Part I

Contents - Previous - Next

Chapter 1: The nature of virus and virus-like disease agents of citrus
Chapter 2: Interactions between virus and virus-like pathogens and the host plant: susceptible, tolerant and resistant citrus species
Chapter 3: Transmission and spread of virus and virus-like citrus pathogens
Chapter 4: Techniques for the detection and identification of virus and virus-like citrus pathogens
Chapter 5: Production of citrus clones free of virus and virus-like pathogens
Chapter 6: Short description of major citrus diseases in the near east
Chapter 7: Citrus stubborn disease in the syrian arab republic and natural transmission of its causal agent, Spiroplasma citri

Chapter 1: The nature of virus and virus-like disease agents of citrus

Viruses, viroids and phloem-restricted prokaryotes
Graft-transmissible diseases of unknown aetiology
Bibliography

Several of the virus and virus-like agents of citrus diseases have been characterized. These are viruses, viroids or phloem-restricted prokaryotes, the term "virus-like" applying to the latter two. Like viruses, viroids and phloem-restricted prokaryotes are graft-transmissible and are therefore said to be "virus-like", a term that is also conveniently used for infectious, graft-transmitted agents that have not yet been characterized.

Viruses, viroids and phloem-restricted prokaryotes

Properties

Viruses, viroids and phloem-restricted prokaryotes are pathogens that produce diseases in susceptible hosts.

Viruses and viroids are obligate cellular parasites which can only multiply in living host cells. In the absence of such cells they are inert, incapable of autonomous replication nor can they be cultured in cell-free media. These properties reflect the fact that viruses and viroids do not possess the structure of cells, but have a simpler structure and are macro-molecules. In contrast, phloem-restricted prokaryotes have a cellular structure. Some, such as the spiroplasmas, can be cultured in cell-free media - others cannot, perhaps because adequate media have not yet been developed or because they are obligate parasites.

Thus, viruses and viroids, on the one hand, and phloem-restricted prokaryotes, on the other, are totally different in nature. However, they have in common the fact that they are endocellular, that is, they are localized within certain cells of their host: for instance, the sieve tubes of the phloem tissue for the spiroplasmas; the sieve tubes and their companion cells for tristeza virus and the parenchyma cells for the exocortis viroid. This endocellular localization explains why viruses and viroids as well as the phloem-restricted prokaryotes can all be propagated by bud multiplication. In addition, they can be transmitted by graft inoculation of tissue-inoculum (bark, bud, leaf-piece, budwood stick) from an infected to a healthy plant. The successful transmission of a pathogen by graft inoculation implies that the transmitted pathogen is able to spread from the inoculum into the receiver plant, which it will then invade, becoming systemically distributed throughout the plant. Plants that are invaded by the pathogen are "systemic" hosts, in contrast to "local" hosts in which the pathogen is only present locally. In systemic hosts, however, certain agents, such as Spiroplasma citri, are sometimes unevenly or poorly distributed.

Until the discovery of viroids and phloem-restricted prokaryotes in the late 1960s, only viruses were thought to be graft-transmissible. Consequently, the graft transmissible pathogens of greening and stubborn diseases of citrus were thought to be viruses. Today they are known to be prokaryotic cells, not viruses. Their endocellular localization and ability to invade host plants systemically explains their graft transmissibility.

Structure and replication of viruses

Viruses are formed in their host cells by the association of their constituents. Simple viruses have only two constituents: a nucleic acid molecule contained within a protein coat or capsid. Therefore, the virus particle or virion is called a nucleoprotein or nucleocapsid. The nucleic acid is the genome of the virus, serving as the chemical support of the properties of the virus. The nature of a given virus is determined by its nucleic acid.

The nucleic acid is either ribonucleic acid (RNA) or deoxyribonucleic acid (DNA). Hence, certain viruses are RNA viruses while others are DNA viruses. Most plant viruses are RNA viruses; for example, CTV and citrus variegation virus (CVV). The protein coat of the virus protects the internal nucleic acid from the harsh extracellular environment and against degradation by nucleases (enzymes that hydrolyse nucleic acids).

The protein coat is made up of a large number of identical proteins, the so-called coat proteins or capsid proteins. The gathering or assembly of the capsid proteins to form the coat or capsid follows two major paths. In one, the capsid proteins are assembled according to a helical mode or symmetry (Fig. 1A). This helical symmetry leads to virus particles or virions with a rod-shaped (Fig. 1B) or filamentous (Fig. 1C) morphology. Virions of CTV have a helical symmetry and are filamentous (Fig. 1C).

In other viruses, the capsid proteins are arranged according to icosahedral symmetry (Fig. 2A). The icosahedron is a body with 20 equilateral triangular facets, 12 vertices and 30 edges. As a geometric body, the icosahedron has a centre of symmetry as well as planes and axes of symmetry. Icosahedral virions, however, have only axes of symmetry. Hence, icosahedral symmetry, as applied to viruses, is restricted to the symmetry axes of the icosahedron (Fig. 2A). In the simplest icosahedral virion there are three capsid proteins on each of the 20 facets of an imaginary icosahedron and they are placed in such a way as to respect the axial symmetries of the icosahedron. The capsid of such a virion contains 20x3=60 capsid proteins. However, most icosahedral viruses have more than 60 capsid proteins. Virions have been found with 180 (Fig. 2B), 240, 420, 540, 960 and 1 500 capsid proteins.

In the case of CTV, the genome of the virus consists of one large RNA molecule. Each CTV virion contains one such molecule and there is only one type of nucleocapsid. Other RNA viruses have divided genomes; for example, in the case of the icosahedral CVV, there are four nucleocapsids. The smallest has a diameter of 25 nm and contains the shortest RNA. The largest measures 32 nm and contains the longest RNA. Here, the genome is made up of several RNA pieces, each one encapsulated in a specific nucleocapsid. Such viruses have divided genomes and are characterized by multiple nucleocapsid components: four in the case of CVV and citrus leaf rugose virus (CLRV) and two in the case of satsuma dwarf virus (SDV) (see Table 1).

The helical or icosahedral nucleocapsid of certain viruses is surrounded by a membraneous envelope derived from a host cell membrane in which proteins of viral origin are embedded. Although most plant viruses are non-enveloped, enveloped animal viruses are common, and an enveloped RNA virus is associated with citrus leprosis.

Table I lists the viruses which have been shown to be the causal agents of, or associated with, diseases of citrus. The pathogens of additional citrus diseases are probably viruses also (see Table 1), but they have not yet been fully characterized. The agent of citrus ring-spot virus (CRSV) is filterable through a 220 nm filter but is highly unstable and difficult to concentrate or purify. It apparently has two nucleoprotein components, as long and short filamentous particles containing single-stranded RNA have been isolated. Similar particles have been observed in Spanish isolates of ringspot, psorosis A and psorosis B (Navas-Castillo, 1991). It is interesting to note that Florida isolate CRSV-6 is able to induce psorosis-like bark scaling on sweet orange plants. In the case of vein enation-woody gall (citrus vein enation virus [CVEV]), spherical virus-like particles of approximately 28 nm in diameter have been observed in gall tissue by electron microscopy and purified from excised enations. The virus is probably a member of the luteovirus group. Flexuous, rod-shaped particles, approximately 654 to 680 nm, were purified from citrons infected with the agent of a California isolate of citrus psorosis virus (CPV). Cowpeas, mechanically infected with the agent of tatterleaf-citrange stunt (citrus tatterleaf virus [CTLV]), were found to contain isometric particles composed of two RNA molecules and a putative capsid protein with a molecular weight of 22 x 103. Other reports indicate CTLV to be a helical virus of 650 nm with a helix pitch of 3.5 nm. These particles could, however, be those of a latent virus found in symptomless citrus material.

Viruses are infectious. In molecular terms, therefore, a virion that has entered a host cell induces this cell to produce hundreds or thousands of new progeny virions, all identical to the infecting virion. In other words, the virus "replicates" in this host cell. The essence of virus replication is becoming increasingly understood. For new virions to be formed, the cell has to produce the two constituents of the virions: nucleic acid molecules and capsid protein molecules. The new virions will be produced by the combination or association of the capsid proteins with the nucleic acid. In the case of icosahedral RNA viruses, capsids without RNA may be formed in an initial stage, and the RNA molecule will penetrate into an empty capsid at a later stage. Most plant viruses are single-stranded RNA viruses. The RNA of these viruses carries at least two important genes which healthy, uninfected cells obviously do not possess: one gene codes for the viral enzyme, RNA replicase, which will be responsible for the synthesis of the new viral RNA molecules; the other gene codes for the capsid protein.

Thus, the formation of new virions occurs in four steps:
i) infecting viral RNA codes for RNA replicase;
ii) RNA replicase synthesizes new viral RNA;
iii) new viral RNA codes for new capsid proteins; and
iv) new viral RNA from ii) and new capsid proteins from iii) combine to form new virions.

TABLE 1 Characterized or partially characterized citrus viruses

Notes:
¹ H: helical. I: icosahedral, isometric
² Citrus mosaic virus, natsudaidai dwarf virus and navel orange infectious mottling virus from Japan are serologically related to SDV.
³ Short and long filamentous particles with single-stranded RNA.

Structure and replication of viroids

Viroids differ from viruses both in their structure and their mode of replication.

Viroids, such as the pathogens of exocortis and cachexia diseases of citrus (citrus exocortis viroid [CEV] and citrus cachexia viroid [CCaV], are small, infectious, single-stranded circular RNA molecules without a protein capsid. While in the virion, viral RNA is coated by capsid proteins, viroids are naked (non-coated) RNA molecules. Viroid RNA is ten times smaller than the smallest viral RNA. For instance, CCaV and CEV have, respectively, 300 and 371 nucleotide residues; the RNA of bacteriophage MS2 has 3 569 residues while that of tobacco mosaic virus (TMV) has 6 399. With some 20 000 residues, the RNA of CTV is one of the largest viral RNAs of plants.

The replication of viroids does not involve viroid-coded proteins. Such proteins have never been detected in viroid-infected cells, nor have they ever been obtained with cell-free systems for in vitro protein synthesis using viroid RNA as messenger RNA. Therefore, the replication of viroid RNA must be dependent on host enzymes.

TABLE 2 Biological properties of citrus viroid RNAs

Source: Duran-Vila et al.,1988a, 1988b and personal communication.
Notes:
¹ Symptom intensity: ++++, severe; +++, moderate; ++, mild; +, symptomless carrier (positive viroid replication); -, symptomless (no viroid replication).
² Note that all viroids replicate in citron.

Other viroids besides those of exocortis and cachexia have been identified in citrus. The citrus viroids (CVs) can be classified into five different groups: CEV, CV-I, CV-II, CV-III and CV-IV. CCaV is a member of group CV-II (CV-IIb, c). Tables 2 and 3 list the biological properties of these viroids. Hop stunt viroid (CHSV) has recently been found in commercial citrus in Sicily, on the basis of DNA-hybridization using DNA-HSV as probe. In fact, this probe reacts with all members of the CV-II group.

Finally, with the knowledge available at present, it appears that exocortis disease constitutes a complex of apparently unrelated viroids, some of which may not produce the classical symptom of the disease (bark scaling) on trifoliate orange.

Phloem-restricted prokaryotes

All living organisms belong to one of three large kingdoms: the archaea (formerly archae-bacteria), the bacteria (formerly eubacteria) and the eucaryota. The latter comprises the so-called "higher" organisms such as plants and animals, including fungi. The cell of these organisms, the eucaryotic cell, is characterized by the presence of a nucleus, a structure in which the cell genome - i.e. the DNA - is surrounded by a double membrane envelope which separates the DNA from the cytoplasm, except during cell division. In contrast, the cell of archaea and bacteria has no nucleus the genomic DNA is not separated from the cytoplasm by a membrane system. Such cells are called prokaryotic. Hence, prokaryotes are unicellular organisms belonging to the archaea or the bacteria.

There are two types of known phloem-restricted prokaryote: bacteria and mollicutes (previously called mycoplasmas) (see Table 4). For instance, the organism associated with citrus greening is a bacterium; the causal agent of citrus stubborn is a mollicute. One of the basic distinctions between bacteria and mollicutes is that bacteria have cell walls while mollicutes do not. The latter are simply surrounded by their cell membrane, a structure common to all living cells. In addition to the cell membrane, the bacteria are enveloped by a bacterial cell wall which is characterized by the presence of a peptidoglycan network, while the archaeal cell wall contains no peptidoglycan.

It has been shown in recent years that mollicutes evolved from bacteria - more precisely from ancestors of the clostridia. Clostridia are bacteria of the Gram-positive type with a low percentage of the bases guanine plus cytosine (G + C) in their DNA. The mollicutes have derived from ancestors of the clostridia by degenerative evolution, that is, by loss of DNA or genome reduction. The amount of DNA in the cell of a mollicute is three to six times less than that in the genera Clostridium, Bacillus and Escherichia. In fact, the mollicutes have the smallest amount of DNA of all self-replicating prokaryotes: they are the smallest and simplest of all living cells. However, they are not primitive organisms as they are the descendants of certain bacteria. Like the clostridia, they have a DNA with a low percentage of G + C, for example, only 26 percent in the case of S. citri.

TABLE 3 Biological properties of citrus viroid RNAs

Source: Duran-Vila et al., 1988a, 1988b; Semancik, 1988; Semancik, Roistacher and Duran-Vila, 1988; and personal communications of Duran-Vila and Semancik in 1989.
Notes:
¹ Symptom intensity: ++++, severe; +++, severe to moderate; ++, mild; +, very mild; +/-, barely visible; -, no symptoms, but positive viroid replication; ?, the type of symptoms induced by infections with single viroids is not yet known.
² According to Garnsey, personal communication, 1989.
³ According to Roistacher, Bash and Semancik, 1994.
⁴ According to Nauer et al., 1988.

TABLE 4: Phloem restricted - prokaryotes of citrus

To date, only one phloem-restricted bacterium has been found in citrus: the organism associated with greening disease (Figs 3 to 21). It has been shown that this bacterium has a membraneous cell wall of the Gramnegative type. Reports claiming culture of the greening bacterium have appeared but, at present, there is no experimental evidence to show that the cultured organism is indeed the bacterial agent of greening.

There are two types of phloem-restricted mollicute. The spiroplasmas, such as S. citri (Figs 22 to 24) - the agent of citrus stubborn-disease - have a helical morphology, are mobile and can be cultured. The mycoplasma-like organisms (MLOs) have no defined morphology: they are "pleiomorphic" and have never been obtained in culture. The MLOs have no cell wall, which is why they have always been assumed to be mollicute-like.

It was shown in 1989 that the MLOs are indeed true mollicutes, as they have DNA with a low percentage of G + C, the size of their genome is similar to that of the mollicutes and the nucleotide sequence of their 16 S ribosomal RNA is that of members of the mollicutes. An MLO is associated with the new citrus disease of increasing concern that is affecting more and more lime trees in Oman (Figs 25 to 30). In India, rubbery wood of citrus also involves an MLO.

Graft-transmissible diseases of unknown aetiology

The virus-like agents of the following graft-transmitted diseases of citrus have not yet been characterized: blight; brittle twig yellows; bud-union crease in Parson's Special mandarin on Volkamer lemon rootstock; concave gum-blind pocket; cristacortis; fatal yellows; fovea; gummy bark; gum pocket-gummy pitting; impietratura; Kassala disease of grapefruit; leaf curl; leathery leaf of mandarins in India (similar to satsuma dwarf); mosaic disease of citrus in India; Meiwa kumquat disease complex; tarocco pit; yellow corky vein (India) and yellow vein.

As the pathogens of these diseases are graft-transmissible, and on the basis of symptomatology, they are assumed to be viruses or viroids rather than phloem-restricted prokaryotes. For instance, the symptoms of gummy bark in sweet orange or those of Kassala disease in grapefruit are similar to those produced by the cachexia viroid in mandarin, which would seem to suggest a viroid aetiology for gummy bark and Kassala disease.

Blight (young tree decline) in Florida, declinio in Brazil, marchitamiento repenting in Uruguay, fruta bolita or declinamiento in Argentina and amachamiento in Mexico are similar diseases. The pathogen has not been transmitted by ordinary graft inoculation with buds or shoots from affected trees. However, the disease has recently been reproduced in Florida by placing mature, healthy trees adjacent to blighted trees and grafting the roots together. Positive transmissions have also been obtained with pieces of root from blight infected trees graft-inoculated to roots of healthy trees, indicating that blight is caused by an infectious graft-transmissible agent. Blight has not yet been reported in the Mediterranean or Near East regions.

Brittle twig yellows in Iran, fatal yellows in California, Meiwa kumquat disease complex in Spain, yellow corky vein in India, kumquat disease in Corsica and yellow vein in California are only of local significance. Leaf curl has been eradicated in Brazil; its agent is kept under quarantine greenhouse conditions in Bordeaux, France.

Kassala disease of grapefruit has not yet been shown to be graft-transmissible. However, as the symptoms of the disease in grapefruit are similar to those of cachexia in mandarin or gummy bark in sweet orange, the possibility of a viroid aetiology is apparent.

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