ON THE ORIGIN OF ANGIOSPERMS: THE EUANTHIAL AND PALEOHERB DEBATE.

Susan Brenner, Wesley Schrock, Ashley Shade, Greg Swartzentruber, Kirsten Wilbur.  FOGGY GOGGLES

ABSTRACT

The evolution of flowering plants has been in controversy ever since Darwin’s voyage on the Beagle in 1831.  What Darwin referred to as “an abominable mystery” has developed into a phylogenetic debate between taxonomists, paleobotanists, and molecular systematicists.  The two prominent theories concerning the origin of flowering plants are the Euanthial theory and the Paleoherb theory.  According to the Euanthial theory, the extant Magnolia represents the link between flowering and nonflowering plants.  Zimmermann’s Paleoherb theory suggests that the origin of angiosperms is found within small, unisexual flowers such as Hamamelididae and Piperales.  Our article examines the opposing Euanthial and Paleoherb theories and their evidences that support the magnoliids and paleoherbs, respectively, as the basal root of the angiosperms.  We believe that of the Euanthial and Paleoherb theories, the Euanthial theory is most plausible due to overwhelming structural support in the magnoliids. 

INTRODUCTION

Flowering plants are taxonomically referred to as angiosperms or anthophytes.  They have true flowers, ovules enclosed in a carpel or ovary, and a dominant sporophyte generation (Hutchinson 1969, Margulis and Schwartz 1999, Takhtajan 1969, Stebbins 1974, Downie and Robinson 2002).  The evolutionary history of angiosperms is important because there is an apparent common ancestor of all flowering plants (Margulis and Schwartz 1999).  By understanding the origins, and thus the diversity of the angiosperms, scientists can conduct further research the medical, economical, and agricultural implications of specific angiosperm families. 

Darwin’s initial questions regarding the origin of flowering plants have sparked numerous hypotheses.  In 1907, Arber and Parkin proposed the first hypothesis widely accepted by the scientific community.  Known as the Euanthial theory, it suggests that the angiosperm flower evolved from a plant that housed bisexual strobilus-like gymnosperm reproductive structures, bearing many spirally arranged ovulate and pollen organs.  According to this theory, the extant Magnoliaceae are the link between flowering and non-flowering plants (Doyle 1997; Martin et al 1992).

Von Wettstein (1924) and Zimmermann (1930) proposed an additional theory. The Pseudanthial theory suggests that the angiosperms originated from a plant that carried unisexual gymnosperm reproductive structures.  According to this theory, the small, simple, unisexual flowers, such as those found in the Hamamelididae and Piperales, are considered to be the most primitive of the angiosperms (Martin et al, 1992).  Thus, the Pseudanthial theory supports genera like those in Hamamelididae and Piperales as the basal root.      

Another early 20^th century rival to the Euanthial theory is the anthophyte hypothesis or the Englerian theory.  This theory suggests that the Gnetales are the closest living link between flowering and non-flowering plants. (Barkmann et al. 2000)  Similarities between the reproductive structures of the Gnetales and those of the angiosperms suggest that the Gnetales are the sister group to the angiosperms (Cornet 2000).  Friedman (1992) believes that the double fertilization character of the flowering plants are closely linked to the fertilization of the Ephedra, which is a primitive genusof Gnetales.  In addition, Boew et al (2000) conducted research using two sequence data sets from mitochondrial genes that rejected the anthophyte hypothesis completely and suggested that the shared characteristics between Gnetales and angiosperms are independently derived.  Thus, though the Englerian theory continues to be part of the angiosperm evolution debate, it is no longer a prominent player. 

Donoghue and Doyle (1986) support one of the most recent hypotheses concerning the origin and basal root of the angiosperms.  They argue that Nymphaeles, the water lily family, is the most primitive extant family of flowers and therefore the link between non-flowering and flowering plants.  Their analysis included developmental and genetic evidence, but further research is necessary to better support that Nymphaeles is the basal root of the Angiosperms. 

Some remaining controversial theories on the evolution of angiosperms consist of combinations of the previous theories.  Barkmann et al (2000) suggest that Amborella and the Nymphaeles together form the basal root of the angiosperms.  Amborella is a flowering shrub that lacks petals.   It is included in family Laurales, which is closely related to family Magnoliaceae (Hutchinson 1969).  According to Hutchinson (1974), the Nymphaeles maintain a primitive character in the petals’ transitions into stamens.  More recently, the genetic research of Soltis et al (2000) suggests that Nymphaeles, Amborella, and a clade of three Magnoliaceae genera are jointly linked to angiosperm origin.  

Of all of these theories on the link between non-flowering and flowering plants, the Paleoherb theory and the Euanthial theory are the most widely accepted and debated.  As illustrated in Figure 1 (taken from Wing et al 1993), the two represent two very different evolutionary histories of the Angiosperms.

Figure 1.  Angiosperm Origins: The two competing hypotheses for angiosperm origins presenting very different pictures about the biology of the earliest flowering plants. The Paleoherb Hypothesis suggests that the basal lineages were herbs with rapid lifecycles, while the Magnoliid Hypothesis suggests that the basal lineages were small trees with slower lifecycles. (Dicots=tricolpate dicots; Magnol=magnoliids; Mono=monocots; Palherbs=paleoherbs).  (Wing et al 1993).

DISCUSSION

The Euanthial theory for the origin of the angiosperms dominates taxonomic systems.  This theory supports the origin of modern angiosperms from the extinct Magnoliaceae and suggests that magnoliids are the basal root of all of the flowering plants.  That is magnoliids are the common ancestor of flowering plant and also the most primitive in structure (Takhtajan 1969, Takhtajan 1991, Hutchinson 1969, Stebbins 1974).  There is substantial structural, geographical, and genetic evidence that supports the Euanthial Theory.  

According to Takhtajan (1969, 1991), similarities between the theorized primitive flowering plant and the Magnoliaceae in vegetative and reproductive structure are evident.  Takhtajan (1991) especially emphasizes the importance of the conservation of reproductive structures within the angiosperms, as reproductive structures are not as easily reversible over time as vegetative structures are reversible.  A distinctive feature of all flowering plants is the presence of the female reproductive carpel, which is a closed megasporophyll in contrast to the strobilus present in non-flowering plants.  The Euanthial Theory suggests that the original flower evolved from the strobilus of a non-flowering plant such as a cycadeoid, which is considered strobiloid in nature.  This strobilus evolved into the flower via the processes of oligomerization, differentiation and fixation (Stebbins 1974, Takhtajan 1991, Bessey 1915).  Oligomerization refers to a slow fusion of flower parts such as the sporophylls and leaves of non-flowering plants.  Stebbins (1974), Hutchinson (1969), and Takhtajan (1969, 1991) agree that the flower of Magnoliaceae is obviously comparable to the strobilus of a cycadeoid, as presented in Figure 2.  Furthermore, the magnolia Tasmannia piperita carpel is considered to be the most primitive carpel because it is not further differentiated into an ovulary or stigma, as are other carpels (Takhtajan 1991). 

Figure 2.  This picture illustrates the strobilus-like flower and primitive carpels of Magnolia.

Further support for the Euanthial Theory includes the exceptionally long axis of the Magnoliaceae flower, which is similar to the hypothesized long axis of the primitive flower.  However, Takhtajan (1991) believes that the long axis on the Magnoliaceae is an evolutionary reversal rather than the retention of the primitive state.  In addition, the spiral arrangement of the flower parts on the axis of the receptacle of the Magnoliaceae is believed to be a primitive feature as compared to the common whorled and cyclic arrangement of flower parts on many other angiosperm species (Takhtajan 1969, 1991, Bessey 1915). 

The Magnoliaceae stamen also supports the Euanthial Theory.  The primitive stamen is believed to have been laminar with three main veins and not differentiated into any filament or anther (Takhtajan 1969, 1991).   According to this theory, the stamen evolved into filaments as a way to enhance pollination by allowing the microsporangia to no longer be sterically hindered, or uneasily accessed by pollinators, as the microsporangia originally were believed to be embedded within the stamen (Takhtajan 1991).  Magnoliaceae flower structure includes petaloid stamens that are also similar to this primitive type.  

Vegetative features of the Magnoliaceae support the Euanthial Theory.  The woody stem of the Magnoliaceae plant is considered to be primitive to herbaceous stems of other angiosperms, as the herbaceous stems are popularly believed to be an evolutionary result of the weakening of cambium activity in the stem (Takhtajan 1991).  Also, the leaves of the Magnoliaceae are simple, oval shaped, and pinnate, which is also believed to be similar to the leaves of primitive flowering plants that evolved eventually into lobed and compound leaves (Arber and Parkin 1907, Cornet 2000, Stebbins 1974, Takhtajan 1969, Takhtajan 1991).

Stebbins (1974) describes how chromosome number could link the Angiosperms to a magnoliid ancestor.  He postulates that chromosomal evolution in the Angiosperms occurred in 3 consecutive steps: aneuploid alterations of the originally low basic chromosome numbers of n=6 to n=8, polyploidy from previously low numbers to numbers around n=19 to n=21, and finally diversification of genera, sometimes accompanied by additional cycles of polyploidy.  Stebbins’ (1974) analysis provides plausible explanation of ploidy in reference to the Euanthial theory.

Geographical distribution and fossil evidence of the angiosperms supports the Euanthial Theory.  Few fossils of early angiosperms exist because of their upland habitat.  Thus, they were isolated from wetlands, which is the ideal condition for fossilization (Stebbins 1974).  Downie and Robinson (2002) state that fossil evidence for a transition from gymnosperm to angiosperm is sparse.  They agree that the fossil record supports a rapid radiation of the angiosperms near the end of the Cretaceous and most of the flowering plant families had appeared by this time.  Takhtajan (1991) and Stevens (1980) believe that Magnoliaceae is a preserved “living fossil” of this time period and should carry more phylogenetic weight, as there are not enough angiosperm fossils to draw direct conclusions concerning their origin. 

Despite structural, geographical, and genetic support for the Euanthial Theory, angiosperm genetic analyses by Martin et al (1993) are inconsistent with the theory.  Magnoliaceae should be deeply rooted in the phylogram after DNA sequencing analysis if it were the primitive ancestor of the extant angiosperms.  However, Magnoliaceae appeared as a secondary branch to Liliidae (Martin et al 1993).  Thus, Magnoliaceae cannot be established as an outgroup relative to the angiosperms based on genetic evidence.  This does not suggest that the Angiosperms did not come from an ancestor of strobiloid nature, such as the cycadoids.  Instead, the argument can be made that the Angiosperms are a product of independent reduction and simplification from an ancestor after the separation of the magnoliids from other angiosperms (Martin et al 1993).

The most supported rival to the Euanthial theory is the Paleoherb theory.  Paleoherbs are a group of several plant orders and families including Piperales, Aristolochiaceae, Nymphaeles, and the monocots.  They have commonly been classified as dicots, but recent studies have shown that they may be more closely related to the monocots.  According to Reveal (1999), Downie & Robertson (2002), and Dahl & Zinniker (2002), the fossil record provides a wide array of flower types, but the earliest kinds found so far have tended to be small and numerous around the axis.  Most of these early flower fossils, found to be about 120 million years old, resemble those of the pepper family, or Piperaceae.  Fossilized flowers of the Magnoliaceae relatives did not appear until about 90 million years ago.  Furthermore, leaves similar to those of the paleoherb Nymphaeaceae seem to be among the earliest known fossils of the flowering plants. 

All of this information leads to the “sneaky herb hypothesis,” which states that the first true angiosperms were weed-like.  According to Reveal (1999), some say that the first angiosperms were divided into two types: a rare magnoliaceous, arborescent marginal forest dweller and a more common piperoid herbaceous forest floor dweller.  He also thought that the piperoid herbs rapidly evolved into more derived groups, most still retaining their herbaceous habit while some evolved into aquatic plants.  According to Reveal (1999), the aquatic based ancestors eventually led to an “evolutionary dead end,” while the terrestrial herbaceous plants evolved into the dicots and the monocots.  Reveal (1999) also suggests that after the large extinction at the Jurassic/Cretaceous boundary, these weed-like plants flourished and differentiated due to their increasingly effective reproductive feature, such as double fertilization.  Reveal (1999) also attributes the increased diversity of the newly formed angiosperms to the co-evolutionary relationship of the plants with the plant-eating insects, which caused the newly evolving plants to have better defense mechanisms as well as pollination strategies.  It is during this time of rapid differentiation and evolution that the magnoliids came about.  According to this theory, the woody magnoliid plants seem to be another “dead end,” rather than the point of origin for all of the flowering plants as had once been thought. 

CONCLUSION

The Euanthial theory, as purposed by Stebbins (1974), Takhtajan (1969, 1991), and Hutchinson (1969), contains a great amount of important morphological and structural evidence that points to the Magnoliaceae as the most primitive angiosperm.  The primitive structure of the magnoliid carpel especially strengthens the Euanthial argument, as well as other conserved reproductive features of the flower.  This same structural evidence is lacking in the Paleoherb theory.  Because there is more solid evidence to support the Euanthial, we believe that the Euanthial theory is the most probable theory of angiosperm evolution of the two discussed. 

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