Leaf Expansion – an Integrating Plant Behaviour

Plant, Cell and Environment (1999) 22, 1463–1473 COMMISSIONED REVIEW Leaf expansion – an integrating plant behaviour E. VAN VOLKENBURGH Department of Botany, Box 355325, University of Washington, Seattle, WA 98195, USA ABSTRACT the phase of leaf development contributing most to surface area and shape of the lamina. Leaves expand to intercept light for photosynthesis, to take Leaves can be considered, functionally, as iterated green up carbon dioxide, and to transpire water for cooling and antennae specialized for trapping light energy, absorbing circulation. The extent to which they expand is determined carbon dioxide, transpiring water, and monitoring the envi- partly by genetic constraints, and partly by environmental ronment. The leaf canopy may be made up of many or few, conditions signalling the plant to expand more or less leaf small or large leaves. They may be simple in shape, like the surface area. Leaves have evolved sophisticated sensory monocotyledonous leaves of grasses or dicotyledonous mechanisms for detecting these cues and responding with leaves of sunflower and elm. Or leaves may be more their own growth and function as well as influencing a complex, with intricate morphologies as different as the variety of whole-plant behaviours. Leaf expansion itself is delicate, sensitive structure of the Mimosa leaf is from the an integrating behaviour that ultimately determines canopy magnificent blade of Monstera. Some species, such as development and function, allocation of materials deter- cactus, do not develop leaves at all, but carry out leaf func- mining relative shoot : root volume, and the onset of repro- tions in the stem. Other plants display small leaves in order duction. To understand leaf development, and in particular, to conserve water, but with the consequence of limiting how leaf expansion is regulated, we must know at the mol- photosynthetic productivity. ecular level which biochemical processes accomplish cell Plant species can be lumped into groups of slow-growers growth. Physiological experimentation focusing on ion and rapid-growers, with contrasting ecological strategies fluxes across the plasmamembrane is providing new mol- paralleled by differences in leaf area (Lambers, Poorter & ecular information on how light stimulates cell expansion Van Vuuren 1998). Slowly growing species live in harsher in some dicotyledonous species. Genetic analyses in Ara- environments, and their low relative growth rate can be bidopsis, corn, and other species are rapidly generating attributed to production of small, or slowly expanding leaf a list of mutations and enzyme activities associated with area. More rapidly growing species may have evolved from leaf development and expansion. Combination of these slowly growing ones, or vice versa, and have a faster rela- approaches, using informed physiological interpretations of tive growth rate associated with more rapid development phenotypic variation will allow us in the future to identify of leaf area (Poorter & van der Werf 1998). Size and shape genes encoding both the processes causing cell expansion, of leaves is to a large extent genetically controlled, imply- and the regulators of these events. ing that these are adaptive features lending advantage to plants in specific habitats. Yet, developmental flexibility Key-words: cell expansion; ion transport; osmoregulation; exists even within an individual plant, with leaf size and phytochrome; proton pump; wall extensibility. shape depending on environmental circumstances prevail- ing during leaf formation. Leaves will remain small if cir- INTRODUCTION cumstances are unfavourable, or they will expand a large surface area when the necessary nutrients are available The diversity of leaf shapes and sizes is a compelling and (Chapin 1991). Plants have developed sophisticated sensing curious feature of our natural surroundings. Leaves attract mechanisms for determining the availability of resources in our attention, and their many distinct characteristics have the soil, atmosphere and light. They respond to these cues aided the catagorization of plants into taxonomic groups. by regulating biochemical processes that control leaf The functions of all these shapes and sizes remain an eco- expansion, developing their leaf canopies accordingly. logical and evolutionary puzzle, one which will be more Given the prominence of leaves in our environment, approachable once we understand the cellular mechanisms their importance for plant function, and our fascination at work in creating the leaf blade. These mechanisms will with their appearance, it is astounding that so little is known be considered here under the description of leaf expansion, about the physiological processes giving rise to these organs. Genetic studies have identified a small but growing Correspondence: Fax: 1 206 6851728; number of genes involved in controlling leaf development, e-mail: [email protected] and physiological studies have described a few biochemical © 1999 Blackwell Science Ltd 1463 1464 E. Van Volkenburgh mechanisms involved in cell division and expansion in for nutrients, thus attracting sufficient carbohydrate and stems and roots. But most studies of leaf function have nitrogen to signal continued division cycles? What if the focused on photosynthetic capacity, light interception, and expansion of meristematic cells were stalled for a time responses of leaves to environmental stresses (sometimes during mid-cycle, perhaps by a transient water deficit – including inhibition of growth), without including detailed would that be enough to reduce carbon/nitrogen import study of the mechanisms regulating leaf expansion. It is and prevent completion of the cell cycle? What do we know, the intent of this brief, and selected, review to promote actually, about the minute-to-minute regulation of cell thoughtful investigation into the mechanisms controlling expansion, and the dependence of the cell cycle on cell leaf expansion. With emerging molecular genetic methods, expansion? it should soon be possible to determine the biochemical Cellular mechanisms for controlling growth are likely to basis for both the processes that drive leaf expansion, and be genetically redundant. This means that identifying phe- the signalling pathways that control it. notypes for genetic variants may be difficult without precise physiological information. The following focuses on mechanisms that may explain short-term regulation of cell Regulation of leaf expansion at the growth, with the recognition that meristematic cells must cellular level enlarge in volume prior to mitosis and cell division. An Once a leaf primordium has been initiated within an apical emphasis on the molecular basis for the physiological meristem, the newly formed organ embarks on a predic- processes controlling cell expansion will help us, in the long table developmental programme leading to the formation run, to identify functions of genes known to affect leaf of a small but recognizable leaf. This early phase of leaf growth and morphology. development is largely accomplished by production of new cells that become anatomically committed to form orga- Biophysical considerations nized tissues creating a dorsiventral structure. At this stage, in dicotyledonous leaves, the blade and petiole become dis- The question of how leaf cells, and for that matter, plant tinct, and vascular patterning is evident. In monocotyledo- cells in general, enlarge is a complex one without many nous leaves, the blade grows to a considerable length before answers as yet. For the last several decades, the regulation the sheath is formed, but even at early stages the vascular of cell expansion has been described and investigated from pattern is clear. As is the case for growing roots and stems, a biophysical point of view starting with the theoretical it is possible in leaves to identify zones of cell division and treatment of Lockhart (1965). Since then, the theory has zones of cell expansion, although these zones are much been amplified and revised (e.g. Passioura & Fry 1992) but more distinct in monocot leaves. In dicot leaves, the in general, these revisions share a similar basis. Cell growth processes of cell division and expansion may overlap spa- theory is based on the observation that the relative growth tially as well as temporally to a considerable extent (Dale rate of cells is a function of the internal hydrostatic or 1988). No matter how much cell division occurs, it is the turgor pressure in excess of the yield threshold of the cell process of cell expansion that creates the surface area of wall, and the extensibility of the cell wall. Turgor pressure the mature organ. Even in the zone of cell division, cells itself is a dependent variable, determined by the osmotic must increase in volume prior to mitosis and cytokinesis gradient attracting water into the cell, the reflection coeffi- (Ray 1987). After cell replication ceases, leaf cells continue cient of the plasmamembrane, the hydraulic conductance of to expand and may obtain a final volume 20 to 50 times that the membranes to water, and the biomechanical properties of their meristematic progenitors (Maksymowych 1973; of the cell wall material (Cosgrove 1981). In theory, growth Becraft 1999). rate could be controlled by any one of these variables, or Variation in leaf size has been attributed to differences by complex changes involving several. in cell number, or cell size, or combinations of the two Over the past 20 years, emphasis has shifted from the (e.g. Granier

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