plant development

Introduction

      a multiphasic process in which two distinct forms succeed each other in alternating generations. One form, created by the union of sexual cells (gametes (gamete)), contains two sets of similar chromosomes (diploid). At sexual maturity, this form, called the sporophyte, produces an offspring (gametophyte) with cells containing only one set of genetic instructions (haploid). At their sexual maturity, gametophytes produce haploid gametes that unite to begin a new cycle.

      Although both plants (plant) and animals (animal) share the chemical basis of inheritance and of translation of the genetic code into structural units called proteins, plant development differs from that of animals in several important ways. Higher plants sustain growth throughout life and, in this sense, are perpetually embryonic; animals, on the other hand, generally have a determinate period of growth, after which they are considered mature. Furthermore, both growth and organ formation in plants are influenced by their possession of a rigid cell wall and a fluid-filled space called the vacuole, two features unique to the plant cell. Conversely, certain features of animal cells are absent in plants. Notable is the lack of cellular movements and fusions that play an important part in tissue and organ development in higher animals.

General features

Life cycles (life cycle)

  ‘The life cycle of all tracheophytes (vascular plants), bryophytes (mosses and liverworts), and many algae and fungi is based on an alternation of generations, or different life phases: the gametophyte, which produces gametes, or sex cells, alternating with the sporophyte, which produces spores. Gametophytes develop from the spores and, like them, are normally haploid; i.e., each cell has one set of chromosomes. Sporophytes develop from a fertilized egg, or zygote, that results from the fusion of gametes (fertilization) formed by the gametophytes; they are accordingly diploid; i.e., each cell has two sets of chromosomes. Although the two generations are phases of one life cycle, they have independent developmental histories; each begins as a single cell, passes through a juvenile period, matures, and gives rise to the alternate phase.

      In various algae and fungi the two generations are alike in form (i.e., are isomorphic), and, despite the difference in chromosome number, their development follows essentially identical pathways. More commonly, however, the alternating generations have different forms (i.e., are heteromorphic); this is true for the bryophytes and for all vascular plants, both angiosperms (flowering plants) and gymnosperms (conifers and allies). General rules for vascular plants are that the sporophyte generation is physically the larger, has a more complex developmental history, produces a greater range of cell types, and expresses a more diverse biochemistry; the gametophyte is often diminutive, reduced in the case of the angiosperms to a mere few cells. In the bryophytes, the gametophyte generation, rather than the sporophyte, is the more conspicuous.

      Although the gametophyte generation in vascular plants is small and has limited physiological capabilities, its cells must convey genes capable of directing the sporophytic developmental pattern, because the pattern is transmitted through the gametes to the zygote. The expression of “sporophytic” genes must therefore be repressed in the gametophyte, probably from the time of spore formation (sporogenesis). Correspondingly, events associated with gamete formation (gametogenesis) or fertilization must somehow free the sporophytic genes and thus permit the zygote to enter the sporophytic developmental pattern. Although it might be supposed that the “switch” is associated with the difference in chromosome number between the haploid spore (a single set) and the diploid zygote (a double set), this has been shown not to be the determining factor.

      The alternation of generations illustrates an important principle, namely that cell lineages arising from single parental cells containing the same genetic potentiality may pursue mutually exclusive developmental patterns. Channelling, or canalizing, events of this nature occur repeatedly in the course of development of an individual plant, beginning with the pattern of cell division from the very first cleavage of the zygote cell.

Body plans

      Collectively plants manifest a wide range of body plans, ranging from the single cell (or unicell), with a single nucleus, through various types of colonial and filamentous forms to massive multicellular structures (multicellular organism). (Algae, including the single-celled forms, have a great deal in common in structure and biochemistry with vascular plants. Bacteria and fungi generally are not considered plants, but because of their various plantlike qualities they are taken as plants for the purposes of this section.)

      For the unicell, development is the same as cell differentiation. Although many unicellular fungi and algae show little differentiation other than that connected with reproduction, others undergo elaborate structural changes that illustrate many principles basic to development in multicellular plants. An important example is the green alga Acetabularia. This alga first produces a rootlike system and stalk and then, later, a flattened umbrella-like cap. The developmental potentialities of this unicell, with its single nucleus, are, however, limited; in order for there to be any advance beyond the state seen in Acetabularia, with the development of greater body mass and a division of labour among different parts, an increase in the number of participating nuclei seems obligatory.

      One method of providing more nuclei is by nuclear division without a corresponding cell division; the result is a coenocytic structure. Plants with this type of multinucleate organization show considerable diversity; examples are found in both algae and fungi. Growth occurs by the extension of the cell wall in certain zones, usually at the tips of filaments, and structural differentiation results from branching and the specialization of parts for particular functions. The aggregation of coenocytic filaments can lead to the development of a three-dimensional body, or thallus, but plants with this type of organization have not achieved great size.

      A more significant type of body plan, one based on the multicellular filament, is found in its most simple form in certain algae known as diatoms (diatom), in which chains of cells of indefinite length arise, although the cells show no evidence of interaction. More advanced is the condition of many other algae, in which there occur branches that may either be identical with the original filament or show structural or physiological specialization. This condition occurs in certain green algae, in which the main branches creep and the lateral branches grow erect; such diversification represents an important developmental innovation and, possibly, the evolutionary beginnings of organ specialization in plants.

      Three-dimensional body forms may evolve from the association of cells in colonies. Cells among the colonial green algae are of definite number; each component cell resembles a free-living unicell, but all are united by cellular connections, or plasmodesmata (plasmodesma), which may be important in coordinating the development of the colony. Colonies are often of precise geometric shape, forming either a circular plate or a sphere. In elaborate ones, certain cells are specialized for reproduction, and others are concerned primarily with movement.

      Another developmental pathway resulting in more massive body structure is by the association of filaments. The reproductive structures of many fungi are composed of large numbers of closely interwoven filaments, which, although not physically connected, do interact in some way to produce structures such as the mushroom cap. Several filamentous body plans are found among the red algae. In one, a single main (axial) filament grows at one end, but, just behind its tip, cells divide to produce a number of lateral filaments that grow parallel with the axial filament. The older parts of the thallus, therefore, seem to be an aggregate of filaments. More massive structures are produced when there are several axial filaments; and, by branching, particularly when accompanied by fusion, dense tissues resembling the basic undifferentiated tissue (parenchyma) of higher plants are formed. In these algae, cellular connections occur between daughter cells of a filament, and others may develop secondarily between cells of neighbouring filaments.

      The transition from a filamentous to a three-dimensional form appears most notably in the brown algae. In certain brown algae, growth is by an axial filament, but, behind the tipmost cell, divisions produce a denser tissue lacking evidence of filamentous organization. In the sporophytes of kelp, one of the largest and most complex of the algae, cell division often is restricted to areas comparable to the growing tips of vascular plants, and, although a filamentous organization may be evident in the centre of the thallus, the surrounding cortical regions are composed of a tissue that is essentially undifferentiated. (The gametophytes of kelp, however, have a simple filamentous organization.)

      Among nonvascular plants, true parenchyma is found in the bryophytes (bryophyte), in both the gametophyte and sporophyte phases. The development of the moss gametophyte illustrates the transition from a filamentous to a highly organized three-dimensional growth form. The moss spore germinates into a filamentous plant, the protonema, which later produces a leafy shoot. This type of transition from simple to more complex growth form is accompanied by the synthesis of new kinds of ribonucleic acids ( RNA's), presumably through the activation of genes that were not expressed during the early growth of the gametophyte.

      Much of the remainder of this section is concerned with the development of the complex body forms of vascular-plant sporophytes, which do not normally pass through any filamentous stages. It may be noted, however, that, in the course of evolution, the capacity for this type of growth has not been lost, since it may be adopted by cells grown in tissue cultures in the laboratory.

Preparatory events

      The sporophytes of all vascular plants produce cells called spore mother cells—since they will give rise to spores—in spore cases (sporangia). Spore mother cells are usually surrounded, during development, by a special nutritive tissue. In the more primitive groups each sporangium holds many mother cells. This is true also in the pollen-producing sporangia of gymnosperms and angiosperms but not in the egg-producing sporangia (ovules), which usually have only one mother cell.

      In certain lower vascular plants, typified by the club moss Selaginella (spike moss), the gametophyte is formed entirely—or almost entirely—within the spore wall. Two kinds of gametophytes develop from the two kinds of spores produced by the sporophyte in different sporangia; the larger spore (megaspore) gives rise to the female gametophyte, the smaller spore (microspore) to the male. This condition is referred to as heterospory. The gametophytes, or prothalli, of other club mosses and most horsetails and ferns are sexually undifferentiated and arise from one kind of spore, a condition termed homospory.

      In these groups the gametophytes develop as free-living and independent plants that ultimately produce the gametes. In general, the male gametes (antherozoids) are produced in globose structures (antheridia) that are either stalked or sunken in the gametophyte. The antherozoids, always many in number, develop from mother cells enclosed in the jacket of the antheridium. Each antherozoid can move by using its whiplike hairs, or flagella, two or three (in the lycopods) or many (in the horsetails and ferns). The female gametes are formed singly in flask-shaped structures (archegonia (archegonium)) that also are either stalked or sunken in the gametophyte. The neck of the flask is closed by neck canal cells, which later break down to permit the entry of the male gamete. The egg itself lies in the basal part, or venter, of the flask, with a ventral canal cell above it. When the male gametes, or antherozoids, are released by the rupture of the antheridium, they swim in a water film to the archegonia and effect fertilization.

      Among the gymnosperms (gymnosperm) the male gametophyte is much reduced and is a parasite on the sporophyte for only a short time. Cell cleavages within the spore wall cut off a prothallial cell, which will give rise to the vegetative (i.e., nonreproductive) part of the plant, and an antheridial cell, which divides into a tube cell and a generative cell. The male gametophyte so formed and contained within the spore wall is the pollen grain. After transfer to the ovule by wind, the pollen grain germinates to form a tube, and the generative cell divides into two cells, one of which forms the male gametes by further division. The gametes bear numerous spirally arranged flagella. The female gametophyte meanwhile develops entirely within the parent sporangium in the ovule. The size of the single functional spore increases greatly as the spore nucleus divides repeatedly to produce numerous free nuclei. Cell-wall formation then begins at the periphery, extending inward until the whole area is divided into cells. Up to four archegonia are formed, sunken in the tissue of the gametophyte, each with a female gamete, or egg.

      The end of the gametophyte phase and the beginning of the sporophyte phase occur at fertilization, when one of the male gametes fuses with the female gamete to form the zygote, which will then develop as the sporophyte. (Development of the sporophyte can, in some cases, be triggered by means other than fertilization, in which case the organism is said to arise parthenogenetically (parthenogenesis).)

      The male gametophyte of angiosperms (angiosperm) is reduced to three cells, one so-called vegetative cell and two male gametes. The division producing the gametes may occur either before dispersal of the pollen grain or later, during the growth of the pollen tube. The female sporangium has one or two coats, or integuments (integument), except for an opening (micropyle) at one end; the sporangium with an integument is called the ovule. The female gametophyte, known in this group as the embryo sac, develops from the parent spore while it is still retained in the sporangium. Three cell divisions result in eight nuclei, which arrange themselves so that three lie at each end and two lie in the centre. The cytoplasm then cleaves and three cells are formed at each pole, leaving two nuclei in a large central cell. The three cells at the micropylar pole (end toward the micropyle) form the egg apparatus. Two of these cells, called synergids, correspond to the neck cells of an archegonium; the third is the egg cell. The three cells at the opposite pole, the antipodals, play a part in embryo nutrition in certain genera. The two polar nuclei in the central cell ultimately unite, becoming the fusion nucleus. The pollen grain is transferred by various agencies (wind, water, animals) to the stigma of the female flower, and, as in the gymnosperms, it germinates to produce a tube. This tube grows through intervening tissues, through an opening (micropyle) of the egg, and enters a cell near the micropyle (synergid), in which the two male gametes are discharged. The unique feature of this phase of angiosperm development is that two fertilizations occur. One male gamete fuses with the egg to give the diploid zygote; the other makes its way to the fusion nucleus in the central cell, already diploid, and by a second fusion gives a triploid primary endosperm nucleus, which is later concerned in the formation of the nutritive tissue, or endosperm.

Early development: from zygote to seedling

Embryo formation

Cleavage of the zygote

      In vascular plants embryo formation, or embryogenesis, usually occurs within a few hours after fertilization, with the first cell division that cleaves the zygote, or fertilized egg, into two daughter cells. Thereafter, rapid cell division provides the building blocks of the primary organs of the embryo sporophyte: the first root, first leaves, and the shoot apex. Temporary structures concerned with embryo nutrition—suspensor and foot—may also be produced. These organs originate in a polarization established at the time of zygote cleavage, but the details of their development vary widely among the different groups.

      In the club mosses (club moss) the zygote divides in a plane at right angles to the axis of the archegonium. The daughter cell toward the neck forms a short filament of cells, the suspensor; the inner cell gives rise to the other organs of the embryo, the shoot, root, and foot. The axis of the embryo is inclined to that of the archegonium and may be almost at right angles. This is in contrast to the behaviour of the true mosses, in which the embryo is oriented along the length of the archegonium, with the foot directed inward and the structures that are equivalent to the shoot, namely the spore capsule and its stalk, directed toward the neck.

      A polarity like that of the mosses appears in the horsetails, in which the zygote divides by transverse and longitudinal walls to form a group of four cells. Of these, the two cells toward the neck give rise to the shoot system; the inner two produce the foot and root.

      The details of early embryogenesis in gymnosperms vary consider-ably. In the cycads and ginkgos, the initial cleavage establishes a polarity opposite to that in the horsetails, the inner cell giving rise to the shoot and the outer producing the root. Many conifers (conifer) are unique in that the zygote undergoes a period of free-nuclear division without cell formation, producing usually four or eight nuclei, which move to the end of the zygote, away from the neck cells, where cleavage begins. In the pines (pine) a further division gives four tiers of four cells. The intermediate tiers extend greatly to form a suspensor; each of the four cells at the lower pole may act as the parent cell of an embryo, a condition sometimes referred to as polyembryony.

      In contrast, there is no free-nuclear stage in angiosperm embryogenesis. The zygote cleaves by a wall more or less at right angles to the axis of the embryo sac. The daughter cell next to the micropyle (basal cell) produces a suspensor and contributes to the root; the inner (terminal) cell gives rise to the shoot system. (Angiosperm embryogenesis is more fully described in the following section dealing with the origin of primary organs.)

      Notwithstanding the variation in the different groups, the pattern of development established in the early cell cleavages is consistent. The primary polarization of the zygote must necessarily be imposed by the adjacent tissues of the sporophyte, but thereafter the fate of daughter cells depends on control established within the young sporophyte itself.

      Although it is often possible to specify the origin of the cell lineages contributing to the various organs and tissue layers, a geometric regularity in cell division is generally maintained through only the first few division cycles in the embryo. The final form of the embryo is thus determined not through the specification of a precise scheme of cell division, as in the development of colonial algae, but through an overall control in which cell and tissue interactions play an important part.

Origin of the primary organs

      Angiosperm embryogenesis can be described in terms of a much studied flowering plant called shepherd's purse (Capsella bursa-pastoris (shepherd's purse)). The zygote divides into two cells (cell), the terminal cell and the basal cell. The terminal cell divides by a wall formed at right angles to the first cleavage wall and then again by a wall formed at right angles to this; a quadrant of cells is thus formed. The partition of the quadrant cells in a transverse plane then produces an octant stage. By transverse divisions, the basal cell forms a filament, the suspensor, of up to ten cells, the end cell of which swells to form an absorbing organ. The attachment cell, or hypophysis, adjoins the octants derived from the terminal cell.

      At this time, the prospective future of each of the zones of the embryo can be specified. Four cells of the octant group will ultimately produce the seed leaves (cotyledons (cotyledon)) and the shoot apex; the other four will form the hypocotyl, the part of the embryo between the cotyledons and the primary root (radicle). The hypophysis will give rise to the radicle and the root cap; the cells of the suspensor will degenerate as the embryo matures.

      The zones of the embryo destined to form the principal organs are established by this first sequence of divisions, and tissue layers are defined during the ensuing divisions. The octant cells divide by curved walls parallel to the surface; in this way the outer layer responsible for producing the epidermis of the shoot system is defined. Divisions of a more irregular nature in the inner zone ultimately define the tissues from which the central cylinder and vascular core of the main axis of the shoot will develop. Simultaneously, the hypophysis forms a group of eight cells by three successive divisions, the planes of which are mutually at right angles. Of these eight cells, the outer four produce the root cap and epidermis; the inner four contribute to the radicle.

      The embryo is at first globular, but it soon becomes heart-shaped by a combination of numerous cell divisions and enlargement in two zones of the outer hemisphere. In this manner two cotyledons form. The volume of tissue between the cotyledons is the prospective shoot apex. The characteristic form of the apex is not established until after germination.

      As the cotyledons become extended, the embryo bends, because of physical restraints, to conform with the cavity of the embryo sac. From the heart-shaped phase onward, the core of the hypocotyl and the radicle appears as a cylinder of narrow and elongated cells. This is the parent tissue of the vascular system of the seedling. The surrounding tissue contributes the cortex layer of the stem and root.

      The embryogenesis of Capsella illustrates only one of several patterns found among flowering plants. Among dicotyledons (dicotyledon), the planes of division of the terminal cell, the form of the suspensor, and the contribution made by the basal cell to the embryo all provide evidence used in determining the embryogenetic plan.

      Monocotyledons, flowering plants the seeds of which contain only one cotyledon, share with dicotyledons such as Capsella the main features of early embryogenesis, including the possession of a suspensor and, in most cases, a fairly regular progression of cell divisions to the octant stage. Thereafter the symmetrical growth pattern is lost through the development of the single cotyledon. In the lily family (Liliaceae), generally accepted as a primitive family of monocotyledons, the cotyledon is derived from an octad of cells arising from the terminal cell. The hypocotyl and stem apex are derived from the proximal cell of a short filament formed by the basal cell, and the root comes from the pair of cells next to it. The suspensor forms from the distal cell or cells of the filament. In the more advanced families of monocotyledons, including the grasses (grass) (Gramineae) and orchids (Orchidaceae), embryogenesis is much less regular. The grass embryo possesses structures that do not occur in any other flowering plants, namely, the scutellum, an organ concerned with the nutrition of the seedling, and the coleoptile and coleorhiza, protective sheaths of the young shoot and the radicle. The scutellum arises from octant cells, which also contribute to the cotyledon. The basal cell forms part of the coleoptile and also gives rise to the shoot apex and the tissues of the root and coleorhiza. The embryo is asymmetrical, with the shoot apex lying on one side in a notch, ensheathed by the coleoptile.

      In marked contrast, embryogenesis of the orchids (orchid) is more simple. Except when a suspensor is formed, early cleavages follow no well-defined plan, and the product is an ovoid mass of tissue called the proembryo. No cotyledon, stem apex, or root apex is organized in this early period; these organs do not appear until after germination has occurred.

Nutritional dependence of the embryo

      During their early growth, the embryos of all vascular plants exist as virtual parasites depending for nutrition on either the gametophyte or the previous sporophyte generation through the agency of the gametophyte or, in the special case of the angiosperms, upon an initially triploid tissue, the endosperm, which is itself nourished by the parent sporophyte.

      The early nutrition of the sporophyte in ferns, horsetails, and club mosses such as Lycopodium is clearly provided by the gametophyte. In these groups the young sporophyte produces a multicellular structure, the foot, which remains embedded in the tissues of the gametophyte throughout early development withdrawing nutrients. Ultimately, both shoot and root of the sporophyte grow out from the gametophyte, but, even after the first leaf has begun to photosynthesize and thus to produce its own food, the gametophyte may persist.

      In Selaginella (spike moss), the gametophytes are sexually distinct. The female gametophyte develops within the wall of the megaspore. The archegonia are exposed after the megaspore wall splits, but the gametophyte never escapes completely. After fertilization, the zygote cleaves, and the outer cell produces a long suspensor that pushes the embryo deeply into the tissues of the gametophyte. A foot is then formed, as in Lycopodium, and further development of the embryo continues at the expense of reserves transferred to the megaspore from the preceding sporophyte generation.

      There are superficial similarities between the nutritional history of the embryo in gymnosperms and in Selaginella, for, in each, the female gametophyte, dependent upon reserves derived from the sporophyte, acts as an intermediary between one sporophyte generation and the next.

      In the pines, the female gametophyte develops within the tissues of the nucellus and acquires abundant food reserves. The proembryo forms after a period of free-nuclear division in the zygote, and the tier of cells above the basal four then elongates to form a suspensor, which pushes the embryonic group deep into the gametophyte. Secondary suspensor cells may form from the basal tier to continue the process. During embryogenesis, the gametophyte continues to grow and to accumulate food materials, which are transferred to the embryo or remain as reserves in the seed.

      The female gametophyte of angiosperms never acquires copious reserves, although starch is frequently present in the central cell and sometimes in the egg itself. The unique feature, here, is that the embryo is nutritionally dependent upon the endosperm, a tissue that, in the genetical sense, constitutes a third organism—neither gametophyte nor sporophyte. Furthermore, as a tissue the endosperm manifests several other special characteristics. The nuclei have three chromosome sets and, therefore, three times the deoxyribonucleic acid (DNA) of haploid cells. As nuclear division ends, the amount of DNA per nucleus increases still further, a condition comparable with that in various plant- and animal-gland nuclei, presumably connected with the nutritional function of the endosperm. Nuclear division takes place at first without cell-wall formation so that a coenocyte is produced; later, partitioning of the cytoplasm results in a cellular tissue.

      The reserves accumulated in the endosperm include carbohydrates (especially starch), lipids, and proteins. As reserves accumulate, the nuclei of the endosperm cells may undergo deformation and degeneration. In many plants the growing embryo consumes the endosperm before seed maturation; in others, the tissue persists in the seed, providing a reserve for the developing seedling after germination. Endosperm is not formed in certain angiosperms. In such cases the embryo depends on the transfer of nutrients directly from the sporophyte.

      Tissues other than the endosperm may become specialized for the early nutrition of the embryo. The antipodal cells of the female gametophyte sometimes acquire glandular properties, as may cells of the nucellus surrounding the embryo sac. In some species the embryo itself develops a suspensor that penetrates the tissues of the parent sporophyte and acts as an absorbing organ.

Dormancy of the embryo

      Among the lower pteropsids (club mosses, horsetails, and ferns), the principal agent of dispersal (dispersion) is the haploid spore and not, as in gymnosperms and angiosperms, the seed, the ripened ovule containing a dormant embryo. Since the embryo of lower pteropsids is not involved in dispersal, it does not usually undergo any marked period of dormancy after the differentiation of the primary organs. Development instead proceeds continuously through dependence upon the gametophyte until the young sporophyte is established as a physiologically independent plant. The embryos of gymnosperms and angiosperms pass into a state of dormancy (afterripening) soon after the differentiation of the primary organs and the sporophyte is dispersed in a seed.

      In the period leading up to dormancy, several changes occur in the embryo. The accumulation of reserves in the cotyledons or elsewhere ceases, respiratory rate declines rapidly, and cell division, with associated protein and nucleic-acid synthesis, stops. Correlated with these events are cellular changes typical of tissues with low metabolic activity. Especially obvious is the general dehydration of the cells that constitute the seed and the thickening of the cell walls of the ovule to form the seed coat (testa). The product is a structure in which the embryo is protected from temperature extremes by its state of desiccation and is often guarded from further drying and from mechanical or biological degradation by the seed coats. The seed coat often contributes to the maintenance of dormancy by physically impeding the passage of water and gases to and from the embryo, by chemically inhibiting germination, and by mechanically restricting the growth of the embryo.

Germination and early growth

      Dormancy is brief for some seeds, for example those of certain short-lived annual plants. After dispersal and under appropriate environmental conditions, such as suitable temperature and access to water and oxygen, the seed germinates, and the embryo resumes growth.

The “breaking” of dormancy

      The seeds of many species do not germinate (germination) immediately after exposure to conditions generally favourable for plant growth but require a “breaking” of dormancy, which may be associated with change in the seed coats or with the state of the embryo itself. Commonly the embryo has no innate dormancy and will develop after the seed coat is removed or sufficiently damaged to allow water to enter. Germination in such cases depends upon rotting or abrasion of the seed coat in the soil. Inhibitors of germination must be either leached away by water or the tissues containing them destroyed before germination can occur. Mechanical restriction of the growth of the embryo is common only in species that have thick, tough seed coats. Germination then depends upon weakening of the coat by abrasion or decomposition.

      In many seeds the embryo cannot germinate even under suitable conditions until a certain period of time has lapsed. The time may be required for continued embryonic development in the seed or for some necessary finishing process—“after ripening”—the nature of which remains obscure.

      The seeds of many plants that endure cold winters will not germinate unless they experience a period of low temperature, usually somewhat above freezing. Otherwise germination fails or is much delayed, with the early growth of the seedling often abnormal. (This response of seeds to chilling has a parallel in the temperature control of dormancy in buds.) In some species, germination is promoted by exposure to light of appropriate wavelengths; in others, light inhibits germination. For the seeds of certain plants, germination is promoted by red light and inhibited by light of longer wavelength, in the “far red” range of the spectrum. The precise significance of this response is as yet unknown, but it may be a means of adjusting germination time to the season of the year, or of detecting the depth of the seed in the soil. Light sensitivity and temperature requirements often interact, the light requirement being entirely lost at certain temperatures.

      In the process of germination, water is absorbed by the embryo, which results in the rehydration and expansion of the cells. Shortly after the beginning of water uptake, or imbibition, the rate of respiration increases, and various metabolic processes, suspended or much reduced during dormancy, resume. These events are associated with structural changes in the organelles (membranous bodies concerned with metabolism), in the cells of the embryo.

The emergence of the seedling

      Active growth in the embryo, other than swelling resulting from imbibition, usually begins with the emergence of the primary root from the seed, although in some species (e.g., the coconut) the shoot emerges first. Early growth is dependent mainly upon cell expansion, but, within a short time, cell division begins in the radicle and young shoot; thereafter, growth and further organ formation (organogenesis) are based upon the usual combination of increase in cell number and enlargement of individual cells.

      Until it becomes nutritionally self-supporting, the seedling depends upon reserves provided by the parent sporophyte. In angiosperms these reserves are found in the endosperm, residual tissues of the ovule, or in the body of the embryo, usually in the cotyledons. In gymnosperms, food materials are contained mainly in the female gametophyte. Since reserve materials are partly in insoluble form—as starch grains, protein granules, lipid droplets, and the like—much of the early metabolism of the seedling is concerned with mobilizing these materials and delivering, or translocating, the products to active areas. Reserves outside the embryo are digested by enzymes secreted by the embryo and, in some instances, also by special cells of the endosperm.

      In some seeds (e.g., castor beans) absorption of nutrients from reserves is through the cotyledons, which later expand in the light to become the first organs active in photosynthesis. When the reserves are stored in the cotyledons themselves, these organs may shrink after germination and die or develop chlorophyll and become photosynthetic.

      Environmental factors play an important part not only in determining the orientation of the seedling during its establishment as a rooted plant but also in controlling some aspects of its development. The response of the seedling to gravity is important. The radicle, which normally grows downward into the soil, is said to be positively geotropic. The young shoot, or plumule, is said to be negatively geotropic, because it moves away from the soil; it rises by the extension of either the hypocotyl, the region between the radicle and the cotyledons (cotyledon), or the epicotyl, the segment above the level of the cotyledons. If the hypocotyl is extended, the cotyledons are carried out of the soil, but, if the epicotyl elongates, the cotyledons remain in the soil.

      Light affects both the orientation of the seedling and its form. When a seed germinates below the soil surface, the plumule may emerge bent over, thus protecting its delicate tip, only to straighten out when exposed to light (the curvature is retained if the shoot emerges into darkness). Correspondingly, the young leaves of the plumule in such plants as the bean do not expand and become green except after exposure to light. These adaptative responses are known to be governed by reactions in which the light-sensitive pigment phytochrome plays a part. In most seedlings, the shoot shows a strong attraction to light, or a positive phototropism, which is most evident when the source of light is from one direction. Combined with the response to gravity, this positive phototropism maximizes the likelihood that the aerial parts of the plant will reach the environment most favourable for photosynthesis.

Later development: the sporophyte plant body

Continuation of organ formation

      Although it is convenient to refer to the early development of the plant sporophyte from the fertilized egg as embryogenesis, the process is never actually concluded as it is in the higher animals. In vascular plants, organ formation (organogenesis) is not confined to early life, and the processes of shoot, root, and leaf formation that occur first in the embryo are repeated, albeit in modified form, throughout the life of the plant. The life span may be short and determinate, as in annual plants such as the cereals, or long, lasting for many years—indeed potentially indefinitely, except for limitations imposed by the environment and accidents—as in trees. The protracted growth of perennials, or plants that resume growth each growing season, tends to lead to increase in size, but bulk is not necessarily directly correlated with age (aging), because individual leaves, flowers, and even whole limbs continuously die and are shed. Some long-lived plants, however, do reach a point at which losses of body mass balance the increase resulting from continued growth and organ formation.

The activity of meristems

 Characteristically, vascular plants grow and develop through the activity of organ-forming regions, the growing points. The mechanical support and additional conductive pathways needed by increased bulk are provided by the enlargement of the older parts of the shoot and root axes. New cells are added through the activity of special tissues called meristems (meristem), the cells of which are small, intensely active metabolically, and densely packed with organelles and membranes, but usually lacking the fluid-filled sacs called vacuoles. Meristems may be classified according to their location in the plant and their special functions. One important distinction is between persistent meristems, typified by those of the growing points, and meristems with a limited life, those associated with organs, such as the leaf, of determinate growth. The regions of rapid cell division at the tips (apices) of the stem and the root are terminal meristems. In the stem apex, the uppermost part is the promeristem, below which is a zone of transversely oriented early cell walls, the file, or rib, meristem. The procambium is a meristematic tissue concerned with providing the primary tissues of the vascular system; the cambium proper is the continuous cylinder of meristematic cells responsible for producing the new vascular tissues in mature stems and roots. The cork cambium, or phellogen, produces the protective outer layers of the bark.

      Among meristems of limited existence is the marginal, or plate, meristem responsible for the increase in surface area of a leaf; it contributes new cells mainly in one plane. Another type of meristem of limited life is called intercalary; it is responsible for the extension of some stems (as in the grasses) by the addition of new tissues remote from the growing points.

      The number of dividing cells in persistent meristems remains roughly constant, with one of the daughter cells of each division remaining meristematic and the other differentiating as a component of a developing organ. The geometrical arrangements in the particular organ determine the way in which this occurs, but in general the consequence is that the meristem is continuously moving away from the maturing tissue as growth continues. It remains, therefore, a localized zone of specialized tissue, never becoming diluted by the interposition of expanding or differentiating cells. In organs such as leaves, flowers, and fruits, in which the growth is determinate, the divisions of meristematic cells become more widely scattered, and the frequency progressively falls as the proportion of the daughter cells that differentiate increases. Ultimately, at maturity, no localized meristem remains.

The contribution of cells (cell) and tissues

      The two major factors determining the forms of plant tissues and organs are the orientation of the planes of cell division and the shapes assumed by the cells as they enlarge. Clearly, if the division planes in a cell mass are randomly oriented and individual cells expand uniformly, the tissue will enlarge as a sphere. On the other hand, if cell division planes are oriented regularly or the expansion of individual cells is directional, the tissue can assume any of a number of shapes. In a stem, for example, the cell division planes of the promeristem are oriented at various angles to the stem axis, so that new cells produced contribute to both width and length. Below this region, in the rib meristem, the proportion of divisions with the cell plate at right angles to the axis increases, so that the cells tend to be oriented in files. The cells in these files expand vertically more than they do horizontally, and, accordingly, the stem develops as a cylinder.

      The factors that control the orientation of cell division planes in meristems are largely unknown. Cell interactions, however, are presumed to coordinate the distribution and orientation of the divisions. In each cell microtubules (microtubule) in the cytoplasm help to orient the nucleus before it divides. Then, at the time of the division, other microtubules arranged in a spindle-shaped figure (the mitotic spindle) are involved in separating the daughter chromosomes and moving them to opposite ends of the parent cell. Thereafter, the residual part of the spindle helps to locate the plate that separates the two daughter cells. Microtubules are also concerned in determining the direction of growth in expanding cells, since they appear to influence the construction of the cell wall by controlling the way cellulose is laid down in it.

      Although change in shape is a form of cell differentiation, the term in the more general sense refers to a change in function, usually accompanied by specialization and the loss of the capacity for further division. Biochemical differentiation often involves a change in the character of the cell organelles—as when a generalized potential pigment body (proplastid) matures as a chloroplast, a chlorophyll-containing plastid. But it may also involve structural changes at a subcellular level, as when organelles change their character in cells engaged in intense metabolic activity.

      The differentiation of plant cells for the movement of materials and the provision of mechanical support or protection invariably depends upon modification of the walls. This usually entails the accretion of new kinds of wall materials, such as lignin in woody tissue and cutin and suberin in epidermal tissues and cork. The accompanying structural changes must be controlled, for the wall materials are not applied at random but according to a pattern appropriate to the particular cell or tissue. The development of patterns during cell-wall growth depends not only on the cytoplasmic microtubules, as in the construction of the cells that will give rise to the water-conducting vessels (xylem elements), but also on cytoplasmic membranes, as in the formation of sievelike end walls (sieve plates) in the cells that will give rise to food-conducting vessels (phloem elements).

      The differentiation of xylem culminates in the death of the participating cells, and the vessels are formed of chains of empty walls. This is an example of “programmed death,” not an uncommon phenomenon in plant and animal development.

The shoot system and its derivatives

The shoot tip

      The gametophytes of mosses and liverworts and the sporophytes of many higher plants have a shoot, or early stem, with a single cell at its tip, or apex, from which all the tissues of the stem arise. This apical cell is usually four-sided (tetrahedral), with three faces directed downward, and the fourth capping the apex. Daughter cells are continually cut off sequentially from the three inner faces, the apical cell preserving its tetrahedral shape. In cell lineages derived from the daughter cells, the division planes may remain oriented in a more or less regular manner, so that, for some distance below the apex, the three sectors can be recognized in the stem. This basic pattern occurs in the arrangement of the “leaves” of some mosses, which lie in three ranks. In many plants, however, division planes in the lower part of the apex show no particular correlation with the planes of cleavage of the apical cell, and the lateral appendages do not reflect any three-part arrangement.

      Gymnosperm and angiosperm apices do not possess apical cells. The generative role is discharged by an ill-defined zone of tissue called the promeristem. Regularities may appear in the distribution of division planes only in the extreme tip region. Over the outer part of the apex, the cells often appear to lie in one to three layers, which constitute the tunica. Enclosed by the tunica lies a core of cells that exhibits no distinct layering; this zone is the corpus. The layers of the tunica normally contribute to the surface layers of the plant, and the corpus provides the deeper lying tissues.

      The tunica–corpus analysis emphasizes the orientation of division planes, but apices can be examined from other points of view—the sizes of cells, the degree of vacuolation, and the concentration of various cell constituents, especially ribonucleic acid (RNA), vary through the apex and this sometimes results in more or less distinctive zones. Both gymnosperm and angiosperm apices have been classified on the bases of such zonal patterns, but the validity of this approach, as well as its usefulness for understanding the function of the apex as a morphogenetic centre, has been questioned.

      Since 1950, a theory of angiosperm apical zonation developed by French and Belgian botanists has been gaining support. This theory proposes that the central region of the apical dome constitutes a mass of cells with relatively low division rates, the méristème d'attente, or “waiting meristem.” Surrounding this region is an annular zone of cells with higher division rates, the anneau initial, or “initiating ring.” Features other than division rates characterize these zones: RNA and protein content are lower in the méristème d'attente than in the anneau initial, and the nucleoli are smaller. In longitudinal section, the differences contribute to the patterns distinguishable in apices, some of which have been used as bases for structural classification. The main contention of the Franco-Belgian school, however, is that the zonation represents a functional difference. The méristème d'attente is regarded as a region mainly concerned with controlling the geometry of the apex. The cells have a restricted metabolism concerned primarily in maintaining a low rate of increase in cell number, and they themselves, as well as their immediate derivatives, take no part in organogenesis or associated differentiation. The anneau initial, by contrast, is that part of the apex that produces the beginnings, or primordia, of lateral organs. Not only is the division rate higher, but the tissue as a whole is involved in metabolic syntheses that precede morphogenesis.

      One difficulty in investigating the stem apex arises from the uncertainty about which aspects are important for the overall function: division planes, division frequency, metabolic patterns, or some combination of these. Still another complication results because the apex is in a state of constant change during the growth of the plant. A long-term developmental trend begins after the definition of the growing point in early embryogenesis and continues thereafter through juvenility and the period of vegetative growth into the reproductive phase. Superimposed on this trend is a cyclical change reflecting the periodic generation of the primordia of leaves and lateral shoots in the region immediately under the apex.

The production of leaves (leaf)

      Leaves originate on the flanks of the shoot apex. A local concentration of cell divisions marks the very beginning of a leaf; these cells then enlarge so as to form a nipple-shaped structure called the leaf buttress. The cells of the leaf buttress may be derived from the tunica alone or from both the tunica and the corpus.

      In the early growth of the leaf primordium, new cells are contributed mainly by meristematic activity at the pole directed away from the stem, so that the buttress extends in length. The subsequent distribution of growth varies among the different groups of vascular plants according to the shape of the mature leaf. In considering the angiosperms, a broad-leaved dicotyledon ( tobacco) and a narrow-leaved monocotyledon (maize [corn]) will serve as examples.

      Apical growth dominates in the tobacco-leaf primordium until a height of about 0.5 millimetre (0.02 inch) is reached. Thereafter, the buttress becomes more and more flattened in the transverse plane by laterally oriented cell divisions and further expansion growth on either side. The dividing zones are the marginal meristems, through the activity of which the leaf gains its laminate form. In each meristem the outer file of cells, or marginal initials, contributes the epidermal layers by continued division. The cells below, the submarginal initials, provide the tissue of the inner part of the leaf. Usually a certain number of cell layers is defined in the mesophyll (the parenchyma between the epidermal layers of a foliage leaf). Cell division is not limited to the region of the marginal meristems but continues throughout the leaf in each of the layers, always in the same plane, until the final cell number is approached. The rate then declines, ceasing in the different layers at different times. Divisions usually end first in the epidermis, then in the lower mesophyll layers of a leaf such as that of tobacco, and last in the main photosynthetic tissue, the palisade layer, just beneath the upper epidermis.

      The vascular pattern in a tobacco leaf is determined early in the development of the vessel primordium. A procambial strand is formed by the elongation of narrow axial cells, and this extends both toward the base and toward the apex, eventually linking with the procambium of the stem. When the marginal meristems become active, the lateral veins of the leaf are initiated first, followed by the third and later order branchings that give the characteristic network of veins in the mature leaf.

      Although the differentiation of the cells of the vascular system begins at the base, the epidermal and mesophyll cells mature from the tip inward toward the stem. The palisade cells elongate in a plane at right angles to the epidermis; those of the lower mesophyll expand irregularly to give lobed forms. The cells of the epidermis, shaped like irregular paving stones, continue to expand in the plane of the leaf after growth ceases in the mesophyll, so that the cells of the internal tissues are pulled apart to form the system of air spaces found in the mature leaf.

      Dicotyledonous leaves are folded in various ways in the bud, the patterns being determined by differential growth in the tissues of the upper and lower surfaces (laminae) of the young leaves. Differential growth may cause the lamina either to roll or fold toward the leaf midrib or to fold near lateral veins, thus pleating the lamina. The folds in the bud are, of course, eliminated during the final phase of leaf expansion.

      In the development of the maize (corn) leaf, the primordium arises first as a prominence some distance below the apical dome. The zone of division and growth extends laterally around the apex so that a complete collar forms; then the margins overlap. Meanwhile the original tip zone continues to elongate, eventually surpassing the stem apex. Tip growth declines thereafter, and further increase in cell number results from meristematic activity at the base. The early development of the vascular system is unlike that in dicotyledons, for several parallel procambial strands, rather than a single midrib, are initiated. The first of these grow toward the apex, but, as tip growth ceases, procambial strands form above and extend toward the base, passing through the node, or point of insertion of the leaf primordium, and into the stem below. As the leaf extends in length, the tissues begin to mature first at the tip, and a wave of differentiation passes down toward the base, where cell division and extension growth may continue long after the tip of the leaf is mature. Protection for this immature and succulent tissue of the leaf base is afforded by the sheaths of older leaves surrounding it.

      These examples illustrate the principles involved in leaf development, but there are many deviations associated with variations in leaf form. Lobing and toothing result from the persistence of cell division and growth in particular stretches of the margin after growth ceases in between. Carried to the extreme, this localized growth gives the feather-like pinnate leaf. Many monocotyledons form cylindrical leaves as a result of a fusion of the margins of the primordium after it has encircled the stem.

Branching of the shoot

      The shoots of most vascular plants branch according to a consistent plan, with each new axis arising in the angle between a leaf and a stem—that is, in a leaf axil. In some plants, buds may also form from the older parts of shoot or root remote from the main apices; these buds, termed adventitious, do not conform to the general plan.

      A lateral shoot apex is initiated on the flanks of the main apex but at some distance below the point of emergence of the youngest leaf primordium. As in the origin of a leaf, generally the outer cell layers contribute to the surface tissues of the new apex by maintaining a consistent pattern of divisions. In some species a tunica of more than one cell layer quickly forms, so that the new apex appears as a miniature version of the main one; alternatively, the differentiation may not become apparent until the new primordium has attained considerable bulk. In all cases, the new apex must reach a minimal volume before it in turn can begin to form its own lateral primordia and to organize true axillary buds. As this volume is attained, méristème d'attente–anneau initial zonation appears. As in the main apex, the formation of new primordia is associated with the annular zone.

      From this point on, the development of the lateral shoot is the same as that of the main shoot, except that growth may not be as rapid because the main apex, or leading bud, dominates and absorbs much of the available nutrient. The early growth of the axillary bud proceeds quite vigorously until a certain number of leaf primordia has been formed; then apical activity slows. Cell division gradually stops, and with it the associated syntheses; thus there is no increase in the DNA of the nuclei of the meristem after the last division. The bud, in effect, passes into a state of dormancy, even though the external conditions for growth are propitious. This phenomenon is known as correlative bud inhibition, since it is determined by the activity of the leading bud of the shoot. If the leading bud is removed, the inhibited lateral buds resume growth, and with it the associated syntheses.

Vascular development

      Cell division planes in the zone just below the apex of the shoot tend to be oriented so that vertical files of cells are formed. This is more evident in the central core than in the surrounding cortical region, for the pattern is not disturbed by the insertion of lateral members. The first signs of the differentiation of the vascular system appear some distance below the apex, in a zone of tissue distinguishable by the smaller cross-sectional area of individual cells. These cells, forming the procambium zone, arise by divisions oriented at right angles to the axis and may form a complete cylinder; generally, however, interruptions occur, the segments being related to the uppermost leaf primordia. In a dicotyledon such as tobacco, the cylinder at its highest level consists of strands running upward toward the points of insertion of the primordia. Thus, as the site of each primordium is determined, a strand forming in the adjacent region of the stem will contribute to the cylinder, but at a higher level than the preceding strand. The link with the earlier formed procambium is not simple, however. The strand passing upward toward a leaf primordium usually is composed of branches arising from strands that enter the two nearest older leaves below it. Because it in turn will contribute a branch for the next leaf, the cylinder is really a hollow network, the “gaps,” or leaf traces, marking the points of departure of the leaf veins.

      During subsequent development, the strands, or vascular bundles, increase in thickness by further cell divisions, and connections form with the vascular systems of axillary buds. The cells differentiate to give the characteristic tissues of the vascular system: phloem vessels (conducting tissue), phloem parenchyma (packing tissue), and phloem fibres (supporting tissue) toward the outside and xylem vessels (woody conducting tissue) toward the inside. The differentiation occurs in an upward direction, so that the maturation of the vascular tissues follows at a more or less constant distance behind the apex.

      Although details differ, the above account of the origin of the primary vascular system is broadly applicable to gymnosperms and many ferns. Vascular development differs somewhat in certain flowering plants. In many monocotyledons, such as maize (corn), the several vascular strands that pass down from each leaf primordium into the stem do not contribute to a single cylinder but are scattered in the ground tissue, or parenchyma, of the stem. Lateral interconnections form principally at the nodes.

      Increase in stem diameter is accomplished in the older stems of dicotyledons by the activity of the cambium, which produces secondary vascular tissue. This meristem, a relic of the procambium, is composed of thin-walled cells, is flattened in the radial plane, and persists between primary vascular tissue, the differentiated outer phloem, and the inner xylem. When secondary thickening begins, the parenchymatous cells between the vascular bundles also resume division, ultimately forming a cambium cylinder. The cells of the cambium divide, producing initial phloem cells toward the outside and initial xylem cells within. Files of cells are also cut off among the initial phloem and xylem cells that remain parenchymatous and are called phloem and xylem rays.

      As in the apical meristem, the number of dividing cells in the cambium remains constant, except that more cells occasionally are added by divisions in the radial plane so that the girth of the cambial cylinder expands in pace with the growth of the xylem within. The addition of new phloem toward the outside compresses the primary phloem and the cortical tissues in a radial direction while stretching them tangentially. These primary tissues do not persist, however. As the girth of the stem increases, the epidermis is disrupted, and the outer layers of the cortex become meristematic, giving rise to the cork cambium, which generates cork cells on the outside. The cork layer, or bark, then takes over the protective function of the epidermis.

The root system and its derivatives

The root tip

      Plants that have a single apical cell in the shoot also have a single apical cell in the root. The cell is again tetrahedral, but sometimes daughter cells are cut off from all four faces, with the face directed away from the axis producing the cells of the root cap. The cells derived from the other faces continue to divide mostly by forming transverse walls, but occasionally also in the longitudinal plane. In this way vertical columns of cells form—tending, because of their mode of origin, to be disposed in three sectors.

      In the roots of gymnosperms, angiosperms, and some lower plants, there is no single apical cell. Again, as with the shoot, such root apices can be analyzed in different ways. Perhaps the most useful approach is based upon tracing the sources of the main tissues in the apical region. Such an analysis has led to the histogen theory, which proposes that the three principal tissues of the root—vascular cylinder, cortex, and epidermis—originate from three groups of initial cells, or histogens, in the apical meristem—plerome, periblem, and dermatogen respectively. A fourth histogen, the calyptrogen, produces the root cap. The histogens have been thought to lie in linear order in the apex, with the initial cells of the vascular system toward the older part of the root, and those of the cap toward the tip.

      The histogen theory is difficult to apply to some types of roots, and there has been uncertainty about the numbers of histogens. The discovery of the “quiescent centre” in the root apex has clarified many features, however. The quiescent centre is a group of cells, up to 1,000 in number, in the form of a hemisphere, with the flat face toward the root tip; it lies at the centre of the meristem, in much the same position, in fact, as the tetrahedral apical cell in certain lower plants. The cells of the quiescent centre are unusual in that their division rate is lower than that in the surrounding meristem. The cells of the centre have other distinctive features as well, notably a lower rate of protein synthesis than that of neighbouring cells.

      The quiescent centre is surrounded by actively dividing cells of the promeristem that are the initial cells of the various tissues of the root. Those abutting the flat, tip-directed face contribute to the root cap; those above the quiescent centre are distributed in a cup shape. The cells in the centre of the cup produce the procambium and so, ultimately, give rise to the vascular cylinder. The annular zone of cells surrounding this central group forms the initials of the cortex; surrounding this, in turn, a ring of initial cells forms the protoderm, the layer corresponding to the epidermis at this level of the root.

      The quiescent centre, a constant feature of the root tip, is apparently generally present in angiosperm and probably also in gymnosperms. The quiescent centre probably plays a role comparable with that of the apical cell in some lower plant roots, maintaining the geometry of the system. It has also been suggested that it may be concerned with the synthesis of growth hormones, although no direct evidence exists. When roots are damaged mechanically or by radiation, the cells of the centre can resume a rapid division rate, and they then participate in regeneration.

      The zone of cell division extends some distance along the length of the root above the tip region. Although the girth may increase by longitudinal divisions and the widening of the daughter cells, most divisions occur in the transverse plane resulting in the formation of longitudinal files of cells.

      In longitudinal section, the tissue zones become progressively better defined away from the tip. An internal protective band, the endodermis, becomes conspicuous as a single sheath of cells surrounding the procambium. The phloem procambium, recognizable by its narrow cells, begins to differentiate in the lower part of the region of elongation. The xylem also becomes distinct, the thickenings appearing first in the upper part of the extension zone. Differentiation keeps pace with the advance of the root tip as new cells are added in the promeristem. When xylem occupies the core, there is no pith as in the shoot, but the cells of the outermost layers of the vascular cylinder remain undifferentiated, forming the pericycle, a tissue important in the formation of lateral roots. Within the bounds of the pericycle, the xylem is star-shaped in section, with the first-formed xylem elements (protoxylem) occupying the ridges. The phloem lies in the intervening grooves. Outside of the endodermis, the cortical cells elongate but remain thin-walled. Above the level of the root-cap sheath, the epidermis forms the outer layer of the root, and, beyond the extension zone, its cells begin to develop root hairs.

      A more complete account can be given for the mechanics of development of the root apex than for that of the stem, mainly because of its greater simplicity. An important difference lies in the absence of a mechanism for the cyclical production of lateral organs at the apex itself.

Branching of the root

      The branching of the root takes place in the older parts and does not directly involve the apical meristem. The tissues concerned are the endodermis and the layer immediately beneath it, the pericycle. The endodermis participates in root branching in certain lower plants with apical cells. A cell of this layer enlarges and forms a tetrahedral cell, which becomes the new apical cell; by further divisions a hemispherical volume of tissue forms around it—the whole constituting a new apex.

      In many other plants, including gymnosperms (gymnosperm) and angiosperms (angiosperm), the lateral roots develop from the pericycle. Cells in this layer enlarge and begin to divide until a dome of tissue develops. Called the incipient apex, the dome pushes out the surrounding endodermis, which may itself resume divisions, its daughter cells enlarging to create a sheath around the new root tip. During further growth, the dome assumes an organization like that of the primary root apex. At first, all cells are meristematic; then, while the primordium is still small, cells in the central zone cease DNA synthesis, and this zone becomes the new quiescent centre. Beyond it, the root cap is produced, and, at the base, initial cells begin to develop the cell files that become the vascular cylinder, cortex, and epidermis. The vascular tissues differentiate from the base outward, and link eventually with xylem and phloem of the parent root. All this development occurs before the tip of the new root emerges from the tissues of the parent root. The growth of the new tip into the cortex first pushes out the endodermal sheath, if one is present, and then bursts it. The cortical cells are themselves crushed and probably resorbed as the root grows on, until finally the tip breaks through the epidermis.

      In most roots, new laterals are initiated in the pericycle opposite to the protoxylem ridges. They tend accordingly to form vertical ranks along the length of the root, reflecting the number of bands of protoxylem. Although lateral roots arise in quite a different way from leaves and axillary shoots at the stem apex, there are certain common features. Pericyclic cells about to produce a root primordium synthesize ribonucleic acid, in anticipation of the period of growth and morphogenesis that will result in a new apex. The same behaviour is seen in the cells of the annular zone, from which leaf primordia arise at the stem apex, and also in the axillary zones at a slightly lower level, from which new stem apices develop.

Later growth

      In the secondary growth of the root, cell division in the primary xylem produces a cambium, which abuts the pericycle over the protoxylem ridges and passes between the phloem strands and the xylem in the grooves. Activity of the root cambium is comparable with that of the stem cambium; phloem elements are cut off outward, and xylem elements are cut off within. With continued growth in thickness, the star-shaped figure of the primary xylem is lost, and the cambium eventually forms a cylindrical sheath. Again, as in the stem, the protective function of the epidermis is ultimately taken over by cork layers produced by a cork cambium in the outer cortex.

Correlations in plant development

Coordination of shoot and root development

      Although the structural organization of the vascular plant is comparatively loose, development of the various parts is well coordinated. Control is dependent upon the movement of chemical substances, including both nutrients and hormones.

      An example of correlation is the growth of shoot and root. The enlargement of aerial parts is accompanied by increased demands for water, minerals, and mechanical support that are met by coordinated growth of the root system. Several factors apparently are concerned with control, because shoot and root affect each other reciprocally. The root depends on the shoot for organic nutrients, just as the shoot depends on the root for water and inorganic nutrients and the flow of ordinary nutrients must, therefore, play some part. More specific control, however, may be provided by the supply of nutrients required in very small amounts. The root depends on the shoot for certain vitamins, and variation in the supply, reflecting the metabolic state of the aerial parts, may also influence root growth. In addition, hormonal factors affecting cell division pass upward from the root into the stem; although the exact role of the hormones (hormone) has not yet been established with certainty, they may provide one way by which the root system can influence the activity of the shoot apex.

      The control of secondary thickening is another important example of growth correlation. As the size of the shoot system increases, the need for both greater mechanical support and increased transport of water, minerals, and manufactured food is met by an increase in stem girth through the activity of the vascular cambium. Generally, the cambium of trees in temperate zones is most active in the spring, when buds open and shoots extend, creating a demand for nutrients. Cell division begins near the bud in each shoot and then spreads away from it. The terminal bud stimulates the cambium to divide rapidly through the action of two groups of plant hormones: auxins (auxin) and gibberellins (gibberellin).

      The inhibition of lateral buds, another example of correlated growth response, illustrates a reaction opposite to that occurring in the control of cambial activity. Lateral buds are inhibited in general because axillary shoots grow more slowly or not at all, while the terminal bud is active. This so-called apical dominance is responsible for the characteristic single trunk (tree) growth seen in many conifers and in herbaceous plants such as the hollyhock. Weaker dominance results in a bushy growth form with repeated branching. The fact that lateral, or axillary, buds become more active when the terminal bud is removed suggests that hormonal control is involved.

      The flow of auxin from the shoot tip is, in part, responsible for inhibiting axillary buds. The nutritional status of the plant also plays a role, apical dominance being strongest when mineral supply and light are inadequate. Because axillary buds are released from inhibition when treated with cell-division promoting substances (cytokinins (cytokinin)), it has been suggested that these substances are also concerned in regulating axillary-bud activity.

Determination of mature form

      After its establishment as an independent plant, the sporophyte passes through a juvenile period before reaching maturity and becoming reproductive. Juvenility may be brief or, as in the case of trees, may extend over several years. The duration is determined partly by internal factors and partly by environmental controls related to the seasons.

Internal control of development

      In some ways juvenility is a continuation of developmental trends initiated in the embryo. In many plants, new organs are produced sequentially through early life, each of progressively more mature form. The first leaf of the young fern sporophyte, for example, is small and relatively simple, and the vascular system consists of a few forked strands. As growth proceeds, succeeding new leaves are of increasing complexity, and the shape begins to resemble that typical of the reproductive frond; in addition, vasculation shifts to the mature pattern, often one with a network of veins. Comparable trends occur in flowering plants, in which leaves at successive levels of plant maturity often show a progressive increase in the complexity of lobing or toothing.

      Some of the changes associated with the juvenile period can be attributed to the gradual enlargement of the growing point, necessarily small in the embryo; its volume increases progressively with development. This increase in cell number is usually associated with the emergence of a “mature” zonation pattern. The typical internal structure of the shoot apex does not develop until a specific number of leaves form.

      Gradual structural change in the growing point, however, does not adequately account for all aspects of juvenility. Sometimes, the transition from juvenile to adult leaf form is not graded but sudden. The juvenile leaves of species of the gymnosperm Chamaecyparis, for example, are needlelike and spreading; the adult leaves are scalelike and lie close to the stem. Among flowering plants, various species of Eucalyptus have juvenile leaves that are ovate and mature leaves that are sickle-shaped.

      Such sudden transitions from juvenile to adult form, referred to as phase change, seem to depend not on slow shifts in the apex but on some determinative event or correlated group of events. The two forms are relatively stable and tend to resist change; for example, cultured tissues taken from the juvenile (ivy-leaved (ivy)) parts of ivy plants maintain a higher rate of cell division, and portions, or cuttings, taken from these parts tend to form roots more readily than those from the adult (simple-leaved) parts.

      The establishment of these relatively stable but not wholly irreversible states is comparable with the determination of shoot and root poles during embryogenesis and, indeed, with the alternation of generations itself. The transmission of differentiated states through cell lineages presumably reflects the action of “switching” devices controlling the expression of different parts of the genetic complement. In this sense, phase change and related phenomena do not differ essentially from those of differentiation and organogenesis in general.

      The transition in plants to the reproductive state is an example of a developmental event with some of the characteristics of phase change. Among seed plants, the reproductive structures are transformed shoots—strobili (including cones) of various kinds in the gymnosperms and flowers (flower) in angiosperms.

      From a developmental point of view, the flower can be regarded as a shoot axis of determinate growth, with the lateral members occupying the sites of leaves differentiating as floral organs—sepals, petals, stamens, and pistils. In the transition to flowering, the stem apex undergoes distinctive changes, the most conspicuous of which is in the shape of the apical region, which is related to the kind of structure to be formed, whether a single flower, as in the tulip, or a cluster of flowers (an inflorescence), as in the lilac. The region of cell division extends over the entire apex, and the ribonucleic acid content of terminal cells increases. When a single flower forms, lateral primordia emerge at higher and higher levels on the flanks of the apical dome, and the entire apex is absorbed in the process, after which apical growth ceases. When an inflorescence forms, early changes are generally comparable to that for the single flower with one major difference—axillary primordia emerge that either become floral meristems or develop as secondary inflorescence branches. These primordia appear closer to the apex than do those of axillary buds on a vegetative shoot. In grasses, the activation of axillary meristems is the most notable early indication of the passage into flowering.

Environmental control of development

      The rate of maturation and the timing of the transition to the reproductive (reproductive system, plant) phase are sometimes governed by internal controls and thus are relatively insensitive to the environment, provided conditions are generally favourable for growth. Frequently, however, the developmental rate is affected profoundly by recurring cycles in the environment, particularly those of temperature and of day length. In effect, these cycles provide a timetable for the plant, thus adjusting flowering, fruiting, and seed dispersal to the season and increasing the chances for successful propagation.

      The control of the developmental rate by temperature is especially evident in many herbaceous plants of temperate climates. These plants, as indicated earlier, often must experience cold, either as seeds or as young plants, before they can begin flower production; otherwise they undergo an excessively long period of leafy, or vegetative, growth. After the cold experience, which can be given artificially, the plant is said to have been vernalized (vernalization), or brought to the spring condition. Again the response is akin to a determination, because the condition attained is transmitted through subsequent cell divisions. Furthermore, there are indications that vernalization induces a persistent modification in the metabolism of apical cells and their derivatives. Ingenious theoretical schemes, offered to explain the apparent paradox that low temperature should actually accelerate a developmental process, are based mostly upon the proposition that a special vernalization hormone (vernalin) is involved. Although little direct evidence for the existence of vernalin exists, a class of hormones found in certain plant species, the gibberellins, does participate. The cold requirements of some species, such as the carrot, can be eliminated by the application of gibberellin, although the amounts needed are substantial.

      The annual cycle of changing day length obviously provides the best of all “clocks” for the regulation of plant development. The effect of day length (or rather length of continuous darkness) on the transition to flowering is part of the general phenomenon of photoperiodism. Certain plants, called short-day plants, grow vegetatively when the nights are shorter than a critical minimum period (days long); exposure to longer nights (days short), however, accelerates development and brings on early flowering. Conversely, long-day plants develop very slowly toward flowering during daily cycles with longer than a minimum of darkness (days short), and are accelerated by exposure to short nights (days long). Other plants either require days of intermediate length for flowering or respond to a sequence of different photoperiods.

      The leaf, rather than the stem apex, is the light-receiving organ in the photoperiodic reaction, although it is at the apex that subsequent developmental changes occur. One commonly accepted view is that, as a consequence of the photoperiodic experience, a specific flower-inducing hormone (as yet not isolated but referred to as “florigen”) is synthesized in the leaf and translocated to the apex. As in the case of vernalization, photoperiod undoubtedly affects the metabolism of the known plant hormones, and so influences many other developmental responses apart from flowering. The effect of the duration of illumination on the carbohydrate balance of the plant may also be important. Nutritional effects on flowering are well known in many species—certain fruit trees, for example.

      Whether or not environmental factors influence the passage into a reproductive state of a plant, the transition must be viewed as part of the general development from juvenility to maturity: in this sense, flowering is not a radical alternative to vegetative growth but its culmination. Yet, entirely new organ types are produced at the flowering apex, presumably under the influence of genes inactive during vegetative growth.

Seasonal adaptations

      Certain plants are perennial and survive from year to year by matching their growth to the progression of the seasons or by suspending growth altogether during unfavourable times, such as winter or a dry season.

      In the temperate zone, some time before winter begins, growth ceases in the shoots of woody plants, resting buds (bud) are formed, and deciduous trees lose their leaves. The resting bud consists of a short axis, with the stem apex surrounded by modified unexpanded leaves, which protect the stem, especially from drying. The cells show marked frost resistance, similar to that of the embryo of the seed. Corresponding changes occur in herbaceous plants, in which the preparation for winter may involve the dying back of aerial parts altogether, leaving protected organs at or below the soil surface.

      Growth sometimes ceases, even under favourable conditions, as a result of internal changes in the plant. This is true for some trees, which cease growth in midsummer. The passage into winter dormancy, however, is often controlled by the shortening of day length at the end of the growing season; in some plants decreasing night temperature also plays a part. Most temperate zone trees cease growth and form resting buds when the day length falls below a critical minimum.

      Photoperiodic control seems to involve the formation of inhibitor compounds. In birches (birch), for example, the leaf perceives the day length “signal” and transmits inhibitory materials to the apex, thus bringing growth to a stop and inducing the formation of a resting bud. The dormancy hormone, abscisic acid, may be concerned in this response and also in leaf abscission.

      Budbreak in certain trees is controlled by photoperiod, growth resuming in the lengthening days of spring; light-perceptive organs are probably the young leaves inside the bud scales. Sometimes budbreak depends only on temperature increases that occur in spring, as in certain plants of Mediterranean climates.

      The resumption of development in buds may result from a change in the balance of growth-inhibiting substances, such as abscisic acid, and growth promoters, notably the gibberellins. Buds can be caused to open prematurely by gibberellin treatment, which, as in the case of vernalization, can sometimes replace a cold experience; moreover, the gibberellin content in the buds of certain woody plants increases during chilling. Other hormones are probably also involved, however, for budbreak in plants such as the grapevine can be promoted by cytokinins, the plant cell-division factors.

      An important general feature of adaptive periodicities is that the developmental changes anticipate the conditions for which they will ultimately provide the appropriate physiological or morphological adjustment. The ability of plants to utilize environmental indicators such as temperature and day-length changes is vital for the survival of plants. The production of such adaptive devices is made possible by the state of continuous embryogeny, already stressed as one of the most important characteristics of plant growth (plant development).

Senescence (aging) in plants

      The growth of the vascular plant depends upon the activity of meristems, which are, in a sense, always embryonic. Continued indefinitely, this mode of growth could mean immortality; indeed, the longest lived individual organisms ever to have existed on earth have been certain species of trees. Plants and plant parts, however, do die, and death is often not the consequence of accident or environmental stress but of physiological decline—aging, or senescence.

      Various kinds of physiological senescence and death occur and may affect particular cells, tissues, organs, or the whole plant. In the formation of the vessels of the xylem, cells conclude their differentiation by dying and contribute their empty walls to the conducting tissue. Individual organs such as leaves usually have a limited life span. Entire shoot systems may gradually die back in the aerial parts of perennial plants, which overwinter underground. And, finally, the whole plant may die after a limited period of growth and the completion of reproduction. This behaviour is found in many annual plants, which complete their life cycle in a single growing season. The life span may extend to two years, as in biennial plants, or longer, as in banana and certain bamboos, which die after flowering and fruiting.

      In the examples cited above, the death of cells, organs, or individual plants appears to be “programmed” and, in some sense, adaptive. This is clearly so with the death of individual cells during differentiation, when residual products contribute to the effective function of the entire plant body. The death of leaves and of shoot systems is part of the plant's adaptation to the cycle of the seasons. In annual species, the death of the whole individual may be viewed in a similar way. The succession of generations in this case is carried on by seeds; the sacrifice of the parent plant may, in fact, contribute to the success of the seedling by making available to the seed a pool of reserves derived from the breakdown of parent tissues.

      Certain features characterize the onset of senescence. The cells show degenerative changes often associated with the accumulation of breakdown products. Metabolic changes accompany the degeneration. Respiration may increase for a period, but the rate ultimately declines as the cellular apparatus degenerates. Synthesis of proteins and nucleic acids ceases, and, in some instances, disintegration of cells has been associated with the release of enzymes through the disruption of membrane-bounded bodies called lysosomes.

      The death of individual cells in tissues such as the xylem appears to be governed by internal factors, but senescence often depends upon interaction of tissues and organs. The presence of young developing leaves often accelerates the aging of older leaves; removal of the younger leaves retards the senescence of the older ones, suggesting control by competition for nutrients. A similar effect is seen in annual plants, in which the development of fruits and seeds is associated with the senescence and, ultimately, the death of the rest of the plant; the removal of reproductive structures slows the rate of aging. In these instances competition obviously has some effect, but it does not sufficiently explain why older, mature organs suffer in competition with those still in active development. The link may lie partly in the capacity of developing organs to draw nutrients to themselves, even from older parts of the plant. Developing organs thus provide “sinks” toward which nutrients tend to move. The senescence of organs drained in this way could result from the progressive loss of certain key constituents; should leaf protein, for example, turn over by breakdown of proteins to their amino-acid constituents and then be resynthesized, a steady drain of amino acids from the leaf would progressively deplete the proteins in the leaf.

      “Sinks” can be only part of the explanation, however, for in detached leaves of plants such as tobacco, protein synthesis decreases, and protein content falls, while the amino-acid content actually rises. Senescence in such instances can hardly depend on the withdrawal of nutrients. Furthermore, leaf senescence can be retarded locally by the application of cytokinins (cytokinin), hormones that stimulate plant cell division. Parallel effects have been demonstrated with growth substances of the auxin type in other plant systems. In the same way that active buds and fruits form sinks for nutrients from elsewhere in the plant, a cytokinin-treated area of a leaf attracts nutrients from other parts of the leaf. Although the metabolism of isolated leaves may differ in many respects from that of attached leaves, leaf senescence probably does not result only from nutrient drainage but also from the synthetic activity of leaf tissues, which may be under hormonal control from other parts of the plant. The root may be important, for roots are known to export cytokinins to the shoot.

      Environmental factors, primarily photoperiod (daily length of darkness) and temperature, play important parts in governing senescence and death in plants. In annual plants, death is the natural conclusion of development; thus, conditions accelerating development automatically advance senescence. This is readily seen in short-day plants, in which precocious reproduction upon exposure to long dark periods is followed by early death. Senescence may be retarded in these cases, however, by hormonal treatments of the kind known to delay degeneration and death in detached leaves. Competition for nutrients between vegetative and reproductive structures cannot be the primary cause of death, for, in species such as hemp, the male plants—which do not produce seeds—die earlier than the females under short-day (long-night) conditions.

      In perennial plants, leaf fall is associated with approaching winter dormancy. In many trees leaf senescence is brought about by declining day length and falling temperature toward the end of the growing season. Chlorophyll, the green pigment in plants, is lost; yellow and orange pigments called carotenoids become more conspicuous; and, in some species, anthocyanin pigments accumulate. These changes are responsible for the autumn colours of leaves. There are some indications that day length may control leaf senescence in deciduous trees through its effect on hormone metabolism, for both gibberellins and auxins have been shown to retard leaf fall and to preserve the greenness of leaves under the short-day conditions of autumn.

      From the foregoing it may be seen that senescence and death are important in the general economy of plants. The paradox that death contributes to survival is resolved when it is understood that the death of the part contributes to the better adaptation of the whole—whether organ, individual, or species. Viewed in this way, death is no more than another—albeit the ultimate—manifestation of development.

John Heslop-Harrison

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