CABBAGE AND CRUCIFER PLANTS

CABBAGE AND CRUCIFER PLANTS. The cole crops broccoli, brussels sprouts, cabbage, cauliflower, collards, kale, and kohlrabi belong to the same species (Brassica oleracea L.) in the Brassicaceae or mustard family. Kale most closely resembles the progenitor to this group of vegetables. Native to European coasts, wild B. oleracea and related species are one to two meters in height with large lobed leaves and a terminal inflorescence of yellow flowers. Different portions of the plant were emphasized during domestication. Broccoli and cauliflower were selected for large edible inflorescences, kohlrabi for an enlarged basal stem, and brussels sprouts and cabbage for leafy buds (axillary and terminal buds, respectively). These vegetable crops grow best in cool climates with adequate soil fertility and ample water. Brassica species are unique in producing glucosinolates, the compounds that impart pungency to various cole crops. Certain forms of these compounds are antinutritional while others are beneficial. On the balance, consumption of cole crops has a positive influence on human health. Cole crops are used fresh, may be canned, frozen, dehydrated, pickled, and fermented. Sauerkraut, made from fermented cabbage, is an ancient process that was used to preserve this vegetable as a source of vitamins and minerals during the winter months.

Plant Biology

Plant description. The cole crops are members of the Brassicaceae family (formerly Cruciferae). This family includes over three thousand species in more than three hundred genera. Plants are usually herbaceous annuals, biennials, or perennials. Cabbage and related cole crops belong to the species Brassica oleracea L.

With exception of certain cabbages and some types of kale, this group has smooth, alternate leaves with lobed or wavy to highly dissected margins. Leaves may be thick and succulent, with or without a waxy bloom. Some types grow to over two meters on a shallow and fibrous root system. The inflorescence is a terminal raceme of showy yellow or white flowers. Flowers possess four perpendicular petals that the medieval Europeans thought resembled a crucifix (thus the former family name Cruciferae). Flowers also have four sepals, a two-celled, superior ovary with a single stigma and style, and six stamens, two of which have shorter filaments than the others. The fruit (seed pod) is a silique with a persistent, beaked style. At maturity, siliques dehisce longitudinally to release the small round brown or black seeds. Seeds mature fifty to ninety days after fertilization. The species is insect cross-pollinated with self-pollination prevented by a sporophytic self-incompatibility system. All naturally occurring B. oleracea are diploid with nine pairs of chromosomes.

With the exception of some cauliflower and broccoli cultivars, the cole crops have a biennial reproductive cycle. Broccoli and cauliflower may be either annual or biennial (Table 1). Except for tropical cauliflowers, vernalization is required for flowering.

During domestication, different plant organs were emphasized. Kale and collards are the least modified from the ancestral form. Cabbage possesses a head composed of overlapping leaves formed on a shortened stem. Brussels sprouts form smaller heads in the leaf axils of the stem. The edible portion of kohlrabi is a shortened and swollen stem. Broccoli has been selected for an enlarged stem and inflorescence that is consumed when flowers are fully developed but have not yet opened. Like broccoli, the head of cauliflower is eaten. However, the head consists of a highly branched mass of undifferentiated shoot apices (curd) that only later may differentiate into floral primordia.

Growth requirements. The B. oleracea are cool season crops, with optimum growing temperatures of about 59–68°F (15–20°C), but plants will grow slowly even at 14°F (5°C). Cole crops are cold and frost tolerant, but developmental stage and type of crop affects the degree of cold tolerance. Young plants are more tolerant than are older plants, and crops whose vegetative parts are eaten are generally more tolerant of low temperatures than crops whose reproductive parts are consumed. Kale and brussels sprouts are the most cold hardy, and can withstand temperatures as low as 14 to 23°F (-5 to -10°C). High temperatures (>77°F or >25°C) will inhibit or impair head development in broccoli. Almost no broccoli cultivars can be grown in the warm tropics because plants fail to form heads. Winter, summer, and tropical cauliflower cultivars have been developed, each of which has a different optimal temperature range. For summer types, the optimum temperature for curd development is 62 to 64°F (17 to 18°C) with small "button" heads induced at temperatures above 68°F (20°C). Some winter types develop curds even at 50°F (10°C) while some tropical types will tolerate temperatures up to 86°F (30°C).

Botanical types and horticultural characteristics. Brassica oleracea vegetables show amazing diversity in form that is reflected in the different botanical variety names assigned to them (Table 1). These names generally describe the origin of the crop, or the edible part that has been accentuated.

The cabbage group is differentiated based on head shape and color, leaf texture, and intended use. Savoy types, with crinkled leaves and looser heads, are used primarily fresh in salads. Smooth-leafed, firm-headed cabbages are used for fresh market and processing. Fresh market types are typically small-headed and may be green or purple. Fresh market types are further differentiated into those sold immediately, and those stored for several months before sale. Processing types (mainly used for sauerkraut) have large heads (up to 4 kg) that are high in dry matter. Cabbage heads can vary in shape from pointed, to round, to oblate.

Firm heads (which depends on the arrangement and thickness of leaves, leaf angle, and freedom from axillary cavities) are preferred. The core (main stem within the head) should be small in diameter and less than half the height of a mature head. A dark-green or purple external color is preferred for market. Fresh market and storage cabbage can have white, green, or purple internal color, but for sauerkraut, white internal color is essential. Uniform size and maturity are necessary for efficient harvest and packing.

While the term "broccoli" is commonly used in the United States to refer to B. oleracea var. italica, elsewhere this crop may be called "sprouting broccoli" or "calabrese" (after a landrace, or farmer-selected variety, from the Calabria district of southern Italy). Other crops that use the name "broccoli" are "broccoli rape" (turnip or B. rapa inflorescences), "heading broccoli" or "cauliflower broccoli" (B. oleracea var. botrytis ), and "Chinese broccoli" (B. oleracea var. alboglabra ). Broccoli may have purple or green heads, be single or multiple-headed, and have annual or biennial (winter type) habit. Cultivars also vary in plant height, head shape, size of flower buds, and stem length.

Important horticultural characteristics for broccoli include yield (which is related to uniform field maturity,

and head size and stem weight), and head and stem color (dark green is preferred for processing). Heads should be firm and supported by a deeply branched stem. Domed heads shed water and are less susceptible to head rot than are flat heads. Smooth heads are needed for fresh market, whereas processors prefer segmented heads. The individual branches or florets should be small, firm, and even in maturity and color. Small flower buds (called "beads") are preferred. Defects include uneven flower bud development ("rosetting"), large bead size, loose heads, depression in center of the head, dead flower buds, leaves in head, and yellow color.

Cauliflower cultivars are differentiated mainly by maturity as previously described. Curds are commonly white, but may also be green, orange, or purple. Summer and some winter types have been selected for leaves that wrap tightly about the head to facilitate curd blanching, while tropical types may lack adequate wrapper leaves for self-blanching. For some cultivars, field workers must break or band the wrapper leaves to provide adequate covering for the curd. Cauliflower is perhaps the most fickle of the cole crops to grow because of its exacting climatic requirements.

Important horticultural characteristics include head size (medium is preferred for fresh market, but it can be large for processing), head weight (less cavity space is better), and large, clasping wrapper leaves that prevent curd exposure. Yield depends on good cover, which permits heads to grow larger before exposure. Heads must be pure white for processing and fresh market. Uniform maturity is important but difficult to achieve, even in F₁hybrids. Over-mature heads will begin to show curd differentiation ("riciness"). Heads should be free from leaves.

Brussels sprouts are late maturing biennials. The main difference among cultivars is in stem length and maturity. Shorter types, while earlier maturing, also tend to be lower yielding than the tall types. For processing, sprouts should be firm and about 1.5 to 3 cm in diameter. Cultivars may have green or purple sprouts.

Cultivar types. Cole crop landraces and cultivars were originally open-pollinated populations, consisting of genetically heterogeneous individuals. Such populations are subject to inbreeding depression in subsequent growing seasons if the grower saves seeds from too few individuals. Some open-pollinated cultivars are still grown, but the majority of contemporary cultivars are F₁ hybrids. Breeders develop inbreds, which are then planted in isolation in pairs to produce the F₁ hybrid seed, relying on self-incompatibility or cytoplasmic male sterility to enforce outcrossing.

Isolation of one-half to one mile between seed fields is required to prevent unwanted cross pollination. Any combination of B. oleracea crops and their wild forms may cross with one another and produce contaminants in a seed lot. B. oleracea does not need to be isolated from B. rapa, B. juncea, B. nigra, B. napus, and Raphanus sativus because these species will cross only with great difficulty.

Phytonutrient constituents. The Greeks and Romans recognized the nutritional and medicinal benefits of cole crops. Today, cole crops are recommended for increased consumption by people in developed countries. Cole crops supplement staple foods of higher caloric value with protein, vitamins, minerals, and dietary fiber. While epidemiological studies have demonstrated the health benefits of cole crops, they do contain some antinutritional constituents.

The vegetable parts of the cole crops have a high water content, are low in lipids and carbohydrates, and as a consequence, have relatively low caloric value (Table 2). They are most notable as a source of soluble and insoluble fiber, calcium and potassium, vitamin C, folate, and carotenoids (b-carotene [beta-carotene] and lutein) when compared to other vegetables of similar water content. Although the protein level is low, cole crops do contain significant levels of the essential sulfur-containing amino acid methionine, but not cysteine.

Several compounds give cole crops their characteristic flavor, and affect health and nutrition (Table 3). Glucosinolates and their breakdown products are the best characterized of these compounds. Glucosinolates are a class of sulfur-containing glucosides of which about fifteen

occur in significant quantities in the Brassicaceae. Within a given species, only three or four glucosinolates may be present in high concentrations. Glucosinolates are found in all Brassica tissues, and are generally highest in seeds, intermediate in young vegetative tissues, and lowest in older vegetative tissues. Myrosinase metabolizes glucosinolates to various isothiocyanates. Normally stored apart from glucosinolates in myrosin cells, myrosinase only comes into contact with its substrate when cells are ruptured. The type of isothiocyanate formed depends on the composition of the precursor glucosinolates, the pH, and the presence of certain cofactors such as ferrous iron. Glucosinolates have little flavor; rather, the breakdown products are responsible for the characteristic flavors of the cole crops. In their most extreme form and concentration, isothiocyanates cause the pungency of horseradish. In the cole crops, these compounds in too high a concentration may impart a bitter or "spicy" flavor. The wild cole crop progenitor has fairly high glucosinolate concentrations, which have been reduced in the domesticated species.

Glucosinolate-derived compounds have both positive and negative nutritional effects. Isothiocyanates are goitergenic in animals and people if consumed in sufficient quantities. In brussels sprouts, degree of bitterness correlates with level of the isothiocyanate goitrin, so named because of past association with goiter.

On the positive side, epidemiological studies have demonstrated that a diet high in fruits and vegetables, and in Brassica vegetables in particular, limits the risk of certain cancers. Glucosinolates may prevent cancer by acting as metabolic detoxicants to facilitate alteration and excretion of cell carcinogens. Sulphoraphane, a sulphinylcontaining isothiocyanate, is a strong inducer of the phase II enzymes responsible for anticarcinogenic activities. While sulphoraphane is found in most cole crops, sprouted broccoli seeds have the highest concentrations. This finding by Paul Talalay's group at John Hopkins University has stimulated the commercial production of broccoli sprouts.

Glucosinolate-derived indole compounds are inducers of liver and intestinal enzymes that reduced tumor formation in rats. Timing is critical, in that while these compounds were effective when ingested prior to the carcinogen, administration after introduction of the carcinogen increased carcinogenesis in rainbow trout.

Other compounds of nutritional importance are flavonoids and S-methylcystine sulfoxide. Broccoli contains relatively high levels of the anticarcinogenic flavonoids kaempfrol and quercetin. Purple cabbage and other purple-or red-pigmented cole crops contain various anthocyanins. While anthocyanins in other crops

have shown anticarcinogenic properties, similar studies have not been carried out for cole crop anthocyanins. S-methylcystine sulfoxide is hydrolyzed by cystine lyase to methyl methanethiosulphinate, a compound that is similar to allyl thiosulphinate found in garlic. These compounds influence flavors, and are anticarcinogenic. Because of the similarities, and the health benefits found associated with these compounds in Allium, further study is warranted in the Brassica.

History

Original extent and domestication. The wild progenitor of Brassica is found on the rocky Atlantic coasts of Europe (Bay of Biscay) and Britain. Researchers now believe that the free living B. oleracea populations found along the Mediterranean coast are feral and weedy escapes from cultivation. Related wild Mediterranean species (B. cretica, B. insularis, B. montana, and B. ruprestris ) may have contributed genetically to the domesticated crops, although molecular data does not support this hypothesis. Definitive archaeological evidence is lacking, but the crop was almost certainly a late domesticate compared to the primary domesticates of the Near East center such as emmer wheat, barley, pea, and lentil.

Different cole crops were likely domesticated in different places at different times, and multiple domestication within a type cannot be ruled out. More recent hybridizations among different types further complicate the picture. Leafy kales and nonheading cabbages were most likely the first domesticates, with some researchers hypothesizing that separate domestications occurred from Greece to Wales. "Stemkales" and headed and sprouting cabbages were described by Greek and Roman writers, although it is unclear whether these crops were the ancestors to the modern cabbage and broccoli. Domestication occurred prior to 1000 b.c.e., and possibly a millennia or more earlier. Broccoli and cauliflower are recent domesticates (possibly as old as 500 b.c.e.) from the eastern Mediterranean, and perhaps as localized as Cyprus and Sicily. The first clear description of broccoli and cauliflower was written about 1100 c.e. in Spain. Brussels sprouts were domesticated in northern Europe (some say Belgium) in about the fourteenth century. Early herbals depicted a kale with enlarged leaf axil buds, inferring that brussels sprouts were derived directly from kale. Kohlrabi may have been derived from marrowstem kale, or from a cross of marrowstem kale with cabbage. The origin of collards is closely associated with cabbage; whether collards are an ancestor or descendant of cabbage is unknown.

Historical diffusion. From Europe and the Mediterranean, cabbage and kale dispersed into Mesopotamia and Egypt. These crops later spread throughout the Old World along trade routes, eventually reaching China where distinctive kale and broccoli types were to compete with the B. rapa cabbages of East Asian origin. When trade with the New World began, all of the cole crops were taken to the Americas. In the tropics, cole crops were widely accepted, except for broccoli, which does not form heads under tropical conditions.

Broccoli and cauliflower diffused from the Mediterranean (cauliflower earlier than broccoli) to elsewhere in the Near East, northern Africa, and Europe. Cauliflower was mentioned in Turkey and Egypt in the sixteenth century and in England and France in the seventeenth century. Both broccoli and cauliflower were first described in the United States in 1806, but production did not flourish until the 1920s. The broccoli industry became established about 1923 when the D'Arrigo Brothers Company began growing broccoli in California and catering to the large Italian immigrant population on the East Coast. Interest in broccoli in central and northern Europe increased after the crop became popular in the United States, and worldwide, broccoli production is increasing.

Procurement

Agriculture and crop husbandry. The majority of cole crop hectarage is found in the milder growing areas. The optimum growing season is determined by an interaction among latitude, altitude, and time of the year, as well as proximity to temperature-moderating oceans and lakes. In the United States, most of the cole crops for processing are produced at northern latitudes (New York, Wisconsin, Oregon, and Washington), the exception being California. The leading state for fresh market production is California, followed by New York, Georgia, Arizona, Texas, and Florida. Winter production in the United States of cole crops is done in Florida, Texas, and California. In the subtropics and tropics, cole crops are generally produced at higher altitudes. Commercial cauliflower production is restricted to the maritime climates of the United States because of its sensitivity to heat during curd formation.

For commercial production, the crops are generally grown in monoculture in 50–75 cm rows with within row spacing of 15–30 cm. Crops may be direct seeded or transplanted. Direct seeding is cheaper, but transplanting generally produces a more even stand with more uniform maturity. Cole crops require about 2.5 cm per week of moisture applied regularly throughout the season. In most production areas, natural precipitation is supplemented with irrigation.

Optimum soil pH is 5.5–6.5. Liming low pH fields improves micronutrient uptake and reduces incidence of club root. Plentiful amounts of nitrogen, potassium, and phosphorus are required for optimum plant growth. Nitrogen may be applied as a split application. Cole crops require adequate quantities of boron, calcium, and magnesium.

Harvesting and packing. Cabbage may be hand-or machine-harvested. Generally, heads intended for fresh market are hand-harvested, while those destined for storage or sauerkraut are mechanically harvested.

Broccoli and cauliflower are entirely hand-harvested. The greatest impediments to automating harvest are lack of cultivars with suitable plant architecture and a nonuniform maturity across a field. Even with F₁ hybrids and transplants, microenvironment differences will cause differential maturation in different parts of the field. Growers typically harvest two or three times at several-day intervals to maximize harvest of heads at optimum maturity. Attempts to develop a selective harvester for these crops have not been successful to date.

Brussels sprouts may be hand-or partially machine-harvested. The lower buds on the plant mature before those on the upper portion of the stem. Sprouts are harvested by hand at three or four-week intervals during the growing season by breaking the petioles of the lower leaves, then snapping the mature sprouts. If a single harvest is desired, the terminal growing point is removed when sufficient height and lower bud development has been achieved. Upper buds will then catch up with lower buds in growth, resulting in near-uniform-sized sprouts along the stem. Plants are then cut in the field; the leaves are removed and sprouts are sheared from the stalk using a sprout cutter.

In large-scale operations, broccoli, cauliflower, and cabbage harvested for fresh market are packed in the field. After broccoli heads are cut from the plant, leaves are removed and a mechanical cutting and banding machine is used to trim the stems to 15–20 cm in length. Two to four heads are bundled using rubber bands or a twist-tie. The prepared heads are then packed in a box and quickly cooled to 32°F (0°C) using slurry ice (40% ice and 60 percent water), which is hosed directly into the box. Cauliflower heads are harvested for fresh market when they grow to 15–20 cm in diameter. They are trimmed of most leaves (leaving a few basal leaves to protect the heads from damage), sorted to uniform size (typically six, twelve, or twenty-four heads per crate), and packed into crates or cartons. Individual heads may be wrapped with perforated film. Cauliflower is cooled to 32–36°F (0–2°C) for shipping and storage. Cabbage heads are harvested when firm and 1–1.5 kg in weight. Wrapper leaves are trimmed and heads are sorted and packed into crates or cartons and cooled to 32–36°F (0–2°C). Vacuum cooling, rather than slurry ice, is used to cool cabbage and cauliflower. Hand-harvested brussels sprouts are carried from the field in containers, washed and sorted for size and firmness, and quickly cooled (usually vacuum cooling) to 32°F (0°C). Sprouts are packaged in cellophane bags or baskets.

Storage and Processing. All of the cole crops are stored at near freezing, typically 30–36°F (–1–2°C) and at high (90–100 percent) relative humidity. Cabbage can be stored up to four months under ambient conditions and up to six months in modified atmosphere storage. Broccoli can be stored for only one to two weeks, cauliflower for two to three weeks and brussels sprouts for three to four weeks under optimal conditions in normal atmosphere storage.

The cole crops may be preserved by canning, freezing, pickling, dehydration, or fermentation. Broccoli, cauliflower, kale, collards, and brussels sprouts are usually processed by freezing. Cabbage may be dehydrated, or fermented to produce sauerkraut. Brussels sprouts, cabbage, and cauliflower may also be pickled. Kale and collards may be canned.

Seeds of the cole crops, especially broccoli, are consumed as sprouts. Extracts of cabbage-derived anthocyanins are being used commercially as red food colorants.

BIBLIOGRAPHY

Decouteau, Dennis R. Vegetable Crops. Upper Saddle River, N.J.: Prentice-Hall, 2000.

Dickson, Michael H., and D. H. Wallace. "Cabbage Breeding." In Breeding Vegetable Crops. Edited by Mark J. Bassett, pp. 395–432. Westport, Conn.: AVI Publishing Company. 1986.

Fahey, Jed W., Yesheng Zhang, and Paul Talalay. "Broccoli Sprouts: An Exceptionally Rich Source of Inducers of Enzymes That Protect Against Chemical Carcinogens." Proceedings of the National Academy of Sciences, USA 94 (1997): 10367–10372.

Gómez-Campo, C., ed. Biology of Brassica Coenospecies. Amsterdam and New York: Elsevier, 1999.

Hedrick, U.P., ed. Sturtevant's Edible Plants of the World. New York: Dover, 1972.

Luh, Bor Shiun, and Jasper Guy Woodroof, eds. Commercial Vegetable Processing. 2nd ed. New York: Van Nostrand Reinhold, 1988.

Nieuwhof, M. Cole Crops: Botany, Cultivation, and Utilization. London: L. Hill, 1969.

Peirce, Lincoln C. Vegetables: Characteristics, Production, and Marketing. New York: Wiley, 1987.

Rubatsky, Vincent E., and Mas Yamaguchi. World Vegetables: Principles, Production, and Nutritive Values. 2d ed. New York: Chapman and Hall, 1996.

Sauer, Jonathan D. Historical Geography of Crop Plants: A Selected Roster. Boca Raton, Fla.: CRC Press. 1994.

James R. Myers

Cultivars

The term "cultivar" is used to distinguish a kind of vegetable from a botanical variety. Cultivars are things like "Excelsior" broccoli or "Snow Man" cauliflower. Cultivars may be open-pollinated, pure lines or inbreds, or F₁ hybrids. A botanical variety refers to a group of similar cultivars. For example, broccoli is classified as Brassica oleracea var. italica (the botanical variety of the cole family that comes from Italy). Sometimes the term "variety" is used interchangeably with "cultivar." For example, many garden seed catalogs use the term "variety." The terms "open-pollinated," "pure line," "inbred," and "F₁hybrid" refer to the genetic structure of a cultivar. Open-pollinated varieties (often referred to as OPs) are usually a mix of genetically heterozygous plants forming a heterogeneous population. OPs are usually cross-pollinated and can be variable for horticultural traits. If a plant from an OP population is self-pollinated for several generations, it becomes an inbred line. With approximately six generations of self-pollination, a line will become genetically homozygous, and the population will be homogeneous. Crops that are normally self-pollinated (such as beans or peas) are called "pure lines" when inbred. F₁hybrids are developed by crossing two inbred lines. The cross must be repeated to produce F₁ hybrid seed because selfed or crossed seed from the F₁ hybrid will not breed true. F₁ hybrids are genetically heterozygous but form homogenous populations.

Glucosinolate-Derived Compounds

Glucosinolate-derived compounds have also been implicated in plant defense against pathogens and vertebrate and invertebrate pests. While they may deter generalized predators and pathogens, certain pathogens and insects can detoxify these compounds, and they may in fact serve as an attractant. Further research is needed to clarify the complex and varied roles played by glucosinolate-derived compounds. If consumed in moderation, the beneficial effects of cole crops on health far outweigh deleterious effects.

Sauerkraut

Fermenting cabbage to make sauerkraut is an ancient practice. The process is simple, and facilitated long-term storage of the crop. Sauerkraut is made by salting shredded cabbage and placing the mixture in an anaerobic container to ferment. Salt draws moisture from the cabbage leaves to produce a brine solution (ideally 2.25 percent). The brine inhibits growth of most microorganisms but allows certain anaerobic bacteria to propagate. Leuconostoc mesenteroides initiates the process, while others (primarily Lactobacillus, Streptoccocus, and Pediococcus spp.) continue fermentation. There are a number of conditions that need to be met, or a poor quality product will result. Salt must be evenly distributed, otherwise soft or pink kraut will form. Temperature will affect the composition of the microbial population, which in turn determines the pH and mix of flavor components. Temperatures below 18°C will produce sauerkraut with the best flavor, highest acidity, and ascorbic acid. Nonanaerobic conditions will allow yeast and molds to grow, which will impart undesirable flavors and odors, and will cause spoilage. Sauerkraut is preserved by canning. Sauerkraut is typically consumed with meat or poultry, but may also be used in salads. Sauerkraut juice may be blended with other vegetable or fruit juices to produce a novel and pleasing product.

Today, many people mainly associate sauerkraut with a condiment served on their hotdog bun at a baseball game. In northern Europe during the winter and on Western sailing ships, sauerkraut was an essential staple. The pickling process preserved about one-third of the vitamin C contained in the cabbage leaves, and provided a source of this essential vitamin at times when it was unavailable from other foods. For example, Captain Cook carried sauerkraut on his voyages of exploration as a preventative for scurvy. Fermented products, such as kimchi in Korea, which is made with Chinese cabbage (B. rapa ) or Daikon radish (Raphanus sativus ) serve a similar purpose in the temperate Asian world.