Tulip breaking virus
D. H. M. van Slogteren
Bulb Research Centre, Lisse, The Netherlands
- Described by Cayley (1928) and McKay, Brierley & Dykstra (1929).
- Selected synonyms
- Tulip mosaic virus (Rev. appl. Mycol. 36: 303)
- Tulipa virus 1 (Rev. appl. Mycol. 36: 303)
- Marmor tulipae (Rev. appl. Mycol. 28: 514)
- Tulipavirus vulgare (Rev. appl. Mycol. 38: 677)
- Lily mottle virus (Rev. appl. Mycol. 24: 59)
- A virus with flexuous filamentous particles, c. 740 nm long,
sap-transmissible to two genera of Liliaceae and transmitted by a few species of
aphids in the non-persistent manner. Causes colour breaking in the perianth of
tulips. World-wide distribution.
Causes flower breaking in red and purple varieties of tulip species and their
hybrids; it affects the amount of anthocyanin in the vacuoles of epidermal cells
in the petals (Dufrénoy, 1931
), resulting in different types of
colour-breaks depending on the variety of tulip and on the strain of the virus. White-
and yellow-flowered varieties are incapable of breaking because they lack
anthocyanins, their colour being determined by colourless or yellow plastids in
the mesophyll. Infected plants may also show leaf mottle (Fig.5
has been known since tulips were introduced to Europe in the 16th century. Paintings
of the 16th and 17th century often include tulips and these are always of the broken
type. Although in the 17th century broken tulips were highly valued, nowadays they
are not, because infected plants are no longer true to varietal type and the
production of offsets is decreased. The virus is also found in lily species, causing
mild to moderate mottling in the leaves.
World-wide. Reported in all temperate regions where tulips are grown;
particularly common in southern Europe where the aphid vectors are abundant early
in the growing season.
Host Range and Symptomatology
Reported to infect only two plant genera, Tulipa
in the Liliaceae. Transmissible by inoculation of sap and by bulb-grafting. As
early as 1637 Dutch growers produced new varieties of tulip with flower breaks by
grafting tulip bulbs with broken flowers to bulbs with uniformly coloured flowers
- Diagnostic species
- Lilium formosanum. Mottle or streak symptoms in the tip leaves about 2
weeks after mechanically inoculating seedlings with extracts from petals, leaves
or bulb scales of infected tulip. Leaves and flowers produced later are distorted
(Brierly & Smith, 1944;
- Propagation species
- The tulip varieties Croisette, Grand Pride and Paljas are good sources for virus
- Assay species
- No local lesion host reported.
Severe strains (STBV) and mild strains (MTBV) have been distinguished by the
type and severity of flower break symptoms they cause (van Slogteren & de Vos,
; van Slogteren & Asjes, 1970
In certain varieties STBV causes full break
symptoms, in which anthocyanins fail to form in parts of the petals so that the
colour of the mesophyll (either white or yellow) is exposed (Fig.1
). In the same
varieties MTBV causes self break symptoms in which the colour in parts of the
petals is intensified because anthocyanins are formed in excess (Fig.2
). 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 full break and self
break symptoms are present, together with some unbroken areas, in different parts
of the same petal (Fig.3
). Plants infected with a mixture of strains when young
(sprouts about 3 cm long) may develop atypical symptoms in the current season
), with full break restricted to the basal part of the petal and severe
self break in the upper parts
(van Slogteren & de Bruyn Ouboter, 1941
). Other varieties were found by
to be incapable
of full breaking; these always show self break symptoms whether infected with
STBV or MTBV or a mixture of both strains.
Transmission by Vectors
Transmitted by at least 4 species of aphids in the non-persistent manner. Of
these Myzus persicae
is the most efficient; the others are Aphis
gossypii, Doralis fabae
and Macrosiphum euphorbiae. McKenny-Hughes
) reported that Yezabura tulipae
transmits between stored
tulip bulbs, but this has not been confirmed by others (Brierley & McKay,
; van Slogteren & de Bruyn Ouboter, 1941
). Transmission by Myzus
is enhanced when the aphid is starved for 1-2 hr before the
acquisition access feed, the optimum acquisition period being 2-5 min.
Transmission through Seed
Transmission by Dodder
A good immunogen. Antisera with titres greater than 1/1000 have been prepared
against different isolates (van Slogteren & de Vos, 1966
). For microprecipitin
tests the virus is concentrated by ammonium sulphate precipitation. Dilution
end-points are increased by immersing infected leaves in water at 50°C before
extracting the sap. Precipitates are of the flocculent (flagellar) type.
STBV reacted with both the homologous antiserum and with antiserum to MTBV,
but MTBV reacted with neither antiserum, presumably because too little virus was
present (van Slogteren & de Vos, 1966
). An observation by McWhorter (1938)
suggests that MTBV does not protect against super-infection with STBV: he
inoculated tulips showing self break with STBV and 5 out of 9 plants then
developed full break.
Tulip breaking virus is a member of the potato virus Y group (Brandes &
Wetter, 1959); Bartels (1971) found a distant serological relationship to tobacco
etch virus, cross-reactions with both heterologous antisera being positive. Also,
tulip breaking virus reacted with antiserum to henbane mosaic virus but henbane
mosaic virus did not react with antiserum to tulip breaking
Stability in Sap
Infectivity in tulip sap is lost after 10 min at 65-70°C and after dilution
). In lily sap it is retained for 4-6 days
at 18°C (Brierley & Smith, 1944
Attempts to obtain highly purified virus preparations have failed because of
the small amounts of virus in leaf extracts and because the particles aggregate.
Preparations for immunizing rabbits were partially purified by a method used for
potato virus M
(Rozendaal & van Slogteren, 1958
Properties of Particles
Particles are flexuous filaments (Fig.6
14 nm wide and with a modal
particle length of 740 nm (Brandes & Bercks, 1965
Relations with Cells and TissuesMcWhorter (1941)
, using light microscopy, found two kinds of intracellular
inclusions in epidermal cells of infected tulip leaves. Using electron microscopy
of ultra-thin sections, Yamaguchi, Kikumoto & Matsui (1963)
of parallel particles in infected tulip petals, and T. C. Allen (pers. comm.) found
pinwheel inclusions in infected cells of both tulip and lily (Fig.7
Tulips infected with cucumber mosaic virus
show a flower break which might be
confused with that caused by tulip breaking virus but is usually distinctive
because it is confined to the margins of the petals (van Slogteren, 1966
lilies, tulip breaking virus is sometimes found together with lily symptomless virus
(van Slogteren, unpublished), a virus described earlier by Civerolo, Semancik &
and by Allen & Lyons (1969)
Brierley & Smith (1944) reported four additional hosts of tulip breaking virus
in the Liliaceae (Calochortus sp., Fritillaria pudica, Zygadenus
fremontii and Ornithogalum thyrsoides). However, this report needs
confirming because the virus used in these experiments came from lily and may have
been contaminated with lily symptomless virus.
- Allen & Lyons, Phytopathology 59: 1318, 1969.
- Bartels, Phytopath. Z. 71: 87, 1971.
- Brandes & Bercks, Adv. Virus Res. 11: 1, 1965.
- Brandes & Wetter, Virology 8: 99, 1959.
- Brierley & McKay, Phytopathology 28: 123, 1938.
- Brierley & Smith, Phytopathology 34: 718, 1944.
- Cayley, Gdnrs' Chron. 83: 435, 1928.
- Civerolo, Semancik & Weathers, Phytopathology 58: 1481, 1968.
- Dufrénoy, C. r. Séanc. Soc. Biol. 108: 51, 1931.
- Hoog, Gdnrs' Chron. 94: 471, 1933.
- McKay, Brierley & Dykstra, Yb. U.S. Dep. Agric. 1928: 596, 1929.
- McKenny-Hughes, Ann. appl. Biol. 18: 16, 1931.
- McKenny-Hughes, Ann. appl. Biol. 21: 112, 1934.
- McWhorter, Phytopathology 25: 898, 1935.
- McWhorter, Ann. appl. Biol. 25: 254, 1938.
- McWhorter, Stain Technol. 16: 143, 1941.
- Rozendaal & van Slogteren, Proc. 3rd Conf. Potato Virus Diseases, Lisse-Wageningen, 1957: 20, 1958.
- van Slogteren, Meded. Rijksfac. Landb. Wetensch. Gent 31: 986, 1966.
- van Slogteren & Asjes, Daffodil Tulip Yb. 35: 85, 1970.
- van Slogteren & de Bruyn Ouboter, Meded. LandbHoogesch. Wageningen 45(4), 54 pp., 1941.
- van Slogteren & de Vos, Proc. Conf. Pl. Viruses, Wageningen 1965: 320, 1966.
- Wetter, Arch. Mikrobiol. 37: 278, 1960.
- Yamaguchi, Ann. phytopath. Soc. Japan 23: 240, 1958.
- Yamaguchi, Ann. phytopath. Soc. Japan 26: 131, 1961.
- Yamaguchi, Kikumoto & Matsui, Virology 20: 143, 1963.
Figs 1-5 courtesy of Bulb Research Centre, Lisse; Fig.6 courtesy of C. J.
Asjes, Bulb Research Centre, Lisse; Fig.7 courtesy of T. C. Allen, Oregon State University, Corvallis, Oregon, USA.
Tulip cv. Croisette showing full break symptoms.
Tulip cv. Croisette showing self break symptoms.
Tulip cv. Croisette showing average break symptoms.
Tulip cv. Pride of Haarlem showing current season symptoms.
Mottled leaf of infected tulip cv. Paris.
Aggregates of particles in leaf-dip preparation mounted in
phosphotungstate. Bar represents 500 nm.
Pinwheel inclusion bodies in tissue of infected lily cv. Bright Star.
Bar represents 500 nm.