A truffle is the fruiting body of a subterranean ascomycete fungus, predominantly one of the many species of the genus Tuber. In addition to Tuber, many other genera of fungi are classified as truffles including Geopora, Peziza, Choiromyces, Leucangium, and over a hundred others. These genera belong to the class Pezizomycetes and the Pezizales order. There are several truffle-like basidiomycetes excluded from Pezizales including Rhizopogon and Glomus. Truffles are ectomycorrhizal fungi and are therefore usually found in close association with tree roots. Spore dispersal is accomplished through fungivores, animals that eat fungi.These fungi have significant ecological roles in nutrient cycling and drought tolerance.
Some of the truffle species are highly prized as food. French gastronome Jean Anthelme Brillat-Savarin called truffles “the diamond of the kitchen”.Edible truffles are held in high esteem in French, Italian, Croatian, Slovene, Ottoman, Middle Eastern and Spanish cuisine, as well as in international haute cuisine. Truffles are cultivated fungiculturally and are also harvested from natural habitats.
The first mention of truffles appears in the inscriptions of the neo-Sumerians regarding their Amorite enemy’s eating habits (Third Dynasty of Ur, 20th century BC) and later in writings of Theophrastus in the fourth century BC. In classical times, their origins were a mystery that challenged many; Plutarch and others thought them to be the result of lightning, warmth and water in the soil, while Juvenal thought thunder and rain to be instrumental in their origin. Cicero deemed them children of the earth, while Dioscorides thought they were tuberous roots.
Rome and Thracia in the Classical period identified three kinds of truffles: the Tuber melanosporum, the Tuber magnificanus and the Tuber magnatum. The Romans, however, did not use these and instead used a variety of fungus called Terfez, also sometimes called a “desert truffle.” Terfez used in Rome came from Lesbos, Carthage, and especially Libya, where the coastal climate was less dry in ancient times. Their substance is pale, tinged with rose. Unlike truffles, terfez have little inherent flavour. The Romans used the terfez as a carrier of flavour, because the terfez tend to absorb surrounding flavours. Indeed, since Ancient Roman cuisine utilized many spices and flavourings, the terfez were appropriate in that context.
Truffles were rarely used during the Middle Ages. Truffle hunting is mentioned by Bartolomeo Platina, the papal historian, in 1481, when he recorded that the sows of Notza were without equal in hunting truffles, but they should be muzzled to prevent them from eating the prize.
Renaissance and modern times
During the Renaissance, truffles regained popularity in Europe and were honoured at the court of King Francis I of France. However, it was not until the 17th century that Western (and in particular French) cuisine abandoned “heavy” oriental spices, and rediscovered the natural flavour of foodstuffs. Truffles were very popular in Parisian markets in the 1780s. They were imported seasonally from truffle grounds, where peasants had long enjoyed their secret. Brillat-Savarin (1825) noted characteristically that they were so expensive they appeared only at the dinner tables of great nobles and kept women. A great delicacy was a truffled turkey.
Truffles long eluded techniques of domestication, as Jean-Anthelme Brillat-Savarin (1825) noted:
The most learned men have sought to ascertain the secret, and fancied they discovered the seed. Their promises, however, were vain, and no planting was ever followed by a harvest. This perhaps is all right, for as one of the great values of truffles is their dearness, perhaps they would be less highly esteemed if they were cheaper.
However, truffles can be cultivated. As early as 1808, there were successful attempts to cultivate truffles, known in French as trufficulture. People had long observed that truffles were growing among the roots of certain trees, and in 1808, Joseph Talon, from Apt (département of Vaucluse) in southern France, had the idea of transplanting some seedlings that he had collected at the foot of oak trees known to host truffles in their root system.
For discovering how to cultivate truffles, some sources now give priority to Pierre II Mauléon (1744–1831) of Loudun (in western France), who began to cultivate truffles around 1790. Mauléon saw an “obvious symbiosis” between the oak tree, the rocky soil and the truffle, and attempted to reproduce such an environment by taking acorns from trees known to have produced truffles, and sowing them in chalky soil. His experiment was successful, with truffles being found in the soil around the newly grown oak trees years later. In 1847, Auguste Rousseau of Carpentras (in Vaucluse) planted 7 hectares (17 acres) of oak trees (again from acorns found on the soil around truffle-producing oak trees), and he subsequently obtained large harvests of truffles. He received a prize at the 1855 World’s Fair in Paris.
These successful attempts were met with enthusiasm in southern France, which possessed the sweet limestone soils and dry, hot weather that truffles need to grow. In the late 19th century, an epidemic of phylloxera destroyed many of the vineyards in southern France. Another epidemic killed most of the silkworms there, too, making the fields of mulberry trees useless. Thus, large tracts of land were set free for the cultivation of truffles. Thousands of truffle-producing trees were planted, and production reached peaks of hundreds of tonnes at the end of the 19th century. In 1890, there were 75,000 hectares (190,000 acres) of truffle-producing trees.
In the 20th century, however, with the growing industrialization of France and the subsequent rural exodus, many of these truffle fields (champs truffiers or truffières) returned to wilderness. The First World War also dealt a serious blow to the French countryside, killing 20% or more of the male working force. As a consequence, newly acquired techniques of trufficulture were lost. Also, between the two world wars, the truffle groves planted in the 19th century stopped being productive. (The average life cycle of a truffle-producing tree is 30 years.) Consequently, after 1945, the production of truffles plummeted, and the prices have risen dramatically. In 1900, truffles were used by most people, and on many occasions. Today, they are a rare delicacy reserved for the rich, or used on very special occasions.
A critical phase of the cultivation is the quality control of the mycorrhizal plants. It takes between 7 and 10 years for the truffles to develop their mycorrhizal network, and only after that the host-plants come into production. Both a complete soil analysis to avoid contamination by other dominant fungus and a very strict control of the formation of mycorrhizae are necessary to ensure the success of a plantation. Total investment per hectare for an irrigated and barrier-sealed plantation (against wild boars) can cost up to €10,000. Considering the level of initial investment and the maturity delay, farmers who have not taken care of both soil conditions and seedling conditions are at high risk of failure.
In New Zealand and Australia
The first black truffles (Tuber melanosporum) to be produced in the Southern Hemisphere were harvested in Gisborne, New Zealand, in 1993.
New Zealand’s first burgundy truffle was found in July 2012 at a Waipara truffle farm. It weighed 330 g and was found by the farm owner’s beagle.
In 1999, the first Australian truffles were harvested in Tasmania, the result of eight years of work. Trees were inoculated with the truffle fungus in the hope of creating a local truffle industry. Their success and the value of the resulting truffles has encouraged a small industry to develop. A Western Australian venture, The Truffle and Wine Company, had its first harvest in 2004, and in 2005 they unearthed a 1-kg (2.2-lb) truffle. In 2008, an estimated 600 kilograms (1,300 lb) of truffles were removed from the rich ground of Manjimup. Each year, the company has expanded its production, moving into the colder regions of Victoria and New South Wales.
In June 2010, Tasmanian growers harvested Australia’s largest truffle from their property at Myrtle Bank, near Launceston. It weighed in at 1.084 kilograms (2 lb 6.2 oz) and was valued at about A$1,500 per kg.
In the United States
While there have been some notable successes in truffle farming in the United States in the recent past, and farmers have planted trees that may produce large harvests in the near future, all current harvests are small scale.
Tom Michaels, owner of Tennessee Truffle, began producing Périgord truffles commercially in 2007.At its peak in the 2008–2009 season, his farm produced about 200 pounds of truffles, but Eastern filbert blight almost entirely wiped out his hazel trees by 2013 and production dropped, essentially driving him out of business.Eastern filbert blight similarly destroyed the orchards of other once promising commercial farmers such as Tom Leonard, also in East Tennessee, and Garland Truffles in North Carolina. Newer farmers such as New World Truffieres clients Pat Long in Oregon and Paul Beckman in Idaho, or Nancy Rosborough of Mycorrhiza Biotech in Gibsonville, NC, are still in the early stages and waiting for their harvests to increase in size. Likewise, Ian Purkayastha of Regalis Foods has set up a small farm in Fayetteville, Arkansas.
The origin of the word truffle appears to be the Latin term tūber, meaning “swelling” or “lump”, which became tufer- and gave rise to the various European terms: Danish trøffel, Dutch truffel, English truffle, French truffe, German Trüffel, Greek τρούφα trúfa, Italian tartufo, Polish trufla, Romanian trufă, Spanish trufa, and Swedish tryffel.
The German word Kartoffel (“potato”) is derived from the Italian term for truffle because of superficial similarities. In Portuguese, the words trufa and túbera are synonyms, the latter closer to the Latin term.
Phylogeny and species
Phylogenetic analysis has demonstrated the convergent evolution of the ectomycorrhizal trophic mode in diverse fungi. The subphylum, Pezizomycotina, containing the order Pezizales, is approximately 400 million years old. Within the order Pezizales, subterranean fungi evolved independently at least fifteen times. Contained within Pezizales are the families Tuberaceae, Pezizaceae, Pyronematacae, and Morchellaceae. All of these families contain lineages of subterranean or truffle fungi. The oldest ectomycorrhizal fossil is from the Eocene about 50 million years ago. This indicates that the soft bodies of ectomycorrhizal fungi do not easily fossilize.Molecular clockwork has suggested the evolution of ectomycorrhizal fungi occurred approximately 130 million years ago.
The evolution of subterranean fruiting bodies has arisen numerous times within the Ascomycota, Basidiomycota, and Glomeromycota.For example, the genera Rhizopogon and Hysterangium of Basidiomycota both form subterranean fruiting bodies and play similar ecological roles as truffle forming ascomycetes. The ancestors of the Ascomycota genera Geopora, Tuber, and Leucangium originated in Laurasia during the Paleozoic era.Phylogenetic evidence suggests that the majority of subterranean fruiting bodies evolved from above-ground mushrooms. Over time mushroom stipes and caps were reduced, and caps began to enclose reproductive tissue. The dispersal of sexual spores then shifted from wind and rain to utilizing animals.
The phylogeny and biogeography of the genus Tuber was investigated in 2008 using internal transcribed spacers (ITS) of nuclear DNA and revealed five major clades (Aestivum, Excavatum, Rufum, Melanosporum and Puberulum); this was later improved and expanded in 2010 to nine major clades using large subunits (LSU) of mitochondrial DNA. The Magnatum and Macrosporum clades were distinguished as distinct from the Aestivum clade. The Gibbosum clade was resolved as distinct from all other clades, and the Spinoreticulatum clade was separated from the Rufum clade.
The truffle habit has evolved independently among several basidiomycete genera.Phylogenetic analysis has revealed that basidiomycete subterranean fruiting bodies, like their ascomycete counterparts, evolved from above ground mushrooms. For example, it is likely that Rhizopogon species arose from an ancestor shared with Suillus, a mushroom forming genus.Studies have suggested that selection for subterranean fruiting bodies among ascomycetes and basidiomycetes occurred in water-limited environments.
The black truffle or black Périgord truffle (Tuber melanosporum), the second-most commercially valuable species, is named after the Périgord region in France. Black truffles associate with oaks, hazelnut, cherry, and other deciduous trees and are harvested in late autumn and winter. The genome sequence of the black truffle was published in March 2010.
Summer or burgundy truffle
The black summer truffle (Tuber aestivum) is found across Europe and is prized for its culinary value. Burgundy truffles (designated Tuber uncinatum, but the same species) are harvested in autumn until December and have aromatic flesh of a darker colour. These associate with various trees and shrubs.
Tuber magnatum, the high-value white truffle or trifola d’Alba Madonna (“Truffle of the White Madonna” in Italian) is found mainly in the Langhe and Montferrat areas of Italy of the Piedmont region in northern Italy and, most famously, in the countryside around the cities of Alba and Asti.A large percentage of Italy’s white truffles also come from Molise.
The “whitish truffle” (Tuber borchii) is a similar species found in Tuscany, Abruzzo, Romagna, Umbria, the Marche and Molise. It is not as aromatic as those from Piedmont, although those from Città di Castello come quite close.
Geopora spp. are important ectomycorrhizal partners of trees in woodlands and forests throughout the world. Pinus edulis, a widespread pine species of the Southwest, is dependent on Geopora for nutrient and water acquisition in arid environments. Like other truffle fungi, Geopora produces subterranean sporocarps as a means of sexual reproduction. Geopora cooperi, also known as pine truffle or fuzzy truffle, is an edible species of this genus.
A less common truffle is “garlic truffle” (Tuber macrosporum).
In the U.S. Pacific Northwest, several species of truffle are harvested both recreationally and commercially, most notably, the Leucangium carthusianum, Oregon black truffle; Tuber gibbosum, Oregon spring white truffle; and Tuber oregonense, the Oregon winter white truffle. Kalapuya brunnea, the Oregon brown truffle, has also been commercially harvested and is of culinary note.
The pecan truffle (Tuber lyonii) syn. texense is found in the Southern United States, usually associated with pecan trees. Chefs who have experimented with them agree “they are very good and have potential as a food commodity”. Although pecan farmers used to find them along with pecans and discard them, considering them a nuisance, they sell for about $160 a pound and have been used in some gourmet restaurants.
The term “truffle” has been applied to several other genera of similar underground fungi. The genera Terfezia and Tirmania of the family Terfeziaceae are known as the “desert truffles” of Africa and the Middle East. Pisolithus tinctorius, which was historically eaten in parts of Germany, is sometimes called “Bohemian truffle”.
Rhizopogon spp. are ectomycorrhizal members of the Basidiomycota and the order Boletales, a group of fungi that typically form mushrooms. Like their ascomycete counterparts, these fungi are capable of creating truffle-like fruiting bodies Rhizopogon spp. are ecologically important in coniferous forests where they associate with various pines, firs, and Douglas-fir. In addition to their ecological importance, these fungi hold economic value as well. Rhizopogon spp. are commonly used to inoculate coniferous seedlings in nurseries and during reforestation.
Hysterangium spp. are ectomycorrhizal members of the Basidiomycota and the order Hysterangiales that form sporocarps similar to true truffles. These fungi form mycelial mats of vegetative hyphae that may cover 25-40% of the forest floor in Douglas-fir forests, thereby contributing to a significant portion of the biomass present in soils. Like other ectomycorrhizal fungi, Hysterangium play a role in nutrient exchange in the nitrogen cycle by accessing nitrogen unavailable to host plants and by acting as nitrogen sinks in forests.
Glomus spp. are arbuscular mycorrhizae of the phylum Glomeromycota within the order Glomerales. Members of this genus have low host specificity, associating with a variety of plants including hardwoods, forbs, shrubs and grasses. These fungi commonly occur throughout the Northern hemisphere.
Members of the genus Elaphomyces are commonly mistaken for truffles.
The mycelia of truffles form symbiotic, mycorrhizal relationships with the roots of several tree species including beech, birch, hazel, hornbeam, oak, pine, and poplar. Mutualistic ectomycorrhizal fungi such as truffles provide valuable nutrients to plants in exchange for carbohydrates. Ectomycorrhizal fungi lack the ability to survive in the soil without their plant host.In fact, many of these fungi have lost the enzymes necessary for obtaining carbon through other means. For example, truffle fungi have lost their ability to degrade the cell walls of plants limiting their capacity to decompose plant litter. Plant hosts can also be dependent on their associated truffle fungi. Studies have demonstrated that Geopora, Peziza, and Tuber spp. are vital in the establishment of oak communities.
Tuber species prefer argillaceous or calcareous soils that are well drained and neutral or alkaline. Tuber truffles fruit throughout the year, depending on the species, and can be found buried between the leaf litter and the soil. The majority of fungal biomass is found in the humus and litter layers of soil.
Most truffle fungi produce both asexual spores (mitospores or conidia) and sexual spores (meiospores or ascospores/basidiospores). Conidia can be produced more readily and with less energy than ascospores and can disperse during disturbance events. Production of ascospores is energy intensive because the fungus must allocate resources to the production of large sporocarps.Ascospores are borne within sac-like structures called asci, which are contained within the sporocarp.
Because truffle fungi produce their sexual fruiting bodies underground, spores cannot be spread via wind and water. Therefore, nearly all truffles depend on mycophagous animal vectors for spore dispersal.This is analogous to the dispersal of seeds in fruit of angiosperms. When the ascospores are fully developed, the truffle will begin to exude volatile compounds that serve to attract animal vectors. For successful dispersal, these spores must survive passage through the digestive tracts of animals. Ascospores have thick walls composed of chitin to help them endure the environment of animal guts. Animal vectors include birds, deer, and rodents such as voles, squirrels, and chipmunks. Many species of trees, such as Quercus garryana, are dependent on the dispersal of sporocarps to inoculate isolated individuals. For example, the acorns of Q. garryana may be carried to new territory that lacks the necessary mycorrhizal fungi for establishment. Some mycophagous animals depend on truffles as their dominant food source. Flying squirrels, Glaucomys sabrinus, of North America play a role in a three-way symbiosis with truffles and their associated plants. Glaucomys sabrinus is particularly adapted to finding truffles using its refined sense of smell, visual clues, and long-term memory of prosperous populations of truffles. This intimacy between animals and truffles indirectly influences the success of mycorrhizal plant species.
After ascospores are dispersed, they remain dormant until germination is initiated by exudates excreted from host plant roots. Following germination, hyphae will form and seek out the roots of host plants. Arriving at roots, hyphae will begin to form a mantle or sheath on the outer surface of root tips. Hyphae will then enter the root cortex intercellularly to form the Hartig net for nutrient exchange. Hyphae can spread to other root tips colonizing the entire root system of the host. Over time, the truffle fungus accumulates sufficient resources to form fruiting bodies. Rate of growth is correlated with increasing photosynthetic rates in the spring as trees leaf out.
In exchange for carbohydrates, truffle fungi provide their host plants with valuable micro and macronutrients. Plant macronutrients include potassium, phosphorus, nitrogen, and sulfur whereas micronutrients include iron, copper, zinc, and chloride. In truffle fungi, as in all ectomycorrhizae, the majority of nutrient exchange occurs in the Hartig net, the intercellular hyphal network between plant root cells. A unique feature of ectomycorrhizal fungi is the formation of the mantle on outer surface of fine roots.
Truffles have been suggested to co-locate with the orchid species Epipactis helleborine and Cephalanthera damasonium., though this is not always the case.
Truffle fungi are ecologically important in nutrient cycling. Plants obtain nutrients via their fine roots. Mycorrhizal fungi are much smaller than fine roots and therefore have a higher surface area and a greater ability to explore soils for nutrients. Acquisition of nutrients includes the uptake of phosphorus, nitrogen, iron, magnesium and other ions. Many ectomycorrhizal fungi form fungal mats in the upper layers of soils surrounding host plants. These mats have significantly higher concentrations of carbon and fixed nitrogen than surrounding soils. Because these mats are nitrogen sinks, leaching of nutrients is reduced. Mycelial mats can also help maintain the structure of soils by holding organic matter in place and preventing erosion. Often these networks of mycelium provide support for smaller organisms in the soil, such as bacteria and microscopic arthropods. Bacteria feed on the exudates released by mycelium and colonize soil surrounding them. Microscopic arthropods such as mites feed directly on mycelium and release valuable nutrients for the uptake of other organisms. Thus, truffle fungi, along with other ectomycorrhizal fungi, facilitate a complex system of nutrient exchange between plants, animals, and microbes.
Importance in arid-land ecosystems
Plant community structure is often affected by the availability of compatible mycorrhizal fungi. In arid-land ecosystems, these fungi become essential for the survival of their host plants by enhancing ability to withstand drought. A foundation species in arid-land ecosystems of the Southwest United States is Pinus edulis, commonly known as pinyon pine. Pinus edulis associates with the subterranean fungi Geopora and Rhizopogon. As global temperatures rise, so does the occurrence of severe droughts detrimentally affecting the survival of arid-land plants. This variability in climate has increased the mortality of P. edulis. Therefore, the availability of compatible mycorrhizal inoculum can greatly affect the successful establishment of P. edulis seedlings. Associated ectomycorrhizal fungi will likely play a significant role in the survival of P. edulis with continuing global climate change.
Because truffles are subterranean, they are often located with the help of an animal possessing a refined sense of smell. Traditionally, pigs have been utilized for the extraction of truffles.Both the female pig’s natural truffle-seeking, as well as her usual intent to eat the truffle, are due to a compound within the truffle similar to androstenol, the sex pheromone of boar saliva, to which the sow is keenly attracted. Studies in 1990 demonstrated that the compound actively recognized by both truffle pigs and dogs is dimethyl sulfide.
In Italy, the use of the pig to hunt truffles has been prohibited since 1985 because of damage caused by animals to truffle mycelia during the digging that dropped the production rate of the area for some years. An alternative to truffle pigs are dogs. Dogs pose an advantage in that they do not have a strong desire to eat truffles and can therefore be trained to locate sporocarps without digging them up. Pigs will attempt to dig up truffles.
Fly species of the genus Suilla can also detect the volatile compounds associated with subterranean fruiting bodies. These flies will lay their eggs above truffles to provide food for their young. At ground level Suilla can be seen flying above truffles.
The volatile constituents responsible for the natural aroma of truffles are released by the mycelia, fruiting body or derive from truffle-associated microbes. The chemical ecology of truffle volatiles is complex, interacting with plants, insects and mammals, which contribute to spore dispersal. Depending on the truffle species, life cycle or location, they include:
- Sulfur volatiles, which occur in all truffle species, such as dimethyl mono- (DMS), di- (DMDS) and tri- (DMTS) sulfides, as well as 2-methyl-4,5-dihydrothiophene, characteristic of the white truffle T. borchii and 2,4-Dithiapentane occurring in all species but mostly characteristic of the white truffle T. magnatum. Some of the very aromatic white truffles are notably pungent, even irritating the eye when cut or sliced.
- Metabolites of non-sulfur amino acid constituents (simple and branched chain hydrocarbons) such as ethylene (produced by mycelia of white truffles affecting root architecture of host tree), as well as 2-methylbutanal, 2-methylpropanal and 2-phenylethanol (also common in baker’s yeast).
- Fatty acid-derived volatiles (C8-alcohols and aldehydes with a characteristic fungal odor, such as 1-octen-3-ol and 2-octenal). The former is derived from linoleic acid, and produced by mature white truffle T. borchii.
- Thiophene derivatives appear to be produced by bacterial symbionts living in the truffle body. The most abundant of these, 3-methyl,4-5 dihydrothiophene, contributes to white truffle’s aroma.
A number of truffle species and varieties are differentiated based on their relative contents or absence of sulfides, ethers or alcohols, respectively. The sweaty-musky aroma of truffles is similar to that of the pheromone androstenol that also occurs in humans. As of 2010, the volatile profiles of seven black and six white truffle species have been studied.
Because of their high price and their pungent aroma, truffles are used sparingly. Supplies can be found commercially as unadulterated fresh produce or preserved, typically in a light brine.
As the volatile aromas dissipate quicker when heated, truffles are generally served raw and shaved over warm, simple foods where their flavor will be highlighted, such as buttered pasta or eggs. Thin truffle slices may be inserted into meats, under the skins of roasted fowl, in foie gras preparations, in pâtés, or in stuffings. Some specialty cheeses contain truffles as well. Truffles are also used for producing truffle salt and truffle honey.
While in the past chefs used to peel truffles, in modern times, most restaurants brush the truffle carefully and shave it or dice it with the skin on so as to make the most of the valuable ingredient. Some restaurants stamp out circular discs of truffle flesh and use the skins for sauces.
Truffle oil is used as a lower-cost and convenient substitute for truffles, to provide flavouring, or to enhance the flavour and aroma of truffles in cooking. Many “truffle oils”, however, do not contain any truffles, while others will include pieces of one of the many inexpensive, unprized truffle varietals, which have no culinary value simply for show. The vast majority is oil which has been artificially flavoured using a synthetic agent such as 2,4-dithiapentane
Because a greater variety of aromatic molecules in truffles are soluble in alcohol, it can be used to carry a more complex and accurate truffle flavour than oil without the need for synthetic flavourings. However, many commercial producers of “truffled” alcohol use 2,4-dithiapentane regardless, as it has become the dominant flavor most consumers, who have never been exposed to fresh truffles but only truffle oils, associate with them. Because most Western nations do not have ingredient labeling requirements for spirits, there is often no way for consumers to know if additional flavorings have been used. Although used as a spirit in its own right and mixed in a range of cocktails, truffle-flavored alcohol is also used by chefs to flavour dishes