Chenopodium

Salsola - Chenopodiaceae

Salsola kali growing with silvery Sea Buckthorn on a sand dune. British Isles, v.c. 6

Salsola, the saltworts are a fascinating and historically significant group of plants. Salsola is a genus of the Chenopodiaceae. Almost half of Chenopodiaceae genera are halophytes ('salt-loving'). Brine is water rich in salts, mostly sodium chloride but other salts, such as calcium, magnesium, potassium and sulfate can also reach levels that are toxic for most plants. Halophytes can thrive in salty soils and/or habitats likely to be splashed by brine by either tolerating the salt or excreting it. Salsola is a large genus, with 100 to 200 species, though there has been some disagreement over which species should be included, based on genetic data. I would caution against hastily ripping genera apart based on comparisons of the sequences of selected genes due to the high levels of horizontal gene transfer in plants. Molecular phylogenetics is a useful tool but not a magic bullet.

Salsola kali, flower spike, British Isles, v.c. 15

Apart from its spiny leaves, the flowers of Salsola are unmistakable. The five sepals (or tepals) enclose 5 stamens with yellow anthers and a style that divides into 2 or 3 segments bearing stigma tissue to receive pollen. The flowers are wind-pollinated (reportedly both self and cross-pollinated) and the flowers form in late Summer and early Autumn. The fruit is crowned by the style base and the sepals remain to enclose it and develop a transverse papery wing on their backs. The single seed is enclosed in a thin brown testa that adheres to the fruit wall. These wings, 3 major and 2 minor, make the 'flowers' unmistakable during the fruiting stage. The shape of the minor wings is of diagnostic help, since in Salsola australis they are broad and obovate (wider at the apex) so that the five form quite a complete contour (Borger & scott, 2009) whereas in Salsola tragus the minor wings are linear or narrowly elliptic. The wings assist wind dispersal of the fruit. In Salsola kali, shown here, the two minor wings are narrow, giving the fruit an irregular contour. Sometimes the wings barely develop. Note the two minor wings at the sides, with two broad wings below and one above:

Salsola kali, British Isles, v.c. 6, fruit with wings, wet with rain

The plants shown here are Salsola kali in the strict sense. Salsola australis was at one time included with (or confused with) S. kali, but is fruit form more perfect contours. Note also the two lateral bracts behind the flower, which are similar to but slightly shorter than the leaf below. The flower has formed in the axil of this leaf. Both bracts and leaves are very fleshy and end in a spinous tip. Flowers form in the axils of the leaves of the ends of the branches, forming spikes which are arranged in a panicle (branched inflorescence). Each of the five stamens has anthers consisting of 4 pollen sacs and the filament ends in a curved appendage. Being wind pollinated, the pollen depends on chance to find a receptive stigma, so the flowers produce large quantities of pollen grains.

Salsola kali, British Isles, v.c. 15

Salsola kali grows mainly on sandy shores, but can also be found on shingle (here it was on a shingle ridge along with Maritime Mayweed, Tripleurospermum maritimum in the splash zone.

Salsola kali, British Isles, v.c. 15

Salsola of Western fame

In North America, Salsola is invasive and various species are called Russian Thistle due to their introduction from Russia as a contaminant of flax seed. Salsola kali occurs in coastal areas, Salsola tragus inland. Salsola tragus (and also sometimes Salsola australis) are tumbleweeds. Although not the only plant to form tumbleweeds, Salsola is the most famous. After flowering, the plant dries and detaches itself at the base. The rounded bush-like form of these species can then tumble several miles in the wind, scattering its seeds as it does so, each tumbleweed dispersing between about 50 000 and 150 000 seeds! The fruit and their seeds persist in place, but the branches fragment as the weed tumbles. It is no wonder then that they spread across North America so rapidly. Introduced in South Dakota in 1873, they reached Colorado by 1892 and spread to two-thirds of the state over the next two years. The Old West is defined as the period beginning after the American Civil War in 1865, but when it ended depends on the authority, some defining its end in 1890, others in the early 1900s. Although tumbleweeds are of western movie fame, whether or not people saw them in the Old west depends on where they lived and when we consider the Old west to have ended! (Ref.: Ellen Blankers, 2014).

Salsola kali, British Isles, v.c. 15

In Salsola australis, fruit are shed before and during the tumbleweed stage and up to 20 000 seeds may be produced.

Salsola kali, British Isles, v.c. 15

The stems, and the margins of leaves and bracts of Salsola kali are covered in cartilaginous borders bearing cartilaginous hairs.

Salsola kali, British Isles, v.c. 15

Salsola can be protandrous (male parts ripening first) or protogynous (female parts ripening first) depending on species. This helps ensure cross-pollination, which is often preferable. Some can produce cleistogamous flowers, however, which ripen without opening, effecting self-pollination. During the male phase, when the male organs are ripe, the yellow anthers protrude from the flower and are possibly important in attracting pollinators in some species.

The typical sequence of flowering in Salsola kali is as follows:

1. In the closed flower bud, the two stigma arms are pressed together, concealing their stigmatic surfaces, and held upright.

2. When the flower is open, the stigmas curve backwards to expose the stigmatic surfaces, which are covered in tiny papillae (wart-like structures). The stigma is of the dry type (secreting no fluid prior to pollination). The stigma is long in annuals like Salsola kali, and deeply divided into two stigmatic arms covered in papillae, but is short in perennial species (Toderich et al. 2012).

3. Once pollinated, the stigma shrinks and dies, but the style base persists in the fruit.

4. The stamens, at the base of the flower facing the pistil, elongate their filaments during the male phase. If this phase occurs first then the stamens can be seen protruding from the otherwise closed flower bud.

Salsola kali, British Isles, v.c. 15

The fruit wall in Salsola, generally contains salt glands and crystals whose function may be to ensure optimal local soil conditions for germination. The rounded, flattened seed lies horizontal within the fruit and contains an elongated embryo wound up into a conical spiral. There are no obvious food reserves outside the embryo. When the seed imbibes water, the embryo uncoils, breaking the thin seed coat and fruit wall around it and the uncoiling motion forces the radicle (embryonic root) into the soil (Borger & scott, 2009). Usually two cotyledons (embryonic leaves are produced). This ensures rapid germination, lasting about 48 hours.

Salsola kali, British Isles, v.c. 15

Salsola is adapted for dry conditions, whether for salty windy shorelines (as in Salsola kali) or more inland deserts and semiarid regions (as in Salsola tragus). The fleshy (succulent) leaves are resistant to desiccation and their increased volume also enables them to absorb more salt. Thick waxy cuticles help protect the leaves from desiccation and also from damaging ultraviolet light (UV-B). Cells in the hypodermis of the leaf (the layer immediately beneath the epidermis) contain calcium oxalate crystals, at least in in Salsola soda (Milić et al., 2013) which could potentially also protect against harmful UV-B rays. Beneath these cells are the main photosynthetic mesophyll cells and these give way to the water-storage cells that pack the middle of the leaf.

Salsola kali, British Isles, v.c. 15

Salsola exhibits C4 photosynthesis rather than the far more common C3 photosynthesis. C4 photosynthesis is an adaptation to high temperatures, aridity and high light intensities. In C3 photosynthesis, oxygen competes with carbon dioxide for the key enzyme. If the enzyme processes carbon dioxide, then photosynthesis occurs as intended, if it processes oxygen then photorespiration occurs, which is wasteful. However, photorespiration is small except at high light intensities and high temperatures. C3 is so-called because the carbon dioxide is 'fixed' into a 3-carbon compound, using energy harvested from light, that is then used to make other organic molecules, which can all take place in the same cell.

Salsola kali, British Isles, v.c. 15

In C4 photosynthesis, carbon dioxide (CO₂) is fixed into a 4-carbon compound which is then shipped to the bundle sheath cells (cells that form the sheath of major vessels in both C3 and C4 plants) which are specialized to complete the process: the shipped C4 compound releases carbon dioxide inside the bundle sheath cells and there is so much of it coming from all the surrounding mesophyll cells that the CO₂concentration in the bundle sheath cells (BSC) is very high. The BSC then refixes the carbon dioxide but because there is so much, it out-competes oxygen and no significant amount of photorespiration occurs. However, the BSC need light energy to refix the CO₂, which is being fixed twice and this means that more energy is required. In high light intensities, sufficient light reaches the bundle sheath, which is situated deep within the leaf, and eliminating photorespiration means that there is an overall gain in efficiency. These plants may also use lenses and light-guides within the leaf to convey light to the bundle sheath. C4 plants are rare in cold climates, however, since the small amount of photorespiration occurring in C3 plants under cold conditions makes C3 photosynthesis more economical.

Salsola kali, British Isles, v.c. 15

In order to carry out efficient C4 photosynthesis, C4 plants have specialized leaf anatomy. The typical anatomy of the more common C3 leaf has been explained previously, the palisade mesophyll (and to a lesser extent the spongy mesophyll) are the sites of photosynthesis and are rich in chloroplasts to harvest light energy. The C4 leaf, in contrast, has specialized anatomy, called Kranz anatomy. In Kranz anatomy, the bundle sheath arrange the vascular tissue is very well developed, typically forming a double-helix of chloroplast-rich cells wrapped around the vein. Since the mesophyll cells have to transport fixed carbon to the bundle sheath, they form stacks of cells radiating from the bundle sheath like spokes. This allows the C4-compound to be transported directly from cell to cell, apparently through the plasmodesmata (specialized junctions between plant cells that allow the transport of small molecules and ions from one cell to the other).

Salsola kali, British Isles, v.c. 15

The wings on the fruit can be translucent, whitish or pink/reddish in color and aid dispersal by the elements.

Salsola kali, British Isles, v.c. 15

Adaptations to Coastal Life

Let us consider an example first.

Salsola soda (Salsola inermis) is an annual and succulent shrub up to 70 cm tall and occurs naturally in southern and eastern Europe and North Africa, on the Atlantic coasts of France and Portugal and the Black Sea coast, but is naturalized along the Pacific coast of N. America. The anatomy of this species was studied by Milić et al. 2013 (https://doiserbia.nb.rs/img/doi/0352-4906/2013/0352-49061325055M.pdf).

The leaves are succulent and rounded or elliptical in cross-section and covered by a thick waxy cuticle overlying a single-layer of epidermal cells. Beneath the epidermal cells is a single layer of thicker-walled chlorenchyma (chlorophyll-containing cells) forming a hypodermis (an additional protective layer beneath the cuticle). These hypodermal cells contain calcium oxalate crystals. Beneath the hypodermis are the mesophyll cells (main photosynthetic cells). The outermost layer are of palisade cells (columnar cells). There is a ring of peripheral veins (bundles of vessels), each enclosed by a bundle sheath (BS). As a C4 plant the BS cells contain chloroplasts and are in direct contact with the layer of palisade cells. In between the vascular bundles, the palisade mesophyll overlies the spongy mesophyll which grades into water storage parenchyma cells making up the bulk of the leaf. In the center of this water-storage tissue is the main central vessel. This particular arrangement is called salsoloid Kranz anatomy and is thought to be more-or-less typical of all Salsola species.

Salsola kali, British Isles, v.c. 15

Not all Salsola are coastal. Populations of S. soda found further inland had less succulent leaves with less water-storage tissue and a higher density of stomata (tiny pores that can open or close to obtain carbon dioxide from the atmosphere for photosynthesis, see: Transport in Plants). The name 'soda' refers to the high sodium content. Tissues of Salsola generally have a high sodium (salt) content and, like Glassworts, can be used in the manufacture of glass.

Salsola kali, British Isles, v.c. 15

Coastal habitats are typically characterized by high light levels (there is often no shade on shores) and dry conditions. The soil is often porous and drains easily (sand or gravel) and salt from the sea create a desiccating environment. Adaptations in coastal plants are therefore often not very different from those in xerophytes (plants adapted to dry and often hot habitats) and some Salsola species can also be found inland in semiarid regions. Some of these adaptations in Salsola are:

Thick cuticle: made of waxes this reduces water loss and perhaps also helps screen out damaging UV-B rays from sunlight.
Calcium oxalate crystals in outer cell layers: thought to protect underlying photosynthetic tissues from UV-B.
Stomata reduced in number and sometimes sunken or enclosed to reduce water loss (in Salsola they tend to be slightly sunken).
Retention of salt: the soil is salty so the plant has to draw up salt in order to obtain water and nutrients and this salt must either be tolerated, as in Salsola, or excreted (as in Atriplex and Chenopodium).
Succulent leaves: this may act as a water store but some evidence suggests that water-storage allows the plant to absorb and retain more salt; it also reduces the surface area / volume ratio of the leaves, reducing water-loss.
Salsola has C4 metabolism with corresponding Kranz anatomy.

Salsola kali, British Isles, v.c. 15

The wiry roots appear not to form mutualistic mycorrhizae with fungi to assist in nutrient uptake. This is likely because such fungi are less abundant in unstable soils such as sand and shingle.

Salsola kali, British Isles, v.c. 15

Salsola australis, at one time confused with S. kali, but is sometimes considered a distinct species (and with good reason) is diploid (2n = 18) and produces a mixture of winged and wingless fruits and occurs naturally in Australia. In contrast, S. kali is tetraploid (2n = 36) and occurs naturally in much of Europe, including Scandinavia, and North Africa. This is likely a strategy to ensure that some but not all seeds end up dispersal over long distances. Seeds need to replenish the existing population first and foremost, before risking long journeys to find new suitable locations. It is an annual or biennial and either remains in place when seeding or detaches and tumbles, being more-or-less spherical when mature though less compact than S. tragus. It can sometimes re-sprout from the base in the second year as a low-lying plant.

Salsola kali, British Isles, v.c. 15