trends in plant science Reviews Progress in the molecular genetic analysis of trichome initiation and morphogenesis in Arabidopsis Daniel B Szymanski Alan M Lloyd and M David Marks Arabidopsis trichomes are large unicellular structures that develop on the surface of most shoot derived organs In leaves the number spacing and shape of trichomes is tightly regulated and this process has been used as an experimental system to study the control of cell fate and pattern formation The control of trichome initiation is complex both the potential of a cell to adopt the trichome cell fate and an intricate signaling pathway determine the pattern of trichome initiation events Several important new results suggest that trichome initiation and morphogenesis are redundantly regulated by both positive and negative factors A testable model for the control of trichome initiation is presented I n plants the control of cell fate is a central issue during vegetative development phase The potential to acquire the triembryo development meristem function and the transition chome cell fate is highly regulated 3 7 For example the first trifrom vegetative to reproductive phases The regulation of cell chome at the leaf tip appears only after the leaf grows to 100 mm fate requires a balance of cell proliferation differentiation inter in length5 Subsequent initiation events proceed basipetally as the cellular communication and morphogenesis control All of these leaf grows As leaf development progresses cell division patterns developmental processes are involved in the formation of become less regular islands of dividing cells can be observed unicellular trichomes in the shoot epidermis of Arabidopsis The among differentiated pavement cells with their characteristic integration of these processes is complex and progress in lobed morphology Trichome initiation in the expanding leaf understanding control mechanisms has been slow Trichome occurs within these islands of cells and often defines points along development has provided a simple model to gain mechanistic the perimeter of a circle with an existing trichome defining the insight into the control of cell fate and morphogenesis Because of center Fig 1 The developmental window during which cells their amenability to genetic analysis and the physical accessibility have the potential to acquire trichome cell fate is further limited of the leaf epidermis diverse molecular pharmacological cells beyond a certain developmental stage lose the ability to and cytological approaches have been used to study different respond to trichome differentiation signals4 aspects of trichome development Here we summarize recent data on the molecular genetics of leaf trichome initiation and Genetic analysis of trichome initiation morphogenesis Genetic screens for trichome initiation and spacing mutants have Trichomes defined as hair like structures that extend from the been useful in addressing two important questions epidermis of aerial tissues are present on the surface of most ter 1 What genes control entry into the trichome pathway restrial plants1 Plant trichomes comprise a diverse set of structures 2 What controls the spacing of initiation events and many plants contain several types of trichomes on a single leaf It has been difficult to demonstrate their function clearly but a b several ideas have gained widespread 6 acceptance The presence of trichomes can increase the boundary layer thickness 5 between the epidermal tissue and the envi3 ronment and can reduce heat and water loss In many species trichomes are thought 4 1 to protect the plant against insect or 2 6 pathogen attack either by secreting chemical components or by physically limiting 4 insect access to or mobility on vegetative tissues The stellate trichomes of ArabidFig 1 Scanning electron micrographs of the adaxial surface of Arabidopsis leaves that opsis do not have a secretory anatomy but illustrate aspects of trichome spacing and morphogenesis a An example of secondary at a functional level they might limit herbitrichomes white arrows initiating around an existing central trichome black arrow vore access to the leaf in the field 2 Numbers to the left of each labelled trichome indicates its developmental stage 5 Arabidopsis trichome initiation Cellular determinants of the potential to enter the trichome pathway Trichome differentiation is integrated with leaf development hormone levels and the 214 May 2000 Vol 5 No 5 trichome expansion with pointed branch tips 6 mature trichome with a papillate cell wall Scale bar 5 100 mm b Additional stages of trichome development 1 isodiametric expansion in the plane of the epidermis 2 stalk emergence and polar expansion 3 branch initiation 4 expansion of the stalk and branches with a blunt tip morphology 6 see a Scale bar 5 50 mm 1360 1385 00 see front matter 2000 Elsevier Science Ltd All rights reserved PII S1360 1385 00 01597 1 trends in plant science Reviews GL1 TTG1 GL3 CPC GL1 TRY TTG1 Trichome initiation TRY GL3 GL2 Endoreduplication Morphogenesis Trends in Plant Science Fig 2 A model summarizing the genetic control of trichome initiation and the early phases of trichome morphogenesis GLABROUS1 GL1 TRANSPARENT TESTA GLABRA1 TTG1 and GLABROUS3 GL3 are required for normal trichome initiation GL1 and TTG1 are also required for normal trichome spacing and have the capacity to limit trichome initiation CAPRICE CPC and TRIPTYCHON TRY negatively regulate trichome initiation GL2 and GL3 redundantly regulate aspects of trichome morphogenesis and GL3 also promotes endoreduplication in trichomes TRY negatively regulates GL3 activity in trichomes In each example arrows indicate a positive influence blocked lines indicate negative regulation Loss of function mutations in the GLABROUS1 GL1 and TRANSPARENT TESTA GLABRA1 TTG1 genes result in a nearly complete loss of leaf trichome initiation8 The effects of mutations in GL3 are less severe trichomes are observed but branching is either reduced or eliminated9 Genetic analyses of gl1 gl3 and ttg1 mutants have not indicated clear epistatic relationships between these genes In addition GL1 and TTG1 can negatively regulate trichome initiation Weakly semi dominant mutations in TRIPTYCHON TRY also result in a partial loss of negative regulation of trichome initiation and give rise to limited trichome clustering9 11 The try trichomes also display an elevated branch number and DNA content Mutations in CAPRICE CPC do not result in a