Dispersal by Open Sesame!

In certain instances, “open sesame” might be something you exclaim to magically open the door to a cave full of treasure, but for the sesame plant, open sesame is a way of life. In sesame’s case, seeds are the treasure, which are kept inside a four-chambered capsule. In order for the next generation of plants to have a chance at life, the seeds must be set free. Sesame’s story is similar to the stories of numerous other plant species whose seeds are born in dehiscent fruits. But in this instance, the process of opening those fruits is fairly unique.

Sesamum indicum is a domesticated plant with a 5000 plus year history of cultivation. It shares a genus with about 20 other species – most of which occur in sub-Saharan Africa – and belongs to the family Pedaliaceae – the sesame family. Sesame was first domesticated in India and is now grown in many other parts of the world. It is an annual plant that is drought and heat-tolerant and can be grown in poor soils and locations where many other crops might struggle. However, the best yields are achieved on farms with fertile soils and adequate moisture.

image credit: wikimedia commons

Depending on the variety and growing conditions, sesame can reach up to 5 feet tall and can be unbranched or highly branched. Its broad lance-shaped leaves are generally arranged directly across from each other on the stem. The flowers are tubular, similar in appearance to foxglove, and are typically self-pollinated and short-lived. They come in shades of white, pink, blue, and purple and continue to open throughout the growing season as the plant grows taller, even as fruits formed earlier mature. The fruits are deeply-grooved capsules with at least four separate chambers called locules. Rows of tiny, flat, teardrop shaped seeds are produced in each chamber. The seeds are prized for their high oil content and are also used in numerous other ways, both processed and fresh. One of my favorite uses for sesame seeds is tahini, which is one of the main ingredients in hummus.

The fruits of sesame are dehiscent, which means they naturally split open upon reaching maturity. Compare this to indehiscent fruits like acorns, which must either rot or be chewed open by an animal in order to free the seeds. Dehiscence is also called shattering, and in many domesticated crop plants, shattering is something that humans have selected against. If fruits dehisce before they can be harvested, seeds fall to the ground and are lost. Selecting varieties that hold on to their seed long enough to be harvested was imperative for crops like beans, peas, and grains. In domesticated sesame, the shattering trait persists and yield losses are often high.

Most of the world’s sesame crop is harvested by hand. The plants are cut, tied into bundles, and left to dry. Once dry, they are held upside down and beaten in order to collect the seeds from their dehisced capsules. When harvested this way, naturally shattering capsules may be preferred. But in places like the United States and Australia, where mechanical harvesting is desired, it has been necessary to develop new, indehiscent varieties that can be harvested using a combine without losing all the seed in the process. Developing varieties with shatter-resistant seed pods, has been challenging. In early trials, seed pods were too tough and passed through threshers without opening. Additional threshing damaged the seeds and caused the harvest to go rancid. Mechanically harvested varieties of sesame exist today, and improvements in these non-shattering varieties continue to be made.

In order to develop these new varieties, breeders have had to gain an understanding of the mechanisms behind dehiscence and the genes involved in this process. This research has helped us appreciate the unique way that the capsules of the sesame plant dehisce. As in the seed bearing parts of many other plant species, the capsules of sesame exhibit hygroscopic movements. That is, their movements are driven by changes in humidity. The simplest form of hygroscopic movement is bending, which can be seen in the opening and closing of pine cone scales. A more complex movement can be seen in the seed pods of many species in the pea family, which both bend and twist as they split open. In both of these examples, water is evaporating from the plant part in question. As it dries it bends and/or twists, thereby releasing its contents.

dehisced capsules of sesame (Sesamum indicum); photo credit: wikimedia commons (Dinesh Valke)

The cylindrical nature and cellular composition of sesame fruits leads to an even more complex form of hygroscopic movement. Initially, the capsule splits at the top, creating an opening to each of the four locules. The walls of each locule bend outward, then split and twist as the seed falls from the capsule. In a study published in Frontiers in Plant Science (2016), researchers found that differences in the capsule’s inner endocarp layer and outer mesocarp layer are what help lead to this interesting movement. The endocarp layer is composed of both transvere (i.e. circumferential) and longitudinal fiber cells, while the mesocarp is made up of soft parenchyma cells. The thicknesses of these two layers gradually changes along the length of the capsule. As the mesocarp dries, the capsule initially splits open and starts bending outwards, but as it does, resistance from the fiber cells in the endocarp layer causes further bending and twisting (see Figure 1 in the report for an illustration). As the researchers write, “the non-uniform relative thickness of the layers promotes a graded bi-axial bending, leading to the complex capsule opening movement.”

All this considered, a rock rolling away from the entrance of a cave after giving the command, “Open sesame!” almost seems simpler than the “open sesame” experienced by the fruit of the sesame plant.

See Also: Seed Shattering Lost – The Story of Foxtail Millet

Seed Shattering Lost – The Story of Foxtail Millet

For a plant to disperse its seeds, it must first let go of them. Sounds obvious, but it is a key step in the dispersal process and an act that is actually coded in a plant’s DNA. As fruits ripen and seeds mature, an abscission layer is formed that separates the seed-bearing fruits from the plant. No longer attached to their parents, seeds are left to their own devices. If all goes well, they will find themselves in a suitable location where they can germinate and grow into a whole new plant, fully equipped to make seed babies of their own.

The releasing of mature seeds is known as shattering, a term most commonly used in reference to grasses and plants with dehiscent seed pods (i.e. fruits that split open when ripe, such as those in the bean and mustard families). In grasses, seeds form along a central stem called a rachis. As the seeds ripen, they separate from the rachis and drop from the plant. In some cases, the rachis is brittle and a section of it breaks off with each seed that falls.

Seed shattering is not a desirable trait when it comes to food crops. It’s easy to see how yields can be poor if seeds disperse before they are harvested. Thus, an essential step in domesticating certain agricultural crops was selecting plants that lacked this particular trait. Instead of dropping mature seeds, such plants hold on to them, making them easy to collect. A simple and naturally occurring mutation in the genes of these plants allowed early farmers to select varieties that were more ideal for agriculture than their wild progenitors.

Genetic studies of agricultural crops have located genes in a number of species that code for seed shattering, confirming that domestication in many cases involved selecting plants with this gene turned off. A recent study, published in Nature Biotechnology (October 2020), took a different route in locating this gene, looking instead at a weedy, wild relative of a crop that was domesticated at least 8000 years ago. Green foxtail (Setaria viridis) is the wild antecedent of foxtail millet (Setaria italica), a crop that, while still commonly grown for food in parts of Asia, is mostly grown for hay, silage, and bird seed in North America. Recently, interest in foxtail millet and other millets (a term used to refer to the grains of several different species of grasses) is on the rise due to the ability of these crops to tolerate drought and heat.

Illustration of three Setaria species from Selected Weeds of the United States (Agriculture Handbook No. 366) published in 1970

Setaria viridis is an abundant, widespread weed adapted to human disturbance. It’s of Eurasian origin but has been present in North America since the early 1800’s and was likely introduced both intentionally and accidentally. It’s an annual grass with prominent, bristly flowerheads that are easily recognizable and the reason for its common name, green foxtail. A handful of other closely related, similar-looking species are also common weeds in North America. Due to useful traits including its short life cycle, small genome, and self-fertility, S. viridis has been used frequently as a model species to carry out a variety of scientific studies. The study referred to above aimed to further enhance the use of green foxtail, particularly when it comes to crop science.

Researchers traveled across the United States collecting nearly 600 samples of green foxtail in order to better understand its genome. They found that the North American population of green foxtail is composed of multiple introductions and that, as the species has followed humans around, it has quickly adapted to diverse climates found across the continent. In examining the genome, they were able to identify the genetic underpinnings for three traits that have importance to agriculture: response to climate, leaf angle (which is used as a predictor of yield in grain crops), and seed shattering.

foxtail millet (Setaria italica) via wikimedia commons

The seed shattering gene – which the researchers named Less Shattering 1 (SvLes1) – was an especially interesting discovery. When compared to the orthologous gene found in foxtail millet, they found that a frameshift mutation had caused a disruption in the gene, turning it off. Using CRISPR (a gene editing tool) they were able to recreate a similar interruption in green foxtail, which resulted in a loss of seed shattering similar to that of foxtail millet. It became clear that selecting plants with this mutation was an essential step in the domestication of this ancient grain.

An excerpt about seed shattering from Fruit from the Sands by Robert N. Spengler III: 

In many of the world’s domesticated grains, especially those from the founder crops of southwest Asia (i.e. wheat and barley), the earliest phenotypical trait of domestication that archaeobotanists look for is a tough rachis, the small stem by which an individual grain or small cluster of grains is attached to the ear. In their wild form, most grains are programmed to detach easily after the grain ripens; however, in domesticated cereals, the grains remain attached to the ear throughout the harvesting process. This change is an inadvertent result of human harvesting with sickles: as people reap their harvest, the grains with a brittle rachis are dropped and those with a tough rachis are collected, stored, and replanted for successive harvests.

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