Leaf and Internode Introductory article

Andrew Hudson, University of Edinburgh, Edinburgh, UK Article Contents Christopher Jeffree, University of Edinburgh, Edinburgh, UK . Introduction . Parts of the Monocot and Dicot Leaf Leaves of different species show wide variation in morphology and anatomy, usually . Physiology and Function associated with specialized roles in photosynthesis. Formation of leaves, from naive . Control of Leaf Initiation meristematic cells at the growing shoot tip, differs subtly in monocotyledonous and . Growth and Patterning of the Leaf dicotyledonous plants, although it appears to involve conserved gene functions. . Cell Type Specification in the Leaf . Heteroblasty Introduction dicot leaf usually has a net-like vascular system, in which Leaves are the most variable of plant organs. They differ veins branch and rejoin. Major veins are usually thicker widely in shape, size and anatomy between different than the surrounding blade tissue. The blade is often species, and even within individual plants. Most leaves similar in composition along its length and width, although are specialized photosynthetic organs, but others are its edge may form specialized structures, such as spines. In adapted to different roles as, for example, spines or scales contrast, many leaves show an asymmetric distribution of for protection, tendrils for support, or the traps of tissues along the depth of the blade, with palisade insectivorous plants. Although differing structurally, mesophyll cells towards the upper (adaxial) surface and leaves share a number of characters that distinguish them spongy mesophyll cells below. Further differences are often from other organs of the plant. seen between epidermal cells of the adaxial and abaxial surfaces. 1. They occur on the sides of stems and (together with Many dicots produce compound leaves with a number of leaf-like parts of the flower) are therefore termed individual leaflets on a common stalk (rachis) (Figure 1b). lateral organs. Each leaflet resembles a simple leaf in structure and 2. Unlike the shoot, they have a limited capacity for development (although it has no axillary meristem growth. associated with it). In addition, both simple and compound 3. They are associated with secondary meristems (ax- leaves can form blade-like outgrowths (stipules) from the illary meristems) that form at the junction between the base of the petiole (Figure 1b). Compound leaves have upper (adaxial) part of the leaf and the stem and allow probably evolved from simple leaves on a number of branching of the shoot. occasions, and simple leaves may also have arisen by 4. Most leaves show dorsoventral asymmetry. They are reduction of compound leaves. Some species are able to usually flattened and may also have different tissues in produce both simple and compound leaves during their their upper (adaxial) and lower (abaxial) parts. lifetimes. Leaves probably evolved in a common ancestor of The leaves of monocotyledonous plants (monocots) euphyllous plants (e.g. flowering plants, conifers and differ from dicots in several respects. ferns). Although the leaf-like organs of more primitive plants (e.g. mosses) have similar photosynthetic functions, 1. Many monocot leaves are sword shaped and lack a they probably arose independently on more than one narrower petiole (Figure 1c). The basal part (the sheath) occasion. tightly encircles the stem and may overlap at its margins or form a tube, but the blade is usually free. Specialized structures are found at the sheath–blade boundary: the ligule, a membrane or fringe of hairs Parts of the Monocot and Dicot Leaf that form a seal between the adaxial leaf and stem, and the auricle, which can act as a hinge between sheath The leaf of a dicotyledonous plant (dicot) typically consists and blade (Figure 1d). of a flattened leaf blade joined to the stem by a narrower 2. All but the most minor veins run parallel to each other petiole (Figure 1a). The petiole is usually continuous with along the long axis of the leaf and rejoin only near its the major central vein of the leaf (the midrib) and no tip. Other tissues (e.g. epidermal hairs or stomata) may distinct boundary may be apparent between petiole and be arranged in similar longitudinal stripes. blade, or between the lower (abaxial) petiole and the stem. 3. Monocot leaves tend to show less differentiation However, specialized structures may form at the base of the between adaxial and abaxial tissues. petiole allowing leaf movement or loss under unfavourable conditions (as occurs in deciduous trees). The blade of a

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Although these generalizations are valid for the leaves of are branched, hooked or produce sticky or toxic com- grass-like monocots (e.g. maize), other monocots have pounds as a defence against pests (particularly insects) dicot-like leaves with broader blades, veins that branch (Figure 2c). They may also protect against damage by UV laterally from a central midrib, and more obvious light or reduce water loss by trapping a layer of still air differentiation of adaxial and abaxial tissues (Figure 1d). around the leaf surface. This has led to the suggestion that ancestral monocots had The vascular tissues of the leaf resembles those in the rest leaves similar to dicots, and that grass-like leaves arose by of the plant, consisting of xylem, phloem and associated reduction of the dicot-like blade and increased growth of a cells. Xylem is responsible for supplying the leaf with water region closer to the stem. Compound leaves in monocots and dissolved inorganic compounds. Phloem supplies the are found only in palms. Unlike compound dicot leaves, developing leaf with organic compounds, and exports these form from a single primordium, which becomes excess products of photosynthesis from mature leaves compound as cells between leaflets die late in development. (usually in the form of sucrose). The vascular cells of minor veins are surrounded by a single layer of photosynthetic bundle-sheath cells. In C4 plants (e.g. maize) bundle-sheath cells are responsible for fixation of carbon dioxide that is Physiology and Function produced from organic acids (usually malic) imported from neighbouring mesophyll cells. The bundle-sheath Most leaves are specialized photosynthetic organs and cells of C4 plants are large, have large chloroplasts and are show adaptations to light harvesting and gas exchange in intimate contact with neighbouring mesophyll cells – a (uptake of carbon dioxide, loss of oxygen). Their flattened characteristic arrangement termed Krantz anatomy shape presents a large area to incident light. Palisade (Figure 2d). mesophyll cells are responsible for most of the photosyn- thetic activity of the leaf. They are located adaxially (and therefore usually towards the light), contain numerous chloroplasts and have a large proportion of their surface ControlofLeafInitiation area exposed for gas exchange (Figure 2a). Spongy mesophyll cells, although also photosynthetic, have fewer The position at which leaves occur on a stem is termed a chloroplasts, but are separated by more extensive air node and the stem tissue separating neighbouring nodes an spaces. The exposed surface area of mesophyll cells may internode. Leaves occur either singly or in groups at each therefore exceed the external surface area of the leaf by node. Because the rate of leaf initiation and growth is almost 20 times. affected by environmental conditions, leaf age is conve- Exchange of gases between the internal air spaces and niently measured in plastochrons – one plastochron being the external atmosphere occurs through pores (stomata) in the time between initiation of leaves at successive nodes. the epidermis (Figure 2b). In many plants, stomata are more Each leaf arises from a group of initial cells within the frequent in the abaxial epidermis. Each pore is bounded by flank of the shoot apical meristem. The initials form a a pair of specialized epidermal cells (stomatal guard cells) primordium growing in a new axis (Figure 3a), while that regulate its aperture. An increase in guard cell turgor surrounding cells form either stem tissues or axillary pressure occurs in conditions favourable for photosynth- meristems. Leaf initials are present in at least four cell esis (light or depletion of internal carbon dioxide by layers of the dicot meristem and may differ in number photosynthesis) causing stomata to open. Water stress or between species (e.g.  100 cells at primordium initiation high internal carbon dioxide cause guard cells to lose in Arabidopsis thaliana,  150 in tobacco). Surgical turgor and stomata to close. Therefore the plant can experiments suggest that the identity of leaf initials is balance the requirement for photosynthetic gas exchange specified at least one plastochron before they form a with water loss by transpiration. Gas exchange and water primordium and that existing primordia may produce an loss through other epidermal cells is limited by a thickened inhibitory signal that prevents adjacent meristem cells external cell wall impregnated with the fatty polymer, assuming leaf fate (thus explaining the regular spacing of cutin, and a hydrophobic surface layer (the cuticle) leaves on stems – termed phyllotaxy). Repression of leaf containing cutin and waxes (Figure 2b). The cuticle also fate in the meristem requires homeobox transcription reduces wetting of the leaf (e.g. by rain) and forms a barrier factor genes of the knotted1 family, which are expressed in against attack by pathogens. the meristem and stem initials, but excluded from leaf Many leaves produce epidermal hairs (trichomes) initials before primordium initiation. Conversely, MYB consisting of one or more specialized cells. Many trichomes transcription factor genes of the phantastica family repress

Figure 1 Parts of the monocot and dicot leaf. (a) A simple leaf of the dicot, Antirrhinum majus (snapdragon). (b) A compound leaf of the dicot Pisum sativum (garden pea). (c) Part of the grass-like monocot leaf of Zea mays (maize). (d) The broad monocot leaf of Spathiphyllum wallisii.

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Figure 2 Leaf anatomy. (a) A section of the leaf blade of bean (Phaseolus vulgaris) showing adaxial and abaxial epidermal cell layers (e), a single layer of palisade mesophyll cells (pm) and several layers of spongy mesophyll (sm). This picture is of a mature leaf that was frozen and then broken before viewing in a scanning electron microscope. Bar, 50 mm. (b) The abaxial epidermis of a wheat leaf blade with a pair of stomatal guard cells (gc). The cuticle formed on the leaf surface includes numerous wax crystals. Key: e, epidermal cell; sa, stomatal aperture. Bar, 20 mm. (c) The abaxial epidermis of an immature bean leaf with both hooked and glandular trichomes. Labelled as in (a). Bar, 100 mm.

(d) A section through a maize leaf showing typical Kranz anatomy associated with C4 photosynthesis. This stained section was made perpendicular to the long axis of the leaf. Key: e, epidermis; m, mesophyll; bs, bundle sheath; v, vascular cells. Bar, 50 mm. Photograph provided by Jane Langdale, University of Oxford. knotted1-like genes in leaf initials and promote primor- because mutations that affect the identity of one of these dium initiation. domains tend also to prevent lateral growth. Although the primordia of monocot leaves differ from dicots in being flattened at emergence (Figure 3b), analysis of mutants has revealed that similar adaxial–abaxial interactions might Growth and Patterning of the Leaf recruit meristem cells to form the margins of leaf primordia, giving them their characteristic flattened shape. The primordium of a dicot leaf flattens after initiation as Differences between the adaxial and abaxial parts of a the blade grows laterally. Fate mapping has shown that dicot leaf are specified before primordium initiation, and a division of all cells in the tobacco leaf primordium number of regulatory genes needed for either adaxial or contribute to growth in length and width and there are abaxial cell fate in Arabidopsis thaliana show patterned no specialized meristematic regions as found at shoot expression in leaf initials at, or before, primordium apices. Growth in width might be controlled by interaction formation. Analysis of their mutant phenotypes has between adaxial and abaxial domains of the primordium,

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Figure 3 Leaf initiation. (a) The shoot apex of the dicot, Antirrhinum majus, showing the shoot apical meristem (SAM) and primordia of leaves formed from it (p). Leaves are produced in opposite pairs and numbered according to increasing age. (b) The apex of the monocot, barley. Leaf primordia (p) are more flattened than those of dicots, produced singly, and encircle the whole meristem. Bars, 100 mm. suggested (1) that adaxial and abaxial fates are mutually with the view that compound leaves arose independently in exclusive, and (2) that adaxial identity promotes formation different plant groups. Tomato leaves are exceptional in of the axillary meristem at the junction between leaf and expressing knotted1-like homeobox genes, and elevated stem. The mechanisms specifying differences along the homeobox gene expression can cause an increase in length of the leaf have been studied in the monocot maize, compounding. Unlike tomato, pea leaves do not express in which the ligule and auricle mark the boundary between knotted1-like genes and require activity of a LEAFY-like sheath tissue and the blade further towards the tip transcription factor (which also specifies flower formation) (Figure 1c). The differences must be specified early because to form a compound, rather than simple structure. ligule formation is visible by the time the leaf is 2–3 plastochrons old (about 1 mm in length). Although knotted1-like homeobox genes are normally expressed only in the meristem, they might be responsible for Cell Type Specification in the Leaf patterning the long axis of the leaf because misexpression in leaves causes sheath tissue to develop in place of the Specification of two epidermal cell types – stomatal guard blade. Specification of this axis directs expression of genes cells and trichomes – has been analysed in detail in in particular regions, for example liguleless genes that are Arabidopsis. Each pair of guard cells is produced from an needed for ligule formation in cells around the sheath– epidermal precursor by several rounds of unequal cell blade boundary. division. The smallest daughter cell divides again to form a Cell divisions usually cease first at the tip of the leaf, and pair of guard cells while the surrounding daughter cells last in the basal region. However, the duration of division assume different fates. Although this pattern of division also varies for different cell types at similar positions (e.g. can explain spacing of stomata, a different mechanism has trichomes often stop dividing and differentiate before been found to operate in spacing of trichomes. Mutations neighbouring epithelial cells). Most of the growth in area of in the TRYPTICHON (TRY) gene allow adjacent epider- the leaf is caused by expansion of cells after they have mal cells (which may be descended from different ceased division. precursors) to differentiate as trichomes, suggesting that Control of compound leaf architecture appears to trichome initials normally repress trichome fate in their involve different mechanisms in pea and tomato, consistent neighbours by TRY-dependent signalling. A number of

5 Leaf and Internode other transcription factor genes are expressed specifically termed phase change), and therefore leaf form, have been in trichome initials, and are required for normal trichome identified in maize and A. thaliana. For example, reduction initiation, growth and branching. in activity of the Arabidopsis gene, TERMINAL FLOW- Specification of vascular tissues in the leaf is poorly ER1, causes more rapid phase change whereas increased understood, although indirect evidence suggests involve- expression slows it. In some cases, the transition between ment of the phytohormone auxin. High levels of auxin are forms may be more abrupt, or involve more dramatic proposed to promote both vascular cell fate and to increase differences. For example, seedlings of gorse, Ulex euro- uptake of auxin from surrounding tissues, therefore paeus, produce flattened leaves whereas more mature inhibiting vascular fate in neighbouring cells. plants produce only needle-like spines. In other species, the transition may be regulated by environmental signals. Deciduous trees may switch from production of leaves to Heteroblasty protective bud scales in response to day length and aquatic plants may produce different leaf forms when submerged in Because of similarities in their structure and development, water or exposed to air: for example Ranunculus aquaticus leaves are considered equivalent to cotyledons (seed leaves) produces compound leaves with filamentous leaflets when and floral organs. This has been supported by analysis of submerged, but lobed leaves above the water surface. genes that specify the difference between these organs. For example, mutations that reduce activity of the LEAFY Further Reading COTYLEDON gene in Arabidopsis thaliana allow cotyle- dons to develop with leaf-like characters. Similarly, loss of Bell A (1991) Plant Form. An Illustrated Guide to Flowering Plant activity of floral homeotic genes, which together specify the Morphology. Oxford: Oxford University Press. identity of floral organs, leads to production of flowers Esau K (1977) Anatomy of Seed Plants. New York: John Wiley. consisting only of leaves. Freeling M (1992) A conceptual framework for maize leaf development. Developmental Biology 153: 44–58. Most plant species also produce foliage leaves with Hetherington AM (ed.) (1994) The Tansley Review Collections. 1: Leaf different forms (a phenomenon termed heteroblasty). In development and function. New Phytologist 128: 19–507. most species the transition between forms occurs gradually Steeves TA and Sussex IM (1989) Patterns in Plant Development. as the plant matures. Genes that regulate maturation (also Cambridge, UK: Cambridge University Press.

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