Introduction of Plant Virusis
Introduction of Plant Virusis
Introduction of Plant Virusis
INTRODUCTION TO PLANT
VIRUSES
C H A P T E R
1
What Is a Virus?
This chapter discusses broad aspects of virology and highlights how plant viruses have led the
subject of virology in many aspects.
O U T L I N E
Comparative Plant Virology, Second Edition 3 Copyright # 2009, Elsevier Inc. All rights reserved.
4 1. WHAT IS A VIRUS?
virus disease is a Japanese poem that was writ- determining exactly what a virus was. In the latter
ten by the Empress Koken in A.D. 752 and part of the nineteenth century, the idea that infec-
translated by T. Inouye: tious disease was caused by microbes was well
established, and filters were available that would
In this village not allow the known bacterial pathogens to pass
It looks as if frosting continuously
through. In 1886, Mayer (see Figure 1.2A)
For, the plant I saw
In the field of summer described a disease of tobacco that he called
The colour of the leaves were yellowing Mosaikkrankheit, which is now known to be caused
by the Tobacco mosaic virus (TMV). Mayer demon-
The plant, which has since been identified as strated that the disease could be transmitted to
Eupatorium lindleyanum, has been found to be healthy plants by inoculation with extracts from
susceptible to Tobacco leaf curl virus, which diseased plants. A major observation was made
causes a yellowing disease. in 1892 by Iwanowski, who showed that sap from
In Western Europe in the period from about tobacco plants displaying the disease described
1600 to 1660, many paintings and drawings by Mayer was still infective after it had been
were made of tulips that demonstrate flower passed through a bacteria-proof filter candle.
symptoms of virus disease. These are recorded However, based on previous studies, it was
in the Herbals of the time and some of the ear- thought that this agent was a toxin. Iwanowski’s
liest in the still-life paintings of artists such as experiment was repeated in 1898 by Beijerinck
Ambrosius Bosschaert. During this period, (see Figure 1.2B), who showed that the agent mul-
blooms featuring such striped patterns were tiplied in infected tissue and called it contagium
prized as special varieties, leading to the phe- vivum fluidum (Latin for “contagious living fluid”)
nomenon of “tulipomania” (Box 1.1). to distinguish it from contagious corpuscular
Because of their small genomes, viruses have agents (Figure 1.2C).
played a major role in elucidating many of the Beijerinck and other scientists used the term
concepts in molecular biology, and the study of virus to describe the causative agents of such
plant viruses has produced several of the major transmissible diseases to contrast them with
findings for virology in general. The major steps bacteria. The term virus had been used more
in reaching the current understanding of viruses or less synonymously with bacteria by earlier
are shown in the timeline in Figure 1.1. workers, but as more diseases of this sort were
Details of these “breakthroughs” can be found discovered, the unknown causative agents
in Hull (2002; plant viruses), Fenner, (2008; verte- came to be called “filterable viruses.” Similar
brate viruses), and Ackermann (2008; bacterial properties were soon after reported for some
viruses). Plant viruses played a major role in viruses of animals (e.g., the filterable nature of
BOX 1.1
TULIPOMANIA
Tulips were introduced into the Netherlands in the late sixteenth century. Bulbs that produced ”broken-
coloured” flowers were in great demand and created a rapidly expanding market, leading to
hyperinflation.
(continued)
Semper Augustus tulip with flower colour break (one of the most favoured varieties)
One bulb cost 1,000 Dutch florins (guilders) in 1623, and by 1635, 6,000 florins. To understand the
value of this, one Viceroy tulip bulb was exchanged for goods that were valued at almost 2,400 florins:
4 tons of wheat (448 florins) 4 barrels of beer (3 florins)
8 tons of rye (558 florins) 2 barrels of butter (192 florins)
4 fat oxen (480 florins) 1,000 lbs cheese (120 florins)
8 fat pigs (240 florins) 1 bed with accessories (100 florins)
12 fat sheep (120 florins) 1 silver goblet (60 florins)
2 hogsheads of wine (70 florins)
By 1636 there was much speculation, and futures were being taken out on these bulbs. In early
1637 one bulb was valued at 10,000 florins, but a few weeks later, the bubble burst and many people
were left bankrupt. It was not until the 1920s that the viral aetiology of tulip flower breaking was
discovered and that the symptoms were caused by an aphid-transmitted potyvirus. Today, 100 flor-
ins is equivalent to about U.S. $30,000.
A B
the agent causing foot and mouth disease in In 1935, Stanley announced the isolation of this
1898) and of bacteria in 1915. Over the course virus in an apparently crystalline state but con-
of time, the word filterable has been dropped, sidered that the virus was a globulin containing
leaving just the term virus. no phosphorus. In 1936, however, Bawden and
As shown in the timeline in Figure 1.1, in the his colleagues described the isolation from
subsequent development of virology, many of TMV-infected plants of a liquid crystalline nucle-
the studies ran in parallel for viruses of plants, oprotein containing nucleic acid of the pentose
vertebrates, invertebrates, and bacteria. In fact, type. Around 1950, Markham and Smith showed
when viewed overall, there is evidence of much that the RNA of Turnip yellow mosaic virus was
cross-feeding between the various branches of encapsidated in a protein shell and was impor-
virology. However, there were differences tant for biological activity. This led to the classic
mainly due to the interactions that these experiments of Gierer, Schramm, Fraenkel-Con-
viruses have with their hosts. For instance, ver- rat, and Williams in the mid-1950s that demon-
tebrates produce antibodies that counter strated the infectivity of naked TMV RNA and
viruses, whereas plants, invertebrates, and bac- the protective role of the protein coat.
teria do not. Another factor that has contribu- In parallel with these biochemical studies,
ted to advances is the simplicity of the system physical studies in the late 1930s using X-ray
exemplified by studies on bacteriophage being analysis and electron microscopy confirmed that
linked to studies on bacterial genetics. TMV had rod-shaped particles and obtained
The development of plant, and other, virol- accurate estimates of the size of the rods. Atten-
ogy can be considered to have gone through five tion turned to the structure of these particles,
major (overlapping) ages. The first two, Prehis- and in 1956, Crick and Watson suggested that
tory and Recognition of viral entity, were just the protein coats of small viruses are made up
described. After these two came the Biological of numerous identical subunits arrayed either
age, between 1900 and 1935, when it was deter- as helical rods or as a spherical shell with cubic
mined that plant viruses were transmitted by symmetry. This led to Caspar and Klug (1962)
insects and that some of these viruses multi- formulating a general theory that delimited the
plied in, and thus were pathogens of, insects in possible numbers and arrangements of the pro-
a manner similar to some viruses of vertebrates. tein subunits forming the shells of the smaller
One of the constraints to plant virology was the isodiametric viruses (see Chapter 5). Our recent
lack of a quantitative assay, until Holmes in knowledge of the larger viruses with more com-
1929 showed that local lesions produced in plex symmetries and structures has come from
some hosts after mechanical inoculation could electron microscopy using negative-staining
be used for the rapid quantitative assay of infec- and ultrathin-sectioning methods.
tive virus. This technique enabled properties of The current Molecular age started in about
viruses to be studied much more readily and 1960 when the full sequence of 158 amino acids
paved the way for the isolation and purification in the coat protein of TMV was determined.
of viruses a few years later. The sequence of many naturally occurring
The Biochemical/Physical age started in the strains and artificially induced mutants was
early 1930s. The high concentration at which also determined at about the same time. This
certain viruses occur in infected plants and work made an important contribution to estab-
their relative stability was crucial in the first lishing the universal nature of the genetic code
isolation and chemical characterisation of and to our understanding of the chemical basis
viruses because methods for extracting and of mutation. This age continued with the
purifying proteins were not highly developed. sequencing of representatives of most, if not
C
B
FIGURE 1.3 Size comparison of different organisms. A. Organisms classified according to genome size. The vertical axis
gives an approximate indication of numbers of species within the size range of each group. B. Size comparison among a
bacterium, several viruses, and a viroid. C. Comparison of size of rhinovirus and a pinhead. A. Modified from Hinegardner
[1976; in Molecular Evolution, (F.J. Ayala, Ed.), pp. 179-199, Sinauer, Sunderland, MA]; B. With kind permission from
Springer Science þ Business Media: Arch. Virol., Interference between proflavine treated reovirus and related and unrelated
viruses, vol. 15, 1965, pp. 200–2009, E. Zalan; Arch. Virol., Die Interferenz zwischen dem Polyoma-virus and dem Stomatitis-
vesicularis-Virus in der Maus, vol. 15, 1965, pp. 210-219, D. Falke; Arch. Virol., Properties of a new attenuated type 3 polio-
virus, vol. 15, 1965, pp. 220-233, J. Šimon. C. http://web.uct.ac.za/depts/mmi/stannard/linda.html.
mechanism of transposition. Class I mobile mobile genetic elements move directly from one
genetic elements, or retrotransposons, move in position to another within the genome using a
the genome by being transcribed to RNA and then transposase to “cut and paste” them within the
back to DNA by reverse transcriptase. Class II genome. In many properties, retrotransposons
TABLE 1.2 Distinguishing Criteria for Viruses resemble retroviruses, and they are classified as
Metaviruses and Pseudoviruses. However, there
Criteria That Do Not
Criteria That Distinguish Distinguish Viruses is debate as to whether these are really viruses in
Viruses from Cells from Cells the strictest sense. We can now define a virus, as
shown in Box 1.2.
1. Lack of continuous 1. Size To be identified positively as a virus, an agent
membrane separating
must normally be shown to be transmissible and
virus from host during
replication to cause disease in at least one host. One of the
basic tenets of pathology is that to prove that a dis-
2. Absence of protein- 2. Nature and size of
synthesising system genome ease is caused by a certain infectious agent, one
3. Contain either DNA or 3. Contain both DNA and
must fulfill Koch’s postulates, which were
RNA RNA devised for bacteria; modifications of the postu-
4. Replication is by synthesis 4. Absence of rigid cell
lates have been suggested to account for specific
of a pool of components envelope properties of viruses (Table 1.3). Today, however,
and not by binary fission it is not always possible to fulfill these postulates
5. Obligate cell parasitism for viruses. For instance, plant cryptoviruses
6. Absence of energy- rarely cause detectable disease and are not trans-
yielding system missible by any mechanism except through seeds
7. Complete dependence or pollen. Usually, it is satisfactory to show a clear
on host cell for amino association of the viral genome sequence with the
acids disease after eliminating the possibility of joint
infection with another virus.
BOX 1.2
DEFINITION OF A VIRUS
A virus is a set of one or more nucleic acid tem- from pools of the required materials rather than
plate molecules, normally encased in a protec- by binary fission, (3) located at sites that are not
tive coat or coats of protein or lipoprotein, that separated from the host cell contents by a lipo-
is able to organise its own replication only protein bilayer membrane, and (4) continually
within suitable host cells. Within such cells, giving rise to variants through several kinds of
virus replication is (1) dependent on the host’s change in the viral nucleic acid.
protein-synthesising machinery, (2) organised
A problem arises as to how much weight is assigned. Of the 1,037 plant viruses listed in
put onto each character. In practice, the nature the eighth ICTV report, 751 are true species
and sequence of the genomic nucleic acid are and 286 are tentative species. Further studies
the major characters that are used, but other prop- will provide enough data to classify the tenta-
erties, such as particle shape and composition, tive species. A common problem is determining
antigenic relationships, and biology, are also whether a new virus is truly a new species or a
considered to be important. Any classification strain of an existing species. Conversely, what
of viruses should be based not only on evolu- was considered to be a strain may, on further
tionary history, as far as this can be deter- investigation, turn out to be a distinct species.
mined from the genotype, but should also be This is due to the population structure of viruses
useful in a practical sense. Most of the pheno- that, because of continuous production of errors
typic characters used today in virus classifica- in replication, can be considered a collection of
tion will remain important even when the quasi-species. The concept of quasi-species is
nucleotide sequences of most viral genomes discussed in more detail following.
have been determined. With the species forming the basis of the clas-
sification system, they can be grouped into other
taxa on various criteria. To date, the taxonomic
B. Families, Genera, and Species levels of order, family, and genus have been
The main building block of a biological clas- defined by the ICTV, and it is likely that there
sification is the species. In day-to-day prac- will be pressure for further higher and interme-
tice, virologists use the concept of a “virus” as diate taxa. No formal definition for a genus
being a group of fairly closely related strains, exists, but it is usually considered “a population
variants, or pathovars. A virus defined in this of virus species that share common characteris-
way is essentially a species in the sense sug- tics and are different from other populations of
gested for angiosperms and defined by the ICTV. species.” Currently, 80 genera of plant viruses
In 1991, the ICTV accepted the concept that are recognised. In some cases—such as the Rhab-
viruses exist as species, adopting the following doviridae—numerous viruses are recognised that
definition: obviously belong to that family but for which
there is not enough information to place them
A viral species is a polythetic class of viruses that either in existing genera or for creating new
constitutes a replicating lineage and occupies a partic-
genera; these viruses are listed as “unassigned.”
ular ecological niche. [Polythetic denotes a taxonomic
group classified on the basis of several characters,
Genera are named either after the type species—
as opposed to a monothetic group.] for example, Caulimovirus after Cauliflower mosaic
virus—or are given a descriptive name, often
The species has formed the basis of modern from a Greek or Latin word, for a major feature
virus classification being established in of the genus—for example, Closterovirus, from
subsequent ICTV reports, especially the seventh the Greek klostr (kloster), which is a spindle
and eighth, in which a List of Species-Demarcat- or thread, or that describes the virus particle
ing Criteria is provided for each genus. This shape, such as Geminivirus, from the Latin gemi-
enables viruses to be differentiated as species nus, meaning “twins.”
and tentative species, which are viruses that Similarly, genera are grouped together into
have not yet been sufficiently characterised to families on common characteristics (Table 1.4).
ensure that they are distinct and not strains of There are 17 families recognised for plant
an existing virus or do not have the full charac- viruses; some, such as Reoviridae and Rhabdoviri-
teristics of the genus to which they have been dae, are in common with animal virus families.
TABLE 1.4 Criteria Demarcating Different on virus classification, will no doubt lead to the
Virus Taxa designation of further plant virus families. The
family is either named after the type member
I Order genus—for example, Caulimoviridae, named after
Common properties between several families including:
the genus Caulimovirus—or given a descriptive
name, as with the genus, for a major feature of
Biochemical composition
the family—for example, Geminiviridae, which
Virus replication strategy
describes the virus particles.
Particle structure (to some extent) Only three orders have been accepted thus
General genome organisation far by the ICTV. The Mononegavirales contains,
among other families, the Rhabdoviridae, which
II Family contains two plant virus families. In practice,
genome nucleic acid sequence data are increas-
Common properties between several genera including:
ingly being used to delimit genera, species, and
Biochemical composition
strains (Figure 1.4). A detailed discussion of
Virus replication strategy virus classification, the currently accepted taxa,
Nature of particle structure and how the ICTV operates are provided in
Genome organisation Fauquet et al. (2005).
III Genus
C. Naming Viruses (Species)
Common properties with a genus including:
Questions of virus nomenclature have gener-
Virus replication strategy
ated more heat over the years than the much
Genome size, organisation, and/or number of more practically important problems of how to
segments
delineate distinct virus species. When a family
Sequence homologies (hybridisation properties) or genus is approved by the ICTV, a type species
Vector transmission is designated. Some virologists favour using
the English vernacular name as the official spe-
IV Species cies name. Using part of a widely known vernac-
ular name as the official species name may
Common properties within a species including:
frequently be a very suitable solution, but it could
Genome arrangement
not always apply (e.g., with newly discovered
Sequence homologies (hybridisation properties) viruses). Other virologists favour serial number-
Serological relationships ing for viruses (species). The experience of other
Vector transmission groups of microbiologists is that, although num-
Host range bering or lettering systems are easy to set up in
Pathogenicity the first instance, they lead to chaos as time
Tissue tropism passes and changes must be made in taxonomic
groupings. The idea of Latinized binomial names
Geographical distribution
for viruses was supported by the ICTV for many
years but never implemented for any viruses.
Seventeen of the genera have not yet been In successive editions of the ICTV reports,
assigned to families and are termed “floating virus names in the index have been listed by
genera.” The acquisition of further data on these the vernacular name (usually English) followed
floating genera, together with changing attitudes by the family or genus name—for example,
A B
C
FIGURE 1.4 Differentiation of taxa by pairwise identities of sequences of variants of A. RT/RNaseH nucleotide
sequences of Banana streak virus isolates; B. Nucleic acid sequences of the L1 gene of members of the Family Papillomaviridae;
C. Amino acid sequences of coat proteins of potyviruses. A. With kind permission from Springer Scienceþ Business Media:
Arch. Virol., The diversity of Banana streak virus isolates in Uganda, vol. 150, 2005, pp. 2407-2420, G. Harper; B. From Virus
Taxonomy, 8th Report of the National Committee on the Taxonomy of Viruses, Fauquet et al., p. 5, Copyright Elsevier (2005);
C. Reichmann et al. ( Journal of General Virology 73, 1–16, 1992).
tobacco mosaic Tobamovirus, Fiji disease Fiji- overlap and confusion. For instance, among
virus, and Lettuce necrotic yellows rhabdovirus. plant viruses, AMV was used to designate
This method for naming a plant virus is becom- Alfalfa mosaic virus and Arabis mosaic virus and
ing increasingly used in the literature. could also justifiably be used for Abutilon mosaic
virus, Agropyron mosaic virus, Alpina mosaic virus,
Alstromeria mosaic virus, Alternantha mosaic virus,
D. Acronyms or Abbreviations
Aneilema mosaic virus, or Anthoxanthum mosaic
Abbreviations of virus names have been used virus. Therefore, in 1991 the Plant Virus section
for many years to make the literature easier to of the ICTV initiated a rationalisation of plant
read and more succinct to present. The abbrevi- virus acronyms and has subsequently updated
ation is usually in the form of an acronym using the list regularly in ICTV reports (Box 1.3).
the initial letters of each word in the virus name. There are no efforts to create a common
As the designation of the acronym was by the acronym system for viruses from different
author of the paper, it was leading to much kingdoms. Thus, CMV can mean Cucumber
BOX 1.3
mosaic virus (of plants), Canine minute virus (of describe variants within a species and, in real-
vertebrates), or Clo Mor virus (of invertebrates). ity, take a pragmatic approach. Characters have
Thus, acronyms have to be taken in context. to be weighed up as to how they would con-
tribute to making subdivisions and to commu-
nication, not only between virologists but also
E. Plant Virus Classification
to plant pathologists, extension workers, farm-
The current classification of plant viruses is ers, and many other groups. An example is
shown in Figure 1.5. the luteovirus Beet western yellows virus
(BWYV), which has a wide host range, includ-
ing sugar beet in the United States. For many
F. Virus Strains years, Beet mild yellows virus, which infected
A virus species is not a uniform population sugar beet in Europe, was regarded as a strain
because in each infected cell, a wide range of of BWYV. Confusion arose when it was discov-
variants is present. This situation is termed a ered that the European luteovirus that was
quasi-species (Box 1.4). most closely related to BWYV did not infect
The quasi-species concept makes it difficult sugar beet but was common in the oilseed rape
to strictly define a strain. However, one must crop. This caused many problems in explaining
FIGURE 1.5 Classification of plant viruses. From Virus Taxonomy, 8th Report of the National Committee on the Taxon-
omy of Viruses, Fauquet et al., p. 18, Copyright Elsevier (2005).
BOX 1.4
QUASI-SPECIES
to farmers that the BWYV in their overwinter- nouns or parts of proper nouns. Also, in for-
ing oilseed rape crop would not infect their mal use, the name of the taxon should precede
beet crop the next year. the name being used—for example, the family
Caulimoviridae, the genus Mastrevirus, and the
species Potato virus Y. An example of classifica-
G. Use of Virus Names
tion, nomenclature, and orthography is shown
The ICTV sets rules, which are regularly in Box 1.5.
revised, on virus nomenclature and the orthog- In informal use, the family, subfamily, genus,
raphy of taxonomic names (see the eighth ICTV and species names are written in lowercase
report). The last word of a species is virus, and Roman script, the taxon does not include the
the suffix (ending) for a genus name is -virus. formal suffix, and the taxonomic unit follows
For a subfamily, it is -virinae; for a family, it is the name being used—for example, the caulimo-
-viridae; and for an order, it is -virales. In formal virus family, the mastrevirus genus, and the
taxonomic usage, the virus order, family, sub- potato virus Y species. In even less formal cir-
family, genus, and species names are printed cumstances, but still widely used, the taxonomic
in italics (or underlined), with the first letter unit is omitted and the taxon for higher taxa can
being capitalized; other words in species names be in the plural—for example, caulimoviruses,
are not capitalized unless they are proper mastreviruses, and potato virus Y.
Number % Total Number % Total Number % Total Number % Total Number % Total
Data from Fauquet et al. (2005), using numbers of assigned, unassigned, and tentative virus species.
VI. SUMMARY Hull, R. (2001). Matthew’s plant virology, 4th ed. Academic
Press, San Diego.
Murphy, F.A., Fauquet, C.M., Bishop, D.H.L., Ghabrial, S.A.,
• Plant viruses are important pathogens. Jarvis, A.W., Martelli, G.P., Mayo, M.A., and Summer,
• The study of plant viruses has made M.D. (1995). Virus taxonomy. Sixth Report of the Interna-
tional Committee on Taxonomy of Viruses. Springer-Verlag,
important contributions to the Wien, Austria.
understanding of viruses in general—for Rivers, T.M. (1937). Viruses and Koch’s postulates. J. Bacteriol.
example, the recognition of viruses as 33, 1–12.
pathogens, the structure of virus particles,
and the infectious nature of RNA.
• This chapter defines a virus, contrasts it with Further Reading
similar agents, and discusses how viruses Fauquet, C.M. (2008). Taxonomy, classification, and nomen-
are classified. clature of viruses. Encyclopedia of Virology, Vol. 5, 9–23.
Grandbastien, M.-A. (2008). Retrotransposons of plants.
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