TABLE 7 Citrus virus and virus-like diseases: rutaceous and non-rutaceous plants that are symptomatic

Disease (or agent) Symptomatic Plants
Blight Sweet orange and Grapefruit (when grafted on Rough lemon, Citrus volkameriana, Rangpur lime, evidence of disease is lower on mandarins and lemons)
Brittle twig yellows Sweet orange in Iran
Bud-union crease (Marumi and Nagami kumquat agent) Parson's Special mandarin on C. volkameriana (Corsica)
Bud-union crease Sweet orange on Rough lemon (South Africa and Spain)
Cachexia-Xyloporosis Citrus macrophylla, Clementine, Kumquat, MANDARINS, Rangpur lime, Satsuma, Sweet lime, TANGELOS (Nocatee, Orlando, Seminola, Wekiwa), Cucumis sativus (cucumber)
Concave gum-Blind pocket Clementines, Grapefruits, MANDARINS, Siamelo, SWEET ORANGES, Tangelos (Orlando, Sampon, Sunshine, Waft), Dweet tangor
Cristacortis Citrus pectinifera, Clemea, Clementine, Grapefruits, MANDARINS, Rough lemon, Satsuma, Siamelos, SOUR ORANGE, Sweet lime, SWEET ORANGES, TANGELOS, Dweet tangor
Exocortis CITRANGES, Etrog citron, Harvey lemon, Mandarin limes, PONCIRUS TRIFOLIATA, Rangpur lime, Sweet lime, Tahiti lime, Chrysanthemum (CEV), Gynura aurantiaca (CEV), Petunia hybrida, Tomato, Solanum spp.
Fatal yellows Citrus macrophylla and lemon on C. macrophylla, in California
Fovea Murcott tangor in Florida
Greening Catharanthus roseus, (dodder transmission), Citrons, Grapefruits, Kumquats, Lemons, MANDARINS, Pomelos, Rough lemon, Rangpur lime, Sweet lime, SWEET ORANGES, TANGELOS, West Indian lime
Gummy bark Rough lemon, SWEET ORANGE
Gum pocket P. trifoliata
Impietratura Bergamot, C. VOLKAMERIANA, Clementine, Grapefruits, Lemons, Rough lemon, Sour orange, SWEET ORANGES, Tangelos, Dweet tangor
Infectious variegation-Crinkly leaf Citron (Etrog), Clementine, Grapefruits, LEMONS, CLEOPATRA MANDARIN, Pomelos, SATSUMA, Sour orange, Sweet lime, Sweet oranges, West Indian lime, Chenopodium quinoa, Crotalaria spectabilis, Cucumis sativus, Gomphrena globosa, Momordica balsamina, Phaseolus aureus, P. vulgaris, Vigna sinensis
Kumquat (Meiwa) agent(s) Inoculation of the agent(s) induces vein clearing of sweet orange, Troyer citrange, Citrus macrophylla, Dweet tangor, Marsh grapefruit, Orlando tangelo, Sour orange and Cleopatra mandarin, stem pitting in Etrog citron, graft incompatibility on Troyer citrange (Spain)
Kumquat (Marumi and Nagami) agent Inoculation of the agent induces bud-union crease of Parson's Special mandarin on Volkameriana lemon (Corsica)
Leaf curl Citrons, Grapefruits, Lemons, Mandarins, Pomelos, Sweet lime, SWEET ORANGES, West Indian lime
Leaf rugose Mexican lime, Eureka lemon, Duncan grapefruit, Bush bean (cultivar Red Kidney), Crotalaria spectabilis, Vigna unguiculata, Chenopodium quinoa, Cucumis sativus, Momordica balsamina
Leathery leaf in India See Satsuma dwarf
Leprosis Grapefruits, Mandarins, Rough lemons, SOUR ORANGE, SWEET ORANGE
Mosaic (India) Sweet orange, Kagzi lime, Rangpur lime, Grapefruit, Mandarin, Lemon, Pomelo, Aegle marmelos
Mosaic (Japan) See Satsuma dwarf
Multiple sprouting Bergamots, Grapefruits, Kumquats, Lemons, Sour orange, Sweet oranges
Natsudaidai virus (Japan) See Satsuma dwarf
Navel orange infectious mottling (Japan) See Satsuma dwarf
Phytophthora Bergamot, Citrons, Citrus macrophylla, Clementine, Grapefruit, Lemons, Mandarins, Rangpur lime, Rough lemon, Satsuma, Sweet lime, SWEET ORANGE, Tahiti lime, West Indian lime
Psorosis A Bark scaling: GRAPEFRUITS, Mandarins, SWEET ORANGE, Tangelo (Orlando) Symptoms on leaves: Citrons, Grapefruits, Lemons, Mandarins, Pomelos, Rough lemon, SOUR ORANGE, SWEET ORANGES, DWEET TANGOR, Tangelos, WEST INDIAN LIME, Chenopodium quinoa
Ringspot Citrange Troyer, Citremon 1449, Citrus excelsa, GRAPEFRUITS, Lemons, Mandarin (Parson's Special, Szinkom), Poncirus trifoliata (Pomeroy), Rangpur lime, Rough lemon, Severinia buxifolia, Sour orange, Sweet oranges, Dweet tangor, West Indian lime, cowpea, bean, Chenopodium quinoa, Gomphrena globosa, Crotalaria spectabilis, Petunia hybrids, Zinnia elegans
Rubbery wood Lemon, small-fruited acid lime
Rumple Lemon (Eureka, Femminello, Lisbon, Villafranca)
Satsuma dwarf (leathery leaf in India) Citranges (Carrizo, Morton, Troyer), Citrus excelsa, C. junos, Clementine, Grapefruits, Eureka lemon, Mandarin (Dancy, Cleopatra, King), Natsudaidai, Poncirus trifoliata, Rough lemon, Satsuma, Sour orange, Sweet oranges, Tangelos, West Indian lime, Chenopodium capitatum and quinoa, Nicotiana tabacum, Petunia hybrids, Phaseolus aureus, P. vulgaris, Physalis floridana, Sesamum indicum, Vigna sinensis
Seedling yellows Grapefruits, LEMONS (Eureka, Lisbon), Minneola tangelo, Pomelos, SOUR ORANGE, West Indian lime
Stubborn Calamondin, Catharanthus roseus and many other non-rutaceous species, Citrange, Grapefruit, Kumquat, Lemon, Mandarin, Mandarin limes, Pomelo (Chandler), Rough lemon, Satsuma, Sour orange, Sweet lime, SWEET ORANGES, Tangelos, West Indian lime
Sweet orange vein clearing Sweet orange
Tatterleaf-Citrange stunt Citrus excelsa, CITRANGE (Carrizo, Rusk, Troyer), Citremons (1448, 1449), Satsuma or sweet orange on P. trifoliata, Chenopodium quinoa, Blackeye cowpea, Masterpiece bean
Tristeza I - STEM PITTING WHETHER USED AS SEEDLINGS, SCIONS OR ROOTSTOCKS
a) Strains of California, Florida, Spain: Walve citrange, Etrog citron, Citrus excelsa, C. hystrix, C. junos, C. macrophylla, Sweet lime, West Indian lime
b) Strains of South Africa, South America, Japan: Species and varieties in a) and: Citranges (Morton, Rusk, Savage), Grapefruits, Hassaku, Kumquats, Limequats, Pomelos, Sweet orange (Mediterranean, Pera), Tahiti lime, Tangor
c) Strains of certain areas of Brazil, Japan, Southeast Asia, Cameroon, Mauritius, Reunion: Species and varieties in a) and b) and Citrumelo 1452, Rangpur lime, Tangors
II - DECLINE WHEN GRAFTED ON SOUR ORANGE (OR ON LEMONS) Species or varieties except lemons and sour orange
III - DECLINE UNDER CERTAIN CONDITIONS Mandarins on Rangpur lime (Brazil), Sweet orange on Rangpur lime (Brazil), Sweet orange on P. trifoliata (?) (South America), Sweet orange on Troyer citrange (California)
Vein clearing (Meiwa kumquat) agent Sweet orange, Troyer citrange, C. macrophylla, etc. See Kumquat agent(s)
Vein enation-Woody gall On leaves: Citrons, Lemons, Mandarins, ROUGH LEMON, SOUR ORANGE, Sweet oranges, WEST INDIAN LIME Galls on trunk: C. VOLKAMERIANA, Rangpur lime, Rough Lemon, West Indian lime
Witches' broom Small-fruited acid lime trees in Oman and the United Arab Emirates, Troyer citrange, Catharanthus roseus (dodder transmission), P. trifoliata, Eureka lemon, Rough lemon, Citron, Palestine sweet lime, Sweet limetta
Yellow vein Citron (Etrog), Citrus macrophylla, C. volkameriana, Kumquats, Lemons, Limequats, ROUGH LEMON, Tangelos, WEST INDIAN LIME
Zonate chlorosis Grapefruits, KUMQUATS, LEMONS, MANDARINS, P. TRIFOLIATA, SWEET ORANGES, Tahiti lime, West Indian lime

Note:
Names in capital letters: most susceptible species, varieties or combinations.

TABLE 8 Citrus virus and virus-like diseases: rutaceous and non rutaceous plants which are symptomless

Disease Symptomless plants
Blight Sweet orange or Grapefruit on Swingle citrumelo, Sweet orange and Cleopatra mandarin are less affected than trees on other rootstocks
Cachexia-Xyloporosis Citranges, Citrons, Citrumelos, Grapefruits, Lemons, Poncirus trifoliata, Pomelos, Rough lemon, Sour orange, Sweet oranges, Tangelos (Webber, Williams), West Indian lime
Concave gum-Blind pocket Citranges, Citrons, Lemons, Rough lemon, P. trifoliata, Sour orange, Sweet lime, West Indian lime
Cristacortis Bergamot, Citranges (Carrizo, Troyer), Citrons, Citrus hystrix, C. volkameriana, Lemons, P. trifoliata, West Indian lime
Exocortis Clementine, Grapefruits, Lemons (Eureka, Lisbon), Mandarins, Pomelos, Rough lemon, Sour orange, Sweet oranges, Tangelos, Tangor, West Indian lime
Greening Citranges, P. trifoliata
Gummy bark Citrus amblicarpa, Grapefruits, Lemons, Mandarins, Rangpur lime, Sour orange, Orlando tangelo, P. trifoliata, West Indian lime
Gum pocket Troyer citrange, Empress mandarin, Rangpur lime
Impietratura Chinotto, Citron, Kumquat
Infectious variegation-Crinkly leaf Willowleaf mandarin, P. trifoliata
Leaf curl Troyer citrange, Cleopatra mandarin, P. trifoliata, Rangpur lime
Leprosis Sweet orange (Valencia late in Florida)
Multiple sprouting Citranges, Citrumelos, P. trifoliata
Phytophthora Citranges (Carrizo, Morton, Rusk, Troyer), Citrus excelsa, C. junos, Pomelos, P. trifoliata, Siamelos, Sour orange, Tangelo seminole
Psorosis A (bark scaling) Citranges, Lemons, Mandarin (Comun de Concordia), P. trifoliata, Rough lemon, Sour orange, Citrus daidai, Clausena sp.
Rumple Clementine, Grapefruits, Mandarins, Sour orange, Sweet orange
Satsuma dwarf Etrog citron, Hassaku, Tahiti lime, Orlando tangelo, Chenopodium amaranticolor, Cucumis sativus, Nicotiana glutinosa, Viburnum odoratissimum
Seedling yellows Mandarins, Rough lemon, Sweet orange
Stubborn Citrange (Cunningham, Troyer), P. trifoliata
Tatterleaf-Citrange stunt Aeglopsis chevalieri, Lemons, Rough lemon, Severinia buxifolia, Sour orange, Sweet orange, West Indian lime
Tristeza I - NO STEM PITTING WHETHER USED AS SEEDLINGS, SCIONS OR ROOTSTOCKS:
Citranges (Carrizo, Troyer), Citrumelo 4475, Lemons, Mandarins, P. trifoliata, Rangpur lime, Rough lemon, Satsuma, Sour orange, Sweet orange, Tangelo. (Some tristeza isolates do stem pit some of these hosts
- Lemons, Mandarins, Rangpur lime, Rough lemon and Sweet orange)
II - NO DECLINE WHEN GRAFTED:
Mandarins, Sweet oranges on Citranges (Carrizo, Troyer), Citrumelo 4475, Cleopatra mandarin, P. trifoliata, Rangpur lime, Rough lemon
Yellow vein P. trifoliata

TABLE 10 Insect and mite vectors of virus and virus-like disease agents of citrus

Disease Agent Vector Type of vector Persistent; semi- persistent or non- persistent agent
Greening BLO Diaphorina citri Kuw. Psyllid Persistent
Trioza erytreae Del Guercio Psyllid Persistent
Leathery leaf (India) Virus Aphis gossypii Glover Aphid Not known
Leprosis Capillovirus (?) Brevipalpus phoenicis (in Brazil) Mite  
Brevipalpus californicus (in Florida) Mite  
Brevipalpus obovatus (in Argentina and Venezuela) Mite  
Mosaic (India) Probably virus Myzus persiceae Sulz.    
Aphid   Aphis craccivora Koch   Non-persistent
Psorosis (Argentina) Virus Not identified, but evidence of natural spread    
Ringspot (Texas, Florida) Virus Not identified, but evidence of natural spread    
Rubbery wood MLO Not identified, but natural spread is suspected    
Satsuma dwarf Virus Not identified, but evidence of natural spread    
Stubborn Spiroplasma Neoaliturus (Circulifer) haematoceps Mulsant & Rey Leafhopper Persistent
Neoaliturus (Circulifer) tenellus Baker Leafhopper Persistent
Scaphytopius nitridus Baker Leafhopper Persistent
Scaphytopius acutus delongi Baker Leafhopper Persistent
Tristeza Closterovirus Toxoptera citricida Kirk. Aphid Semi- persistent
Aphis gossypii Glover Aphid Semi- persistent
A. citricola van der Goot (= A. spiraecola Patch) Aphid Semi- persistent
A. craccivora Koch Aphid Semi- persistent
M. persicae Sulz. Aphid Semi- persistent
Toxoptera aurantii Bsy. Aphid Semi- persistent
Dactynotus jaceae L. Aphid Semi- persistent
Vein enation-Woody gall Luteovirus T. citricida Kirk. Aphid Persistent
A. gossypii Glover Aphid Persistent
M. persicae Sulz. Aphid Persistent
Witches' broom MLO The leafhopper Hishimonus phycitis is a putative vector Leafhopper Persistent

TABLE 11 Relationships between citrus disease agents and homopterous insect vectors

Citrus disease agents Spiroplasma, BLO, MLO Mosaic virus (India) Tristeza virus vein enation Virus
Type of agent Persistent agent Non-persistent agent Semi-persistent agent Persistent agent
(circulative) (non-circulative) (non-circulative) (circulative)
(propagative) (non-propagative) (non-propagative) (non-propagative)
  (stylet-borne)    
Vectors Leafhoppers, psyllids Aphids Aphids Aphids
Localization of agent in plant Phloem-restricted Not phloem-restricted Phloem Phloem-restricted
  Superficial cell-layers    
Acquisition period Long (24-48 hours) Brief (minutes or less) Long (24-48 hours) Long
  (insect has to find phloem tissue) (time for sap-sampling puncture) (insect has to find phloem tissue) Long
Incubation period Long (8-12 days) None (insect is immediately infectious) None Long
Retention period Very long (whole life of insect) Short (a few hours at most) Quite long (2-3 weeks) Very long (perhaps whole life of insect)
Multiplication of agent in insect Yes No No No
Transovarial transmission No No No No

TABLE 12 Indicator plants for the detection of the major virus and virus-like agents of citrus

Agents of Indicator plant Symptoms observed Time required for symptom expression (temperature condition)
Blight (uncharacterized) Adult Valencia sweet orange on rough lemon, graft inoculated with root pieces from candidate tree Blight syndrome 2 years at least
Cachexia (viroid) Parson's Special mandarin on rough lemon1 Gumming at graft union(Figs 58, 59) 1-2 years (warm)
Concave gum-Blind pocket(uncharacterized) • Sweet orange seedling Vein flecking, oak-leaf patterns on young leaves A few weeks (cool)
• Sweet orange seedling tree Cortical symptoms A few years
Cristacortis (uncharacterized) • Sweet orange seedling Vein flecking, oak-leaf patterns on young leaves A few weeks (cool)
• Orlando or Wekiwa tangelo seedling Stem pitting 1-2 years
Exocortis complex (viroid complex) Etrog citron 861 -S1 on rough lemon1 Leaf epinasty and/or stunting midvein necrosis, petiole necrosis, leaf tip browning (Fig. 90) Weeks to months (warm)
Greening (BLO) Sweet orange seedling Leaf yellowing and mottling with zinc deficiency-like patterns Several months (Asian form: warm; African form: cool)
Gummy bark (uncharacterized) Sweet orange on rough lemon Gumming of sweet orange and sometimes rough lemon bark, bud-union constriction Several years
Gum pocket-Gummy pitting Sweet orange on Poncirus trifoliata Gum pockets in the bark and wood of P. trifoliata Several years
Impietratura, (uncharacterized) • Sweet orange seedling Vein flecking, oak-leaf patterns on young leaves A few weeks (cool)
• Fruiting grapefruit Gum in fruit albedo A few months
Infectious variegation-Crinkly leaf (ilarvirus) • Lemon seedling, Etrog citron Leaf variegation and/or crinkle A few weeks
• Cowpea (cultivar Black) Chlorotic lesion on mechanically infected leaves A few days
Leaf rugose (ilarvirus) • Mexican time seedling Leaf puckering A few weeks
• Eureka lemon seedling Pinpoint chlorotic spotting A few weeks
• Red kidney, Bush bean Local lesions A few days
Psorosis A (scaly bark) (virus) • Sweet orange seedling Vein flecking, oak-leaf patterns on young leaves A few weeks (cool)
• Sweet orange tree Bark scaling and flaking A few years
Ringspot (virus) • Sweet orange seedling Necrotic shoot reaction ring patterns, mottled chlorotic areas on young leaves. Chlorotic patterns on mature leaves. Stem lesions A few weeks
Chenopodium quinoa Necrotic local lesions on mechanically infected, fully expended leaves. No systemic infection A few days
Rubbery wood (MLO) Lemon seedling Flexible, downward bent shoots A few months
Satsuma dwarf (virus) • Satsuma mandarin Stunting, boat- or spoon-shaped leaves Several months (cool)
• Sesame, C. quinoa Local lesions on mechanically infected leaves A few days
Stubborn (Spiroplasma citri) Madame Vinous or Hamlin sweet orange seedling Leaf tip chlorosis, leaf mottle, leaf cupping, stunting A few months (warm)
Tatterleaf-Citrange stunt(virus) C. excelsa seedling Deformed leaves with chlorotic zones A few months
• Rusk citrange seedling Deformed leaves with chlorotic leaf blotch. Stem with zigzag growth pattern A few months
C. quinoa Chlorotic local lesions and systemic chlorotic mottle A few days
Tristeza (closterovirus) Small-fruited acid lime seedlings Leaf vein clearing, leaf cupping, stem pitting, stunting Weeks to months (cool)
Tristeza with seedling yellows reaction Grapefruit, lemon, sour orange seedlings Stunting, leaf yellows at seedling top A few months
Vein enation-Woody gall (luteovirus) • Small-fruited acid lime seedling Vein enations A few months
• Small-fruited acid lime or rough lemon seedlings Galls on stems near thorns in association with wounds A few months
Witches' broom (MLO) Small-fruited acid lime seedling Small to very small leaves, witches' brooms Several months (warm)

1 Other vigorous rootstock seedlings such as C. volkameriana may be used.

TABLE 13 Techniques for the detection of virus and virus-like agents of citrus or constituents of the agents

Disease Techniques Agent or agent-constituent detected
Blight Sodium dodecyl sulphate (SDS)- polyacrylamide gel electrophoresis (PAGE) Immunospot, western blot Proteins (pathogenesis-related proteins?)
Cachexia Sequential PAGE (sPAGE) and silver staining of the viroid RNA bands Cachexia viroid(s)
Exocortis sPAGE Exocortis viroid(s)
Greening • Electron microscopy (Figs 3-21) Greening BLO in sieve tubes
• Enzyme-linked immunosorbent assay(ELISA) with monoclonal antibodies (MA) Greening BLO
• Immunofluorescence (MA) on leaf midrib sections Greening BLO in phloem tissue
• DNA probes BLO DNA
Infectious variegation-Crinkly ELISA Viral coat protein
Leaf rugose ELISA Viral coat protein
Psorosis (California isolate) PAGE Double-stranded RNAs
Stubborn • Culture of S. citri S. citri
• ELISA (polyclonal antibodies, PA) Membrane proteins of S. citri
S. citri DNA probes S. citri DNA
• Amplification by polymerase chain reaction (PCR) of spiralin-gene sequences Spiralin-gene of S. citri
• Electron microscopy (Figs 22-24) S. citri in sieve tubes
Tatterleaf • PAGE Double-stranded RNAs
• ELISA Viral coat protein
Tristeza • Electron microscopy Bundles of tristeza virions in phloem tissue
• ELISA DIBA (dot immuno binding assay), IEM (immuno electron microscopy) with polyclonal or monoclonal antibodies Viral coat protein
• cDNA probes Viral RNA
• Light microscopy after azure A staining of sections Aggregates of tristeza virions
• PAGE Double-stranded RNAs
Vein enation • Electron microscopy Virions
• PAGE Double-stranded RNAs
Witches' broom • ELISA (monoclonal antibodies, MA) Membrane proteins of Witches' broom MILO
• Immunofluorescence (MA) on leaf midrib sections Witches' broom MILO in phloem tissue
• DNA probes MLO DNA
• Electron microscopy (Figs 25-30) Witches' broom MLO in sieve tubes