Tulip breaking virus[lower-alpha 1] is one of five plant viruses of the family Potyviridae that cause color-breaking of tulip flowers. These viruses infect plants in only two genera of the family Liliaceae: tulips (Tulipa) and lilies (Lilium).
Also known as the tulip break virus, lily streak virus, lily mosaic virus, or simply TBV, tulip breaking virus is most famous for its dramatic effects on the color of the tulip perianth, an effect highly sought after during the 17th-century Dutch "tulip mania".[3]
Tulip breaking virus is a potyvirus.[4] A distant serological relationship between Tulip breaking virus and tobacco etch virus was discovered in 1971.[5]
Tulip breaking virus (TBV), tulip top-breaking virus (TTBV), tulip bandbreaking virus (TBBV), Rembrandt tulip-breaking virus (ReTBV), and lily mottle virus (LMoV) have all been identified as potyviruses by serology and potyvirus-specific polymerase chain reaction (PCR). In addition, sequence analysis of amplified DNA fragments has classified them all as distinct viruses or strains; recently TTBV has been found to be strain-related to turnip mosaic virus.[6]
Effects of the virus
The virus infects the bulb and causes the cultivar to "break" its lock on a single color, resulting in intricate bars, stripes, streaks, featherings or flame-like effects of different colors on the petals. These symptoms vary depending on the plant variety and age at the time of infection. Different types of colour-breaks depend on the variety of tulip and the strain of the virus. The color variegation is caused either by local fading, or intensification and overaccumulation of pigments in the vacuoles of the upper epidermal layer due to the irregular distribution of anthocyanin; this fluctuation in pigmentation occurs after the normal flower color has developed. Because each outer surface is affected, both sides of the petal often display different patterns.[citation needed]
In the lily species, the virus causes mild to moderate mottling or streaking in the leaves about two weeks after inoculation, and then causes the plant to produce distorted leaves and flowers.[7]
The virus also weakens the bulb and retards the plant's propagation through offset growths; as it progresses through each generation the bulb grows stunted and weak. Eventually it has no strength to flower, and either breaks apart or withers away, ending the genetic line. For this reason the most famous examples of tulips from color-break bulbs– the Semper Augustus and the Viceroy– no longer exist.[8]
History
Gouache on paper drawing, before 1640, of the Semper Augustus, famous for being the most expensive tulip sold during tulip mania. The effects of Tulip breaking virus are seen in the striking streaks of white in its red petals.
Long thought to be the earliest recorded plant virus, it is now thought that TBV comes second; the earliest reference to a virus-induced leaf chlorosis (possibly tobacco leaf curl virus) was recorded in Japan in 752 AD.[9]
"Breaking" symptomology was first described in 1576 by Carolus Clusius, a Flemish professor of Botany at Leiden, who noted the variegation, or "rectification", so termed because it was believed that with the offset production of an entirely new "broken" bloom the plant was distilling, or rectifying, itself into a pure life form.[10][11]
Clusius's observations continued; in 1585, he was the first to note that "broken" plants also slowly degenerated. "...any tulip thus changing its original colour is usually ruined afterwards and so wanted only to delight its master's eyes with this variety of colours before dying, as if to bid him a last farewell."[12] It was not known that the virus was responsible for this effect, so for centuries breeders believed that it was environmental conditions that attenuated the bulb and caused single colour tulips to break and streak. They tried to induce "rectification" through frequent soil changes (causing the bulb to go to seed); varying the planting depths so the plant had to struggle in too much or too little soil; applying too much or too little manure; using soil that was either too poor or too rich; or storing the bulbs in exposed conditions so that they would be 'acted' upon by the rain, wind, sun, and extremes of temperature. However, as early as 1637 Dutch growers were able to produce new broken varieties through bulb grafting, by combining "broken" bulbs infected with the virus with healthy bulbs that produced uniformly colored flowers.[13]
At the end of the eighteenth century, the notion that "breaking" in tulips was a manifestation of some kind of chronic disorder or weakness in the bulb was certainly considered among botanists; but it was still more or less believed that adverse environmental conditions were to blame. A comment by William Hanbury in 1770 that: "All variegations are diseases in a plant and nothing is so proper to bring this about as a defect in nutriment."[14] bears out this general attitude. Given the lack of knowledge of human infectious diseases at this time (and well into the 19th century) this was not an unusual conclusion,[15] but what is surprising is that while tulip mosaic disease has a far more impressive and documented history than any other plant virus, the realization that it was a communicable plant disease, let alone a virus, came surprisingly late– a decade after the end of World War I. "Plant virus" to plant pathologists at the time was almost synonymous with the tobacco mosaic virus, which had been discovered in 1897, quite soon after bacteriology had become established as an academic subject. Since the prime characteristics of the tobacco mosaic virus are that it damages the leaves and flowers of the plant, stunts growth, and lowers quantity and quality of the crop, it is puzzling to many academics and scientists that twenty more years passed before "breaking" was even suspected of being virus-induced.[16]
Pathogen discovery
By the mid-1920s, biochemistry was coming into its own, and its impact was felt in virus research. Eventually, it was a series of bulb manipulation experiments begun in 1928 by Dorothy Cayley at the John Innes Horticultural Institution in Merton, South London, England that led to the discovery of the virus. The record of Cayley's experiments are held at the Institution's current location in Norfolk. Caley discovered that by mechanically transferring infected tissue from broken bulbs to healthy bulbs during their dormant state, the virus that caused the break in color would also be transferred.[17] These experiments were further refined down to minute amounts, which led her to correctly conclude that the "virus or enzyme infection" was sap-transmissible, probably transferred by an insect, and the degree of breaking was proportional to the amount of infected tissue introduced.[18]
The virus was eventually proved to be transferred in a non-persistent manner by at least four species of aphids, specifically Myzus persicae (the most efficient), Macrosiphum euphorbiae, Aphis fabae, and Aphis gossypii. McKenny-Hughes reported in 1934 that Dysaphis tulipae transmitted the virus between stored tulip bulbs, but this has not been confirmed.[1] The transfer of the virus is non-persistent, which means it is accomplished through the insect feeding. In non-persistent transmission, viruses become attached to the distal tip of the stylet in the insect's mouthparts, so that the next plant it feeds on is inoculated with the virus.[19] The virus does not affect the seed that produces a bulb, only the bulb itself, its leaves and blooms, and its daughter offsets.
It was not until the 1960s that TBV was shown to have flexuous filamentous particles (mostly measuring about 12×750nm) and finally proved to be a virus. The genetic code of TBV has now been sequenced and the virus is recognized as a member of the genus Potyvirus (family Potyviridae). Understanding the genetic diversity of viruses that cause similar symptoms continues to be refined.[20] Like other members of the genus it is now readily detected and identified by serological, molecular, and optical techniques.[17][21][22]
Viral strains
Two separate strains of the virus– Severe Tulip Breaking Virus (STBV) and Mild Tulip Breaking Virus (MTBV)– have been determined by the type and severity of the symptoms they cause.[1] In certain varieties STBV causes full breaking or light breaking, when due to a lack of anthocyanin, pigment present in the surface chromoplast cells fades and the lighter color (white or yellow) of the internal mesophyll is exposed, appearing as irregular streaks or fine featherings. In the same varieties MTBV causes self breaking or dark breaking, which occurs because anthocyanins are formed in excess, so the color in the epidermal cells is intensified in dark streaks or elongated flecks and sworls. Breaking commonly occurs along the edges and tops of petals and sepals. The most common type of breaking found in naturally infected plants, called average break, is caused by infection with a mixture of STBV and MTBV; both light breaking and dark breaking symptoms are present, together with some unbroken areas, in different parts of the same petal. Plants infected with a mixture of strains when young may exhibit both effects, with light breaking symptoms restricted to the basal part of the petal and severe dark breaking effects in the upper parts.[1] Some varieties were later found to be incapable of light breaking, and always showed dark breaking symptoms no matter whether infected with STBV or MTBV or a mixture of both strains.[23][failed verification] Although they still can be infected, white and yellow flowered varieties are incapable of breaking since they lack anthocyanins; their color is determined by colourless or yellow plastids in the mesophyll.[1] Other outward symptoms can include leaf mottling.[24]
Distribution
Control of the virus is notoriously difficult. Its distribution is world-wide and had been reported in all temperate regions where tulips are grown; it is particularly common in southern Europe where the aphid vectors are abundant early in the growing season. Virus transmission by aphids causes millions of dollars of damage in the flower bulb sector annually. Mineral oils and pyrethroids are applied weekly during the growth season to decrease the virus transmission in flower bulbs, and current research projects are attempting to learn about the risk of non-persistent virus transmission in relation to aphid population dynamics.[25]
Most recently, population dynamics of aphids in tulip fields were monitored during three growing seasons. Simultaneously, the period of TBV transmission by aphids was investigated experimentally by exposing small tulip plots during specified intervals to naturally occurring aphids. Finally, timing of virus spread was correlated with aphid population dynamics and weather conditions. In 2007 it was discovered that TBV transmission started in April, while the first aphids were not found until May. Apparently, the first aphids of the season had already contributed, in great extent, to the virus transmission, which was observed locally in the tulip plots. In addition, a second, but distinct, TBV isolate was identified, which resulted in the design of an improved TBV detection assay. These results should enable formulation of crop protection guidelines that are fine-tuned with the risk of virus transmission, which will help decrease environmental damage caused by pesticides.[25]
In an effort to restrict the virus, the United States, Great Britain and other countries prohibit the commercial sale of broken bulbs, or bulbs known to be infected by the virus. As TBV-infected bulbs gradually degenerate, the virus can be minimized by removing and destroying 'broken' bulbs quickly before aphids spread the virus to other bulbs or cross-contaminating lily hosts.
Broken tulips today
Today, tulips like Rem's Sensation displaying a "broken" effect are stable variants and the result of breeding, not viral infection,[26] although many tulip fanciers feel these "modern" variants are a poor substitute when compared to the long-extinct rare cultivars like Semper Augustus.[27] Modern tulip varieties infected with the virus are fragile, and are usually much smaller than normal healthy blooms, with a reduced stem length. There are only a few varieties of older, truly "broken" tulips still in existence such as Zomerschoon, but only because the worst aspects of the virus have somehow remained benign. One such example is the rare Absalon, which dates from 1780; a "bizarre" colored variety, it displays gold flames against a dark chocolate brown background.[28]
Plum pox, also known as sharka, is the most devastating viral disease of stone fruit from the genus Prunus. The disease is caused by the plum pox virus (PPV), and the different strains may infect a variety of stone fruit species including peaches, apricots, plums, nectarine, almonds, and sweet and tart cherries. Wild and ornamental species of Prunus may also become infected by some strains of the virus.
Zucchini yellow mosaic virus (ZYMV) is an aphid-borne potyvirus, regarded as a major pathogen of cucurbits in most regions of the world where these crops are cultivated.
Lettuce mosaic virus (LMV) is a typical potyvirus, which causes one of the major virus diseases of lettuce crops worldwide.
Potyvirus is a genus of positive-strand RNA viruses in the family Potyviridae. Plants serve as natural hosts. Like begomoviruses, members of this genus may cause significant losses in agricultural, pastoral, horticultural, and ornamental crops. More than 200 species of aphids spread potyviruses, and most are from the subfamily Aphidinae. The genus contains 190 species and potyviruses account for about thirty percent of all currently known plant viruses.
Papaya ringspot virus (PRSV) is a pathogenic plant virus in the genus Potyvirus and the virus family Potyviridae which primarily infects the papaya tree.
Bidens mottle virus (BiMoV) is a pathogenic plant virus in the plant virus family Potyviridae. BiMoV is a flexuous filamentous particle, 720 nm long, and belongs to the Potyviridae genus Potyvirus. Like other viruses in this genus, Bidens mottle virus is transmitted both mechanically by sap and by aphids in a stylet-borne fashion.
Pepper mottle virus (PepMoV) is a plant pathogenic virus in the genus Potyvirus and the virus family Potyviridae. Like other members of the Potyvirus genus, PepMV is a monopartite strand of positive-sense, single-stranded RNA surrounded by a capsid made for a single viral encoded protein. The virus is a filamentous particle that measures about 737 nm in length. Isolates of this virus has been completely sequenced and its RNA is 9640 nucleotides long. This virus is transmitted by several species of aphids in a nonpersitant manner and by mechanical inoculation.
Potato virus Y (PVY) is a plant pathogenic virus of the family Potyviridae, and one of the most important plant viruses affecting potato production.
Tobacco etch virus (TEV) is a plant virus in the genus Potyvirus and family Potyviridae. Like other members of the genus Potyvirus, TEV has a monopartite positive-sense, single-stranded RNA genome surrounded by a capsid made from a single viral encoded protein. The virus is a filamentous particle that measures about 730 nm in length. It is transmissible in a non-persistent manner by more than 10 species of aphids including Myzus persicae. It also is easily transmitted by mechanical means but is not known to be transmitted by seeds.
Soybean mosaic virus (SMV) is a member of the plant virus genus Potyvirus. It infects mainly plants belonging to the family Fabaceae but has also been found infecting other economically important crops. SMV is the cause of soybean mosaic disease that occurs in all the soybean production areas of the world. Soybean is one of the most important sources of edible oil and proteins and pathogenic infections are responsible for annual yield losses of about $4 billion in the United States. Among these pathogens, SMV is the most important and prevalent viral pathogen in soybean production worldwide. It causes yield reductions of about 8% to 35%, but losses as high as 94% have been reported.
Tulips are spring-blooming perennial herbaceous bulbiferous geophytes in the Tulipa genus. Their flowers are usually large, showy, and brightly coloured, generally red, orange, pink, yellow, or white. They often have a different coloured blotch at the base of the tepals, internally. Because of a degree of variability within the populations and a long history of cultivation, classification has been complex and controversial. The tulip is a member of the lily family, Liliaceae, along with 14 other genera, where it is most closely related to Amana, Erythronium, and Gagea in the tribe Lilieae.
Apium virus Y (ApVY) is a plant pathogenic virus in the genus Potyvirus and the virus family Potyviridae.
Celery mosaic virus (CeMV) is a plant pathogenic virus in the genus Potyvirus and the virus family Potyviridae .
Commelina mosaic virus (CoMV) is a plant pathogenic virus in the genus Potyvirus and the virus family Potyviridae. Like other members of the Potyvirus genus, CoMV is a monopartite strand of positive-sense, single-stranded RNA surrounded by a capsid made for a single viral encoded protein. The virus is a filamentous particle that measures about 707-808 nm in length. This virus is transmitted by two species of aphids, Myzus persicae and Aphis gossypii, and by mechanical inoculation.
Passion fruit woodiness virus (PWV) is a plant pathogenic virus in the genus Potyvirus and the virus family Potyviridae. Like other members of the genus Potyvirus, PWV is a monopartite strand of positive-sense, single-stranded RNA surrounded by a capsid made for a single viral encoded protein. The virus is a filamentous particle that measures about 745 nm in length.
Watermelon mosaic virus (WMV) also known as Marrow mosaic virus, Melon mosaic virus, and until recently Watermelon mosaic virus type 2 (WMV-2), is a plant pathogenic virus that causes viral infection in many different plants. The virus itself is referred to as Watermelon Mosaic Virus II or WMV-2 and is an isolate of the U.S. WMV-2 is a ssRNA positive strand virus that is part of the Potyviridae or Potyvirus clade. Like all RNA viruses, it contains a protein capsid which protects the inner viral RNA. First described on squash in Florida, WMV arose from a unique recombination of genetic material contributed by Soybean mosaic virus (SMV) and Bean common mosaic virus (BCMV) along with Peanut Stripe virus (PSV).
''Narcissus white streak virus (NWSV) is a plant pathogen of the family Potyviridae which infects plants of the genus Narcissus, and is transmitted by aphids. It is among the commonest and most serious of the viral infections that infect narcissi, but appears to be confined to N. tazetta.
The cardamom mosaic virus (CdMV) is a mosaic virus that affects the production of green cardamom (E. cardamomum). It is a member of the genus Macluravirus (recognized under the family Potyviridae by ICTV in 1988), and is transmitted through aphids (P.caladii) and infected rhizomes, the former in a non-persistent manner.
Carrot virus Y (CarVY) is a (+)ss-RNA virus that affects crops of the carrot family (Apiaceae), such as carrots, anise, chervil, coriander, cumin, dill and parsnip. Carrots are the only known crop to be infected in the field. Infection by the virus leads to deformed roots and discolored or mottled leaves. The virus is spread through insect vectors, and is currently only found in Australia.
The Lily mottle virus (LMoV), is a plant virus of the Potyviridae virus family that causes asymptomatic to mild diseases of individual plant parts in plants of the lily family (Liliaceae). However, a frequently occurring simultaneous infection with other plant viruses, which on their own only cause moderate or no disease, can cause the entire plant to perish. This coinfection leads to considerable crop damage in lily cultivation and is therefore of great economic importance. Lily mottle virus is spread by aphids and in horticulture during vegetative propagation by splitting the lily bulb. LMoV was regarded as a synonym for a subtype of the Tulip Breaking Virus (TBV) that occurs in lilies, although since 2005 it has been classified as a closely related but independent virus species of the genus Potyvirus.
References
1 2 3 4 5 van Slogteren, D. H. (October 1971). "Tulip breaking virus". Descriptions of Plant Viruses. Lisse, The Netherlands: Bulb Research Centre.
↑ Brandes, J.; Wetter, C. (1959). "Classification of elongated plant viruses on the basis of particle morphology". Virology. 8 (99): 115. doi:10.1016/0042-6822(59)90022-4. PMID13669326.
"Tulip breaking or mosaic"(PDF). Report on Plant Disease 634. Department of Crop Sciences, University of Illinois, Urbana-Champaign. Sep 1990. Archived from the original(PDF) on 25 May 2013. Retrieved 18 March 2014.
Beckerman, Janna (April 18, 2011). "Tulip Break Virus". Purdue University: Plant and Pest Diagnostic Laboratory. Archived from the original on 18 March 2014. Retrieved 18 March 2014.
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