Seed Evolution

Hyperlink to Seed Evolution Webpage 1

Seed Evolution Webpage 2 (this webpage)

Angiosperm seed evolution and species diversification: Darwin's abominable mystery

Angiosperms are the regarded as one of the greatest terrestrial radiations of recent geological times. This occurred in the Cretaceous era (see MYBP time scale figure): The major lineages originated 130-90 MYBP, following by a dramatic rise to ecological dominance 100-70 MYBP, and >250000 angiosperm species are known today. Charles Darwin described the rapid rise and early diversification within the angiosperms as 'an abdominable mystery'. This diversification is also manifested on the level of the seed, it's longevity and germination control is part of the species adaptation to environmental factors, e.g. to the season: temperature, light and water.

Among other reasons, the 'invention' the double fertilization that gives rise to seeds with triploid endosperm is proposed to be a major reason for the evolutionary success of the angiosperms. Two hypotheses for the evolutionary origin of the endosperm are favored today (Friedman and Williams, 2004):
(1) The endosperm is a sterilized homolog of an embryo (Sargant 1900, Friedman 1995)
(2) The endosperm is the sexualized homolog of a portion of the megagametophyte (Strasburger 1900, Coulter 1911)

Primitive angiosperms, e.g. Nymphaceae, have a 4-celled, 4-nucleate embryo sac and double fertilization gives rise to a diploid endosperm. Based on this and on additional findings, Friedman and Wiliams (2004) are in support for the hypothesis that this diploid endosperm originated from a supernumerary embryo (altruistic sibling embryo, hypothesis 1). Modular duplication resulted in the 7-celled, 8-nucleate embryo sac of most of today's angiosperms. In this case double fertilization gives rise to a triploid endosperm found in most angiosperms. Other researchers (e.g. Nowack et al., 2006) support hypothesis 2.

The endosperm is an embryo-nourishing tissue and is, depending on the species, parially or fully obliterated during seed development. However, most angiosperm species have retained an endosperm layer in the mature seed. In many of these cases, the endosperm not only functions as nourishing tissue, but is also involved in the control of seed germination in response to the environment and to developmental factors. Endosperm weakening is a prerequisite for the germination of many endospermic seeds including Solanaceae and Brassicaceae species.


Seed plant evolution hyperlinks
DT - Devonian Times by Dennis C. Murphy
UCMP - University of California Museum of Paleontology
Links for Paleobotanists - University Würzburg
Tree of Life Web Project (Tolweb)
Deep Time - Phylogenetic Tree of Angiosperms
Angiosperm Phylogeny Website (Stevens 2006, Missouri Botanical Garden)
Oleanane: Taylor et al., Paleobiology 32: 179-190 (2006)
Gigantopteroids: www.gigantopteroid.org (John M. Miller)

Seed phylogeny - Morphological and physiological trends in seed evolution

Structural seed types based on comparative internal morphology
BASAL seed types (B1-B4) - basal division according to Martin (1946) Embryos (black) usually relatively small, and restricted to the lower half of the seed, except in some of the lateral type B4. Seeds usually medium to large. Endosperm (orange) abundant and generally starchy except in the rudimentary type B1. The seed types capitate B3 and lateral B4 are only found in monocots, wheras the seeds types rudimentary B1 and broad B2 are wider distributed.
	BASAL seed type B1- Embryo RUDIMENTARY Abundant endosperm and tiny embryo. Embryos small, globular to oval-oblong, cotyledons usually rudimentary and obscure but sometimes they are evident. Seeds generally medium to large size. Examples: Magnolia spp. (Magnoliaceae, Magnoliales, Magnoliids, Basal Angiosperms); Anemone spp. and Trollius spp. (Ranunculaceae, Ranunculales, Basal Eudicots).
	BASAL seed type B2 - Embryo BROAD Embryo as wide as or wider than high, peripheral or nearly so. Examples: Nymphaea spp. (Nymphaceae, Nymphales, Basal Angiosperms).
	BASAL seed type B3 - Embryo CAPITATE Embryo expanded above into head-like form. Monocots only. Examples: Commelina spp. (Commelinaceae, Commelinales, Commelinids, Monocots).
	BASAL seed type B4 - Embryo LATERAL Embryo basal-lateral or lateral, inclined to expand in the plane of the periphery, small to half or rarely larger. Monocots only, typical for Poaceae seeds, e.g. cereal grains. Examples: Triticum spp. (Poaceae, Poales, Monocots).
PHERIPHERAL seed type P - pheripheral division according to Martin (1946) Embryos (black) ordinarily elongate and large, often curved, cotyledons narrow or expaneded. "Endosperm" (orange) conspicuously starchy, often central; "endosperm" ia actually perisperm in most cases.
	PHERIPHERAL seed type P - Embryo PERIPHERAL Characteristics as described for the P-division. Examples: Beta vulgaris and Chenopodium album (Amaranthaceae, Caryophyllales, Caryophyllids).
AXILE seed types (LA, MA, FA) - axile division according to Martin (1946) Embryos (black) small to total, central (axile) straight, curved, coiled, bent or folded. Endosperm (orange) not strachy except in some monocot families of the LA-subtype. Well presented in Gymnosperms and Angiosperms. The axile division includes the linear, miniature and foliate subdivisions.
LINEAR AXILE seed types (LA) - linear subdivision of the axile division according to Martin (1946)
	LINEAR AXILE seed type LA - Embryo LINEAR AXILE Embryo generally several times longer than broad, straight, curved or coiled, cotyledons not expanded. Seed size normally not minute. Examples: Pinus spp. (Pinaceae, Pinales, Gymnosperms); Allium spp. (Alliaceae, Liliales, Monocots); Iris spp. (Iridaceae, Asparagales, Monocots); Apium graveolens and Daucus carota (Apiaceae, Apiales, Asterids); Nicotiana spp. and Petunia hybrida (Solanaceae subfamily Cestroideae, Solanales, Asterids); Capsicum annuum and Lycopersicon esculentum (Solanaceae subfamily Solanoideae, Solanales, Asterids).
MINIATURE AXILE seed types (MA) - miniature subdivision of the axile division according to Martin (1946)
	MINIATURE AXILE seed types MA - Embryo MINIATURE AXILE Seeds small to minute with embryos that are stocky or minute; seed coverings generally delicate and often cellular-reticulate. Endosperm not starchy. Within the MA-seed type subdivision Martin (1946) distinguished between dwarf or micro MA-seed types. The evolution of the small seed size (e.g. dwarf seeds, MA) is described elsewhere, e.g. in Moles et al. (2005) and in Baskin and Baskin (2005) and Baskin and Baskin (2007). Small embryos in dwarf seeds may or may not be undifferentiated (not differentiated into organs) or underdeveloped (differentiated, but needs to grow). The assignment of seeds to a dormancy class requires that studies be done to determine if embryos grow inside the seed before germination can occur. Embryos of Drosera anglica are small, but fully developed, they don't grow in the seed prior to germination (seeds have PD). Embryos of Campanula americana are underdeveloped and need to grow prior to germination (seeds have MD). DWARF (REMOVED AS SEED TYPE) seed size is 0.2 to 2 mm long. Embryos are varible in relative size, small to total, generally stocky, usually oval to elliptic or oblong. Cotyledons inclined to poorly developed. Examples: Drosera angelica (Droseraceae, Caryophyllales, Caryophyllids); Campanula americana (Campanulaceae, Asterales, Asterids); Begonia spp. (Begoniaceae, Cucubirtales, Rosids). MICRO (REPLACED BY UNDIFFERENTIATED AS SEED TYPE) seed size is < 0.2 mm, i.e. minute-sized seeds. Embryo minute to total. Testa generally globular and consisting of relatively few cells (ca. 50-150). Examples: Orchidaceae species. REVISION OF THE MA-TYPE (2007): A revision of Martin's seed classification system, with particular reference to his dwarf-seed type was proposed by Baskin and Baskin (2007). According to this revision, the dwarf category has been removed and the micro category replaced by UNDIFFERENTIATED to reflect the state of the embryo in fresh seeds. The "dwarf seed type" per se is of limited value to seed biologists and these seeds are assigned to the other ten seed types irrespective of their size. Martin's conclusion that dwarf seeds are more advanced in evolution compared to medium or large seeds with rudimentary embryos. However, according to this revision, seed size is not longer a criterium for the assignment to a specific seed type. The "micro seed type" is now replaced by a "undifferentiated seed type", indicating that the embryo in fresh seeds lacks organs. Most of these seeds are of micro-size, but there are also relatively large seeds whose embryos lack organs at the to time of maturity.
FOLIATE AXILE seed types (FA1-FA4) - foliate subdivision of the axile division according to Martin (1946) Embryos (black) large, generally quarter to total, central rather than peripheral. Cotyledons expanded. Seeds generally medium to large. Endosperm (orange) generally not starchy. In mature FA2, FA3, and FA4 seed types the embryo occupies most of the seed; there is little or no endosperm, the nutrients are stored in the cotyledons.
	FOLIATE AXILE seed type FA1 - Embryo SPATULATE AXILE Embryo spatulate axile (erect). Cotyledons thin to thick and slightly expanded to broad. Examples: Ephedra spp. (Ephedraceae, Gnetales, Gymnosperms); Fraxinus excelsior and Syringa spp. (Oleaceae, Lamiales, Asterids); Lactuca sativa and Helianthus annuus (Asteraceae, Asterales, Asterids); Vitis spp. (Vitaceae, Vitales, Rosids); Ricinus communis (Euphorbiaceae, Malphighiales, Rosids); Cucumis spp. (Cucurbitaceae, Cucurbitales, Rosids).
	FOLIATE AXILE seed type FA2 - Embryo BENT AXILE Embryo bent axile (spatulate but bent in jackknife form). Cotyledons generally thick. Examples: Rhus spp. (Anacardiaceae, Sapindales, Rosids); Trifolium spp., Melilotus alba, Glycine max and Pisum sativum (Fabaceae, Fabales, Rosids); Lepidium spp., Arabidopsis spp., and Brassica spp. (Brassicaceae, Brassicales, Rosids).
	FOLIATE AXILE seed type FA3 - Embryo FOLDED AXILE Embryo folded axile. Cotyledons usually thin, extensively expanded and folded in various ways. Examples: Most Acer spp. (Sapindaceae, Sapindales, Rosids); Geranium spp. and Pelargonium spp. (Geraniaceae, Geraniales, Rosids); Malva rotundifolia (Malvaceae, Malvales, Rosids).
	FOLIATE AXILE seed type FA4 - Embryo INVESTING AXILE Embryo investing axile (erect). Cotyledons thick, overlapping, encasing the somewhat dwarfed stalk for at least half its length. Endosperm wanting or limited. Examples: Fagus sylvatica (Fagaceae, Fagales, Rosids); Ceanothus spp. (Rhamnaceae, Rosales, Rosids).

Evolutionary trends of angiosperm seeds