Plant Architecture & Phyllotaxy

D. Andrew White, 2008

Natura facit saltum

It is widely presumed that evolution proceeds through rather subtle mutation events. Those small variant that enhance survival are preferentially selected. The attendant assumption being: that those mutations that are not subtle tend to be non-viable. Generally there is no need to posit abrupt transitions, or saltations, in the evolutionary process. However, botanical evidences for evolutionary saltation are fairly unambiguous.

There is ample evidence that plant bauplans can be re-arranged by single mutation events. Heterochrony and heterotopy both allow for the possibility of modular re-combination (Smith 2001, Rutishauser & Moline 2005). Furthermore, there are sufficient evidences of discontinuities in plant form. From these gaps in form, it can be induced that saltatory transformations may have occurred in the evolution of plants. Though, as a semantic note, these kinds of transformations are not usually referred to as ‘saltations’.

Developmental genetics has redefined homology in terms of genetic transcription and the ontogenetic ramifications thereof (Bharathan & Sinha 2001, Geeta 2003, Champagne & Sinha 2004). The implications of these finding are, that heterochrony and heterotopy can now be understood, to a large degree (Rutishauser & Moline 2005, Kelogg 2006). It is these developmental features that make it possible to hypothesise a series of mechanisms that could account for modular recombination in plants.

Polyploidy can result in the abrupt formation of a new species. In the sense that a polyploid can be reproductively isolated from its parent stock, it is a saltatory change (De Bodt 2005, Zhang 2003). Polyploidy usually does not result in a significant change in a plant’s fundamental architecture or bauplan. Thus in the sense that there is no abrupt morphologic change, polyploidy is generally not considered to be ‘saltation’ per se.

Early in the twentieth century Arber suggested that some of the key features of the Monocotyledons originated sharply from mutation events (Arber 1920). In the 1960s van Steenis catalogued a number of plant forms that were not easy to account for via gradual transformation. Good in the mid-century suggested that some of the floral structures in the Angiosperms may have arisen through sudden re-arrangements (Good 1974). Stidd suggested that some key features of plant forms may have originated as perturbations of the ontogenetic systems. Stidd interpreted the fossil record such as to suggest that some of these transitions may have been saltative (Stiidd 1987). Takhtajan discussed what later came to be labelled modular recombination (Takhtajan 1991). The implication being that implied that plant evolution can occur through abrupt transitions.

Modularity is a ubiquitous feature in plant development. Plants, as a whole, are composed of reiterations of self-similar homologous units or modules. Plants are metameric in architecture. The vascular anatomy, branching patterns, root architectures, flowers, inflorescences, and leaf forms, are all modular in their construction (Rouane 1983, Dengler et al 2001, Fleurant et al 2004). The architectures of plants are such that they have been likened to algorithms or computer programs (Jean 1983, Prusinkiewicz & Remphrey 2000, Mündermann et al 2003, White 2005, Prusinkiewicz et al 2007).

One of the implications of modularity is the possibility of modular recombination. A mutation could perhaps perturb the ontogenetic programme of a plant. It has been observed that plant species can differ in the relative arrangement of their homologous ‘organs’ or ‘modules’. Indeed, there do appear to be numerous examples of plant structures that cannot easily be derived through the gradual transformation from one state to another. Nevertheless, in most cases these discontinuities can be explained by positing relatively minor re-orderings in the relative position of component modules.

In the 1970s Hallé and Olderman defined and catalogued the Architectural Models of plants. These models are idealised descriptions of the basic above ground organisation of plants. Secondary characteristics, such as colour and size, do not figure into these models. The models deal with the relative arrangement of main component modules. The basic modules include: growing points, leaves, stems, or flowers. The models are based on such factors as whether the stems bifurcate or trifurcate, the degree of apical dominance, and whether the structure of the lateral branches match or differ from the primary stem (Hallé et al 1978). The parameters used to define the models have been modified over the years. And recently the concept of architecture has been simplified further into developmental models. These are essentially algorithms that describe the same basic features, but in more mathematically concise terms (Prusinkiewicz et al 2007).

One of the primary algorithm-like features of plants is their leaf-bud arrangements, i.e. their phyllotaxis. Phyllotaxy follows a similar logistics to the aforesaid Architectural Models. Buds can be arranged variously in spiral, distichous, decussate or polymerous whorls. Transitions between phyllotaxies tend to be abrupt, even where they occur on the same plant. Phyllotactic arrangements of buds develop on the basis of a combination of a few principles governing the placement of primordia on a meristem (Jean 1983). In a somewhat simplified summary: each successive primordium develops so as to distance itself from the other primordia in its vicinity (Douady & Couder 1992, Reinhardt 2005). There are a limited number of phyllotactic permutations. One consequence of this is that there exist discontinuities between the phyllotaxies within a taxonomic group, or even within a species.

As with all general rules there are exceptions. Homologies can be of mixed form. Consequently, modules are not always demarcated as cleanly as implied by classical morphology. For example, in the Podostemaceae the vegetative thallus seems to share features of both leaf and stem (Rutishauser & Grubert 1999, Oko et al 2001). Similarly, the bladderworts (Utriculariaceae) lack a clear morphologic distinction between shoots, leaves and roots (Sattler & Rutishauser 1989). These exceptions do no totally negate the idea of modularity in plants. The architectures of these aberrant plants can also be modelled algorithmically.

Mutations that affect the basic architecture, within species, have been well documented Hallé has catalogued a number of these architectural mutants in both herbaceous and arborescent plants. These recur in unrelated taxonomic groups (Hallé 1978). Architectural Models are therefore examples of homoplasy. The data indicate that the same models have evolved in separate clades independently.

The Euphorbiaceae have a variety of architectural patterns. The castor-bean (Ricinus) follows Leeuwenberg’s model, with basically trichotomous branching and central terminal inflorescences. Rubber (Havea) usually grows according to Rauh’s model with self-similar branches in tiers. Some of the Euphorbia species follow Prévost’s model with dichotomous branching and a strong central leader. The secondary stems are often trichotomous (Hallé et al 1978). Presumably, there must have been architectural restructurings in the evolution of the Euphorbiaceae.

Almost invariably architectural mutants and terata can be characterised by architectural models that already exist naturally in other species. Many such architectural mutants within species have been documented. For example, the palm Hyphaene ventricosa normally follows Corner’s model, with a strong apical leader. A mutant form with Schoute’s model has dichotomous branching (Hallé 1978). Mutations affecting apical dominance are especially common. Some of the differences hinge on phyllotaxis. But in all cases, the mutation causes a discrete programmatic change in the order of modular arrangement.

One of the most well documented architectural mutations was the evolution of maize (Zea mays) from the wild teosinte grass. Teosinte like many grasses has laterals with mixed male and female flowers, i.e. Corner’s model. The cultivated maize has laterals that are strictly female flowers, with the male flowers on the terminal leader, i.e. Holttum’s model. The archaeological evidence suggests that the teosinte-to-maize transition was fairly abrupt (Iltis 2000). Mutant forms of maize still occur in which there is a partial reversion to the teosinte architecture (Hallé 1978).

The composites (Asteraceae) usually have a compound flower. Typically these groups of florets are subtended by a common circle of phyllaries, or the involucre. The involuces are variously either spirals or whorls. The whorled involucre has had various interpretations. Possibly the pseudanthium is derivable from a compressed raceme. In which case, the involucre is derived from the bracts of the basal set of florets (Takhtajan 1991). Alternatively, the involucre could have arisen from the proliferation of the single stipule that normally subtends an inflorescence. Or possibly, as Good suggested, the polymerous involucre could have arisen suddenly, through a single mutation event (Good 1974).

Morphologic studies suggest that the whorled phyllotaxis can arise as if spontaneously. In fact, in some extant species, whorls arise abruptly at certain phases in a plant’s lifecycle (Rutishauser 1999, Rutishauser & Moline 2005). It is therefore quite possible that the involucres could form in one step, without a gradual series of intermediate forms. Possibly this is what happened in the ancestral composites, the whorled phyllaries could have arisen in a single step.

Aquatic flowering plants often have whorled leaf arrangements (Rutishauser 1999). For example, the aquatic plant Hippuris has polymerous whorls. The waterwheels (Aldrovanda) also have whorls of leaf-traps (Adamec 2000). This whorled arrangement is one of the potential phyllotactic patterns that recur sporadically in diverse clades (Jean 1983). Whorls form if sets of primordia develop in synchronous pulses upon the meristem. This results in stems with whorls of phyllomes arranged in distinct nodes along the stem (Rutishauser 1999, Rutishauser & Moline 2005).

In some cases, the main mode of evolution was probably through the reduction or abortion of superfluous modules. In other cases, the proliferation of modules seems to have occurred. For example, Eudicots generally have a determinate number of petals, whereas the Magnolid flowers are usually indeterminate. Differences in the number of modules are not usually called ‘saltations’. Nevertheless, the basic principle is analogous to architectural mutation. In both cases a relatively small change in the developmental programme can be amplified through reiteration, or absence of reiteration.

In classical morphology the true leaf is subtended by a stipule. Furthermore, the leaf is located on a distinct node in the stem. In the garden bean, Phaseolus vulgaris, the distinctions between petiole and stem are somewhat indistinct. Very commonly, there are leafy stipels at the base of leaflets. Furthermore, these leaflets sometimes arise from a distinct nodelet at on the petiole (Rutishauser & Isler 2001). It is as if the petiole of the bean has acquired some of the traits of a stem. In fact, the interpretation of petioles as being partial-homologues of stems has some support from developmental genetics (Bharathan & Sinha 2001, Champagne & Sinha 2004).

In the family Gesneriaceae there are architectures that are hard to explain through gradual transformations. The genera Monophyllaea and Streptocarpella have members for which the main vegetative leaf is clearly an expanded cotyledon. Some species lack all other kinds of leaves (van Steenis 1969, Rothwell 1987). This architecture has been attributed to saltation, possibly as having arisen from a single-step mutation event. Perhaps this kind of mutation occurred via the retention of the juvenile form via neoteny (Rothwell 1987). It is also a form of archallaxis, as the leaf primordia after the cotyledons can be suppressed, in some of the species.

Sports arise among plants whereby the flowers become modified in some fashion (peloria). Methysticodendron apart from its non-fused corolla seems to be a version of Brugmansia which has fused trumpet-flowers. The opposite trend occurs in the catchfly Silene cucubalus where terata can have separated petals, instead of the fused corolla typical of the genus (van Steenis 1969). Bilaterally symmetrical, or zygomorphic, flowers sometimes revert to radial symmetry. The Lcyc epimutant of toadflax (Linaria vulgaris) has actinomorphic flowers, instead of the zygomorphic flowers typical of the species (Cubas 2004).

More extreme re-arrangements are possible. In the Petunia a mutant can occur in which the fused corolla is staminate. These petal-borne anthers can even have fertile pollen (Vallade et al 1986). In the gymnosperm Ginkgo biloba deformities occur in which the ovule occurs on stock that is flattened, like the megaphyll of the putative ancestor (Rothwell 1987). Both of these examples could be described as monstrosities. It is unlikely that they would ultimately be viable in the wild. Nevertheless, they illustrate the phenomenon of ectopy or organ misplacement.

In the water-lily Nymphaea prolifera the inflorescence is subtended by a common corolla. The ‘mother’ corolla is composed of actual petals. This anomalous inflorescence is a clear example of ectopy (Rutishauser & Isler 2001). This abnormal form also seems to support the contention of Process Morphology that homologues can come in mixed forms, and the boundary between module types is not always distinct (Rutishauser & Moline 2005).

In Acacia longipedunculata there is a shift of phyllotaxis. The seedling has bipinnate leaves that are spirally arranged. As the plant matured matures the leaves become decussate and then eventually whorled (Rutishauer & Sattler 1984). Phyllotactic shifts during a lifecycle are not uncommon. The under-water leaves of the bladderworts (Utricularia) are generally either distichous or whorled, depending on the species. The aerial shoots and the inflorescences are often spirally arranged. (Sattler & Rutishauser 1989, Rutishauser 1999). The transition from one phyllotaxy to another, even within an individual plant, is almost invariably abrupt (Jean 1974, Douady et al 1992).

In garden peas (Pisum sativum) there are a variety of mutations that influence leaf architecture. Wild-type peas have pinnate leaves wherein the terminal series consists of tendrils. The afila mutant has tendrils in place of all of its leaflets. The tendril-less mutant has leaflets but no tendrils. In recent decades, the developmental genetics of these mutations have been elucidated (Gould & Cutter 1985). A difference in a single gene can make the difference between a leaf compound and an entire leaf (Bharathan & Sinha 2001, Kim et al 2003).

Within a species the heterophyllous series can be discontinuous. Maples can display a discontinuous series of leaf forms, even within species. Acer negundo, or box-elder, has usually three, five or seven-foliate compound leaves. The transitions between these forms are discontinuous. They are not due simply to deeply cleft sinuses separating-off the leaflets. The dwarf maple (Acer glabrum) typically has entire leaves. But trifoliate leaves do occur, even on the same tree. Deeply cleft leaf lobes do occur, but the transition to compound leaf is abrupt. The honey locust (Gleditsia triacanthos) typically has pinnate leaves, with a few bipinnate leaves as well. Mixed form leaves also occur, where a few of the secondary axes are compound. Again, the leaflets do not seem to be merely deeply cleft leaf lobes (White 2005).

It has long been noted that leaflets resemble whole leaves. Leaflets seem to be partial-homologues of entire leaves. A leaflet’s petiolule is therefore probably a partial homologue of the entire leaf’s petiole. The findings of developmental genetics have tended to support the theory of partial-homologues (Champagne & Sinha 2004).

In those organisms that display heteroblasty, there is sometimes an abrupt transition from one leaf-form to another. This is can occur if there is a deletion or suppression of later stages in development. The evolutionary version of this would be an abbreviation of early growth phases, or archallaxis (Gould 1977). For example, the early suppression of marginal lamina, in a leaf primordium, would result in a highly modified form in the later phases of a leaf’s growth. The allometrics of this early-phase abbreviation could automatically result in a later-phase leaf that resembles a naked-petiole. Indeed, such abbreviations could explain the origins of phyllodes, or even spines (Kerstetter & Poethig 1998).

A putative example of archallaxis would be the derivation of the monocot leaf from a petiole-derived phyllode. Such a derivation was suggested by Arber in the 1920’s. In their mode of growth, parallel venation, and other details, monocot leaves resemble the phyllodes of some of the legumes. Possibly, the ancestral monocot leaf may have lost its reticulated venation in a single mutation event (Arber 1920, Boke 1940, Kaplan 1973).

Phyllodes, in the Fabaceae, are often derived from leaves that fail to form leaflets. In the Acacia longipedunculata a semi-continuum exists between setaceous stipules, phyllodes, pinnate leaves and bi-pinnate leaves. The transition can occur in the same plant, as the seedling transforms from bi-pinnate juvenile leaves into the phyllodes that typify the mature shoots. The transition is not perfectly continuous. The phyllode-leaf intermediates have tiny protuberances, rather than complete leaflets (Rutishauer & Sattler 1984).

Petiole-derived phyllodes differ radically from the reticulated leaves in related species. In the sub-marginal portion of a reticulated leaf there are a series of growth- centres. For a simple leaf, the common growth-centre is a procambial arc. In the compound leaf, unevenly expanding growth-centres give rise to successive waves of lobes or leaflets (Cusset 1986). A petiole-derived phyllode fails to develop a laminar margin, and also thereby fails to form leaflets. The phyllode becomes a naked-petiole. This phyllode retains the parallel venation typical of a petiole (Arbor 1920, Boke 1940, Arbor 1950).

An incomplete series of transitions occurs in the leaf and spine forms in the Cactaceae. In the Cylindropuntia there are transitional forms between the tiny glochids and larger spines. In the early stages, the primordia of the leaf and spine are also similar. In mature stages, the spine and leaf are sharply differentiated. Those primordia destined to become spines fail to develop mesophyll, stomata, and vasculature that characterise the normal leaf (Boke 1944, Rowley 2002). Cactus spines are probably an example of abbreviation or archallaxis. They differ from the phyllodes in having an even greater abbreviation of their later growth phases.

Architectural mutations can vary as to whether they are dominant or recessive. Some of these sports are actually epimutants. Whatever their origin, these architectural abnormalities are useful morphogenetic tools. They help to delineate the potential range of morphologies that can occur within a given taxonomic group. It would be reasonable to conclude that a heritable mutation could likewise alter the ontogenetic programme of a plant in an analogous manner.

Most of the discontinuities in plant form, discussed herein, can be modelled as relatively minor changes, changes that are amplified as the modification is reiterated. They are analogous to a single-operand change in an algorithm. Most viable architectural mutations were almost certainly not drastic examples of ectopy or heterotopy. Often in fact they must have been predominantly heterochronic changes. They were tiny alteration in the spacing of primordia within a meristem, changes in the degree of apical dominance, or changes in the number of modular reiterations. Yet because these mutations alter the growing points, and those growing points are reiterated, the overall appearance of the mutant can differ greatly from its parent form (Hallé 1978).

Similar to architectural models would be mutations that perturb the trajectory of development, such as occurs in archallaxis. In these cases, the component modules themselves may become altered. Archallaxis is basically an alteration in the sub-modules that compose the module, or an architectural alteration. In the case of phyllodes for example, there is a shift in the growth-centres towards the petiole, and away from the margins. Clearly, however, the ontogenetic programmes of both the phyllode and leaf are homeotic. They are slight variations on the same fundamental logistics.

Any claim that architectural mutations must always be neutral would be unjustified. Subtle features in plant form can greatly influence survivability (Givnish 1978, Kikuzawa et al 1996). It is likely that most architectural mutations would tend to diminish survivability. Though, it is plausible that architectural mutations might be less likely to be deleterious than would be mutations that disrupt the component modules.

Architectural mutations may have, as a whole, a greater likelihood of retaining their functionality. At least, this may be expected relative to mutations that disrupt the modules themselves. (1) Architectural mutations often seem to depend on a very few genes. They are therefore probably fairly likely to occur. (2) These mutations often do not greatly disrupt the component modules. The functionality of the modules could therefore be retained. (3) If the functionality of the modules is retained, there may be a greater likelihood that the overall architecture also would also remain viable.

In recent decades there has been an acknowledgement that ontogeny can influence the trajectory of evolution. This is the ‘evo-devo’ approach that often borrows metaphors from cybernetics. The basic idea is that it is easier to reroute a developmental programme, through slight adjustments, than it is to totally change the logistics of the said programme. The component modules are not disrupted, but retain their functionality. The rearrangements could be temporal (heterochronic) or they could be spatial (heterotopic). That is, such mutations would actually have very minor local effects. These ‘minor’ alterations can then be amplified through reiteration. Or, they may be exaggerated through the allometrics of growth.

Evo-devo interpretations are compatible with the metaphor of morphospace. This is the idea that certain morphologies are more probable than others, as dictated by the mechanics of growth. But it would not be only allometric factors that constrict the range of likely forms. Modular organisms can be subject to modular recombination. Some of these permutations would be more probable than others. In addition to this morphospace, there is the metaphor of the fitness landscape. Architectural mutations would probably differ in the degree to which they affect the survivability of the whole plant. Only a portion of the morphologically-possible-forms would actually be viable.

Nature seems to make ‘leaps, at least sometimes, at least with plants. These abrupt transitions are usually the result of modular re-combinations or architectural mutations. Architectural mutations could be a factor that helps to confine the morphospace within which plants can evolve.

References

Adamec L. (2000) Rootless aquatic carnivorous plant Aldrovanda vesiculosa: physiological polarity, mineral nutrition, and importance of carnivory. Biologica Plantarum. 43: 113-119.

Arber, A. 1920. Leaf-Base Phyllodes Among the Liliaceae. Botanical Gazette. 69, 4, 337-340.

Arber, A. (1950) The Natural Philosophy of Plant Form. Cambridge University Press. Cambridge.

Baillaud, L. (1999). Structures répétitives spatiales et spatiotemporelles des plantes. Phytomorphology. 49, 4, 377-404.

Bharathan, G. and Sinha, N.R. (2001). The Regulation of Compound Leaf Development. Plant Physiologist. 127, 1533-1538.

Boke, N.H. 1940. Histogenesis and Morphology of the Phyllode in Certain Species of Acacia. Am. J. of Bot. 27, 2, 73-90.

Boke, N.H. 1944. Histogenesis of the Leaf and Areole in Opuntia Cylindrica. Am. J. Bot. 31, 6, 299-316.

Champagne, C. and Sinha, N. (2004) Compound leaves: equal to the sum of their parts? Development. 131, 4401-4412.

Cubas, P. 2004. Review: Floral zygomorphy, the recurring evolution of a successful trait. BioEssays. 26, 1175-1184.

Cusset, G. (1986) La morphogenèse du limbe des Dicotylédones. Can. J. Bot. 64, 2807-2839.

De Bodt, S.; Maere, S. and Van de Peer, Y. 2005. Genome duplication and the origin of angiosperms. Trends Eco Evol. 20, 11, 592-597.

Dengler, N.G. and Tsukaya, Hirokazu. (2001) Leaf Morphogenesis in Dicotyledons: Current Issues. Int. J. Plant Sci. 162,3, 459-464.

Douady, S. and Couder, Y. (1992) Phyllotaxis as a physical self-organized growth process. Physical Review Letters. 68, 2098-2101.

Fleming, A.J. (2003) The Molecular Regulation of Leaf Form. Plant Biol. 341-349.

Fleurant, C.; Duchesne, J. and Raimbault, P. (2004) An allometric model for trees. J. Theoret. Biol.. 27, 1, 137-147.

Geeta, R. 2003. Book Review: Variation and Diversication in Plant Evo-Devo. Am. J. Bot. 90, 8, 1257-1261.

Gillham, N.W. (2001) Evolution by Jumps: Francis Galton and William Bateson and the Mechanism of Evolutionary Change. Genetics. 159, 1383-1392.

Givnish, T.J. (1978) On the adaptive significance of compound leaves, with particular reference to tropical trees. Tropical Trees as Living Systems. P.B. Tomlinson and M.H. Zimmermann (eds.). Cambridge University Press. New York. 351-380.

Good, R. (1974) Features of Evolution in the Flowering Plants. Dover Publications, Inc. New York.

Gould, S.J. (1977) Ontogeny and Phylogeny. Harvard University Press. Cambridge.

Gould, K.S., Cutter, E.G. and Young, J.P.W. (1986) Morphogenesis of the compound leaf in three genotypes of the pea, Pisum sativum. Can J. Bot. 64, 1268-1276.

Hallé, F. (1978) Architectural Variation. In: Tropical trees as living systems P.B.Tomlinson & H. Zimmerman (eds.). Cambridge University Press, Cambridge. 209-220.

Hallé, F. and Oldeman, R.A.A. (1970) Essai sur l’Architecture et la Dynamique de Croissance des Arbres Tropicaux. Masson. Paris.

Hallé, F. (1978) Architectural Variation. In Tropical trees as living systems. P.B.Tomlinson & H. Zimmerman (eds.). Cambridge University Press, Cambridge.

Hallé, F.; Oldeman, R.A.A and Tomlinson, P.B. (1978) Tropical Trees and Forests: An Architectural Analysis. Springer, New York.

Iltis, H.H. 2000. Homeotic sexual translocations and the origin of maize (Zea mays, Poaceae): A new look at an old problem. Economic Botany. 54, 7-42.

Jackson, D. (1996) Plant morphogenesis: designing leaves. Current Biology. 6. 8, 917-919.

Jean, R.V. (1983) Croissance Végétale et Morphogenèse. Masson. Paris.

Kaplan, D.R. (1973) The Problem of Leaf Morphology and Evolution in the Monocotyledons. The Quarterly Review of Biology, 48, 3, 437-457.

Kellogg, E. A. 2006. Evolution of Flowers and Inflorescences: Progress and challenges in studies of the evolution of development. J. Experimental Bot. 57, 13, 3505-3516.

Kerstetter, R.A. and Poethig, R.S. 1998. The Specification of Leaf Identity during Shoot Development. Annual Rev. Cell Develop. Biol. 14, 373-398.

Kikuzawa, K.; Koyama, H., Umeki, K., and Lechowicz, M.J. (1996) Some evidence for an adaptive linkage between leaf phenology and shoot architecture in sapling trees. Functional Ecol. 10, 252-257.

Kim, M..; Pham, T.; Hamidi, A.; McCormick, S.; Kuzoff, R.K.; and Sinha, N. (2003). Reduced leaf complexity in tomato wiry mutants suggesting a role for PHAN and KNOX genes in generating compound leaves. Development. 130. 4405-4415.

Linberg, D.R. (1998) William Healey Dall: A Neo-Lamarckian View of Molluscan Evolution. The Veliger. 41, 3, 227-238.

Maizonnier, D. and Cornu, A. 1986. La morphogenèse florale chez le pétunia. I. Analyse d’un mutant à corolle staminée. Can. J. Bot. 65, 761-764.

Manos, P.S.; Zhou, Z-K. and Cannon, C.H. (2001) Systematics of Fagaceae: phylogenetic tests of reproductive trait evolution. Int. J. Plant Sci. 162,6, 1361-1379.

Mündermann, L.; MacMurchy, P.; Pivovarov, J.; and Prusinkiewicz, P. (2003) Modelling lobed leaves. Proceedings of Computer Graphics International CGI. 60-65.

Okamoto, M. (1989) New interpretation of the inflorescence of Fagus drawn from the developmental study of Fagus crenata, with description of an extremely monstrous capsule. Am. J. Bot. 76, 1, 14-22.

Ota, M.; Imaichi, R. and Kato, M. (2001) Developmental morphology of the thalloid Hydrobryum japonicum (Podostemaceae). Am. J. Bot. 88, 3, 382-390.

Poethig, S. (2003) Phase Change and the Regulation of Developmental Timing in Plants. Science . 301, 334-336.

Prusinkiewicz, P. and Remphrey, W.R. (2000) Characterization of architectural tree models using L-systems and Petri nets. In: L’ arbre - The Tree 2000: Papers presented at the 4th International Symposium on the Tree. M. Labrecque (Ed.) 177-186.

Reinhardt, D. (2005) Regulation of phyllotaxis. Int. J. Dev. Biol. 49, 539-546.

Rothwell, G.W. (1987) The Role of Development in Plant Phylogeny: a paleobotanical perspective. Rev. Palaeobot. Palynol. 50, 97-114.

Rouane, P. (1983) la forme des feuilles palmées: Essai de modélisation. Bull. Soc. Bot. Fr. 130, 4/5, 325-328.

Rowley, G. 2002. What is an areole? Brit. Cactus & Succulent J. 21, 1, 4-11.

Rutishauser, R. (1999). Polymerous Leaf Whorls in Vascular Plants: Developmental Fuzziness of Organ Identities. Int. J. Plant Sci. 160, 6, S81-S103.

Rutishauser, R. and Grubert, M. 1999.The architecture of Mourera fluviatilis (Podostemaceae): developmental morphology of inflorescences, flowers, and seedlings. Am. J. Bot. 86, 907-92.

Rutishauser, R. and Sattler, R. 1984. Architecture and development of the phyllode – stipule whorls of Acacia longipedunculata: controversial interpretations and continuum approach. Can. J. Bot. 64, 1987-2019.

Rutishauser, R. and Isler, B. (2001). Developmental Genetics and Morphological Evolution of Flowering Plants, Especially Bladderworts (Utricularia): Fuzzy Arberian Morphology Complements Classical Morphology. Annals Bot. 88, 1173-1202.

Rutishauser, R. and Moline, P. (2005) Evo-Devo and the search for homology (“sameness”) in biological systems. Theory in Biosciences. 124, 213-241.

Sargent, C.S. 1965. Manual of the Trees of North America. Vol.1. & 2. Dover Publications, Inc. New York.

Sattler, R. and Rutishauser, R. (1989) Structural and dynamic descriptions of the development of Utricularia foliosa and U. australis. Can. J. Bot. 64, 1989-2003.

van Steenis, C.G.G.J. (1969) Plant speciation in Malesia, with special reference to the theory of non-adaptive saltatory evolution. Biol. J. Linn. 1, 97-133.

Smith, K.H. (2001) Heterochrony revisited: the evolution of developmental sequences. Biol. J. Linn. Soc. 73, 168-186.

Stidd, B.M. (1987) Telomes, Theory Change, and the Evolution of Vascular Plants. Rev. Paleobot. Palynol. 50, 115-126.

Takhtajan, A. 1991. Evolutionary Trends in Flowering Plants. Columbia University Press. New York.

Tattersal, A.D.; Turner, L.; Knox, M.R.; Ambrose, T.H.; Ellis, T.H.N. and Hofer, J.M.I. (2005) The Mutant crispa Reveals Multiple Roles for PHANTASTICA in Pea Compound Leaf Development. Plant Cell. 17, 1046–1060.

Tsukaya, Hirokazu (2005) Leaf shape: genetic controls and environmental factors. Int. J. Developmental Biol. 49, 547-555.

Tooke, Fiona and Battey, Nick. (2003) Models of shoot apical meristem function. New Physiologist. 159, 37-52.

Vallade, J., Maizononnier, D. and Cornu, A. (1986) La morphogenèse florale chez pétunia. I. Analyse d’un mutant à corolle staminée. Can. J. Bot. 65, 761-764.

Waites, R.; Selvadurai, H.R.N.; Oliver, I.R. and Hudson, A. (1998) The PHANTASTICA Gene Encodes a MYB Transcription Factor Involved in Growth and Dorsoventrality of Lateral Organs in Antirrhinum. Cell. 93, 779-789.

White, D. Andrew. (1992) Relationships between foliar number and cross-sectional areas of sapwood and annual rings in red oak (Quercus rubra) crowns. Canadian Journal of Forest Research. 23, 1245-1251.

White, D.A. (2005) Architectural mutation and leaf form, for the palmate series. J. Theoretical Biol. 235, 2, 289-301.

White, D. Andrew. 2005. Architectural mutation and leaf form, for the palmate series. Journal of Theoretical Biology. 235 (2): 289-301.

It is perhaps now common knowledge that Earth owes its oxygen rich atmosphere to photosynthetic organisms, cynanobacteria, green algae and plants. About two thirds of the organic matter produced per year is by land plants, and the rest by aquatic plants. However, at least half of the oxygen in Earth's air comes from photosynthetic algae in the oceans, algae such as the diatoms and other planktonic plants. Oceanic algae are apparently more effective in liberating oxygen than land plants.

The atmospheres of Venus and Mars are very similar in composition, despite their vastly different temperatures. Earth has a special air about it.

James Lovelock, an atmospheric scientist at Princeton, proposed the now famous "Gaia Hypothesis" in the early 1970s. James Lovelock was driven to his hypothesis by the astounding observation that the Earth's atmosphere is not in chemical equilibrium. Rather, Earth's atmosphere is in dynamic equilibrium. It is held in an unstable mixture of nitrogen and oxygen by photosynthesis, which in turn is powered by the Sun. Lovelock made the prediction that Mars is either poorly stocked with life, or completely devoid of life. The atmosphere of Mars can be explained by abiotic chemical processes, Earth's atmosphere cannot. Both the Martian and Venusian atmospheres are dominated by carbon dioxide (98% +). If all of the carbon locked up in Earth's limestone, chalk, oil and coal were to be liberated, and to react with oxygen, Earth's atmosphere would then come to resemble that of Venus.

According to most theoretic models, the Sun should not have remained stable in radiant output during its long duration. Yet life has not been exterminated by any solar vagary. Also, the amount of carbon dioxide has never been so much that life was blotted out by a run-away greenhouse effect. Nor has the carbon dioxide level ever fallen so low that all living things were obliterated by an extreme glacial epoch. There are other details of the ecosystem that are likewise controlled by the collective action of algae and plants. These processes keep the Earth's biosphere in dynamic equilibrium.

Earth has rain. Venus is too hot for rain, and Mars is now too cold for rain. Rain, being slightly acidic, erodes surface rock and generates carbonates from the reaction of carbon dioxide and basic elements. These carbonates are washed into ocean sediments, forming limestone and dolomite. The net result being a culling of carbon dioxide from the air. Green plants play a major role also, they remove carbon dioxide, and release dioxygen. Many protozoa, with carbonate shells, store up carbon as they live. The precipitation of a portion of these testae to the ocean floor is another carbon sink. Vast sediments of chalk testify to the quantity of carbon removed from the air by these plankta. Furthermore, not every living thing is recycled in the food chain. Sometimes large plants are covered in water borne mud, hence coal is formed. Some of the fats and oils of organisms becomes trapped in sediments, resulting in the formation of petroleum. All of these processes also remove carbon dioxide from the air. Over the eons these carbon sinks have greatly reduced Earth's store of carbon dioxide gas.

Even though there are some abiotic processes that remove carbon dioxide, there are no simple chemical reactions that liberate free oxygen. Earth's atmosphere is about twenty one percent oxygen gas (dioxygen). Dioxygen is too reactive to endure for long in an atmosphere. It is now known, with a great deal of certainty, that photosynthesis is the driving force behind Earth's rich unstable atmosphere.

Science has tended to confirm the existence of the Gaian balance. However, Gaia's explanation has eluded science. It is difficult to comprehend how such a fine balance could have originated, through the independent natural selection of its constituent organisms. Perhaps, as Lovelock suggested, complex ecosystems tend to develop feedback loops that tend to self-stability. Some mathematical models seem to support this hypothesis. The latest climatic models suggest that the latent heat of the oceans keeps the Earth's temperatures within liveable bounds. And that even if the Earth had a much more elliptical orbit, the Earth's oceans and atmosphere would resist extreme seasonal swings. Gaia, according to this hypothesis, may be a fortunate consequence of both thermodynamics and ecodynamics on a grand scale. Others propose that the Gaian balance is evidence of a Creator Deity. Just because this Theistic evolution hypothesis falls outside of the scope of empirical science, at present, does not imply that it can be dismissed.

Some people have argued against the existence of a perfect Gaian balance. For example, there is evidence that there was an extreme glacial epoch just prior the Cambrian. This ice age was so extreme that it is possible that life had a "close call" with total obliteration. The oceanic ice may have become so thick that most photosynthetic bacteria and algae barely survived. However, within ten million years of ice age's end the frond-like Ediacaran creatures were thriving. A few tens of million more and the oceans were teaming with protozoa, plants and animals. Since life obviously did survive, perhaps there was not a total freeze-over. Or perhaps, algae survived near volcanic hot-spots. Even this close call, if it was one, was not an isolated disaster. There been seven or so major extinctions since the Cambrian. Some extinction events, evidence suggests, may have been due to asteroid/comet impacts. The mere existence of such 'close calls' has been used as evidence that the Earth was just plain lucky. On the other hand, the fact that life has survived all of these disasters has been interpreted as evidence for the robust resiliency of the Gaian balance.

The Gaia Hypothesis is not without its critics. As originally framed, the hypothesis was a little too wildly metaphorical - almost metaphysical. It left the impression that earth is demonstrably sentient. In later more detailed versions of the hypothesis Lovelock was less metaphoric. His mechanism for Gaia was in essence merely ‘feedback stabilisation’ - i.e. complex interconnected systems tend to resist change. This toned down version of Gaia was a far cry from claiming that Earth is literally alive.

The word Gaia comes from the Greek name of the Earth Goddress. This was originally intended to be taken metaphorically, not literally. Nevertheless, it is not surprising that the Gaia Hypothesis has become a doctrine of the so-called New Age religion(s). Believers in vital force, Earth energies, telluric forces, ley lines, dowser’s energy lines, earth lights, qi gong and feng shui, have all referenced the Gaia Hypothesis as 'evidence' of their claims. All of these claims go beyond the realm of science into speculative metaphysics. All involve suppositions that do not follow logically from the scientific evidence currently available. No doubt these concepts and wild fancies reflect the psychological appeal of the Earth Mother archetype. One can appreciate the mythopoetic allure of these ideas, but it is unwise to take them too literally.

What ever the true origin of the Gaian Process, it certainly now exists. Green plants are essential to it. We owe our every breath to them.

Cyanobacteria

Since photosynthesis powers the majority of the Earth's biota, one would think that the Plantae Kingdom dominates the world. This is not exactly true.

In 1988 two oceanographers, Sallie W. Chrisholm and Robert J. Olson, discovered the most common genus of cyanobacterium. Prochlorococcus is probably the most important single taxon of photosynthetic organism alive on Earth today. By shear number and ubiquity the bacterial genus dominates the seven seas. This common blue-green alga is a genus of cyanobacterium or bacterial alga. The Prochlorococcus are only 0.5 to 0.7 microns wide, and live mostly within 200 metres of the surface, where there may be 1-3 x 10⁵ cells per millilitre of sea water. They have a mere 1.7 x 10⁶ base pairs in their DNA, which is very brief for an independent organism. This group of bacters accounts for roughly a quarter of all photosynthetic oxygen liberation, and a similar proportion of all biotic carbon dioxide absorption, on Earth. Together with other algae they account for more than half of all oxygen production and half of all carbon dioxide consumption. There are at least 35 species of Prochlorococcus known. Its cells are spread thinly, but widely, through all of the world's oceans. Indirectly the sea is powered by algae such as them. The sea could be considered like one big leaf.

Judging by what is visible to the human eye, the oceans seem top-heavy with carnivorous animals. Seaweeds and other visible plants comprise a minority of what is visible in the sea. In the sea there are several layers of carnivores eating carnivores before one reaches algae-eaters. Hence,the greater bulk of the oceanic flora is invisible to the human eye!

Mycorrhizae & Symbiosis

Symbiosis is the co-existence of two different species, each of which mutually benefits the other. Lichens are symbiotic combinations of algae and fungi, allowing the fungus to photosynthesise like a plant! Many mammals use bacteria to aid in their digestion of foodstuffs. Mycorrhizal fungus-plant interactions are one of the most interesting examples of symbiosis.

Vascular plants commonly have a symbiotic relationship with fungi. In this relationship the fungal mycelia intertwine with the rootlets of plants. Roots can absorb water and highly soluble minerals. Fungi are generally better at absorbing low mobility ions, such as phosphorous, than are plants. Fungi, however, do not produce sugar and are not themselves photosynthetic. Fungi must feed upon sugars which originate, ultimately, from green plants.

The term mycorrhizae is given to those soil fungi commonly found in association with plant roots. Mycorrhizae gain sugar from the roots of plants and, as if by way of trade, pass disolved minerals to the plants' rootlets. This system is symbiosis at its best. The plant gains enhanced mineral uptake. The fungus gains an energy source.

Endomycorrhizae occur where fungal hyphae penetrate the root cells. Arbuscular endomychorrhizae form branching hyphae inside cells of rootlets. ‘Arbusculars’ are most common in the Glomales order of the glomeromycetes. Ectomycorrhizae have hyphae which encircle rootlets and the spaces between the outer layer of rootlet cells. Often these hyphae form complete sheaths around the tips of rootlets. Ectomycorrhizae are commonly formed by the ascomycetes, basidiomycetes, and some of the zygomycetes. Some plant species have strictly ecto- or endo-mycorrhizae, but not both. However, other plant species can have both forms of mycorrhizae. Certain species can even switch mycorrhizal forms during their life cycle.

Glomales & Endogones

Glomeromycota were, until recently, classified in the phylum Zygomycota. However, genetic comparisons in the 1990s suggested that the glomales are best considered a taxon unto themselves. The members of the Order Glomales are mostly, if not entirely, asexual. The glomales can produce branched sporangia, each sporangium with very few spores. Glomales are arbuscular endo-mychorrhizal fungi, their hyphae penetrate the cell walls of rootlets. The genus Glomus is one widespread example of an endo-mycorrhizal symbiont. Most of common glomale fungi are obligate mycorrhizals. A few of the glomeromycetes (e.g. Geosiphon spp) live symbiotically with cyanobacteria instead of roots.

Glomales are a very widespread clade of mycorrhizal fungi. Many plants have glomales as their main root associates. Fossil evidence suggests that the mycorrhizal association between glomale-like fungi and plants is very ancient. Probably both land-plants and fungi have had an association since times premordial.

As if to add superfluous complexity, there seems to be yet another layer of symbiosis in the glomales. The glomales often have little bladder-like extensions on their mycelia. In these chambers there are colonies of endobacteria. Some of the genes of the Candidatus Glomeribacter gigasorarum seems to be involved in mineral uptake. So quite possibly the ‘glomeribacters’ are symbiotic.

Mycorrhizal fungi in the genus Endogone are still often classed as zygomycetes. These fungi form ectomycorrhizal sheaths around rootlets. Endogones are not imperfect fungi. The sporocarps of the endogone fungi are small puffy masses under forest duff. Mice often feed on these fruiting bodies.

Confusingly, genetic studies show that the endogones are more closely related to some of the chytrid moulds than to other pin-moulds. However, unlike the chytridiomycetes they do not have flagellated gametes. Presently endogones are not considered to be true chytrids. Probably chytrids are simply those archaemycetes that have retained flagellated gametes. Those archaemycetes which are non-aquatic seem to have lost the need for flagellated gametes. Chytrids may be considered the more fully aquatic members of the Archaemycota.

References

Daniel, W.D., Helms, J.A. and Baker, F.S. 1979. Principles of Silviculture. McGraw-Hill Book Company. New York. 215-221.

Grierson, Donald and Covey, Simon N. 1988. Plant Molecular Biology. Second Edition. Blackie. Glasgow.

Heinrich, Bernd. 1997. The Trees in My Forest. Cliff Street Books. New York. 180-187.

Bonfante, P. 2003. Plants, Mychorrhizal Fungi and Endobacteria: a Dialog Among Cells and Genomes. Biol. Bull. 204: 215-220.

Schüßler A, Schwarzott D, and Walker C. 2001. A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycological Research 105(12): 1413-1421.

Global Warming