For centuries debate has existed regarding the way in which the leaf evolved. Scientists such as Malpighi believed that Nature made leaves to digest food. Others such as Goethe believed that some parts of a plant would transform into leaves. Cesalpino and Linnaeus believed that true leaves were metamorphosed layers of the wood of the stem, while Wolff believed that leaves developed as a result of altered nourishment in the plant. Unlike the previous hypotheses, present day theories, such as the Telome and Enation theories, suggest different patterns of evolution for megaphyll leaves than for microphyll leaves. While these theories do contradict each other on several points, they are still the most strongly supported ideas of leaf evolution that have been proposed.
 

Leaves first appeared during the Devonian Period, which occurred 395-345 million years ago. The first plants to develop megaphylls were the Progymnosperms. Margulis and Schwartz (1998) propose that the three groups of Progymnosperms that existed during this period were the Aneurophytales, the Archaeopteridales, and the Protopityales. Gastaldo (1997) proposed that the Archaeopteridales were the first to develop a functional leaf, a megaphyll, which consisted of laminate structure that were divided or entire.

Scagel et al. (1969) proposed that during the Early Devonian Period, most plants were less than 30 cm tall and not differentiated into stems, roots, and leaves. Instead, forking above ground axes had stomata and terminal sporangia, which demonstrate that they were both green and photosynthetic. Rothwell (2000) proposed that rhiziods anchored underground and surface rooted axes. He also proposed that these plants were non-seed plants with a homosporous life cycle and free-living gametophytes.

Rothwell (2000) proposed that some plants from the Devonian had multicellular extentions (enations) along their axes that were above ground. These enations helped to increase the light-capturing surface of the photosynthetic tissue, and eventually gave rise to microphylls. The aboveground axes became branching systems and microphylls, while the underground axes became roots (Rothwell, 2000).

Rothwell (2000) proposed that other plant groups were derived from modifications of forking axes. Devonian plants showed quite a diversity of structure. Some plants had equally forked axes, while large, centrally located axis as well as smaller lateral-borne axes comprised more specialized plants. In plants where lateral systems branched in only one plane, the side branches were flat like leaves. Photosynthetic tissue then filled in the spaces between forks of the laterals, producing megaphylls through the process that Zimmermann (1952) described in his Telome Theory called syngenesis.

Rothwell (2000) further proposed that by the middle of the Devonian Period, plants with microphylls and those with megaphylls diversified. Many even grew to the size of shrubs but were restricted in size by the limited diameter that their aboveground stems and roots could achieve. Once lateral growth, or secondary growth, was developed in plants, they overcame this size restriction. At the same time, many plants evolved downward-growing, central rooting systems. By the end of the Devonian Period, forests contained many giant trees and larger plants.

There are many reasons for which the development of leaves was very beneficial to plants. Prance (1985) and Raven and Johnson (1996) state that the leaf serves to capture the sunlight that is necessary for photosynthesis to occur. Prance (1985) further states that inside the leaves are numerous vascular strands, which act as the pipelines through the leaf and allow the products of photosynthesis to be transported. Leaves also allow for transpiration to occur. Prance (1985) and Raven and Johnson (1985) state that through transpiration, the water absorbed by the roots can be transported throughout the plant, and finally to the leaves, where it can be used in photosynthesis. It is also through transpiration that leaves are able to absorb the minerals from the soil that are needed for photosynthesis.

Harvey-Gibson (1919) discussed several past theories of leaf evolution. In the 1600's Malpighi discussed the evolution of leaves as a contrived by Nature for the digestion of food. He said that Nature also provided the leaves with numerous special glands for sweating and the gradual elimination of moisture. By removing moisture, the leaves condensed their sap and made it more easily digestible by the plant.

Von Sachs (1890) further discussed past theories of leaf evolution. The doctrine of metamorphosis, published by Goethe in 1790, was the first doctrine to distinguish between different parts of the plant. The first sentence of his theory states that "it is open to observation that certain exterior parts of plants sometimes change and pass into the form of adjacent parts, either wholly or in a greater or less degree." He believed that if, for instance, the ovaries of a plant are changed into large leaves, the plant in question had actually given rise to a new plant. There were several problems with Goethe’s theory. One was that he did not understand the difference between abnormality and normal changes, those abnormal changes that occurred spontaneously and evolutionary changes that occurred over time as a result of genetic force. Also, Goethe saw only 2 parts of a plant - the leaf and the stem. Because of this, he called any structure that originated on the stem a leaf, an idea that led him to a false definition of the leaf. Because many structures, including petals, stamens, and the stomata, were all defined as leaves, it was not correct to describe the changes in them without describing the changes in the organism as a whole. Because the structures he described as leaves were not actually leaves, but were instead a mixture of petals, stamens, and any structure that protruded from the stem, his idea of metamorphosis was not a good explanation. In summary, his incorrect opinion was that leaves developed as a result of a change from a different plant structure. This theory also led him to believe that all leaf forms developed independently from each other.

Von Sachs (1890) also discussed Cesalpino and Linnaeus as believing that true leaves were metamorphosed layers of the wood of the stem. However, they used the word metamorphose in a different context, meaning simply that the leaves were a result of the changing of the actual substance of the cortex.

Von Sachs (1890) said that Caspar Friedrich Wolff, in 1766, was the first to think about the leaf in a systematic method. He attempted to give a physical explanation of leaf formation, proposing that all stem appendages were leaves, and that leaves developed as a result of altered nourishment in the plant.

Today, there are two accepted theories describing leaf evolution. The Telome Theory describes the evolution of the megaphyll, while the Enation Theory describes the evolution of the microphyll.

Presently, there are 2 popularly accepted theories describing the evolution of the leaf. The first of these is the Telome Theory. Foster and Gifford (1959) stated this theory as describing the changes that occurred in early vascular plants that led to the presence of megaphylls. Complex venation and a leaf gap in the stele of the stem are characteristic of megaphylls. Clausz (1999) said that the leaf gap in the stele is the result of complex differentiation that occurred to produce megaphylls, and is described by the stelar theory. Most megaphylls have either a siphonostele or a eustele. Zimmermann (1952) proposed that the emergence of these megaphylls occurred in two stages. In the first stage, several plant phyla, called the "Urtelomes," developed the basic telome structure through a series of elementary steps. In the second stage, the telomes of these "Urtelomes" underwent changes that resulted in the first megaphylls.

Zimmermann (1952) proposed that the telome structure emerged in plants during the Devonian period. These land plants had existed since the Precambrian period. There is evidence that these first plants had a polar organization of the cell, chlorophylls a and b, and pyrenoids. The first elementary step towards the creation of telomes was the interconnection of cells. The cells were separated by a variety of materials. Genera such as Oltmannsiella had a plasma or gelatinous coating, while Ulothrix contained solid walls between cells. The second step toward a telome structure was rotation of the cell axes. This caused new cell walls to be oriented in all directions instead of being placed parallel to each other. This caused localized growth resulting in filament branching. The third step toward a telome structure was differentiation in the apical cell, meristemical tissue, and permanent tissue. The second and third steps together also had some profound effects. They either caused rotation of the axis in the meristemical tissue but not in the apical cell, as seen in Sphacelaria, or they caused rotation of the axis in the apical cell, as seen in Equisetum. Dichotomy was also caused in this step. This results when a sister cell to the apical cell is equally favored in growth. These two bifurcated telomes grow to be isotomous since no differentiation takes place to separate them. The fourth step towards telomes involves the shifting from predominantly haploid plants to diploid ones. This is caused by the postponement of meiosis into gametangia. The fifth and last step is the differentiation of permanent tissue.

Zimmermann (1952) said that these steps produced "Urtelomes," such as the phylum Thalassiophyta. Genera of this group had undifferentiated bifurcated telomes and usually contained a central bundle. Based on findings of the oldest land plants, the spores were probably formed throughout the telomes. These plants also probably had planospores instead of air-borne spores, and isomorphic instead of heteromorphic alternation of generations. Each of these steps was performed independently of each other, occurring in multiple combinations.

Zimmermann (1952) proposed that the formation of the megaphyll from the "Urtelome" plants occurred in several steps. The representative phylum for this period from the Upper Silurian to the Middle Devonian periods was the Rhyniaceae. These early plants were herbacious and had dichotomous branching (Holt, 2000). The isomorphic alternation of generation was replaced by heteromorphic alternation of generation, with a large sporophyte and small thallophytic gametophyte. Terminal sporangia produced air-borne spores through meiosis that were homosporous. The central bundles became part of the protostele, as xylem, and phloem began to be formed by elongated parenchyma cells. Aerial parts had stomata, and basal bodies had root hairs. The Bryophytes also developed from the Thalassiophyta, but with a dominant gametophyte, while Rhyniaceae is thought to have had a delicate gametophyte. The Bryophyte sporophyte was dependent on the gametophyte for survival, leading to a reduced single fertile telome. This relationship required water for fertilization, so this group grew close to the ground, often preserving the thallophytic structure.

Zimmermann (1952) based his Telome Theory on the taxonomy that was available at the time, which proposed that the Rhyniaceae gave rise to three different groups, the Lycopsida, Sphenopsida, and Pteropsida, which each underwent differentiation of the sporophyte to give the Kormophyta. He proposed that this differentiation was performed through six steps. In the first step, overtopping, a contrast in shoots between axis and leaves took place, causing the leaflets and leaves to arrange alternately). Zimmermann (1969) proposed that there were several variations of overtopping, resulting in a predominance of the upper-most telome (anadromic), the lower-most telomes (catadromic), or equal predominance of both telomes. Zimmermann (1952) proposed that the second step, planation, arranged the telomes and mesomes in a plane, causing the leaves to also be arranged in a plane. In the third step, syngenesis, the telomes and mesomes were connected by parenchyma or by their steles. The presence or absence of both overtopping and syngenesis led to variations of vein structures in these early plants, including the introduction of a net-veined structure. This syngenesis of the stele led to the different stele types observed, as indicated by the stelar theory. However, only the metaxylem took part in syngenesis, while the protoxylem remained unconnected. Therefore the protoxylem of these plants still showed the same furcated structure as the early land plants. The fourth step toward a leaf structure was reduction of the telomes. This occurred gradually, as the telomes and mesomes became shorter and shorter. The fifth step was incurvation, in which tissue growth of the two sides of the organ was unequal, resulting in a bend of the telome as one side grew faster than the other. The final step towards a leaf structure was longitudinal differentiation. This allowed for differentiation of the individual leaves within a shoot, allowing them to display various forms. We know that these steps were independent of each other because it is possible to find one of these steps occurring in a group independently of the others steps.

Although Walter Zimmermann proposed the Telome Theory in the early 1950’s, recent work on the theory still shows its validity. Boyer and Stein (1999) developed a model to test the Telome Theory and examine in detail the elementary steps described by Zimmermann. Herr (1998) proposed a revision to the Telome Theory, based on the development of primary leaves in primitive ferns. In Rhynia, he found that after overtopping, the apical cell could go from dividing in three planes to dividing in two planes. This change resulted in flattened branches, instead of cylindrical branches, in a process which Herr called fascination. When these flattened branched underwent growth reduction, they produced the same lamina that Zimmermann (1952) proposed evolved from lateral fusion of adjacent tissues during syngenesis.

The Enation Theory describes the evolution of microphylls. Bold et al. (1987) described a microphyll as a leaf that has unbranched veins and does not leave a gap in the stele of the stem. Bold et al.(1987) said that the Enation Theory states that microphylls are emergences, or enations, of the stem that have evolved veins. Esau (1953) said that fossil evidence shows that the first emergence of a microphyll occurred in the Psilotum, a Devonian plant. In these plants, the vein did not extend into the enation, but a small secondary vein did branch from the main vein of the plant. The Telome theory also suggests an evolution of microphylls, stating that they are the result of the reduction of Devonian plants that had already developed megaphylls. However, the fossil record shows more support for the evolution of microphylls proposed by the Enation theory. Therefore, the Enation theory is the better accepted of the two.

There seem to be questions not yet resolved by the Enation Theory and the Telome Theory concerning the origin of leaves. The Telome Theory, for example, is in conflict with the stelar theory that is supported by most morphologists. However, at this time, there are no alternative theories to explain these occurrences. Research does continue in this area, by such persons as Boyer and Stein (1999) and Herr (1998), to try to achieve a more thorough understanding of the elementary steps proposed by Zimmermann in his Telome Theory and to try to make sense of the discrepancies between this theory and the stelar theory. Also research is needed to try to understand whether microphylls evolved simply as reduced megaphylls, as proposed by Zimmermann, or by a completely different route, as proposed by the Enation Theory.

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