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.
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.
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 |