A wide diversity of topics, ranging from the fine structure of cells to the gross morphology of the shoot, will be discussed in this chapter, providing a brief summary of the large amount of accumulated knowledge that exists on the botany of wheat. Modern agronomic methods, however, are often based on, for example, the developmental changes occurring within the shoot, which are only revealed using methods that entail knowledge of the development and structure of the shoot. Some researchers will require more detailed information about the morphology and anatomy of, for instance, the leaf in relation to the canopy structure and photosynthesis or infection by a pathogen, thus in this chapter key references are provided to detailed, relevant studies.
The mature wheat plant is the culmination of all the development and growth processes throughout the life cycle. All the structures, such as leaves, tillers and ears, have attained their full size, although not all will be present at maturity because some structures, particularly those produced early in the life cycle, will have senesced and may have rotted or blown away.
The plant is made up of a root and shoot system. Two types of roots are found, the seminal roots and the nodal roots (adventitious or crown roots), which arise from the lower nodes of the shoot. The shoot is made up of a series of repeating units or phytomers, each potentially having a node, a leaf, an elongated internode and a bud in the axil of the leaf (Figure 2.1).
There are from 6 to 16 or more of these units forming the vegetative part of each shoot. From four to seven of the most distal units have an elongated internode. The portion of the shoot with elongated internodes is the elongated stem or culm. In the proximal or basal units, the internode remains short and the nodes are packed closely together. A leaf is inserted at each node although at maturity the basal leaves are usually dead and may have disappeared. The shoot is terminated by an ear or spike bearing about 20 spikelets. In the ear, the phytomer is made up of the spikelet (the axillary bud) and the rachis (node and internode); the development of the leaf is suppressed.
Tillers, which have the same basic structure as the main shoot, arise from the axils of the basal leaves. At anthesis, only some of the tillers that have developed survive to produce an ear. Others die and may be difficult to find in the mature plant.
Each leaf comprises the sheath, wrapping around the subtending leaf, and a lamina (blade). At the junction of the sheath and lamina, there is a membranous structure, the ligule, and a pair of small, hairy projections, the auricles. The base of the leaves on the culm is thickened to form a hard knot or pulvinus.
The elongated distal internodes increase in length from the basal to the most distal, the peduncle (Figure 2.1).
Diagram of a 'mature' plant, alternative numbering system for leaves and internodes
Different systems for identifying leaves and internodes have been developed, their form depending on the use to which they are put. As with the total number of leaves, the number of nodes on the shoot are often not known with certainty. Some systems use the uppermost leaf (the flag leaf) or the uppermost internode (the peduncle) as the reference and numbering proceeds basally. Other systems are used in development studies where the position and emergence of each leaf is noted, and leaves and nodes are numbered from the base distally; culm leaves and internodes may be identified in a separate series (Figure 2.1).
THE SEED, GERMINATION AND SEEDLING EMERGENCE
The seed, grain or kernel of wheat (more pedantically, the caryopsis) is a dry indehiscent fruit. The dorsal side (with respect to the spikelet axis) is smoothly rounded, while the ventral side has the deep crease (Figure 2.2). The embryo or germ is situated at the point of attachment of the spikelet axis, and the distal end has a brush of fine hairs. The embryo is made up of the scutellum, the plumule (shoot) and the radicle (primary root) (Figure 2.3). The scutellum is the region that secretes some of the enzymes involved in germination and absorbs the soluble sugars from the breakdown of starch in the endosperm. Surrounding the endosperm is a metabolically active layer of cells or the aleurone layer, the testa or seed coat and the pericarp or fruit coat. In the plumule region of the embryo, the coleoptile, about four leaf primordia and the shoot apex or dome can be distinguished.
Wheat grain, showing different aspects and cross section to illustrate the depth of the crease
The coleoptile is well developed in the embryo, forming a thimble-shaped structure covering the leaf primordia and the shoot meristem. At germination, it bursts through the pericarp and testa and grows through the soil mainly by the action of an intercalary meristem, which forms about 10 mm behind the tip and stays at this position throughout the growth of the coleoptile. Vascular tissue and stomata differentiate during the growth of the coleoptile.
The fully elongated coleoptile is a tubular structure typically about 50 mm long and 2 mm in diameter. It is white in colour except for two lateral strands of chlorophyllous tissue associated with the vascular strands. The end of the coleoptile is bullet-shaped and closed except for a small pore 0.25 mm long a short distance behind the tip and on the side opposite the scutellum.
Two vascular bundles are found laterally placed with reference to the scutellum-coleoptile plane. One or two lines of stomata extending from the base to the tip are found in the outer epidermis associated with each vascular bundle. They tend to be more numerous towards the tip. Stomata also occur in the inner epidermis though they are less frequent. The guard cells of the stomata do not have the characteristic dumbbell shape, such as those found in the leaf, but are kidney-shaped, similar to dicotyledon guard cells.
The other cells of the outer epidermis have thickened walls that are finely wrinkled, the crests of the wrinkles occurring at 1 to 2 mm intervals. The inner epidermis has an unthickened wall, which is not wrinkled. The parenchyma tissue between the outer and inner epidermis is composed of large regular cells, which contain plastids.
Longitudinal section of the embryo from a mature grain, with the apex and leaves of the shoot present and a tiller bud visible
Source: Kirby and Appleyard, 1985. (Courtesy of Kluwer Academic Publishers)
When a seed is sown in a suitable moist and aerated soil it germinates. The radicle emerges first and then the plumule. As growth continues, the radicle and about four other seminal roots develop. The coleoptile emerges shortly after the radicle and forms a sheathing structure through which the developing leaves grow. The coleoptile increases in length until it emerges through the soil surface, when further elongation ceases. If the seed is sown very deeply, the coleoptile may cease growth before it reaches the soil surface. Under such conditions, the first leaf may emerge from the coleoptile, but as it is not adapted to pushing through soil, it usually becomes buckled and crumpled, never emerges from the soil and eventually the seedling dies.
When a seed is sown at depths greater than 40 to 60 mm, the internode between the coleoptile and the first leaf (epicotyl) elongates, pushing the crown (the shoot apex and the ensheathing leaves) to within about 40 mm of the soil surface (Figure 2.4) (Kirby, 1993). In wheat, unlike oats and maize, the internode between the scutellum and coleoptile (the mesocotyl) does not elongate. In the case of very deeply sown seeds (more than 100 mm), the internode between leaves 1 and 2 and sometimes between leaves 2 and 3 may also elongate.
The wheat plant has two types of roots, the seminal (seed) roots and roots that initiate after germination, the nodal (crown or adventitious) roots. About six root primordia are present in the embryo. At germination, the primary root bursts through the coleorhiza, followed by the emergence of four or five lateral seminal roots. These form the seminal root system, which may grow to 2 m in depth and support the plant until the nodal roots appear. Nodal roots are associated with tiller development and are usually first seen when the fourth leaf emerges and tillering starts. Compared with the seminal roots, they are thicker and emerge more or less horizontally; when they first appear they are white and shiny (the white root stage). Nodal roots occur on the lower three to seven nodes (depending on environmental conditions and final number of leaves on the shoot). The uppermost node on which roots occur, at the base of the culm, may be above soil level, and the roots may not penetrate the soil but appear as short pegs protruding from the stem. At maturity, the root system extends to between 1 and 2 m deep or more depending on soil conditions. Most roots occur in the top 30 cm of soil.
A deeply sown seeding (left) with coleoptile removed, showing the development of the sub-crow internode and the position of the crown, compared to a seedling sown at optimum depth (right); note the difference in tillering
Source: Kirby and Appleyard, 1987.
(Courtesy of Arable Unit RASE))
While the general classification of seminal and nodal roots is adequate for most purposes, these terms are not strictly accurate or unambiguous and more complicated systems have been devised (Klepper et al., 1984). At each node, a root arises from one of four quadrants, which may be designated X (the quadrant centred on the midrib of the leaf attached at that node) Y, A and B. Using this system, any root can be identified by the node at which it arises (node or leaf numbering as for tiller nomenclature) and the quadrant from which it grows. Thus, root 2X is the root arising at node (leaf) 2 in the leaf midrib position (Klepper et al., 1984).
The young seminal root has a root cap behind which the root is bare until the root hair zone. A transverse section of the root in the root hair zone reveals an epidermis in which some cells have become long unicellular root hairs and a cortex of parenchymatous cells surrounding an inner cylinder of tissue, the stele. The walls of the cells at the cortex-stele interface (the endodermis) are thickened by a casparian strip. The stele has alternate bands of xylem and phloem arranged around a central metaxylem vessel (Esau, 1953).
Further back from the root hair zone, lateral branch roots arise from within the stele, adjacent to the phloem. They grow through the cortex and ramify into the soil, their structure resembling that of the main root. In the older regions of the root, the cortex dies leaving only the stele so that the root appears to become thinner as it gets older. In the deeper regions of the soil, the anatomy of the nodal roots is similar to that of a seminal root. Where the roots emerge from the node, near the soil surface, the outer part of the cortex develops a thick band of sclerenchymatous tissue beneath the epidermis, giving the root considerable mechanical strength. The region of thickening extends for about 40 mm so that the roots emerging around the stem form a root-soil plate. This anchors the plant firmly in the soil and prevents it from being blown over. When lodging occurs through the overturning of the plant, rather than because of stem breakage (root lodging), the whole root plate is torn from the soil (Ennos, 1991).
SHOOT APEX DEVELOPMENT
The apex is already well formed in the embryo, and from germination onwards it changes in form and complexity as, at first, leaves and, later, flowers are formed (Bonnet, 1966; Gardner et al., 1985; Kirby and Appleyard, 1987; Williams, 1975). The change in the form of the apex results from two parallel processes: first, the initiation of primordia (Kirby, 1974) and second, from the increasing complexity of each primordium as development proceeds.
At first the apex is conical in shape and initiates leaves (Figure 2.5a). As development proceeds the apex becomes more cylindrical in shape, indicating that the initiation of spikelet primordia has begun (Figure 2.5b). The next recognizable stage is the double ridge stage (Figure 2.5c). Each of the primordia initiated on what will eventually become the ear has two parts (the double ridge). The lower, smaller ridge is a leaf primordium, the further development of which is more or less completely suppressed, but vestiges may be seen at maturity beneath the lowest spikelet on the ear as a ridge of tissue sometimes referred to as a collar. The upper, larger ridge eventually differentiates to become the spikelet. The double ridge stage is sometimes considered to be the beginning of floral differentiation, but it occurs when from 40 to 80 percent of the spikelets have been initiated.
From the double ridge stage onwards, attention is focused on the differentiation of the spikelets, as the various floral structures (glumes, lemma and palea, lodicules, stamens and carpel) are initiated (Figure 2.5d-f).
Eventually, when about 20 spikelet primordia have been initiated, the final number of spikelets is determined by the formation of a terminal spikelet. This occurs when the last initiated primordia, instead of becoming spikelet primordia, develop into glume and floret primordia (Figure 2.5g). The terminal spikelet stage is regarded as a key stage in wheat phenology. At the terminal spikelet stage, the shoot apex is a fully formed embryo ear and further development is described in section "Ear and ear formation".
Studies of the anatomy of the shoot have revealed that the leaf and the florets originate in different tissues (Williams, 1975). Leaf primordia arise from the superficial layer of cells (dermatogen, tunica), while the spikelet primordia are initiated in the deeper layers of the apex, the corpus or core (Figure 2.6).
The leaf is divided at the ligule into a cylindrical sheath and the flat blade or lamina. The sheath is tubular at the base, but nearer to the blade it is split and the margins overlap. The lamina has a fairly well-marked midrib, along which runs the major vascular bundle of the leaf. It divides the blade into two subequal parts, each of which has a number of parallel lateral ribs or veins. Each vein marks the position of a vascular bundle, and the tissue over the bundle is raised producing a ridge so that the adaxial surface of the blade is corrugated. The abaxial surface is more or less flat. The midrib extends down into the sheath for a short distance as a pronounced ridge. The leaf blade naturally assumes a twist, and just below the tip, usually about two-thirds along the leaf, there is frequently a constriction. This constriction is produced by the constraint upon growth produced by the closely investing ligule of the subtending leaf during development. The ligule is a thin colourless flap of tissue about 1 to 2 mm in length, which encircles the leaf or the culm above it beyond where the blade diverges. Associated with the ligule are the auricles, two small earlike projections fringed with unicellular hairs.
Successive stages of shoot apex development from a vegetative apex (a) to terminal spikelet stage (g)
Source: Adapted from Kirby and Appleyard, 1987.
(Courtesy of Arable Unit RASE)
Longitudinal section of shoot apex at the double ridge stage
At the base of the leaf sheath of the culm leaves, there is a thicker zone called variously the joint knot or pulvinus. It is considerably thicker and generally lighter green than the sheath above or the stem below. The node of the stem is below the joint and its position is marked by a slight constriction of the stem. The joint has an important function, lifting the ear of a lodged stem off the ground and restoring it to a more or less vertical position.
Leaf shape and size change with leaf position. The lowermost leaf on the main shoot has parallel sides to within 1 cm or so of the tip so that the tip itself is characteristically blunt. The leaves above the first have more or less parallel sides for about two-thirds their length above which they taper to a sharp point. The last leaf produced upon the culm, the flag leaf, tapers from about the lower third, giving the leaf an elongated ovate shape.
In spring wheat, lamina length increases with increasing leaf number from the base, reaching a maximum one or two leaves before the flag leaf after which the length declines so the flag leaf is somewhat shorter than the longest leaf. Lamina width increases with leaf position so that the flag leaf is the widest leaf. Sheath length also increases with leaf position, markedly so for the culm leaves. Winter wheat shows comparable size changes, but associated with the long vegetative period, the first-produced leaves show little change. Heteroblastic development is also seen in some anatomical features of the leaf.
There are three main features of the anatomy of the leaf. The ad- and abaxial epidermis of the mature leaf enclose the mesophyll, which is traversed at intervals by the vascular tissue (Esau, 1953). The vascular tissue and mesophyll are organized in alternate strips of tissue running parallel with each other along the long axis of the leaf. The vascular tissue lies beneath the ridges of the lamina and the associated thickening capping the vascular bundle of the midrib, and the major veins extend from the ad- to the abaxial epidermis.
The adaxial epidermis is a complex tissue with several cell types (Esau, 1953). The bulliform (bubble-shaped) cells are the largest cells lying between the veins at the bottom of the furrows. When seen in optical section, they are roughly coffin-shaped with the long axis of the cell running parallel to the long axis of the leaf. Flanking the bulliform cells are long cylindrical cells with a smaller diameter than the bulliform cells, alternating in a regular manner with stomata. There is usually a single row of stomata between each rank of bulliform cells and the vascular tissue. Each stoma is made up of two characteristic shaped guard cells and has two associated accessory cells. The stoma length varies from 42 to 51 µm. The frequency of stomata varies from about 63/mm2 to 109/mmThere are more on the adaxial surface and are more densely distributed towards the tip. On the other flank of the row of stomata, over the veins there are long cylindrical cells characterized by thickened wavy walls. The long cells are interspersed in a regular manner by short cells of two types, cork cells and silica cells. Short, unicellular hairs occur mainly over the veins and on either side of the row of stomata.
The abaxial epidermis has fewer cell types, mainly the long cylindrical cells with wavy walls interspersed by short cells. Stomata occur in the same position relative to the veins as in the adaxial epidermis and, although hairs occur, they are less frequent than on the adaxial epidermis.
The epidermis on both surfaces of the leaf has a cuticle with strongly developed epicuticular wax. The form of the wax depends upon the surface of the leaf and the position of the leaf on the stem. This occurs as lobed plates, simple plates, flat ribbons and tubes, the amount and form of the wax depending on the position and surface of the leaf.
The mesophyll cells are of a complex lobed shape, resembling armed palisade cells (Esau, 1953). When viewed in transverse section, the subepidermal cells of the mesophyll are elongated similar to palisade cells. The cells in the middle layers of the leaf are not so elongated. Viewed in longitudinal section, the lobed nature of these cells is apparent. In the leaves at the base of the plant, the degree of lobing is low and the dimensions of the lobes are large. With ascending leaf position up the stem, the degree of lobing increases and the diameter of the lobes decreases. The effect of these changes is to increase the cell surface area per unit area of leaf with ascending leaf position up the stem.
There is variation in the compactness and arrangement of the mesophyll cells. Some cultivars have a relatively loose arrangement of cells, while in others the cell arrangement is more compact and files of cells radiate in a regular manner from the vascular bundles. Prominent sub-stomatal cavities occur, particularly beneath the stomata of the abaxial surface of the leaf.
The vascular bundle has the structure typical of a C3 plant. The phloem is abaxial to the xylem and in the larger bundles consists of regularly arranged sieve tubes and companion cells. The xylem has two large, prominent xylem vessels between which are smaller metaxylem vessels and fibres. Adaxial to the metaxylem, there is an area of disrupted protoxylem. The conducting elements are surrounded by an inner (mestome) sheath and an outer (parenchyma) sheath, though these are not as clearly defined as in some other C3 plants. The cells of the mestome sheath are small and thick-walled and are without chloroplasts. Those of the outer bundle sheath are large and thin-walled and contain chloroplasts. In longitudinal section, the cells of the bundle sheaths are elongated with blunt ends. The walls of the mestome sheath are lignified, and sometimes the wall adjacent to the conducting elements is thicker than the other walls of the cell. The complex fine structure of the mestome sheath is important in regulating the transport of water and solutes (OBrien and Zee, 1971).
The small veins that interconnect the main longitudinal veins consist only of a single sieve tube and xylem vessel and two files of parenchyma cells. They pass through the mestome and parenchyma sheaths and connect directly with the metaxylem and metaphloem of the main bundles. They do not have bundle sheaths, and the vessel walls have a complex fine structure depending on the adjacent mesophyll walls.
The major bundles run parallel with each other the whole length of the leaf. The small transverse veins, which constitute about 7 percent of the total length, occur every 2.5 to 3 mm (Figure 2.7). Towards the tip of the leaf, the smaller longitudinal bundles terminate in a Y-shape, the forks of the Y comprising small transverse veins that link to the longitudinal veins at either side. At the pointed tip of the leaf, the veins converge and connect with each other. The distance between the longitudinal veins varies from about 0.3 mm in the first leaf to about 0.15 mm in a culm leaf (Black-man, 1971).
Leaf sheath base
In the mature, erect stem, there is a ring of vascular bundles in the joint nearer to the inner wall of the cylindrical leaf sheath. Unlike the sheath above the joint where each bundle has prominent sclerenchyma girder, there is no sclerenchyma and lignification is minimal. Associated with each vascular bundle and peripheral to it, there is a massive zone of collenchyma. The parenchyma cells of the ground tissue of this region are arranged in regular files and have very short vertical axes.
The tissue of the joint remains capable of further elongation long after meristematic activity has ceased in the base of the leaf sheath and the internode. When the stem is bent from the vertical, as for instance when the crop is lodged, the lower side of the joint grows by cell elongation and raises the peduncle and ear to a vertical position.
Each leaf is initiated at the shoot apex. It appears first as a bump on the flank of the apex, which by continued lateral and acropetal growth forms a crescent-shaped ridge and later, as it overtops the shoot apex, becomes cowl-shaped (Figure 2.5a). Further growth gives rise to a split cylindrical structure with the margins overlapping. When the leaf is about 20 mm long, the ligule is initiated. The leaf eventually grows up through the sub-tending leaf sheaths, the lamina expands and lastly the growth of the sheath stops.
Cytologically, the events that lead to the formation of a leaf sheath begin with perclinal divisions in the outermost cell layer (tunica) of the apex, which occur first in the mid-position of the leaf and extend round the flanks of the apex to give rise to the crescent-shape bump. Growth then becomes apical and marginal. After the leaf overtops the apex, apical growth ceases, and increase in length is by cell division throughout the primordium. Later growth is centred at the basal part of the young leaf in an intercalary meristem. At this stage, there is no distinction between sheath and lamina, but when the leaf is about 20 mm long, the ligule develops from the adaxial protoderm and a further intercalary meristem produces the cell division, which gives rise to the sheath. The concentration of growth at an early stage in the basal intercalary meristems means that the tip of the leaf matures before the base and that the lamina expands and stops growth before the sheath.
Drawing of the venation of leaf 1 (upper rank) and leaf 6 (lower rank), a culm leaf, showing from left to right the tip, the mid-part of the lamina and the mid-part of the sheath; note the blunt tip of leaf 1
Source: Blakman, 1971.
(Courtesy of Clarendon Press Oxford)
Procambium, which later differentiates to form the vascular tissue, first appears in the median position about two plastochrons after primordium initiation. It is not continuous with the main vascular system of the shoot. It extends both basipetally and acropetally, and six plastochrons after initiation, it connects with the vascular system in the nodal complex of the leaf. The first lateral procambium is seen about four plastochrons after initiation, and further strands are initiated in intermediate positions as the leaf becomes more mature (Sharman and Hitch, 1967).
The procambium of the small transverse vascular bundles does not initiate until the leaf is almost completely differentiated. Cells in the files of mesophyll cells do not elongate, and a row of disc-shaped unelongated cells extends between the longitudinal vascular strands. These rows of disc-shaped cells occur at intervals of 10 to 15 cells in the mesophyll cell files. Each disc cell then divides tangentially, and the daughter cells also divide once, tangentially. This produces a row of four cells. The two outermost cells differentiate to become parenchyma cells, while the abaxial inner cell becomes a sieve element and the adaxial inner cell becomes a tracheary element.
The terminal four to seven internodes of the shoot elongate to form the flowering stem or culm, and internode elongation is complete by the time of anthesis. Internodes increase in final length from the base of the culm to the uppermost internode, which carries the ear, or the peduncle (Figure 2.1). The basal internodes are shorter than the enclosing sheath of the subtending leaf, while the peduncle and the penultimate internode are longer than enclosing sheaths, revealing a length of bare stem and carrying the emerged ear clear of the sheath. Sometimes, in environmentally stressful conditions, internode elongation is restricted and the ear remains partially enclosed in the flag leaf sheath.
The strong, thickened sheaths of the culm leaves are structurally important for stem strength and stiffness, and the knot or pulvinus is instrumental in carrying the ear aloft if the plant is lodged (laid flat usually by wind or rain).
The outermost tissue layer, the epidermis, has longitudinal lines of stomata. It encloses a mechanically strong sclerenchymatous tissue in which, beneath lines of stomata, are bands of chlorophyll containing parenchyma, similar to the leaf mesophyll. Small vascular bundles also occur in this tissue. The largest bundles are found in the innermost layer of parenchymatous tissue (Percival, 1921).
The stem is solid at the nodes, but between the nodes the central pith breaks down to form an internodal lacuna and the stem is hollow. Vascular bundles are arranged around the internode and run its full length. There are two concentric rings of vascular bundles, those in the outer ring much smaller than those in the inner ring. Generally, there are about 20 bundles in the inner ring and 25 in the outer ring (Patrick, 1972a; Percival, 1921).
At each node, some bundles diverge and enter the attached leaf, while other bundles pass through and enter the next internode. While their route can be traced through the nodal region, bridging strands between the bundles are such that it is thought that there can be ready interchange of nutrients at each node (Patrick, 1972a, 1972b; Hitch and Sharman, 1971; OBrien and Zee, 1971).
During shoot apex development, all the internode primordia (and most of the spikelet primordia) are initiated before culm elongation commences (usually between the late double ridge and terminal spikelet stages). The lowermost internode of what will become the culm elongates first, followed in succession by the next distal internode, then the next, and so on. Elongation is part of coordinated events at each phytomer in which the lamina, sheath and internode elongate in a well-ordered succession (Kirby et al., 1994).
As the internode elongates, the provascular strands are initiated in the cortex and an intercalary meristem develops at the base of each internode. The bundles continue differentiation in the upper part of the internode, while at the intercalary meristem, where there is rapid expansion, protophloem and protoxylem are formed and destroyed. As maturity approaches and meristem activity ceases, the bundles complete their development and the internodal lacuna is formed.
The wheat plant has the ability to tiller, i.e. to produce lateral branches. At the end of the vegetative phase of development, the plant will consist of, in addition to the main shoot, a number of tillers. Exactly how many are present at this stage varies widely depending on factors such as plant population, sowing date, mineral nutrition and the application of plant growth regulators. Of the tillers present at this time, only a proportion will survive, the rest dying without producing an ear, possibly due to competition for resources, such as light or nutrients.
It may be necessary to identify tillers, e.g. for analyses of the effect of tiller position on tiller yield. Classification systems generally either number the tillers in a series, starting at the coleoptile tiller (the first potential tiller) or identify tillers with reference to the leaf in whose axil they appear (Peterson et al., 1982; Kirby and Appleyard, 1987). In the latter system, which leads to least confusion, the main shoot (MS) bears primary tillers in the axils of its leaves (Tl in the axil of leaf 1, T2 in the axil of leaf 2, and so on) (Figure 2.8). The tiller borne in the axil of the coleoptile is termed TC (TO by some such as Peterson et al., 1982). Each primary tiller has a potential to bear a number of secondary tillers; these are similarly labelled with reference to the primary tillers, e.g. Tl1 is the tiller borne in the axil of leaf 1 of tiller 1. The tiller borne in the axil of the prophyll is coded P: thus TCP is the tiller in the axil of the prophyll of the coleoptile tiller. The system can easily be extended to higher-order tillers (e.g. tertiary tillers, T111 or fourth-order tillers, T1111 and so on).
Tillering normally starts when leaf 3 is fully expanded and leaf 4 is emerging on the main shoot with the appearance of the first leaf of T1 above the ligule of leaf 1. Further tillers are produced in the regular sequence, their appearance coinciding with the emergence of the third leaf above the leaf subtending the tiller. Thus, the relation of tiller to leaf emergence can be described in terms of leaf or phyllochron interval, i.e. the number of leaves that emerge between the emergence of a leaf and that of its subtending tiller (Friend, 1965; Masle-Meynard and Sebillotte, 1981; Klepper et al., 1982). The phyllochron interval is generally similar for all tiller positions, and the rate of leaf emergence is more or less the same on the main shoot and tillers so that the potential increase in numbers of tiller per plant can be predicted. The behaviour of the coleoptile tiller in this sequence is often anomalous. Under most conditions, the frequency of emergence of TC is much lower than that of Tl, although it is affected by sowing depth, temperature, nutrient supply and irradiance.
Nomenclature for leaves and tillers
Source: Kirby and Appleyard, 1985.
(Courtesy of Kluwer Academic Publishers)
Tiller bud initiation and development
Tiller buds are initiated in the axils of the basal leaves of the main shoot. The buds in the axil of the coleoptile and of leaf 1 are present in the embryo. After germination, tiller buds are initiated in the axils of leaves as they are formed. Buds are usually positioned adjacent to the overlapping margin of the subtended leaf and thus tend to be arranged asymmetrically, not on the midline (Williams, 1975). Each bud begins as a ridge of tissue in the axil of the leaf and appears to originate from the tissue of the subtended leaf or its disc of insertion. As the tiller bud meristem grows, the prophyll is initiated on its flanks and encloses the shoot apex. The prophyll is a modified leaf, which appears to have a similar function to the coleoptile, forming a guide for the extension of the young leaves enclosed within it. There is no development of the lamina and it resembles a flattened leaf sheath with two large lateral veins. Subsequent development is similar to that of the main shoot. If the tiller bud continues to grow, then the prophyll extends to the length of the sheath and the first tiller leaf emerges.
In general, buds are not formed in the axils of leaves that subtend an elongated internode, except the lowermost node of the elongated stem where a bud is sometimes found. Where a bud is present at this node, the internodes above and below are short (Williams and Langer, 1975).
Tiller bud initiation is related to the development of the subtending leaf. At the emergence of a leaf, the bud that subtends it is about 1 mm long and is visible on dissection (Stern and Kirby, 1979). If the environment is unfavourable, growth quickly slows and stops, and the bud does not grow to a length of more than 2 to 3 mm. Under favourable conditions, leaf and spikelet primordia are initiated at about the same rate as those of the main shoot (Stern and Kirby, 1979).
There is little variation between the main shoot and the dominant primary tillers (T1, T2 and T3) in the number of spikelets initiated or in the pattern of primordium initiation. Fewer leaves are formed on T1 than on the main shoot, and the number of leaves declines progressively on later formed tillers. Thus the duration of leaf initiation becomes progressively shorter, and this tends to synchronize the development of ears (Stern and Kirby, 1979).
Ear and ear formation
As it approaches anthesis, the ear is completely formed and the pollen grains and carpel are fully developed. After anthesis, the florets open, pollen is released and the carpels are pollinated. The stamens and lodicules, their role fulfilled, die and shrivel, and further growth and development takes place in the carpels, the developing grains. At this stage, the ear consists of the main axis or rachis with each internode ovoid in section and curving around the spikelet. A single spikelet is attached at each node, and the rachis terminates in a spikelet set at right angles to the lateral spikelets. There is a gradient of size and maturity along the ear, with the largest and most advanced spikelets situated in the mid-part of the ear. Under unfavourable growing conditions, the lowermost spikelet and those at the top of the ear may be poorly developed and devoid of fertile florets.
Each spikelet comprises an axis, the rachilla, which bears two glumes and a number of florets (Figure 2.9). Within each spikelet, there are usually from two to four potentially fertile florets. The floret has two sheathing structures, the outer lemma and the inner palea; these envelope two lodicules, three stamens and the carpel (Figure 2.10). Each stamen is made up of a filament, which is very short at this stage, and a yellow anther. The anther is about 3 mm long and has four chambers or loculi containing numerous pollen grains. The spherical pollen grain has a small circular pore and contains a single nucleus and starch grains (Percival, 1921).
The basal part of the carpel, the ovary, is obconical or obovate and white in colour with a smooth surface except at the tip, which has numerous unicellular hairs. The ovary contains a single ovule oriented so that the nucellar apex (micropyle) is slightly below the horizontal mid-plane of the ovule. The ovule has two integuments enclosing the nucellus embedded in which is the embryo sac (Percival, 1921). The embryo sac contains an egg nucleus with two associated nuclei (the egg apparatus), two polar nuclei and between 20 and 30 antipodal cells, which are highly polyploid (Bennett et al., 1973).
Diagram of a spikelet
Source: Kirby and Appleyard, 1987.
(Courtesy of Arable Unit RASE)
The basal florets are generally fertile, but some of the distal florets die sequentially during ear development.
After initiating leaves, the apex changes in form and initiates about 20 spikelet primordia, terminating in a terminal spikelet (Figure 2.5g). Throughout ear development, the most advanced primordia occur in the mid-part of the ear. From the double ridge stage onwards, the various structures of the spikelet are initiated in a centrifugal succession. Thus, the primordia of the glumes are initiated first, followed in succession by the florets. About ten floret primordia are eventually initiated, after which the spikelet apex ceases activity and eventually degenerates. Thus there is a gradient of development of the florets within the spikelet, the most mature floret occurring at the base while the most distal florets develop very little and eventually die (Plate 1).
Within the spikelet, initiation also proceeds centrifugally, the lemma and palea forming first and finally the carpel (Barnard, 1955; Williams, 1975). The development of each floret is determinate as the floret apex is transformed into the carpel. As the stamens develop, they become differentiated into a filament and anther, which eventually has four chambers or loculi containing the pollen grains.
Transverse section of a floret, showing the ovary in the centre, surrounded by three stamens, each anther with four loculi
As each lobe of the anther develops, a column of archeosporial cells (forerunners of the pollen grains) develops by successive mitoses until the pollen mother cells are formed. As they approach meiosis, their development is blocked at pre-meiotic interphase and sub-sequent meiosis takes place synchronously (Bennett et al., 1971). Meiosis in the pollen mother cells is concurrent with that of the egg cell in the ovule. Following meiosis, the pollen grains and the embryo sac complete their development (Bennett et al., 1971). The synchrony of meiosis and the timing of the various stages have been described in detail (Bennett et al., 1975). Externally, meiosis may be recognized by the presence of green anthers when the ear is about to emerge from the inflated flag leaf sheath (the boot).
The carpel is formed by the transformation of the floret apex. After stamen initiation, a ridge of tissue forms on the flanks of the apex and a cowl-shaped structure grows over and eventually enfolds the apex, which then differentiates to form the carpel. Within the ovule, an archeosporium cell differentiates and eventually becomes the megaspore mother cell (Barnard, 1955). As the carpel continues to develop, the tip grows out to form a two-lobed stigma, each one profusely branched.
Anthesis occurs about three to ten days, depending on the environment, after the ear emerges from the flag leaf sheath, when a number of closely correlated events occur in a very short time. The lodicules of each floret swell up, forcing apart the lemma and palea. The filaments of the stamens elongate and may eventually attain a length of about 10 mm. As the filament grows, the anther dehisces, each chamber developing a longitudinal split, starting at the tip of the anther, through which pollen is released. The stigma lobes, which are pressed together before anthesis, move apart, and the receptive branches are spread widely giving a large area for pollen interception. The whole process is complete within about five minutes (Percival, 1921).
Cultivars differ in the degree to which the lemma and palea are separated, and in some closed-flowering types, the lemma and palea do not diverge, the anthers and stigma remaining enclosed within the lemma and palea. In open-flowering types, the stamens dangle from the florets and the stigma spreads widely.
Most carpels are pollinated by pollen from anthers in the same floret, but there is a possibility of pollination from other plants, resulting in cross fertilization. Generally, the lodicules lose their turgor in less than an hour and the floret closes. If the floret has not been pollinated, the stigmas remain receptive for up to about five days after anthesis and the floret may open again, this time by the swelling of part of the ovary, not the lodicules, which degenerate after the first opening.
Sequence of anthesis within an ear
Anthesis occurs first in floret 1 of the spikelets of the upper two-thirds of the ear. The next day or so it progresses to the first floret of the basal spikelet and to the second floret of the upper spikelets. This progression continues so that the third and fourth florets in the basal spikelet are the last in which anthesis occurs (Evans et al., 1972). Often, the higher order florets (three to five), although going through the process of anthesis and becoming pollinated, do not produce grain. Anthesis within an ear is accomplished within four to seven days.
Within the crop, anthesis occurs first in the main shoot, but all shoots commence anthesis within three or four days. The whole process is usually complete in ten days or less, depending on the weather.
Pollination and fertilization
The pollen grain, which has a lifespan of about five hours, when settled on a stigma, germinates in about one and one-half hours to produce a pollen tube. This grows down the style, between the cells, and eventually reaches the embryo sac via the micropyle. Two sperm nuclei move down to the tip of the pollen tube; a tube nucleus is also present, but this may not leave the pollen grain (Percival, 1921). At normal temperatures, the pollen tube reaches the embryo sac in about 40 minutes (Bennett et al., 1973). On reaching the embryo sac, the sperm nuclei are discharged and fuse with the egg nucleus (which develops to become the embryo) and the polar nuclei (which form the endosperm).
Division of the fertilized egg nucleus commences later than that of the endosperm (Bennett et al., 1973). The early divisions produce a five-celled embryo with a basal cell (Percival, 1921), although variation in the pattern of development has been observed. Continuing cell division produces at first a club-shaped structure, which ultimately differentiates to form a mature embryo in the ripe seed.
The growth of the embryo is supported by nutrients derived from the antipodal cells and from the hydrolysis of parenchyma cells of the nucellus and neighbouring endosperm cells. Later in development, transfer cells appear in the nucellar endosperm epidermis, near the base of the embryo and the pro-vascular tissue (Smart and OBrien, 1983; Huber and Grabe, 1987).
Following the fusion of the sperm nucleus and the polar nuclei, cell division is, for a time, synchronous, the number of endosperm cells doubling every four to five hours. At first, the endosperm is coenocytic, but after about three days cell walls are formed (Bennett et al., 1975). Cell wall growth commences at the edge of the embryo sac and furrows inwards to the central vacuole. The cells at the periphery of the endosperm divide, and eventually the entire embryo sac is cellular (Morrison and OBrien, 1976; Morrison et al., 1978). After cell formation is complete, the sub-cellular structures, which will synthesize the protein bodies, and the other cell components are formed (Bechtel et al., 1982; Briarty et al., 1979). Amyloplast division ceases before cell division, and starch grains differ in growth rate in different cell layers of the endosperm (Briarty et al., 1979).
External changes during growth of the grain
Externally, development of the wheat grain is characterized by changes in colour and increases in dry and fresh mass and length. Based on these characteristics, schemes of arbitrary stages have been described (Rogers and Quatrano, 1983; Noda et al., 1994). The recently fertilized grain is creamy white in colour and when squeezed exudes clear liquid. It grows rapidly in length, attaining its maximum length in about ten days, and becomes green in colour as chlorophyll is formed. At this stage, the exudate becomes milky as starch grains are deposited. As growth proceeds, the endosperm becomes firmer (the soft dough and the hard dough stages) until, at physiological maturity, the green colour is replaced by golden-yellow, which deepens as the grain desiccates to dead ripeness.
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