 22: