From spores to seeds

evolution of a powerful reproductive strategy

A seed consists of an embryo with a packet of nutrition (usually), all housed in a protective coat. They range in size from the dust-like seeds of orchids to coconuts. And they all trace their origin to spores. 

The first land plants evolved from green algae, perhaps five hundred million years ago or more, and dispersed their offspring as spores; modern mosses and ferns still do so. A long time passed before seeds evolved (and of course they have not stopped evolving). Botanists have deduced that spores evolved to become seeds by several major steps and conjectured about what innovative features made such steps successful, such that the next generations maintained and continued those traits. I thought it might be interesting to visualize those steps, to begin to understand what was involved with the process.

Start with spores: Spores germinate to form tiny organisms, called gametophytes because they produce gametes (sperm and eggs) that have one set of genetic chromosomes (one set is termed 1N). Sperm swim around, looking for eggs to fertilize, sometimes joining with an egg from the same gametophyte. The fertilized egg and then an embryo with two sets of chromosomes (termed 2N) is held by the gametophyte as it grows into a recognizable moss or fern that will mature and produce spores (therefore called a sporophyte). So the life cycle is complete—alternating a sporophyte generation with a gametophyte generation (see diagram).

Life cycles of spore-producing plant (left) and seed-producing plant (right). Illustration by K. Hocker

In most spore-bearing species, the spores are all alike, making gametophytes that produce both sperm and eggs. However, in a number of lineages, the sexes became separated such that distinct male and female spores were produced, and these became much smaller. Botanists have suggested that, in one of these lineages, the separation of sexes was one of the important early steps on the evolutionary way that led to seed plants. What might have been the advantages to this arrangement? The two sexes would produce two kinds of gametophytes that could now evolve different characteristics and exploit their habitats in different ways. Females could invest all their energies in producing eggs and rearing embryos, no longer investing in producing sperm, and males could invest all of their energies in sperm. Separation of the sexes also helped reduce the rate of self-fertilization, thus reducing the risks of inbreeding.

The next major innovation was the retention of female gametophytes with their embryos on the sporophyte. These gametophytes became even smaller; fossils show step-by-step examples of how maternal tissues eventually formed integuments surrounding a gametophyte and embryo, thus providing a protective covering that we call a seed coat. The whole package is called an ovule, which matures into a seed. That happened about three hundred and fifty million years ago or so.

Presumably those primitive seeds were simply shed, as spores were, to be dispersed on breezes. Having a protective coat may have allowed seeds to remain dormant until conditions were right for germination—something that most spores cannot do.

Then, about a hundred and sixty million years ago, a major division occurred. Some plants, called gymnosperms (naked seed), kept their ovules and seeds exposed on the surface of the spore-bearing structure. Another set of plants, called angiosperms (enclosed seed), began to put additional layers of maternal tissue around the seed, probably by folding a leaf-like ovule-bearing structure to enclose and protect the maturing seeds from desiccation and consumers such as beetles. (The gymnosperms would have had to solve such problems differently). This structure evolved in many different directions in various lineages of angiosperms, forming the pistils in our familiar flowers. The lower part of the pistil became the ovary, housing the seeds, while the upper part became the receptive surface (the stigma) for pollen.

The evolution of pollen is complex, but it broke the sperm cells’ dependence on water. Instead of swimming, wind-or animal-carried pollen became the sperm delivery system. Somehow the many sperm produced by the male gametophytes of seed-plant ancestors were reduced in number, such that each pollen grain contained one very tiny male gametophyte that produced two sperm.

In gymnosperms, one sperm fertilizes the egg, and the other one just degenerates. Nutrition for the embryo and seedling are provided by the female gametophyte, as was true for spores but now the gametophyte and embryo are inside the seed.

A new invention arose, somehow, in the angiosperms: one sperm fertilizes the ovule and the non-fertilizing sperm unites with certain other nuclei in the ovule to create essential food material (commonly starches or oils) for the developing embryo and eventually the early seedling. (The angiosperm ancestors of orchids did this too, but orchid seeds have lost that stored nutrition and depend on mycorrhizal fungi for food.)

After those major steps, natural selection in angiosperms led to the evolution of flowers and a great variety of pollination techniques and fruit types. Much of that diversification was related to interactions with animals.

Moss to Maple

a lightning tour through the evolution of land plants

A maple tree is clearly very different from a moss, yet over a long period of time, and step by step, early moss-like plants evolved to trees, including maples. The fossil record tells us about some of these steps, and experts have agreed upon the probable steps where the fossils don’t tell us. The story centers on solving problems involved with the invasion of land from the sea or fresh water.

Hundreds of millions of years ago, green algae began to colonize land. They already had the mechanisms of photosynthesis: using light to combine carbon dioxide and water into nutritious carbohydrates. And they already had sexual reproduction, which produces new combinations of genes every generation and thus the variation necessary for evolutionary change. Experts say, and there are hints in the fossil record, that the very early land plants formed associations with fungi that provided nutrients, a mutualistic association that almost all land plants have maintained. So those early terrestrial plants were off to a good start.

For sexual reproduction, however, those early plants were entirely dependent on water: eggs and sperm were released into water, where sperm could swim a few centimeters to find a drifting egg to fertilize. That’s OK for plants living in water or even in damp soil, but it won’t work on dry land.

The first land plants are thought to have been more or less moss-like: small plants growing close to the ground. If conditions were not wet enough, these early plants had to wait for sex until conditions improved. (Although most modern mosses still have to wait, as did the early plants, a few are reported to use springtails, mites, or flies to transfer sperm to eggs, but few such animals were present in the early days of the invasion of land).

But even if sperm could swim to an egg, the resulting zygote would be still on its own in a potentially dangerous environment. Somewhere along the line, although sperm were released and still had to swim, eggs began to be retained in special structures on the leaves of the parent plant. Fertilization then occurred within these special structures and the zygote received both protection and some nutrition during development. In mosses, that zygote stays on its mother and grows into a new individual (called a sporophyte) that looks different from its mother and eventually produces spores. Spores are single cells inside a tough coat that disperse on the wind and, if they land in a good spot, grow into new mosses (called gametophytes, because they produce gametes). Thus, the generations alternate between gamete production and spore production.

One generation grows atop the other: a sporophyte has grown from an egg retained and fertilized at the tip of the green moss plant (a gametophyte). Spores will disperse from the capsule and start new green moss plants. Photo by Bob Armstrong

There was still the problem of needing water for the sperm to swim to an egg. The fossil record is poor at this point, but clearly, at some point, moss-like plants began to produce two kinds of spores on their sporophytes: small, male spores with sperm and big, female spores with eggs. The big spores did not disperse but were retained on their mother sporophyte’s leaves, where they received protection and nutrition. The small spores ultimately developed more protective covers; they traveled on the wind and found special landing places near the female spores, where they could fertilize the eggs. In some cases, that special landing place is a droplet of fluid, close to the egg, that engulfs the arriving male spore (if it belongs to the same species as the egg) and pulls it in. That is how pollination came about. The big, female spores began to stock nutritional material inside, for the growth of the embryo, and that was the beginning of the evolution of seeds.

The early land plants (and modern mosses) were often at risk of desiccation. Protection from drying out came with an impervious cuticle over the outer surfaces. But complete imperviousness would not only prevent water loss but also prevent carbon dioxide (for photosynthesis) from entering. Conveniently, surface pores called stomata, which can open and close, allow the entrance of carbon dioxide and help control water loss.

Mosses don’t have a very good system for transporting water from one part of the plant to another. But some of those early land plants developed a vascular system for water transport. This is built from lined-up, hollowed-out cells with reinforced cell walls (called xylem; concentric bundles of xylem became known to us as wood). The resulting channels connect to the stomata. When a stomate is open, water vapor is lost faster than carbon dioxide comes in. This is called transpiration (in parallel with evaporation from a surface). Because water molecules in the vascular channels cling together, transpiration from stomata pulls columns of water up through the channels. No energy expenditure needed, except to open or close stomata. These channels deliver water to leaves and other parts of a plant. The walls of the channels are reinforced to prevent collapse.

The early plants did not have true roots, just small anchoring fibers. True roots did not develop until there was a vascular system to deliver water to them. Conversely, without roots, the nascent vascular system could not draw much water from the soil. But, somehow, early vascular plants did develop roots of some sort, which not only anchored the plant to the soil but also transferred soil water and nutrients to the plant above and to the roots themselves.

Development of a vascular system happened in sporophytes, not in gametophytes, which initially needed to stay small for sexual reproduction (but later began to stay on the sporophyte, as noted above). Those stiffened channels also provide mechanical support, so vascular plants could grow tall. Being tall is often an advantage when competing for light.

The radical remodeling of cells needed for the development of a vascular system in sporophytes may have been facilitated by the fact that sporophytes have two sets of chromosomes (compared to gametophytes and gametes with just one). That means deleterious mutations in one set of chromosomes could be masked by normal genes on the other set.

Thus we arrive at a hypothetical ancestral plant, with some kind of pollination system that does not depend on water, a primitive seed with nutrition for an embryo, a vascular system, roots, and the ability to grow tall, with mutualistic fungal associations. The stage is set for the evolution of seed plants. There are basically two kinds of seed plants: all the flowering plants, including maples, oaks, shooting stars, and lupines, whose seeds are enclosed in layers of maternal tissue, and the conifers and their relatives, whose seeds are borne on the surface of leaves or scales. The evolution of these two branches of the plant evolutionary tree makes another complex story…



benefits in both directions

Mutually beneficial relationships (a type of symbiosis, which just means ‘living together’) are common under the aegis of Mother Nature. Some obvious ones are bees and hummingbirds getting nectar from flowers while moving pollen from plant to plant and robins and bears eating fruits and excreting, and thus dispersing, viable seeds. There are many other mutualisms too, but there is a not-obvious one that is and has been fundamentally important to most of the plants on earth.

Many kinds of fungi form close, mutually beneficial, relationships with plant roots, obtaining some carbohydrates from the plant while transferring phosphorus and other nutrients from the soil to the plants. These are the mycorrhizal (‘fungus-root’) relationships (between the roots of plants and the underground filaments of the fungus) that have often been mentioned in the essays in this space. Many local species of fungus (including, for example, Amanita) participate in such relationships. Experiments have shown the benefits of these relationships to the plant partners; the benefit to the fungi is not always clear, but many of these fungi cannot live without their plant partners. It has been estimated that at least eighty percent of all plants are involved with mycorrhizal partners.

Beyond the critical ecological importance of present-day mycorrhizal mutualisms, however, lies an important historical and evolutionary perspective: researchers have good evidence that the first green plants to colonize the land—a few hundred million years ago– had some kind of close fungal associate. This relationship was not technically mycorrhizal, because the first land plants (derived from freshwater green algae) did not have proper roots, but it was, nevertheless, a close physiological association of fungus with plant. Fungi invaded land well before the green plants did, and must have been adept at foraging for nutrients in the poor soils that then prevailed. So they were there, perhaps availing themselves first of exudates from the photosynthetic plants and eventually drawing nutrition directly from the plants themselves and providing soil nutrients in exchange. If those researchers are right, then all the great diversity of plants we see around us was made possible in the beginning by a mutualism.

All of this raises a big question in my head: if fungal partners have been so important historically and so many kinds of current-day plants have such fungal partners, then why are there a number of plants that do NOT have these partners? For example, mosses are reported to lack fungal partners, although their cousins, the liverworts and hornworts often have them. Examples of non-mycorrhizal plants in our local flora include starworts, paintbrushes, louseworts, sundews, lupines, sweetgale, mistletoes, many members of the mustard family, and numerous others. A look at that abbreviated list tells us that one way to thrive without a fungal partner is to have another means of supplementing nutrition: many of the non-mycorrhizal plants are insectivorous (sundews), or partly parasitic (paintbrush), or harbor nitrogen-fixing bacteria (lupines). In addition, some plants-without-fungal-partners have extraordinary roots (the so-called cluster-roots of lupines, for instance) that give the plant a huge amount of root surface for taking up nutrients. All those ways of supplementing plant nutrition may account for some of the species that lack a fungal partner, but not all, so the question is only partly answered.

By definition, mutualisms involve some reciprocity between participants. But it is not uncommon for the balance to favor one partner more than the other. In fact, there are hundreds of examples of relationships in which one participant simply exploits the other, giving nothing back: what was probably once mutualistic has become exploitative. For instance, orchids produce seeds that require a mycorrhiza for germination, but because the seed contains no food stores for the embryo, the fungi get little or nothing; the orchids apparently control the relationship by chemically attracting the fungal filaments. Some orchids (such as the coralroots) lack green leaves altogether and are totally dependent on their fungi, without reciprocating: the plant gets both nutrients and carbohydrates from the fungus, which draws such sustenance from the soil or other plants. The two-sided arrangement has become one-sided. Undoubtedly there are instances in which the fungus gets one-sided benefits too, and this may have been the case very early in the evolution of the land plants.

In some cases, the relationships are still more complex. Some plants require ‘companion plants’ to support their mycorrhizae, so there are three participants in the relationship. For example, certain Australian Lobelias require the presence of mycorrhizas associated with broombush (Melaleuca uncinata) in order to germinate. Some species in the gentian family (such as centaury, Centaurium) develop full mycorrhizal associations only when certain other plants (such as clover, Trifolium) are present too.

Some plants have very specific requirements as to what fungus makes a good partner. Many orchids are fussy this way. And when plants are introduced to new countries, as the pines have been to the southern hemisphere and eucalypts have been to the northern hemisphere, they may not grow well unless their own particular mycorrhizae are moved with them. The local varieties of fungus won’t do.

In contrast, garlic mustard is a useful herb in the Old World that grows without harm to other plants, with which it coevolved. But when introduced to North America, it became a highly invasive weed, in large part because it kills or damages the plant/fungus partnerships that prevail here, so the native species fail to thrive.