Letters to the twenty-first century botanist. Second series: “What is a seed? – 1”

What is a seed: introduction

The angiosperm seed is the biological package that ensures the protection and dispersal of the zygote, in order to give rise to the filial generation of plants. To carry out this function, seeds are equipped with a remarkable set of traits and physical structures, which are integrated in a complex developmental program. The seed is also the manifestation of a new genetic combination resulting from meiotic recombination after gamete fusion, which may endow it with new characters of selective advantage over its parents and sibs. It thus has a primordial role to play in evolution.

Angiosperm seeds arise from the double fertilization event whereby, in most cases, one sperm nucleus fuses with the egg cell nucleus to form the embryo lineage and the remaining sperm nucleus fuses with a diploid central cell nucleus to yield the triploid endosperm lineage. The two lineages are distinguished by differential genomic imprinting, that is to say different patterns of DNA methylation and histone post-translational modifications, which ensure that gene expression programs during endosperm and embryo development are very different. The balanced development of the two entities is vital, and imbalances caused by aberrant doses of male- or female-origin chromosomes result in hybrid lethality (Jiang, Moreno-Romero, and Santos-Gonzàles 2017). The mechanisms involved, now being revealed, are likely to be a major cause of reproductive isolation during evolution. The endosperm essentially provides nutrient support and protection for the embryo, and has a much-reduced cellular complexity in comparison. The embryo lays down the body plan of the seedling in the form of shoot and root meristems, and the structure of the cotyledons. In some cases nutrient support is supplied by a maternal tissue, the perisperm, but the endosperm remains an important nutrient interface between maternal tissue and the embryo. Final seed volume can vary from minute (seeds of some epiphytic orchid species, which are poorly developed and lack storage reserve tissues, weigh ~1 μg), to enormous (the water-borne coco de mer weighs up to 18 kg).

After a series of cell divisions, the developing seed starts to accumulate storage products that will be remobilized during germination. In monocotyledons, these reserves are mainly deposited in the endosperm, whereas in dicotyledons they are for the most part deposited in the cotyledons of the embryo, although a number of exceptions and part-exceptions occur to this rule. Indeed, the seed during the seed-filling stage becomes an impressive “factory”, the objective being to deposit a maximum of carbon and nitrogen in a limited period and a confined space. To optimize the rate and extent of seed filling, a series of physiological adaptations promote the efficient transfer of nutrients from the mother plant, directly to the embryo or via the intermediate of the endosperm. It remains to be fully understood how interactions between the testa, endosperm, and embryo of the developing seed, and the mother plant, are coordinated to optimize seed filling and maturation. Significantly, many recently reported loci controlling seed size act via maternal effects, principally on the early cell division phase (Li and Li 2015), whereas seed filling, acquisition of desiccation tolerance, and dormancy, are mainly under the control of genes expressed in the zygote.

The storage capacities of the seed have long been exploited by humanity to provide one of its principal food sources, two-thirds of our calorie intake being seed-derived. In addition to the principal storage products – proteins, carbohydrates and lipids – seeds contain a variety of compounds, collectively referred to as antinutrients (see later), which protect against pathogen and parasite ingress. These compounds, and the density of the mature seed, tend to reduce its digestibility. To overcome this, a range of treatments have been developed including soaking, fermentation, removal of the seed coat layers, milling, and diverse cooking procedures (Haileslassie, Henry, and Tyler 2016; Patterson, Curran, and Der 2017).

Owing to the evolutionary pressure to assure the viability of the seeds, a number of mechanisms have evolved to ensure their tolerance to abiotic stresses notably during desiccation. Thus, many seeds are highly resistant to drought stress, and can survive in the desiccated state for many years, awaiting more favorable conditions for germination. At Michigan State University, seed lots buried in soil in 1879 are tested for viability every 20 years. At the last sampling in 2000, seeds of one species, Moth Mullein (Verbascum blattaria L.), were still able to germinate after 120 years (Telewski and Zeevaart 2002). The record, however, is held by a Judean date palm seed of estimated age 2000 years., preserved under conditions of exceptionally low humidity at Masada in Israel, which also germinated in 2005, and grew vigorously (Sallon et al. 2008).

As the environment for seed germination may not always be favorable (competition, lack of water, nutrients, etc.), most seeds in temperate regions or regions with a seasonal climate, but not in the tropics, acquire dormancy. This should be distinguished from a more temporary state, quiescence, exhibited by perennials in drought periods for example. Dormant seeds will not germinate on reaching maturity (even if physiological conditions are suitable), but only after receiving the appropriate signals during a later period. Seed dormancy involves a set of biochemical modifications that arrest cellular metabolism for a duration that depends on both external stimuli and turnover of endogenous components. Dormancy may be of variable length in the different seeds of a batch, which is a bet-hedging strategy for maximizing the probability of germination of offspring under favorable conditions. The biochemical mechanisms that accompany the acquisition of seed dormancy, a shutdown of metabolic activity while retaining cellular viability, are still somewhat enigmatic, as are the details of the molecular events triggering dormancy breakage. A better understanding of these phenomena would help in seed bank management, crucial in safeguarding plant biodiversity but also for new agricultural methods avoiding plowing.

During the quiescent phase, tissue viability has to be maintained. This is achieved by invoking a further series of protective biochemical events conferring longevity, a process that may vary considerably between genotypes and depend on the ambient conditions during seed maturation.

Seeds, typically rich in nutrients, are attractive to many pests and pathogens. However, as stated above, an arsenal of protective chemicals and peptides is produced during seed development, most of which are present in the mature seed, and these, coupled with physical modifications, mainly of the seed coat, prevent most infections and infestations. Some of these protective compounds are highly aromatic, and explain the use of certain seeds such as black pepper, fenugreek, mustard, nutmeg, as sources of spices. Furthermore, the seed coat structure is usually highly resistant to physical ingress when stored at low water potential.

Developing seeds respond actively to the presence of potential pathogens with gene expression reprogramming including the elicitation of hypersensitive reactions (Terrasson et al. 2015). These recent findings indicate the likely importance of these responses in limiting transmission of pathogens by seeds. The lack of plasmodesmatal connections between maternal and zygotic cells additionally reduces the likelihood of pathogen, notably viral, transmission between the mother plant and the seed.

Seed production and dispersal are crucial steps in assuring lineage transmission, dissemination, and also production of new genotypes that can be successful in new environments, and evolutionary pressure has led to numerous refinements of the processes involved. The number and timing of seed production is closely linked to environmental conditions, whereas the composition of individual seeds shows less plasticity, the seed compartment being protected by the mother plant during environmental adversity or nutrient limitations. Angiosperms have evolved several mechanisms for seed dispersal that implicate different vectors; by wind, water, fruit consumption by herbivores, attachment to foraging animals, pod dehiscence. All of these mechanisms place different constraints on seed morphology and composition, leading to further specializations, and resulting in the great diversity of seed morphology.

In the next letters of the series, we intend to cover such topics as the seed as a factory and storage organ and the seed–mother plant interactions during development, the acquisition of desiccation tolerance and the dormancy and longevity of seeds, the role of seed in dispersal, plant movement during evolution, seed responses to abiotic and biotic stresses, the role of seed banks in genetic resource stewardship and how we arrived there, and the emergence of seeds in palaeobotany.

Disclosure statement

No potential conflict of interest was reported by the author.

Notes on contributor

R. Thompson took a PhD in Molecular Biology at the University of Edinburgh, and began working on the regulation of seed development and composition at the Plant Breeding Institute in Cambridge, continuing at the MPI for Plant Breeding Research in Köln, and subsequently at INRA in Dijon. His current interest is understanding how the factors governing legume seed composition are coordinated during development.