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Gilbert SF. Developmental Biology. 6th edition. Sunderland (MA): Sinauer Associates; 2000.

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Developmental Biology. 6th edition.

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Vegetative Growth

When the shoot emerges from the soil, most of the sporophyte body plan remains to be elaborated. Figure 20.20 shows the basic parts of the mature sporophyte plant, which will emerge from meristems.

Figure 20.20. Morphology of a generalized angiosperm sporophyte.

Figure 20.20

Morphology of a generalized angiosperm sporophyte.

Meristems

As has been mentioned, meristems are clusters of cells that allow the basic body pattern established during embryogenesis to be reiterated and extended after germination. Meristematic cells are similar to stem cells in animals.* They divide to give rise to one daughter cell that continues to be meristematic and another that differentiates. Meristems fall into three categories: apical, lateral, and intercalary.

Apical meristems occur at the growing shoot and root tips (Figure 20.21). Root apical meristems produce the root cap, which consists of lubricated cells that are sloughed off as the meristem is pushed through the soil by cell division and elongation in more proximal cells. The root apical meristem also gives rise to daughter cells that produce the three tissue systems of the root. New root apical meristems are initiated from tissue within the core of the root and emerge through the ground tissue and dermal tissue. Root meristems can also be derived secondarily from the stem of the plant; in the case of maize, this is the major source of root mass.

Figure 20.21. Shoot and root meristems.

Figure 20.21

Shoot and root meristems. Both shoots and roots develop from apical meristems, undifferentiated cells clustered at their tips. In roots, a root cap is also produced, which protects the meristem as it grows through the soil. The lateral organs of the shoot (more...)

The shoot apical meristem produces stems, leaves, and reproductive structures. In addition to the shoot apical meristem initiated during embryogenesis, axillary shoot apical meristems (axillary buds; see Figure 20.20) derived from the original one form in the axils (the angles between leaf and stem). Unlike new root meristems, these arise from the surface layers of the meristem.

Angiosperm apical meristems are composed of up to three layers of cells (labeled L1, L2, and L3) on the plant surface (Figure 20.22). One way of investigating the contributions of different layers to plant structure is by constructing chimeras. Plant chimeras are composed of layers having distinct genotypes with discernible markers. When L2, for example, has a different genotype than L1 or L3, all pollen will have the L2 genotype, indicating that pollen is derived from L2. Chimeras have also been used to demonstrate classical induction in plants, in which, as in animal development, one layer influences the developmental pathway of an adjacent layer.

Figure 20.22. Organization of the shoot apical meristem.

Figure 20.22

Organization of the shoot apical meristem. (A) Angiosperm meristems have two or three outer layers of cells that are histologically distinct (here labeled L1, L2, and L3). While cells in certain layers tend to have certain fates, they are not necessarily (more...)

The size of the shoot apical meristem is precisely controlled by intercellular signals, most likely between layers of the meristem (reviewed by Doerner 1999). Mutations in the Arabidopsis CLAVATA genes, for example, lead to increased meristem size and the production of extra organs. STM has the opposite effect, and double mutant phenotypes are consistent with the hypothesis that the two work together to maintain meristem size (Clark et al. 1996). Perhaps they balance the rate of cell division (which enlarges the meristem) and the rate of cell differentiation in the periphery of the meristem (which decreases meristem size) (Meyerowitz 1997).

Lateral meristems are cylindrical meristems found in shoots and roots that result in secondary growth (an increase in stem and root girth by the production of vascular tissues). Monocot stems do not have lateral meristems, but often have intercalary meristems inserted in the stems between mature tissues. The popping sound you can hear in a cornfield on a summer night is actually caused by the rapid increase in stem length due to intercalary meristems.

Root development

Radial and axial patterning in roots begins during embryogenesis and continues throughout development as the primary root grows and lateral roots emerge from the pericycle cells deep within the root. Laser ablation experiments eliminating single cells and clonal analyses have demonstrated that cells are plastic and that position is the primary determinant of fate in early root development. Analyses of root radial organization mutants have revealed genes with layer-specific activity (Scheres et al. 1995; Scheres and Heidstra 1999). We will illustrate these findings by looking at two Arabidopsis genes that regulate ground tissue fate.

In wild-type Arabidopsis, there are two layers of root ground tissue. The outer layer becomes the cortex, and the inner layer becomes the endodermis, which forms a tube around the vascular tissue core. The SCARECROW (SCR) and SHORT-ROOT (SHR) genes have mutant phenotypes with one, instead of two, layers of root ground tissue (Benfey et al. 1993). The SCR gene is necessary for an asymmetrical cell division in the initial layer of cells, yielding a smaller endodermal cell and a larger cortex cell (Figure 20.23). The scr mutant expresses markers for both cortex and endodermal cells, indicating that differentiation progresses in the absence of cell division (Di Laurenzio 1996). SHR is responsible for endodermal cell specification. Cells in the shr mutant do not develop endodermal features.

Figure 20.23. SCR and SHR regulate endodermal differentiation in root radial development.

Figure 20.23

SCR and SHR regulate endodermal differentiation in root radial development. (A) Diagram of normal cell division yielding cortical and endodermal cells. SCR regulates this asymmetrical cell division. (B, C) SCR expression in root and shoot. The SCR promoter (more...)

Axial patterning in roots may be morphogen-dependent, paralleling some aspects of animal development. A variety of experiments have established that the distribution of the plant hormone auxin organizes the axial pattern. A peak in auxin concentration at the root tip must be perceived for normal axial patterning (Sabatini et al. 1999).

As discussed earlier, distinct genes specifying root and shoot meristem formation have been identified; however, root and shoot development may share common groups of genes that regulate cell fate and patterning (Benfey 1999). This appears to be the case for the SCR and SHR genes. In the shoot, these genes are necessary for the normal gravitropic response, which is dependent on normal endodermis formation (a defect in mutants of both genes; see figure 20.23C). It's important to keep in mind that there are a number of steps between establishment of the basic pattern and elaboration of that pattern into anatomical and morphological structure. Uncovering the underlying control mechanisms is likely to be the most productive strategy in understanding how roots and shoots develop.

Shoot development

The unique aboveground architectures of different plant species have their origins in shoot meristems. Shoot architecture is affected by the amount of axillary bud outgrowth. Branching patterns are regulated by the shoot tip—a phenomenon called apical dominance—and plant hormones appear to be the factors responsible. Auxin is produced by young leaves and transported toward the base of the leaf. It can suppress the outgrowth of axillary buds. Grazing and flowering often release buds from apical dominance, at which time branching occurs. Cytokinins can also release buds from apical dominance. Axillary buds can initiate their own axillary buds, so branching patterns can get quite complex. Branching patterns can be regulated by environmental signals so that an expansive canopy in an open area maximizes light capture. Asymmetrical tree crowns form when two trees grow very close to each other. In addition to its environmental plasticity, shoot architecture is genetically regulated. In several species, genes have now been identified that regulate branching patterns.

Leaf primordia (clusters of cells that will form leaves) are initiated at the periphery of the shoot meristem (see Figure 20.21). The union of a leaf and the stem is called a node, and stem tissue between nodes is called an internode (see Figure 20.20). In a simplistic sense, the mature sporophyte is created by stacking node/internode units together. Phyllotaxy, the positioning of leaves on the stem, involves communication among existing and newly forming leaf primordia. Leaves may be arranged in various patterns, including a spiral, 180-degree alternation of single leaves, pairs, and whorls of three or more leaves at a node (Jean and Barabé 1998). Experimentation has revealed a number of mechanisms for maintaining geometrically regular spacing of leaves on a plant, including chemical and physical interactions of new leaf primordia with the shoot apex and with existing primordia (Steeves and Sussex 1989).

It is not clear how a specific pattern of phyllotaxy gets started. Descriptive mathematical models can replicate the observed patterns, but reveal nothing about the mechanism. Biophysical models (e.g., of the effects of stress/strain on deposition of cell wall material, which affects cell division and elongation) attempt to bridge this gap. Developmental genetics approaches are promising, but few phyllotactic mutants have been identified. One candidate is the terminal ear mutant in maize, which has irregular phyllotaxy. The wild-type gene is expressed in a horseshoe-shaped region, with a gap where the leaf will be initiated (Veit et al. 1998). The plane of the horseshoe is perpendicular to the axis of the stem.

Leaf development

Leaf development includes commitment to become a leaf, establishment of leaf axes, and morphogenesis, giving rise to a tremendous diversity of leaf shapes. Culture experiments have assessed when leaf primordia become determined for leaf development. Research on ferns and angiosperms indicates that the youngest visible leaf primordia are not determined to make a leaf; rather, these young primordia can develop as shoots in culture (Steeves 1966; Smith 1984). The programming for leaf development occurs later. The radial symmetry of the leaf primordium becomes dorsal-ventral, or flattened, in all leaves. Two other axes, the proximal-distal and lateral, are also established. The unique shapes of leaves result from regulation of cell division and cell expansion as the leaf blade develops. There are some cases in which selective cell death (apoptosis) is involved in the shaping of a leaf, but differential cell growth appears to be a more common mechanism (Gifford and Foster 1989).

Leaves fall into two categories, simple and compound (Figure 20.24; see review by Sinha 1999). There is much variety in simple leaf shape, from smooth-edged leaves to deeply lobed oak leaves. Compound leaves are composed of individual leaflets (and sometimes tendrils) rather than a single leaf blade. Whether simple and compound leaves develop by the same mechanism is an open question. One perspective is that compound leaves are highly lobed simple leaves. An alternative perspective is that compound leaves are modified shoots. The ancestral state for seed plants is believed to be compound, but for angiosperms it is simple. Compound leaves have arisen multiple times in the angiosperms, and it is not clear if these are reversions to the ancestral state.

Figure 20.24. Simple and compound leaves.

Figure 20.24

Simple and compound leaves.

Developmental genetic approaches are being applied to leaf morphogenesis. The Class I KNOX genes are homeobox genes that include STM and the KNOTTED 1 (KN1) gene in maize. Gain-of-function mutations of KN1 cause meristem-like bumps to form on maize leaves. In wild-type plants, this gene is expressed in meristems. When KN1, or the tomato homologue LeT6, has its promoter replaced with a promoter from cauliflower mosaic virus and is inserted into the genome of tomato, the gene is expressed at high levels throughout the plant, and the leaves become “super compound” (Figure 20.25; Hareven et al. 1996; Janssen et al. 1998). Simple leaves become more lobed (but not compound) in response to overexpression of KN1, consistent with the hypothesis that compound leaves may be an extreme case of lobing in simple leaves (Jackson 1996). The role of KN1 in shoot meristem and leaf development, however, is consistent with the hypothesis that compound leaves are modified shoots.

Figure 20.25. Overexpression of Class 1 KNOX genes in tomato.

Figure 20.25

Overexpression of Class 1 KNOX genes in tomato. The photograph shows the single leaves of (A) a wild-type plant, (B) a mouse ears mutant, with increased leaf complexity, and (C) a transgenic plant that uses a viral promoter to overexpress the tomato homologue (more...)

A second gene, LEAFY, that is essential for the transition from vegetative to reproductive development also appears to play a role in compound leaf development. It was identified in Arabidopsis and snapdragon (in which it is called FLORICAULA), and has homologues in other angiosperms. The pea homologue (UNIFOLIATA) has a mutant phenotype in which compound leaves are reduced to simple leaves (Hofer and Ellis 1998). This finding is also indicative of a regulatory relationship between shoots and compound leaves.

In some compound leaves, developmental decisions about leaf versus tendril formation are also made. Mutations of two leaf-shape genes can individually and in sum dramatically alter the morphology of the compound pea leaf (Figure 20.26). The acacia mutant (tl) converts tendrils to leaflets; afilia (af) converts leaflet to tendrils (Marx 1987). The af tl double mutant has a complex architecture and resembles a parsley leaf.

Figure 20.26. Leaf morphology mutants in peas.

Figure 20.26

Leaf morphology mutants in peas. (A) Wild-type pea plant. (B) The tl mutant, in which tendrils are converted to leaflets. (C) The af mutant, in which leaflets are converted to tendrils. (D) An af tl double mutant, which results in a “parsley leaf” (more...)

At a more microscopic level, the patterning of stomata (openings for gas and water exchange) and trichomes (hairs) across the leaf is also being investigated. In monocots, the stomata form in parallel files, while in dicots the distribution appears more random. In both cases, the patterns appear to maximize the evenness of stomata distribution . Genetic analysis is providing insight into the mechanisms regulating this distribution. A common gene group appears to be working in both shoots and roots, affecting the distribution pattern of both trichomes and root hairs (Benfey 1999).

Footnotes

*

The similarities between plant meristem cells and animal stem cells may extend to the molecular level, indicating that stem cells existed before plants and animals pursued separate phylogenetic pathways. Homology has been found between genes required for plant meristems to persist and genes expressed in Drosophila germ line stem cells (Cox et al. 1998).

This phenomenon, called fasciation, is found in many species, including peas and tomatoes.

By agreement with the publisher, this book is accessible by the search feature, but cannot be browsed.

Copyright © 2000, Sinauer Associates.
Bookshelf ID: NBK10030

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