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Citrus Virus Diseases Bill Dawson All graft-transmissible diseases initially were considered to be caused by viruses Examples of changes •Viroids citrus exocortis cachexia xyloporosis •Phytoplasmas, Spiroplasmas stubborn new phytoplasma in Brazil that causes greening symptoms •Bacteria greening citrus varigated chlorosis http://www.apsnet.org/online/common/names/citrus.asp VIRAL DISEASES Citrus mosaic Satsuma dwarf-related virus Bud union crease Virus for some combinations, otherwise genetic or unknown Citrus leaf rugose genus Ilarvirus, Citrus leaf rugose virus (CLRV) Citrus yellow mosaic genus Badnavirus Crinkly leaf Crinkly leaf ilarvirus (strain of citrus variegation virus) Infectious variegation genus Ilarvirus, Citrus variegation virus (CVV) Navel infectious mottling Satsuma dwarf-related virus Psorosis Spirovirus (ophiovirus) proposed new group Satsuma dwarf Satsuma dwarf virus (SDV) Tatter leaf = citrange stunt genus Capillovirus, Citrus tatter leaf virus (probably a closely related strain of apple stem grooving capillovirus rather than a distinct virus Tristeza = decline and stem pitting, seedling yellows genus Closterovirus, Citrus tristeza virus (CTV) VIROIDS AND GRAFT-TRANSMISSIBLE PATHOGENS (GTP) Algerian navel orange virus Impietratura GTP GTP Blight = young tree decline, rough lemon decline Indian citrus ringspot GTP GTP Blind pocket Leaf curl GTP GTP Cachexia Leathery leaf Citrus cachexia viroid (Hostuviroid) GTP Chlorotic dwarf Leprosis White-fly transmitted GTP GTP associated with Brevipalpus spp. mites Citrus dwarfing Measls Varios viroids GTP Citrus yellow mottle Milam stem-pitting GTP GTP Citrus yellow ringspot Multiple sprouting disease GTP GTP Concave gum Nagami kumquat disease GTP GTP Cristacortis Ringspot diseases GTP Various GTPs Exocortis Vein enation = woody gall Citrus exocortis viroid (CEVd) (Pospiviroid) GTP (possible luteovirus) Fatal yellows Xyloporosis = cachexia GTP Citrus cachexia viroid (Hostuviroid) Gummy bark Yellow vein GTP, possible viroid GTP Gum pocket and gummy pittings Yellow vein clearing of lemon GTP, possible viroid GTP Edited by J.O. Whiteside, S.M. Garnsey, and L.W. Timmer APS Press The American Phytopathological Society 1988 Endemic Viruses of Concern •Tatterleaf / Citrange Stunt •Infectious Variegation •Citrus Leaf Rugose •Psorosis complex •Citrus leaf blotch •Citrus tristeza decline Tatter Leaf and Citrange Stunt virus complex latent infections in Meyer lemons apparently wide spread in China •Host Range and Symptoms when infected cultivars are propagated on trifoliate or hybrids (Swingle citrumelo, Carrizo, Troyer, and Kuharske citrange), trees are stunted and chlorotic, virus-induced incompability can infect a wide range of citrus cultivars causes mild symptoms if not on trifoliate rootstock can infect a wild range of herbaceous hosts Tatter Leaf and Citrange Stunt virus complex continued •Causal Agent one positive-sense RNA two subgenomic RNAs CP ORF 1 A(n) ORF 2 A(n) A(n) •Transmission and Epidemiology graft transmitted by infected budwood mechanically transmitted to a range of hosts thought to be aphid transmitted? •Identification characteristic bud union creasing symptoms on herbaceous hosts •Control virus-free budwood, difficult to remove decontaminate tools, knives use rootstocks other than Poncirus hybrids Wild type virus infected (8 dpi) Wild type virus infected (15 dpi) Healthy Infectious Variegation – Citrus Variegation Virus (CVV) •Host Range and Symptoms can infect most citrus species lemons, sour orange, citron, and grapefruit develop chlorotic leaf symptoms and distortion mild strains exist that cause only mild mottle or chlorotic flecking trees can be stunted, some fruit may be distorted symptoms are less in warm weather can be mechanically transmitted to some cowpeas (chlorotic or necrotic lesions and beans (chlorotic mottle or veinbanding) Infectious Variegation – Citrus Variegation Virus (CVV) continued •Causal Agent ilarvirus – 4 positive-sense RNAs, sperical particles Citrus crinkly leaf virus is a mild variant •Transmission and Epidemiology grafting – budwood mechanically inoculate seed transmitted – apparently rare pollen transmission? •Identification indexing by graft inoculation to lemon or citron mechanical inoculation to cowpea or bean •Control infected budwood can be freed by thermotherapy or shoot tip grafting then use virus-free budwood Leaf Rugose – Citrus leaf rugose virus (CLRV) •Host Range and Symptoms infects a broad range of citrus hosts Mexican lime, Eureka lemon, and Duncan grapefruit develop leaf puckering, pinpoint chlorotic spotting, and stunting can be mechanically transmitted to a range of noncitrus hosts Leaf Rugose – Citrus leaf rugose virus (CLRV) continued •Causal agent ilarvirus – 4 positive-sense RNAs, isometric particles •Transmission and Epidemiology grafting and mechanical transmission no vector known, but get some local spread pollen? •Identification indexing by grafting Eureka lemon or bush bean serology •Control use virus-free budwood decontamination of pruning tools Psorosis (psorosis A, mild; psorosis B, severe; concave gum; ) probably a complex of several diseases, which share common symptoms usually found present in old-line trees often bark scaling •Host Range and Symptoms symptoms stronger on young leaves ranging from chlorotic flecks, to leaf mottling and chlorotic patterns scaling and flaking of bark on the trunk and limbs of sweet orange and grapefruit and occasionally mandarins -- usually not on other citrus wood becomes impregnated with gum concave gum thought to be related, mandarins and sweet oranges are affected, deep concavities in the trunk and main branches Concave Gum Psorosis Psorosis (psorosis A, mild; psorosis B, severe) continued •Causal Agent •Transmission and Epidemiology graft transmitted seed transmission rare apparently some unknown vector •Identification field symptoms of bark scaling indexing by grafting to sweet orange or mandarin seedlings for leaf-flecking •Control use virus-free budwood, use seed only from virus-free trees can use shoot-tip grafting or thermotherapy decontaminate tools Citrus ringspot virus (CRSV) – Psorosis B •Host Range and Symptoms irregular spots or large, irregular chlorotic patterns on mature leaves frequently gum impregnated and are slightly raised on the lower surface fruit may have ringspots some isolates are mechanically transmitted to Chenopodium spp Citrus ringspot virus (CRSV) – Psorosis B continued •Causal Agent ophiovirus, 3 negative-sense RNAs very thin thread-like particles next slide has genome description •Transmission and Epidemiology graft transmissible mechanical transmissible vector suspected but unknown •Control virus-free budwood decontamination of tools The complete nucleotide sequence of a Spanish isolate of Citrus psorosis virus: comparative analysis with other ophioviruses Brief Report S. Mart´ın1, C. L´opez2, M. L. Garc´ıa3, G. NaumOngan´ıa3, O. Grau3, R. Flores2, P. Moreno1, and J. Guerri1 Arch Virol (2005) 150: 167–176 Association of citrus psorosis B symptoms with a sequence variant of the Citrus psorosis virus RNA 2 Velazquez, K (Velazquez, K.)1; Pina, JA (Pina, J. A.)1; Navarro, L (Navarro, L.)1; Moreno, P (Moreno, P.)1; Guerri, J (Guerri, J.) PLANT PATHOLOGY 61: 448-456 The virus induces two different syndromes: psorosis A (PsA), characterized by limited bark scaling lesions in the trunk and main limbs, and a more aggressive form of the disease called psorosis B (PsB) with rampant bark lesions affecting even thin branches and chlorotic blotches in old leaves. In the greenhouse, the PsA and PsB syndromes can be induced by graft inoculating healthy citrus seedlings with non-lesion or with lesion bark inoculum from PsA-affected field trees. PsA- and PsB-inducing CPsV sub-isolates obtained by this procedure from the same tree showed segments of the RNA 2 enabled discrimination between PsA- and PsB-associated sequence variants. (i) PsA-inducing isolates contain PsB-associated sequence variants at low frequency, (ii) the PsB-associated sequence variant is predominant in blistered twigs and gummy pustules affecting old leaves, characteristic of PsB isolates, and (iii) the PsB-associated sequence variant accumulates preferentially in bark lesions of the trunk and limbs. Citrus leaf blotch virus (CLBV) •Host Range and Symptoms first found in kumquat on Troyer citrange rootstock with bud union crease Spain, France, Japan, Australia, Florida associated with abnormal bud unions on poncirus hybrid rootstocks •Causal Agent filamentous particles one positive-stranded RNA with 2 subgenomics p41 p227 p40 Poly-A Poly-A •Transmission and Epidemiology no known vector seed transmitted •Control virus-free budwood alternative rootstocks if necessary Poly-A Citrus tristeza virus Causes four disease syndromes: decline – only on sour orange rootstocks can be quick decline – can be slow seedling yellows -- usually seen in greenhouse on sour orange and grapefruit no disease – mild strains stem pitting – on all rootstocks Department of Plant Industry Budwood certification Dr. Peggy Sieburth Winter Haven Budwood trees tested: Citrus tristeza virus decline isolate (MCA-13 positive) tested yearly OK to have budwood with the mild isolate of CTV Psorosis and Concave gum tested once by biological indexing now starting to test every 6 years Citrus leaf blotch virus (Dweet mottle virus) once every 6 years in budwood source trees and also in seed source trees since it is seed transmitted Citrus tatter leaf virus will start test for next year Infectious variegation virus is not tested for because it is mainly a problem for lemons which are limited in Florida Also test for viroids I, II, III, IV, V, and CEV every 6 years EXOTIC VIRUSES Exotic Viruses of Concern • • • • • • • Citrus chlorotic dwarf (CCD) Citrus yellow mosaic Leprosis Satsuma Dwarf Tristeza stem pitting Vein enation Sudden death Vein Enation (Woody Gall) important commercially only when severe galling occurs on young trees budded to rough lemon rootstocks •Host Range and Symptoms enations on the veins of Mexican lime, sour orange, and rough lemon swelling or galls on the stems of rough lemon and Mexican lime Vein Enation (Woody Gall) continued •Casual Agent spherical viruslike particles •Transmission grafting aphid transmitted – Myzus persicae, Toxoptera, citricida, and Aphis gossipii not mechanically transmitted •Control clean budwood avoid use of rough lemon rootstocks Leprosis and Zonate Chlorosis •Host Range and Symptoms observed primarily on sweet orange sour orange and mandarins are also show symptoms other citrus normally do not show symptoms symptoms are chlorotic lesions, sometimes with a necrotic center later lesions become flat or raised necrotic areas leaves and fruit abscise when lesions are abundant, can get twig dieback can mechanically transmit to Chenopodium spp Leprosis Leprosis and Zonate Chlorosis continued •Causal Agent controversy – may be two different viruses causing similar diseases rare nuclear form that is rod shaped and more prevalent cytoplasmic form of baciliform particles– would be expected to be a rhabdovirus positive-sense RNA virus with 2 RNAs virus is a mite virus – Brevipalpus spp. – virus multiplies in mites •Transmission and Epidemiology transmitted by mites -- millions of individual infections graft transmitted with difficulty virus does not move long distances, systemically •Control eliminate sources of inoculum control mites, acaricides to reduce mite population Satsuma dwarf virus (SDV) •Host Range and Symptoms wide host range in citrus widely spread in Japan stunting and narrow, boat- or spoon-shaped leaves in satsuma mandarin Chenopodium, cowpea, bean, Physalis, Gomphrena Satsuma dwarf virus (SDV) continued •Causal Agent small isometric virus with 2 RNAs genome on next slide •Transmission and Epidemiology graft transmitted by infected budwood mechanically transmitted to herbaceous hosts local spread, maybe a soilborne vector •Control virus-free budwood Nucleotide sequences and taxonomy of satsuma dwarf virus Toru Iwanami,1 Yoshiko Kondo1 and Alexander V. Karasev2 J Gen Virol. 1999 Mar;80 ( Pt 3):793-7. Citrus Sudden Death new disease reported in Brazil in 1999 •Host Range and Symptoms decline disease limited to Rangpur lime and to limited extent on Volkamer lemon during periods of drought rapid death of trees during drought characteristic yellow stain at or below the bud union Citrus Sudden Death -- continued •Causal Agent some controversy, a sobemovirus-like, marafivirus but CTV association genome on next slide • Transmission and Epidemiology spread looks similar to aphid transmission of CTV no vector identified can be grafted? •Identification decline – determine whether on Rangpur lime or Volkamer lemon yellow stain at graft union •Control virus-free budwood irrigation inarching Identification and Genomic Characterization of a New Virus (Tymoviridae Family) Associated with Citrus Sudden Death Disease Walter Maccheroni,1 Marcos C. Alegria,1 Christian C. Greggio,1 João Paulo Piazza,1 Rachel F. Kamla,1 Paula R. A. Zacharias,1 Moshe Bar-Joseph,1, Elliot W. Kitajima,2 Laura C. Assumpção,1 Giovana Camarotte,1 Jussara Cardozo,1 Elaine C. Casagrande,1 Fernanda Ferrari,1 Sulamita F. Franco,1 Poliana F. Giachetto,1 Alessandra Girasol,1 Hamilton Jordão Jr.,1 Vitor H. A. Silva,1 Leonardo C. A. Souza,1 Carlos I. Aguilar-Vildoso,1 Almir S. Zanca,1 Paulo Arruda,1 João Paulo Kitajima,1 Fernando C. Reinach,1 Jesus A. Ferro,1 and Ana C. R. da Silva1* J Virol. 2005 Mar;79(5):3028-37. Citrus Sudden Death inarching Citrus yellow mosaic virus India, perhaps Japan •Host Range and Symptoms mosaic of leaves does not reduce fruit production, but fruit have less juice and ascorbic acid wide citrus host range but apparently does not infect Mexican lime Citrus yellow mosaic virus •Causal Agent badnavirus – double-stranded circular DNA virus •Transmission and Epidemiology mechanically transmitted transmitted by aphids or mealybugs? Citrus chlorotic dwarf virus (CCD) found in Turkey •Host Range and Symptoms causes crinkled and puckered leaves in lemon, tangelo, and sweet orange •Transmission and Epidemiology transmitted by the bayberry whitefly Parabemisia myricae grafting of infected budwood mechanically transmitted •Identification can do greenhouse experiments, but no simple identification •Control CCD in lemon CCD in mandarin CCD in grapefruit Identification of a single-stranded DNA virus associated with citrus chlorotic dwarf disease, a new member in the family Geminiviridae Giuliana Loconsolea, Pasquale Saldarellib, Harshavardhan Doddapanenic, Vito Savinoa, b, Giovanni P. Martellia, b, Maria Saponarib, Virology 432: 162-172 (2012) Citrus Tristeza Virus (CTV) – Decline •Host Range and Symptoms can infect most citrus varieties and relatives Poncirus spp are resistant to most isolates disease is limited to scions on sour orange rootstocks Roots of declining tree – no feeder roots Citrus tristeza virus – decline •Causal Agent positive-stranded RNA virus ~ 20,000 nts RdRp PRO PRO MT p6 p61 p18 p20 HEL p33 HSP70 p27 CP p13 p23 Gold-labeled CP antiserum Gold-labeled CPm antiserum CTV virions From: Tian et al. J. Gen. Virol.80:1111 (1999) p27 (minor capsid protein, CPm) p25 (major capsid protein, CP) Citrus tristeza virus ORF 1a 1b 2 3 4 5 6 p33 HSP70h PRO PRO MT 7 8 9 10 11 CPm p18 p20 HEL IDR 5’ probe 3’ probe RdRp Polyprotein: Replicase p6 ( p61 CP p13 p23 ) () ( ) ( ) ( +1 Ribosomal frameshift: RdRp ) ( ) ( ) ( ) ( ) ( Proteins ) p33 p6 HSP70h p61 CPm CP p18 p13 p20 p23 Citrus tristeza virus (CTV) – decline •Transmission and Epidemiology aphid transmitted by a series of aphids, brown citrus aphid best also melon, cotton aphids transmitted in a semi-persistent manner – ~ 1 hr to ~ 24 hr •Identification in field, identify rootstock – sour orange bud union staining, scion overgrowth, thickened bark at union serology – can detect CTV; can differentiate FL mild from decline biological assay in greenhouse vein clearing and leaf cupping in Mexican lime •Control use alternative rootstock use virus-free or decline-free budwood Citrus tristeza virus (CTV) – stem pitting no severe stem pitting isolates of CTV known to be in Florida every effort is being made to keep them out •Host Range and Symptoms stem pitting does not kill trees reduces vigor, reduces growth, reduces yield and fruit size stem pitting is specific to virus isolate and host some isolates cause stem pitting in grapefruit some isolates cause stem pitting in sweet orange some isolates cause stem pitting in both mandarins are more tolerant •Control keep stem pitting isolates out mild strain cross protection FS674 on DG Risk evaluation of exotic pathogens for citrus Disease Impact Intro Estab Spread Estab m Estab F Detection Control factor 1 factor 2 HLB 10 7 7.1 7 7.03 347.90 2.6 10 1828.7 90454.0 100.00% 100.00% Blackspot 5.8 6.2 8.7 10 8.30 539.40 3.3 6.9 1096.1 71236.4 59.94% 78.75% CTV-SP 6.1 5.8 9.8 9.1 8.23 517.24 2.5 5.5 690.6 43383.8 37.76% 47.96% Canker 7.9 10 7.7 10 9.23 770.00 1 3.5 255.3 21290.5 13.96% 23.54% 7 4.1 10 7.8 7.30 319.80 0.9 8.4 386.3 16923.8 21.13% 18.71% Phaeoram 5.2 3.2 6.8 9.3 6.43 202.37 2 7.2 481.7 15153.3 26.34% 16.75% CCD 1.9 2.9 5.1 4.3 4.10 63.60 10 7.1 553.1 8579.2 30.24% 9.48% Leprosis 2.4 4.2 3.8 3.6 3.87 57.46 4 3.5 129.9 1930.5 7.10% 2.13% Swt. Scab 1.2 2.7 4.7 4.7 4.03 59.64 1.6 3.2 24.8 366.4 1.36% 0.41% Vein Enation 0.2 3.1 4.7 7.9 5.23 115.10 2.5 3.6 9.4 207.2 0.52% 0.23% SDV 0.8 2.6 4.1 3.8 3.50 40.51 1.2 4.8 16.1 186.7 0.88% 0.21% CYM 1.9 2.1 4.1 3.1 3.10 26.69 1 2.6 15.3 131.9 0.84% 0.15% ACD 0.2 1.3 2.1 2.4 1.93 6.55 9 8.9 31.0 105.0 1.69% 0.12% Stubborn 1 4.2 2.1 3.8 3.37 33.52 0.6 4.9 9.9 98.5 0.54% 0.11% Pow. Mil 0.6 1.3 2.3 4 2.53 11.96 0.8 2.7 3.3 15.5 0.18% 0.02% LWB 0.7 1.3 1.8 1.9 1.67 4.45 1.7 1.9 3.8 10.1 0.21% 0.01% Mal Secco 0.4 2.1 1.1 1.8 1.67 4.16 1.3 1.5 1.3 3.2 0.07% 0.00% CVC 4factRel % 6factRel% Mild strain cross protection Purposely inoculate trees with a mild strain of the virus to prevent infection by severe stem pitting isolate Common practice in Brazil, South Africa, Australia How does cross protection work? different strains of CTV do not cross protect against each other must find a mild strain that has close sequence to the severe strain otherwise must make one CTV-based expression vector ORF L1 1a 1b 2 3 p33 L2 MT IDR 4 5 HSP70h 6 7 CPm 8 9 10 11 p18 p20 HEL RdRp p6 p61 CP p13 p23 Green fluorescent protein from jellyfish L1 p33 L2 MT IDR gfp HSP70h p18 p20 HEL RdRp p6 p61 CPm CP p13 p23 DIFFERENTIAL SUSCEPTIBILITY OF DIFFERENT HOSTS TO T36 ML CM MV SO DG 1 mm C mac So Orange No protection against GFP-expressing T36 strain-based virus: T68-1 T3 T30 VT T36 Protection FS 703 protection FS672 challenge No protection FS672 challenge FS 703 protection FS701 challenge No protection FS701 challenge What about CTV decline? •Have to have a mild isolate of the T36 strain •Probably does not exist in Florida •Then have to make one Florida CTV strains PRO PRO MT decline RdRp p6 p61 HEL p33 HSP70 PRO PRO MT mild p18 p20 RdRp p6 p27 CP p13 p61 p23 p18 p20 HEL p33 HSP70 p27 CP p13 p23 Genetic system for CTV cDNA Healthy seedling CTV Infected tree dsRNA Bacteria Virus particles in vitro transcription Protoplast virus RNA Healthy Seedling yellows reaction on sour orange plants rCTV-T36 WT CTV-T36 T36/T30 hybrids p33 HSP70h CPm p18 p20 3’ RdRp p6 p33 p61 HSP70h CP CPm p13 p18 p23 p20 3’ RdRp p6 p33 p61 HSP70h CP CPm p13 p23 p20 p18 3’ RdRp p6 p33 p61 HSP70h CP CPm p13 p23 p20 p18 3’ RdRp p6 p33 p61 HSP70h CP p13 p20 p18 CPm p23 3’ RdRp p6 p33 p61 HSP70h CP CPm p13 p18 p23 p20 3’ RdRp p6 p61 CP p13 p23 PRO PRO MT decline RdRp p6 p61 PRO PRO MT RdRp p6 p27 CP p13 p61 hybrid * + p23 p18 p20 HEL p33 HSP70 PRO PRO MT p18 p20 HEL p33 HSP70 mild SY RdRp p6 p27 CP p13 p61 p23 p18 p20 HEL p33 HSP70 p27 CP p13 p23 Healthy T30 T36 P23+NTR of T30 in T36 Sour Orange P65+p61 of T30 Substitution of p23 gene + NTR of T30 into genome of T36 creates cross-protecting isolate against seedling yellows T36-infected sour orange Healthy sour orange In the center – p23+NTR-T30/T36 hybrid-infected sour orange, later challenged with T36 field test to protect citrus on sour orange rootstocks