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Phallus indusiatus, commonly called in English the bamboo fungus, bamboo pith, long net stinkhorn, crinoline stinkhorn or veiled lady, is a stinkhorn fungus in the Phallaceae family. It has a cosmopolitan distribution in tropical areas, and has been collected in Asia, the Americas, and Africa. The fungus is characterised by a conical to bell-shaped cap on a stipe and a lacy “skirt” that hangs from beneath the cap. Mature fruit bodies are up to 30 cm (12 in) tall with a cap that is 2–4 cm (0.8–1.6 in) long. The cap is covered with a greenish spore-containing slime, which attract flies and other insects that eat the spores and disperse them. It is an edible mushroom used as an ingredient in Chinese haute cuisine; the mushroom is grown commercially and commonly sold in Asian markets. Nutritional analysis has shown that the mushroom is rich in protein, carbohydrates and dietary fiber. The mushroom also contains various bioactive compounds, and has antioxidant and antimicrobial properties.

 

 

 

Taxonomy and naming

Phallus indusiatus was initially described by French naturalist Étienne Pierre Ventenat in 1798,[2] and sanctioned under that name by Christian Hendrik Persoon in 1801.[3] One author anonymously gave his impressions of Ventenat’s discovery in an 1800 publication:

This beautiful species, which is sufficiently characterised to distinguish it from every other individual of the class, is copiously produced in Dutch Guiana, about 300 paces from the sea, and nearly as far from the left bank of the river of Surinam. It was communicated to me by the elder Vaillant, who discovered it in 1755 on some raised ground which was never overflowed by the highest tides, and is formed of a very fine white sand, covered with a thin stratum of earth. The prodigious quantity of individuals of this species which grow at the same time, the very different periods of their expansion, the brilliancy and the varied shades of their colours, present a prospect truly picturesque.[4]

The fungus was later placed in a new genus, Dictyophora, in 1809 by Desvaux;[5] it was then known for many years as Dictyophora indusiata.[6] Christian Gottfried Daniel Nees von Esenbeck placed the species in Hymenophallus in 1817, as H. indusiatus.[7] However, when both Dictyophora and Hymenophallus were variously rendered synonyms of Phallus, the species was reclassified under its original name.[1][6]

Its specific epithet is the Latin adjective indūsǐātus “wearing an undergarment”.[8] The former generic name Dictyophora is derived from the Ancient Greek words diktu- “net”, and pherein “to bear”, hence “bearing a net”.[9] Phallus indusiatus has many common names based on its appearance, including long net stinkhorn, crinoline stinkhorn, bamboo mushroom,[10] basket stinkhorn,[11] bridal veil fungus, or veiled lady.[12] Its Japanese name is Kinugasatake.[13] Alternate common names that refer to its typical growth habitat include “bamboo fungus” or “bamboo pith”, and its Chinese name zhu sheng (竹笙, pinyin: zhúshēng) or zhu sun (竹荪; pinyin: zhúsūn).

Description

Immature fruit bodies of P. indusiatus are egg-shaped to roughly spherical, whitish to pale brown, and up to 5 cm (2.0 in) in diameter.[14] The mature mushroom is up to 30 cm (12 in) tall, and is girded with a net-like structure called the indusium, or “skirt”, which hangs down around 15 cm (6 in) from the conical cap. The netlike openings of the indusium may be polyhedral or round in shape.[15] Well-developed specimens have the indusium reaching the volva and flaring out somewhat before collapsing.[14] The bell-shaped cap is 2–4 cm (0.8–1.6 in) high and covered with a greenish-brown slime termed the gleba. The stalk is 7–25 cm (3–10 in) high and 0.2–0.5 cm in diameter.[15] The method of reproduction for stinkhorns, including P. indusiatus, is different from many mushrooms, which use the air to spread their spores. Stinkhorns instead produce a sticky spore mass on their tip which has a sharp, sickly-sweet odor of carrion to attract bees, and flies.[16] The mature fruiting bodies can be smelled from a considerable distance in the woods, and at close quarters most people find the cloying stink extremely repulsive. The flies land in the gleba and consume the slime, depositing it as excrement elsewhere.[17] In older fungi the slime is eventually removed, leaving the pale off-white, bare pitted and ridged surface exposed.[15] The fruit bodies develop during the night, and are short-lived, typically lasting 1–3 days.[17]

The spores are thin-walled, smooth, ellipsoid, straight to slightly curved in side view, hyaline (translucent), and measure 2–3 by 1–1.5 μm.[18]

The Argentinian mycologist Jorge Eduardo Wright reported finding specimens in Argentina and Bolivia, otherwise identical to the normal variant, with a pink indusium. He named these Dictyophora indusiata var. rosea.[19]

Similar species

Phallus multicolor is similar in overall appearance, but it has a more brightly colored cap, stem and indusiatum, and it is usually smaller. It is found in Australia, Guam, Sumatra, Java, Borneo, Papua New Guinea, Zaire, and Tobago [20] as well as Hawaii. The cap of the Indo-Pacific species Phallus merulinus appears smooth when covered with gleba, and is pale and wrinkled once the gleba has worn off. In contrast, the cap surface of P. indusiatus tends to have conspicuous reticulations that are not obscured even when covered with gleba. Also, the indusium of P. merulinus is more delicate and shorter than that of P. indusiatus, and thus less likely to collapse under its own weight.[21] P. cinnabarinus, a Taiwanese species found under the bamboo Dendrocalamus latiflorus, grows to 13 cm (5.1 in) tall, and has a more offensive odor than P. indusiatus. It attracts flies from the genus Lucida, rather than the house flies of the genus Musca that prefer P. indusiatus.[22] P. echinovolvatus, described from China in 1988, is closely related to P. indusiatus, but can be distinguished by its volva which has an echinulate (spiky) surface, and its higher preferred growth temperature of 30 to 35 °C (86 to 95 °F).[23]

Distribution and habitat

The range of Phallus indusiatus is tropical, including Africa (Congo,[14] Nigeria,[24] Uganda,[25] and Zaire[26]) South America (Brazil[18] Guyana,[27] and Venezuela[28]), Central America (Costa Rica),[29] and Tobago.[30] In North America, its range is restricted to Mexico.[31] Asian localities include Indonesia, Malaysia,[32] southern China, Japan,[17] and Taiwan.[33] It has also been collected in Australia.[34] Like all Phallus species, the fungus is saprobic—deriving nutrients from breaking down wood and plant organic matter. It tends to grow in disturbed ground and among wood chips. In Asia, it grows among bamboo forests, and is typically found after heavy rains.[17][35]

Uses

Edibility

Previously only collected in the wild, where it is uncommon, P. indusiatus was rare and difficult to procure. The mushroom’s rarity meant that it was usually reserved for special occasions. In the time of China’s Qing Dynasty, the species was collected in Yunnan Province and sent to the Imperial Palaces to satisfy the appetite of Empress Dowager Cixi, who particularly enjoyed meals with edible fungi.[36] It was one of the eight featured ingredients of the “Bird’s Nest Eight Immortals Soup” served at a banquet to celebrate her 60th birthday.[37] Another notable use was a banquet held for Henry Kissinger on his visit to China to reestablish diplomatic relations in the early 1970s.[38] One source writes of the mushroom: “It has a fine and tender texture, fragrance and is attractive, beautiful in shape, fresh and crispy in taste.”[39] The dried fungus, commonly sold in Asian markets, is prepared by rehydrating and soaking or simmering in water until tender.[40]

Phallus indusiatus has been cultivated on a commercial scale in China since 1979.[38] In the Fujian Province of China—known for a thriving mushroom industry that cultivates 45 species of edible fungi—P. indusiatus is produced in the counties of Fuan, Jianou, and Ningde.[41] Advances in cultivation have made the fungus cheaper and more available; in 1998, about 1,100 metric tons (1,100 long tons; 1,200 short tons) were produced in China.[10] The Hong Kong price for a kilogram of dried mushrooms reached around US $770 in 1982, but had dropped to US $100–200 by 1988. Further advances led to it dropping further to US $10–20.[38] The fungus is grown on agricultural wastes—bamboo-trash sawdust covered with a thin layer of non-sterilized soil. The optimal temperature for the growth of mushroom spawn and fruit bodies is about 24 °C (75 °F), with a relative humidity of 90–95%.[42] Other substrates which can be used for the cultivation of the fungus include bamboo leaves and small stems, soybean pods or stems, corn stems, and willow leaves.[43]

Nutritional composition Phallus indusiatus, egg stage (dry weight)[24]
Nutritional value per 100 g (3.5 oz)
Energy  ?
Fat 1.66
Protein 33.6
Calcium 61.0 mg (6%)
Iron 36.6 mg (282%)
Magnesium 156 mg (44%)
Manganese 5.1 mg (243%)
Potassium 153. mg (3%)
Sodium 5.1 mg (0%)
Zinc 133.0 mg (1400%)
Percentages are relative to US recommendations for adults.

Jonathan and colleagues have performed a nutritional analysis of P. indusiatus, based on specimens collected from Nigeria. They determined that the egg stage of the fungus contains (per 100 g of fungus, dry weight) 33.6 g of crude protein, 1.66 g of fat, and 3.98 g of carbohydrates. The egg stage was also measured to comprise 20.9 g crude fiber, and 88.76% moisture. The high levels of protein and fiber (which are comparable to values found in meat and vegetables, respectively) suggest that the egg form of P. indusiatus is a good food source. The concentration of several mineral elements, including potassium, sodium, and iron was also favorable compared to fruits and vegetables, although the authors mention that mineral composition in the fungus is dependent on their corresponding concentrations in the soil in which they grow.[24]

Bioactive compounds

The fruit bodies of the fungus contain biologically active polysaccharides. A β-D-glucan called T-5-N, prepared from alkaline extracts,[44] has been shown to have anti-inflammatory properties.[45] The chemical structure of the polysaccharide was found to have a linear chain backbone made largely of α-1→3 linked D-mannopyranosyl residues, with traces of 1→6 linked D-mannopyrosyl residues.[13] The polysaccharide has exhibited tumor-suppressing activity against subcutaneously implanted sarcoma 180 (a transplantable, non-metastasizing connective tissue tumor often used in research) in mice.[45][46]

P. indusiatus contains the chemical 5-(hydroxymethyl)-2-furfural (also known as hydroxymethylfurfural).[47] This compound inhibits tyrosinase, an enzyme that catalyzes the initial steps of melanogenesis in mammals, and is responsible for the undesirable browning reactions in damaged fruits during post-harvest handling and processing.[48] For these reasons, researchers are interested in finding effective tyrosinase inhibitors for the medical, cosmetics, and food industries. Hydroxymethylfurfural occurs naturally in several foods, and is not associated with serious health risks.[47] P. indusiatus also contains a unique ribonuclease (RNase)—an enzyme that cuts RNA into smaller components. The enzyme has several biochemical characteristics that differentiate it from other known mushroom RNases: a unique N-terminal sequence of peptides; an unusual sensitivity to heat, whereby enzyme activity is completely lost after 10 minutes at 100 °C (212 °F); optimal enzyme activity at an acidic pH (4–4.5); and specificity towards RNAs containing sequences with continuous stretches of uracil (polyU) and adenine (polyA).[49]

Two novel sesquiterpenes have been identified from the fruit bodies of the fungus, named dictyophorine A and B. These compounds are based on the eudesmane skeleton (a common structure found in plant-derived flavors and fragrances), are the first eudesmane derivatives isolated from fungi. The dictyophorines promote the synthesis of nerve growth factor in astroglial cells.[50] Other similar compounds isolated and identified from the fungus include the quinazoline compounds named dictyoquinazoles A, B and C.[51] These chemicals—belonging to a class of compounds known to be rare in nature—were shown in laboratory tests to have a protective effect on cultured mouse neurons that had been exposed to neurotoxins.[52] A total synthesis for the dictyoquinazoles was reported in 2007.[53]

Extracts of P. indusiatus have been shown to have both antioxidant and antimicrobial properties.[12][54] Mushroom extracts were tested against a variety of bacteria and fungi pathogenic to humans, and in some cases had antimicrobial activity comparable to the antibiotics ampicillin, tetracycline, and nystatin. The antioxidant effect of the fungus is due to a class of molecules known as polyphenols; this class of compounds, common in some types of legumes and fruits, plays a role in reducing cellular damage resulting from oxidative stress.[12]

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