Joseph H. Williams Dept. of Ecology and Evolution, Univ.

of Tennessee, Knoxville

Progamic Phase interval between pollination and fertilization Plesiomorphy - an ancestral or primitive character Evolutionary novelty - any newly acquired structure or property that permits the performance of a new function, which, in turn, will open a new adaptive zone

Gymnosperms non-flowering plant naked seed have strobili or cones male and female cones haploid endosperm (n) mostly wind pollination occupy land and water of ancient evolutionary origin include 600-750 species

Angiosperms flowering plant enclosed seed have flowers male pollen and female ovules triploid endosperm (3n) mostly insect pollination dwell in land only or more recent evolutionary origin include 250,000 species (80% of all plant species)

Angiosperms > Gymnosperms Flower Closed carpel Highly reduced male and female gametophytes Double Fertilization Sexually formed polyploid endosperm Long styles Multi-seeded ovaries Much faster pollen tube growth rates

Parameters tip wall

Gymnosperms cellulose cellulose microfibrilbased

Angiosperms esterified pectin amorphous callosebased

plug
pollen tube growth rates

esterified pectin
<20 um/h (very slow)

callose
80-600 um/h

Amorphous callose-based wall is faster and more energy efficient than biosynthesis of a cellulose microfibril-based wall. Silencing of genes involved in callose synthesis reduces pollen competitive ability. Properties of Callose Walls and Plugs: Walls: Impermeable Plugs: Seal off the pollen tube

Reduce the risk of damage and allow pollen tubes to grow longer distances

Angiosperms pollen tube tips: esterified pectins Lateral tube wall: with callose secondary wall

Allows faster growth rates because i. The pectic tip is more plastic and rapidly extensible ii. The mature tube cell wall has greater resistance to tension stress due to secretion of callose iii. Callose plugs help maintain positive turgor pressure in the growing tip

A survey of >900 studies indicates that the time interval between pollination and fertilization (fertilization interval) ranges from: 10 hours to >12 months - Gymnosperms 15 minutes to >12months - Angiosperms

 Early

Cretaceous angiosperms and ephedroids (Gnetales) were both diversifying in similar habitats Today 65 species of Ephedra are confined to semiarid habitats whereas angiosperms have radiated into virtually every environment on earth

 Gymnosperm

reproductive evolution is constrained because their slow pollen tube growth rates impose a trade-off between pollen tube developmental time and pollen tube pathway length. pollen tube developmental time = pollen tube pathways = pollen tube growth rate pollen tube developmental time = pollen tube pathways = pollen tube growth rate

 Gymnosperm

pollen tube growth rate evolution is thus severely constrained by the tight linkage of developmental time and pollen tube pathway length.

critical step in early angiosperm prehistory was the origin of their unique pollen tube wall growth pattern. The callose wall and plug preceded the origin of novelties such as true closed carpels, solid styles, and deep multi-ovulate ovaries, as well as the evolution of extreme traits such as fertilization intervals as short as 15 min, pollen tube pathway lengths as longs as 500 mm, and pollen tube growth rates >1,000fold faster than those of gymnosperms. Angiosperm pollen tube wall innovations gave pollen tubes the capacity for rapid and longdistance growth, increasin the evolutionary potential of both pollen tubes and the tissues they interact with.

 Because

angiosperms lack the gymnosperm developmental constraint of slow and static pollen tube growth rates, developmental time and pollen tube pathway length became evolutionary dissociated in derived groups. Angiosperm fertilization biology is distinguished not only by many novelties and extreme traits, but also by much greater independence (modularity) of their developmental processes.

 Elevated

reproductive trait diversity, and perhaps increased modularity as well, are strongly linked to the elevated taxonomic diversity of flowering plants. Rapid reproduction, due in large part to accelerated pollen tube growth rates, is a fundamental life history strategy shared by many of the most diverse herbaceous clades such as grasses and asters. Moreover, the great developmental flexibility of angiosperm pollen tubes expanded the potential for pollen competition and maternal responses to its effects, in turn, speeding the evolution of prezygotic forms of mating systems and reproductive barriers.

 Gymnosperms,

generally lack strong prezygotic barriers. Pollen tube growth rate innovations truly lie at the heart of the tremendous reproductive flexibility and opportunism that Stebbins and others have described as the critical factor in angiosperm success.

The walls of growing plant cells must fulfill two simultaneous and seemingly contradictory requirements. First, they must expand to accommodate cell growth, which is anisotropic in many tissues and determines organ morphology. Second, they must maintain their structural integrity, both to constrain the turgor pressure that drives cell growth and to provide structural rigidity to the plant. These requirements are met by constructing primary cell walls that can expand along with growing cells, whereas secondary cell walls are deposited after cell growth has ceased and serve the latter function.
One of the major constituents of both types of cell walls is cellulose, which exists as microfibrils composed of parallel -1,4-linked glucan chains that are held together laterally by hydrogen bonds (Somerville, 2006). Microfibrils are 2 to 5 nm in diameter, can extend to several micrometers in length, and exhibit high tensile strength that allows cell walls to withstand turgor pressures of up to 1 MPa (Franks, 2003). In vascular plants, cellulose is synthesized by a multimeric cellulose synthase (CESA) complex composed of at least three types of glycosyl transferases arranged into a hexameric rosette (Somerville, 2006). After delivery to the plasma membrane, CESA initially moves in alignment with cortical microtubules (Paredez et al., 2006), but its trajectory can be maintained independently of microtubule orientation. For example, in older epidermal cells of the root elongation zone in Arabidopsis (Arabidopsis thaliana), cellulose microfibrils at the inner wall face are oriented transversely despite the fact that microtubules reorient from transverse to longitudinal along the elongation zone (Sugimoto et al., 2000), suggesting that microtubule orientation and cellulose deposition are independent in at least some cases. Depending on species, cell type, and developmental stage, cellulose microfibrils may be surrounded by additional networks of polymers, including hemicelluloses, pectins, lignin, and arabinogalactan proteins (Somerville et al., 2004). Hemicelluloses are composed of -1,4-linked carbohydrate backbones with side branches and include xyloglucans, mannans, and arabinoxylans. Xyloglucan is thought to interact with the surface of cellulose and form cross-links