Special Reviews

Phase Change and the Regulation of Developmental Timing in Plants

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Science  18 Jul 2003:
Vol. 301, Issue 5631, pp. 334-336
DOI: 10.1126/science.1085328

Abstract

Plants produce different types of organs at different times in shoot development. Along with the major changes in organ morphology that take place during developmental transitions, more gradual patterns of variation occur. The identity of organs produced at a particular position on the shoot is determined by interactions between several independently regulated, temporally coordinated processes. Two of these processes are organ production and the specification of organ identity. Coordination of these processes is accomplished in part by a thermal clock and by signal transduction pathways that mediate the response of plants to light.

The shoot system (i.e., the above-ground part) of higher plants develops by the addition of new structures at the shoot apex. These structures consist of leaves, the section of the stem between successive leaves (internodes), and vegetative or floral buds. The rate at which these structures arise, as well as their size, shape, and identity, change as the shoot develops. Some features— such as leaf and internode size— change in a continuous, quantitative, graded fashion, whereas others change rapidly at predictable times in shoot development (1, 2) (Fig. 1). An example of the latter phenomenon is the transition to flowering, when leaf development is suppressed and lateral buds differentiate as flowers or flower-bearing branches. Similar, albeit less striking, transitions occur earlier in shoot development, when the shoot makes the transition from an embryonic to a postembryonic pattern of development, and later from a juvenile to an adult phase of vegetative development. These transitions are controlled by an array of signal transduction pathways that operate independently and interact in a myriad of ways to produce the tremendous variation in plant morphology encountered in nature (3, 4) (Fig. 2). Determining how these developmental transitions are regulated and how they are synchronized represent major challenges in plant developmental biology.

Fig. 1.

The organization of the maize shoot. Temporal changes in the character of the shoot apex result in spatial variation in organ size, shape, and identity. Some features change in a graded fashion, whereas other features change discontinuously. For example, leaf size varies continuously as the shoot develops, but the leaf epidermis displays either of two differentiation patterns—a juvenile (yellow) pattern and an adult (green) pattern. These patterns are distinguished by differences in epidermal cell shape, cell type, wax production, and cell wall histochemistry, which are evident in scanning electron micrographs (left) and toluidine blue–stained peels (right) of the upper epidermis. Internode length also varies continuously, but internodes associated with leaves that have a juvenile cell pattern are markedly shorter than internodes associated with leaves that have an adult pattern. Such correlated changes allow the development of the shoot to be divided into discrete vegetative phases. The transition to flowering is indicated by a marked reduction in internode length, a change in the arrangement (phyllotaxis) of lateral organs, suppression of leaf development, and the production of short branches from which either male or female flowers (red) arise. Male flowers are produced at the apex of the primary shoot axis (in the tassel) and at the apex of lateral branches arising from juvenile internodes, whereas female flowers are produced at the apex of lateral branches located near the middle of the shoot.

Fig. 2.

The growth and differentiation of the shoot depend on interactions between independent pathways or processes (vertical arrows) that are regulated by a thermal clock and synchronized at various points by cross-talk between these pathways (horizontal arrows).

The extent to which growth and differentiation are temporally coordinated varies in different developmental processes. For example, the number of seed leaves (cotyledons) is nearly invariant within a species, in part because the growth of the shoot apex during embryogenesis is temporally synchronized with the expression of genes that promote cotyledon identity. Experimental conditions (5) or mutations (6) that disrupt this synchrony cause leaves to be transformed into “extra” cotyledons. In contrast, many of the pathways that influence flowering time have little or no effect on the rate of leaf initiation, with the result that early- and late-flowering varieties of plants generally have corresponding differences in leaf number (7); if floral induction and leaf initiation were temporally synchronized, these varieties would flower with the same number of leaves. Shoot morphogenesis cannot be understood, therefore, without knowing how the expression of genes that regulate organ identity is spatially and temporally coordinated with shoot growth.

Phase Change and the Temporal Control of Organ Fate

The postembryonic development of the shoot usually occurs in three more or less discrete temporal phases: a juvenile vegetative phase, an adult vegetative phase, and a reproductive phase (2). The features that distinguish these phases differ between species, but they usually include leaf shape and size, leaf arrangement, patterns of epidermal differentiation, the capacity for adventitious root production, internode elongation, and, most obviously, the capacity to produce flowers or flower-bearing branches (Fig. 1). The transition to the reproductive phase (reproductive phase change or floral induction) has been intensively studied and is understood at many different levels (3, 8). Although genes involved in vegetative phase change have been identified in several species (912), the molecular mechanism of this process is still poorly defined.

Phase change is regulated by as yet unknown factors that originate outside the shoot apex and by the competence of the shoot apex to respond to these factors (8, 13). Because the fate of immature leaf and floral organ primordia can be altered without changing the fate of the cells in the growing tip (shoot apical meristem, or SAM), it is likely that these factors operate directly on all of the undetermined organs at the shoot apex, rather than specifically on the SAM (14, 15). Although stable phase transitions are associated with a change in the SAM and probably require such a change, phase change does not appear to be initiated by the SAM.

Genetic analyses of flowering time in Arabidopsis and other species have identified many of the genes that mediate the effect of hormones, photoperiod, light quality, temperature, and other environmental factors on floral induction (3). These genes operate in several parallel pathways to regulate the activity of a common set of integrator genes. The way in which light interacts with the circadian clock to produce photoperiodic regulation of flowering is described elsewhere in this issue (16). Many of these pathways play no role in vegetative phase change. Although plants normally flower only when they are in an adult vegetative phase, the timing of floral induction can vary markedly relative to the timing of vegetative phase change (1, 17). Futhermore, in Arabidopsis, altering the activity of many flowering-time genes has little effect on the timing of vegetative phase change (18, 19). The major exception to this generalization are genes involved in gibberellin (GA) biosynthesis and signal transduction (18, 20, 21) and phytochrome B (phyB) signal transduction (22). Mutations in these genes simultaneously increase or decrease the number of juvenile and adult leaves, indicating that GA and light regulate the timing of both vegetative and reproductive phase change.

Organ Initiation and Growth

During shoot development, the rate at which leaves are initiated and their size vary in a predictable pattern. In plants with prolonged juvenile, adult, and reproductive phases, such as English ivy (23), these features remain fairly constant during each phase and change during vegetative and reproductive phase transitions. Leaf size and shape vary more continuously in short-lived plants, perhaps because of the rapid progression between these phases.

Variation in the rate of leaf initiation is directly correlated with the frequency of cell division in the SAM, both in wild-type plants and in plants that have abnormal rates of leaf production (2426). These findings suggest that developmental variation in the rate of leaf initiation is driven by changes in the rate of cell division in the SAM. Variation in leaf size along the length of the shoot arises primarily from variation in duration of leaf expansion (27), which is largely attributable to a difference in the duration of cell division during leaf development (i.e., cell division stops sooner in small leaves than in large leaves) (28). These observations imply that the factors that regulate phase change also act to regulate the cell cycle.

Synchronizing Growth and Pattern Formation: The Thermal Clock

Much of the research on developmental timing in plants has been conducted by agronomists interested in predicting the effect of environmental conditions on shoot growth. An important result to emerge from these studies is the concept of thermal time (29, 30). Thermal time (also known as growing degree-days) is the temperature per unit time, minus a species-specific base temperature, summed over the time period of interest—in other words, the cumulative amount of heat to which a plant is exposed. Within a certain temperature range, processes such as leaf initiation, the rate and duration of leaf growth, and flowering time are linearly related to thermal time under a wide range of environmental conditions. Temperature responses are often modified by light, and some formulations take this interaction into account to produce a measure known as photothermal time (31). The linear relationship between the timing of processes in shoot development and thermal or photothermal time implies that plants are able to integrate temperature and use this information to regulate the timing of these processes. The fact that different types of developmental events respond in the same way to thermal time accounts for the observation that shoot morphology does not vary greatly in plants grown at different temperatures, and suggests that a mechanism for integrating temperature may be common to all these processes.

Recent studies in Arabidopsis have provided the first insight into the molecular mechanism of the thermal clock. The number of leaves produced by Arabidopsis plants grown at different temperatures is strongly influenced by light quality. Under some light regimes, Arabidopsis plants produce approximately the same number of leaves at different temperatures, whereas under other light regimes they produce more leaves at low temperatures (∼16°C) than at high temperatures (∼26°C) (3234). This response is mediated primarily by the floral promoter, FT, whose transcription is regulated independently by light and temperature. The reduced leaf number of plants grown at high temperatures can be largely attributed to an increase in the expression of FT at these temperatures (33, 34). Light modulates this temperature response via phyB, which represses FT expression at high temperatures (33). Two other genes that regulate the temperature sensitivity of flowering time are the autonomous pathway genes FCA and FVE. Loss-of-function mutations in either gene completely eliminate the temperature-induced difference in flowering time (34). Both of these genes act upstream of FT, but it is still unknown whether their effect on the temperature response can be attributed to an effect on FT expression.

AModel for Pattern Formation During Shoot Development

The major processes in shoot development are illustrated in Fig. 2. This diagram is necessarily speculative because the component pathways have usually been studied in isolation, rather than in relation to the development of the shoot as a whole. Lateral organ formation is regulated by the pattern of cell division and cell expansion within the SAM. Organ identity is specified independently of this process by three major differentiation programs. Two of these specify different phases of vegetative development; the third regulates the differentiation of reproductive structures. The temporal sequence of these differentiation programs is regulated by threshold responses to graded environmental stimuli, such as light quality and endogenous spatial and temporal information. Differentiation programs are synchronized with organ production and growth via the effect of these programs on cell division and cell expansion, and by a thermal clock that is shared by all of these programs.

Much of the research on phase change has focused on a single event—floral induction. How this process is related to earlier developmental transitions remains to be determined, as does the mechanism of these transitions. Model organisms, such as Arabidopsis and maize, have produced rapid progress in our understanding of plant development in recent years and will be an important source of information about this central problem in shoot morphogenesis.

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