Sorrel (Rumex acetosa L.): Not Only a Weed but a Promising Vegetable and Medicinal Plant

Sorrel (Rumex acetosa L.) is a perennial, dioecious herb occupying a variety of habitats. Sorrel has been utilized as a wild gathered plant for thousands of years and as a cultivated plant for centuries. Primarily roots but also other tissues have been used in folk remedies since ancient times. In recent investigations, different phytochemical and pharmacological activities of Rumex have been analyzed, and many bioactive compounds have been detected. Sorrel is also a tasty plant and its leaves are a good source of macronutrients and micronutrients. However, the presence of high levels of oxalic acid reduces the bioavailability of some minerals, especially calcium, when using uncooked plant parts. Further investigations on different sorrel compounds are needed to show their true effect. It is beneficial that sorrel is easily propagated and there are no serious insect or disease problems. A few types of R. acetosa seeds are presently available commercially, including wild types and a few cultivars.


Introduction
Rumex is a genus with about 200 species of annual, biennial and perennial herbs, rarely shrubs, that belong to the buckwheat family (Polygonaceae) and are distributed in Europe, Asia, Africa and North America, primarily in the northern hemisphere (Flora Europaea 1993;Mabberley 2008). Some of them are considered nuisance weeds, while others are used for their edible leaves or medicinal properties. The present review concentrates on the sorrel R. acetosa L., also called common sorrel, English sorrel, sheep's sorrel, red sorrel, sour weed and field sorrel. The common names of Rumex species are varied and even confusingly overlapping among species. For scientific names, Latin is the primary language. The etymological origin of the genus name Rumex probably comes from the Greek word for spear or dart, due to the spear shaped leaves of the plant (Liddell and Scott 1940). Another theory has been presented by Saleh et al. (1993): evidently, the Romans used to suck the plants to allay thirst, and the name Rumex is thus derived from the Latin word for suck. The species name acetosa is derived from acetum, the Latin word for vinegar, referring to the sharp taste, comparable to the name and taste of sheep's sorrel R. acetosella (Parker 2018).
R. acetosa is a wind-pollinated vigorous perennial, dioecious herb occupying a wide variety of habitats, but being especially common to grasslands, pastures and disturbed land (Korpelainen 1991). It grows to a height of 30-80 cm, the stem being glabrous (Flora Europaea 1993;Mabberley 2008). The leaves are large, hairless, and ovate in outline and have characteristic, pointed basal leaf lobes. The stalk of basal leaves is longish, while stem leaves are almost stalkless. The small pinkish flowers are unisexual (either male of female). The fruit is a triangular achene. R. acetosa is found throughout Europe from the northern Mediterranean coast to the north of Scandinavia and parts of Central Asia, and it occurs as an introduced species in parts of Australia and North America (Flora Europaea 1993;Mabberley 2008). Based on the present knowledge, the species R. acetosa involves thirteen subspecies and five varieties (WFO 2020). A life history capable of responding to different environmental demands is necessary for plants, which possess a wide geographic distribution or inhabit otherwise variable habitats. The response may operate through genetic differentiation among plants occurring in different habitats or through phenotypic plasticity. Sorrels have been shown to exhibit a very plastic morphology and a good amount of genetic diversity (Korpelainen 1992(Korpelainen , 1993(Korpelainen , 1999Ye et al. 2012), and this may help to explain how they can exist in a wide range of environments.
On the basis of a wide coverage of literature on sorrel (R. acetosa), the present review will compile scientific information on the basic biology, wide variety of traditional and present uses, and further use potential, as well as on the chemical and pharmacological properties of this species. We aim to highlight not only the many benefits of sorrel cultivation but also the concerns linked to its use. Our objective is to create a comprehensive review of the knowledge of R. acetosa that can guide further basic and applied research on this plant.

Sex Determination and Life History
The presence of sex chromosomes is not common in plants (Korpelainen 1998), where the majority of species are hermaphroditic. Among angiosperms, about 10% of species are dioecious (Lloyd, 1982), but only rarely they possess sex chromosomes (Grant et al. 1994;Parker 1990). R. acetosa is one of those plant species that has sex chromosomes, namely 2n = 12 + XX in females and 2n = 12 + XY1Y2 in males (Kihara and Ono 1923;Ono 1935;Parker and Clark 1991;Shibata et al. 1999Shibata et al. , 2000. The Y chromosomes play no role in sex determination, but rather it is the ratio of X chromosomes to autosomes, which is decisive for sex determination, i.e., individuals with X: A ratios of ≤0.5 are male, while individuals with X: A ratios of ≥1.0 are female. Individuals with intermediate X: A ratios (polyploids and aneuploids) produce intersex or hermaphrodite flowers. Mariotti et al. (2009) have shown that the rapid accumulation and expansion of DNA satellites have contributed to an increase in the size and differentiation of the nonrecombining Y chromosome that has no function in sex determination. Later, to gain insight into the molecular mechanism of sex determination, Manzano et al. (2017) generated a cDNA library enriched in genes specifically or predominantly expressed in female floral buds. They demonstrated the presence of a flower-specific gene designated FEM 32 and showed that its transcripts accumulate much more in female flowers than in male flowers. Manzano et al. (2017) considered likely that FEM 32 functions in R. acetosa by arresting stamen and pollen development during female flower development. Navajas-Pérez et al. (2005) have estimated that dioecy in the genus Rumex developed about 16 Ma, and the acetosa clade with the sex chromosome system originated 12-13 Ma ago. The results of Navajas-Pérez et al. (2005) further supported the view that sex determination based on the balance between the number of X chromosomes and the number of autosomes has evolved secondarily from male-determining Y mechanisms and that the multiple sex chromosome system, XX/XY1Y2, derived twice from an XX/XY system. Occasionally, intersex inflorescences have been observed (Ainsworth et al. 2005). A genetic, PCR-based method has been developed to reveal the sex of R. acetosa at any life stage (Korpelainen 2002), not just at sexual maturity, when dimorphic flower structures are present.
In dioecious plants, males and females may have different ecological requirements or tolerances, and natural selection can act differently on them. Consequently, the environment differentially influences male and female performance (i.e. fitness), which may lead to biased sex ratios. The cost of reproduction of female plants often exceeds that of male plants, because, besides flowers, females produce seeds and fruits. Potentially, the greater female reproductive effort could result in reduced female growth and/or survival. However, the sex ratios of R. acetosa are typically female-biased (Korpelainen 1991(Korpelainen , 1992. It is notable that since it has a high capacity for vegetative reproduction, the cost difference between the sexes may not be as significant as in strictly sexually reproducing species, and there may be other mechanisms that contribute to the sex ratio bias, e.g., higher male mortality (Korpelainen 1991). Based on a genetic sex identification method, Korpelainen (2002) discovered that sex ratios are still about 1:1 at the seed stage, while there are also observations supporting the view that female-biased sex ratios of R. acetosa are determined prezygotically to some extent (Błocka-Wandas et al. 2007).
Genotypic differences, maternal effects, phenotypic plasticity and the quality of the environment all influence a plant's life history characteristics. Korpelainen (1992) has observed that the males of R. acetosa allocate more resources to reproduction during the time of flower production than do females, whereas females invest more in reproduction during seed production. Thus, males and females show different life history strategies. Altogether females, which are taller and may have a higher resource threshold for the occurrence of sexual reproduction, allocate both a higher amount and a higher proportion of energy to reproduction than do males (Korpelainen 1992). Yet, the operational sex ratios are strongly female-biased. Perhaps, with a greater size, R. acetosa females are better buffered against the resource demands that sexual reproduction creates, and this may lead to a lower female mortality (Korpelainen 1992). Despite differences in life history traits, little sexual dimorphism has been observed in the phenological traits, such as flowering onset, peak, duration and proportion of newly opening flowers (Matsuhisa and Ushimaru 2019). Such lack of phenological differences enhances synchronous flowering with the opposite sex.

Wide Variety of Uses
Wild plants have been harvested in European settlements at least from the Neolithic and Mesolithic periods. Sorrel seeds and charred plant parts indicating food processing have been found in settlement sites throughout Europe (Andersen 1990; Kotzamani and Livarda 2018;Kubiak-Martens 1999;Vanhanen and Pesonen 2016). Wild plants have traditionally been gathered mainly by women and children in many rural areas throughout the world, usually casually and sometimes more systematically. In today's rural societies this practice has been declining, as people increasingly get their foods from the supermarkets. However, during recent years, new trends have been emerging and wild plant harvesting has become more popular, specifically as an urban pastime. Urban wild food harvesting seems to engage people from all walks of life. Today's urban foragers include both men and women, as well as diverse ethnic, economic and social groups. Wild food harvesting is often casual, although small-scale cultivation of wild plants is getting more common. Urban dwellers increasingly enjoy spending time in the nature, and they like to learn about old traditional practices and are willing to utilize wild resources in cuisine (Abbet et al. 2014;Etkin 1994;McLain et al. 2014;Pardo de Santayana et al. 2007). Such newly developed interests in nature may improve appreciation for biodiversity and, consequently, contribute to the conservation of nature as well as to the diversification of crop plants.
Among Rumex species, sorrel, R. acetosa has the greatest use potential. It is a delicious plant, which provides good, months-long harvests of edible leaves that have quite distinctive acidic taste caused by oxalic acid. Sorrel has been utilized for thousands of years, and used as food in diverse dishes, as herbal preparations for various purposes, and as a source of different colors of dyes (Bello et al. 2019;Couplan 2009;Dogan et al. 2015;Sun et al. 2015;Vasas et al. 2015) (Table 1). Relatives in the genus Rumex that are used as food, although less frequently, include, e.g., sheep sorrel R. acetosella, often considered a weed but having edible small leaves, red-veined sorrel R. sanguineus, being actually more ornamental than flavorful, spinach dock (also known as patience dock, garden patience or herb patience) R. patientia, growing much taller and having a quite pleasant flavor, spinach rhubarb R. abyssinicus, a tall plant with leaves that can substitute for spinach and ribs like rhubarb, and French sorrel R. scutatus, used mainly in salads and soups or as a spinach substitute (Mekonnen et al. 2010;Vasas et al. 2015). In some regions, the leaves of other Rumex species, such as R. alpinus, R. hymenosepalus, R. gracilescens and R. pseudonatronatus are utilized as foods, mainly in the form of sour soups, sauces and salads (Abbet et al., 2013;Ahmad et al. 2016;Bello et al. 2019;Dogan et al. 2015;Mekonnen et al. 2010;Vasas et al. 2015).
There have been numerous ethnobotanical and ethnopharmacological reports dealing with the occurrence and traditional uses of Rumex species (e.g. Abbasi et al. 2015;Alzoreky and Nakahara 2001;Dogan et al. 2015;Mekonnen et al. 2010;Vasas et al. 2015) (Table 1). As a cultivated plant, sorrel, R. acetosa has been produced for centuries, and it is a quite widely used herb in native cuisine throughout Europe and parts of Asia, such as India and Vietnam and parts of Africa, such as Ethiopia and Cameroun, where it is grown as a garden herb or vegetable. It is commonly combined with other greens and eaten raw or cooked in soups, stews and pastries. Sorrel is widely mentioned in gardening and recipe books because of its distinctive sour taste, which is  China Xiong (1998) attributed to its high oxalic acid content. The tangy, acidic, sour-lemony flavor of sorrel blends well with a variety of ingredients, such as meat, cheese and milk. Sorrel sprouts and young immature leaves have a more subtle flavour and so are suitable for addition to salads and sandwiches. The more mature leaves are normally cooked and added to soups and stews and used to make sauces. Although R. acetosa is the most commonly used edible Rumex species, some food experts prefer less acidic French sorrel (R. scutatus) for culinary purposes. Primarily roots but also other tissues of many species belonging to the genus have been reported to have various biological activities. They have been used in folk remedies from ancient times as anti-inflammatory, antioxidant, diuretic, antimicrobial, antihypersensitive, diuretic, analgesic, antiviral and anti-fungal agents to treat various health disorders, such as diabetes, constipation, infections, diarrhea, oedema, jaundice, scurvy, and liver and gallbladder disorders (Bae et al. 2012;Demirezer et al. 2001;Gescher et al. 2011;Kucekova et al. 2011;Lee et al. 2005;Taylor, 1996;Vasas et al. 2015;Wegiera et al. 2007). The antioxidant capacity of sorrel is reported to be approximately the same as in Japanese green tea (Alzoreky and Nakahara 2001). The flowers and rhizomes contain compounds that are suggested to have tumor arresting effects (Kucekova et al. 2011;Lee et al. 2005;Tamokou de Dieu et al. 2013). Traditionally, water from boiled sorrel has been used to wash chicken pox sores, boils, shingles-afflicted skin, poison ivy rashes, blisters, acne and other skin sores. It is supposed to ease pain, relieve itches and speed up the healing process (Table 1). Drinking sorrel water flavored with a bit of honey was believed to bring down a fever and help clear sinus infections (Bello et al. 2019).

Chemical and Pharmacological Properties
Based on the traditional knowledge, different phytochemical and pharmacological activities of R. acetosa and other species in the same genus have been studied, including its chemical constituents, pharmacological activities, toxicity and safety. A range of promising medical and other new uses have been recognized (Table 2). A number of bioactive compounds have been detected in phytochemical investigations conducted on Rumex species. The aerial parts contain several flavonoids and polyphenols with antioxidant capacity, while its rhizomes are rich in anthraquinones and polysaccharides suggested to be responsible for, e.g., its antitumor effect (Bicker et al. 2009;Lee et al. 2005). Other isolated bioactive compounds involve emodin, naphthalenes, stilbenoids, triterpenoids, carotenoids, geranin, tannins, vanillic acid, corilagin, gallic acid, sinapic acid and pyrogallol. Bello et al. (2019) mention that over 50 chemical compounds have been isolated from the species.
Sorrel leaves are a good source of macronutrients and micronutrients, and it has been suggested that sorrel leaves could be used as an economic source of plant-based protein (Ladeji and Okoye 1993). However, the presence of high levels of the anti-nutritive factor, oxalic acid, reduces the bioavailability of some minerals, especially calcium, thus causing mineral deficiencies and other serious problems (calcium oxalate stone formation in kidneys, decreased iron absorption). Rhubarb grown primarily for its fleshy leafstalks is another example of a vegetable that contains considerable levels of oxalic acid. The risk of consuming foods high in soluble oxalates has been well documented (Noonan and Savage 1999;Tuazon-Nartea and Savage 2013).
Oxalate accumulation is affected by different factors, such as soil conditions, climate, species or cultivar and plant age. Tuazon-Nartea and Savage (2013)  (2001) Aluminium resistance, phytoremediation Whole plant High tolerance of toxic metal ions Ernst et al. (2004), Tolrà et al. (2005), Wang et al. (2003) investigated the oxalate content of the leaves and stems of green and variegated cultivars of R. acetosa. The larger, more mature leaves of both cultivars contained higher levels of total, soluble and insoluble oxalates than other tissues. The stems also contained considerable levels of oxalates. However, the oxalate content varied considerably between cultivars, and even plants with quite low oxalate contents maintained their characteristic sour taste. In fact, other organic acids than oxalates can cause sour plant taste as well (Pereira et al. 2013). Yet, it was recommended that raw sorrel leaves should be consumed only occasionally or in small quantities as a delicacy because of their unique taste rather than as a significant part of the diet. On the other hand, the products made from sorrel leaves are less of a problem as they contain lower levels of oxalates. Tuazon-Nartea and Savage (2013) and Bello et al. (2019) have showed that cooking reduces the oxalic acid concentration of R. acetosa to a negligible amount. In addition, the oxalate contents can be lowered through selection breeding and appropriate choice of cultivars. Aluminium toxicity is considered a major abiotic stress factor in low pH soils. R. acetosa is a pseudometallophyte that has been identified in several metal contaminated sites and it is well adapted to acid mineral soils with high availability of phytotoxic aluminium ions (Ernst et al. 2004;Tolrà et al. 2005;Wang et al. 2003). Aluminium resistance in R. acetosa implies both an exclusion of Al from root tips and tolerance to high Al concentrations in tissues. Citrate in roots and phenolics in shoots may bind aluminium into non-toxic forms. Anthraquinones, as strong antioxidants, may play a role in a general defence response to the root stress. Based on the existing tolerances, there may be potential to use sorrel for phytoremediation, i.e., for using living plants to clean up soil with hazardous contaminants.

Use Potential and Cultivation
It is clear that further investigations on different sorrel compounds are needed to show their true effect and provide scientific evidence for the medicinal effects of sorrel preparations and to aid the discovery of novel therapeutics and drug discovery. However, the use and cultivation potential of sorrel as a vegetable that provides a nice citrusy flavor to a variety of dishes has been proven (e.g. Jarić et al. 2007;Mattalia et al. 2013;Pieroni et al. 2014). Especially the leaves are a good addition to diets despite the presence of somewhat harmful oxalic acid in fresh plant material (Tuazon-Nartea and Savage 2013). A disadvantage is that the leaves lose quality quickly once harvested, which probably is a reason for sorrel being only rarely sold in markets. Therefore, a viable option would be to grow sorrel in containers that offer added longevity and marketability. Recently, Ceccanti et al. (2020) investigated the suitability of hydroponically grown Rumex acetosa as fresh-cut produce. They discovered that during postharvest storage in plastic boxes sorrel leaves maintained their nutraceutical value quite well. Yet, Ceccanti et al. (2020) emphasized the need for further research to standardize the yield and the nutraceutical content of this species.
R. acetosa is a perennial herb with long roots and smooth, arrow-shaped leaves that grow from a center rosette, and it will grow tall flower stalk as the temperature warms (Korpelainen 1993). Sorrel has preference for well-drained soil in full sun to partial shade. It is susceptible to damage from slugs and aphids, but there are no serious insect or disease problems (www.rhs.org.uk). It is easy to propagate in the garden by dividing the roots or by sowing seeds directly in the soil (H. Korpelainen, pers. obs.). Although sorrel tolerates moderate drought, it performs best when the soil is evenly moist. Once planted, sorrel requires little care to produce masses of leaves (H. Korpelainen, pers. obs.). It can be grown as a potherb as well. Clipping leaves for cooking throughout the growing season enhances the growth of the plant. When the plant produces flower stalks in mid-summer, the whole plant should be cut back to encourage new leaf growth instead of setting seeds. Young leaves are best for culinary uses, either raw or cooked, since older leaves can be bitter and tough, yet usable for cooking (Nedelcheva 2013;Pardo de Santayana et al. 2007). Typically, the large, juicy leaves are boiled like spinach for a hot side dish of tasty greens topped with butter and salt.
A few types of R. acetosa seeds are available commercially, including wild types and a few cultivars. The best known cultivars are 'Belleville' and 'Profusion' (Weaver 2000). 'Belleville' is probably the oldest and most famous one having its origin in the late 1600's, when French gardeners decided to start to improve the flavor and texture of the leaves of wild sorrel. It was domesticated in France during the 1730s and its large, pale green leaves are still a classic ingredient in French cuisine. 'Belleville' seeds are commonly available and it is a very productive easily grown cultivar. Another comparable commercially available cultivar is 'Blonde de Lyon'. On the other hand 'Profusion' is an unusual patented variety, introduced in 1993, which does not flower or produce seeds at all. The leaves are round, dark green and more succulent than most other R. acetosa leaves. 'Profusion' sorrel can be increased only vegetatively by division or cuttings. It produces tender, fleshy leaves all season, long after standard varieties turn tough and bitter. It also makes a great ornamental border plant because it grows in attractive compact mounds of about 20-25 cm. In addition to these, the Royal Horticultural Society of England (www.rhs.org.uk) lists some garden varieties, such as Rumex acetosa subsp. acetosa 'Saucy'.

Conclusions
The present study introduces the biology of sorrel, R. acetosa and reviews scientific knowledge of its chemical and pharmacological properties, and highlights the traditional and present use as well as further potential as a cultivated or wild collected plant. Sorrel is an underutilized plant with considerable potential for greater use as food, medicinal herb and even as a plant for phytoremediation. Thus, this species deserves more attention in both basic and applied research, and in plant production. Our attempt is to increase interest in research, cultivation and utilization of sorrel. At the present, sorrel is largely consumed through wild foraging or growing in home gardens. However, there is potential for much greater commercial use. Sorrel is a vigorous and healthy plant, for which a viable production option would be to grow it in containers that would offer added longevity and marketability. If that was done in greenhouses, year-round production would be possible in diverse climates. Breeding effort could be aimed at developing different looking and tasting varieties, along with a lower oxalic acid content in order to improve its usability and healthiness as a more major source of food. Considering medicinal uses, it is clear that further investigations on different sorrel compounds are needed to show their true effect and provide scientific evidence for the medicinal effects of sorrel preparations and to aid the development of novel therapeutics and drug discovery. The applicability of sorrel for phytoremediation remains as a largely untouched research area.
Funding Information Open access funding provided by University of Helsinki including Helsinki University Central Hospital.
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