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Replication/Accumulation and Symptom Expression of Citrus Viroids on Some Species of Citrus and Related Genera

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Replication/Accumulation and Symptom Expression of Citrus Viroids on Some Species of Citrus and Related Genera Fifteenth IOCV Conference, 2002—Viroids Replication/Accumulation and Symptom Expression of Citrus Viroids on Some Species of Citrus and Related Genera C. J. Barbosa, J. A. Pina, L. Navarro, and N. Duran-Vila ABSTRACT. Plants of 32 species of Citrus and related genera grafted on rough lemon root- stock were inoculated with an artificial mixture of citrus viroids containing Citrus exocortis viroid, Citrus viroid I, Citrus viroid II, Citrus viroid III and Citrus viroid IV. Infection and viroid titers were determined by sPAGE and molecular hybridization analysis. Plants in which viroid infection could not be detected were further indexed by inoculation on Etrog citron 861 S1. Under the conditions of this assay most of the species were symptomless carriers. Only Citrus excelsa, C. ichangensis, C. karna, C. latifolia, C. meyeri and C. pyriformis developed symptoms as a result of viroid infection. Comparative analysis of nucleic acid extracts from bark versus leaf blade tis- sues indicated that in 10 species, viroid that were readily detectable from bark were undetectable from leaf blade tissues by sPAGE. Citrus can be infected by several The objective of this study was to viroids (7) including Citrus exocor- evaluate the response of 32 acces- tis viroid (CEVd) and specific vari- sions of the Instituto Valenciano de ants of Citrus viroid II (CVd-II, Hop Investigaciones Agrarias (IVIA) ger- stunt viroid) that cause the exocor- mplasm bank to viroid infection. tis and cachexia diseases respec- Such a wide-ranging study has not tively (17, 24, 25). Most viroid-host been previously reported. combinations appear to be symp- tomless, and exocortis and cachexia MATERIALS AND METHODS symptoms are only observed when their viroid agents infect sensitive Plant materials and viroid species. Trifoliate orange, its inoculation. Plants of 22 species of hybrids (the citranges) and Rangpur Citrus and 10 species of related gen- lime, used as rootstocks, and the era (Table 1) of the IVIA germplasm Etrog citron indicator have been collection (www.ivia.es) grafted on described as exocortis sensitive spe- rough lemon rootstock were bark- cies. Alemow, Rangpur lime and Pal- graft inoculated with an artificial estine sweet lime used as rootstocks, mixture of citrus viroids maintained and several mandarins, including in Fino lemon. The inoculated clementines, satsumas and their plants were kept under greenhouse hybrids are sensitive to cachexia. conditions at 28-32°C for 5 yr before Reports dealing with the expres- initiating this study. sion of exocortis and cachexia symp- The mixture of citrus viroids toms on sweet limes (23), citrumelo used as inoculum had been previ- (3) and Cleopatra mandarin (13) were ously obtained by graft inoculation based on the observation of symptoms of Fino lemon plants with the fol- on plants infected with field isolates lowing viroid sources: CEVd (E-117) characterized only by the response of (9), Citrus viroid I (CVd-I, Citrus exocortis and cachexia indicators. At bent leaf viroid) (variant Ia) (8), Cit- present, the effect of specific viroids rus viroid II (CVd-II, Hop stunt species has only been tested on Etrog viroid) (IIa-117 and X-707) (14), Cit- citron (7) and trifoliate orange (21), rus viroid III (variant IIIb) (8), and whereas the response of most species Citrus viroid IV (CVd-IV) (16). of Citrus and related genera to viroid In all instances viroid infection infection remains unknown. was determined by sPAGE and 264 Fifteenth IOCVConference,2002—Viroids TABLE 1 DETECTION OF CITRUS VIROIDS ON INOCULATED SPECIES OF CITRUS AND CITRUS RELATIVES z Viroid detection and titer Accession Citrus and citrus relatives number CEVd CVd-I CVd-II CVd-III CVd-IV Symptoms Citrus bergamia Risso and Poit. (cv. Calabria) IVIA–254 4 2334 — Citrus depressa Hay IVIA–238 43243 — Citrus excelsa Wester IVIA-167 13244 + Citrus grandis L. Osb. IVIA-321 11221 — Citrus halimii B.C. Stone IVIA-278 12144 — Citrus hystrix DC. IVIA-178 2 0 1 2 2 — Citrus ichangensis Swing. IVIA-235 2 2 0 3 3 + Citrus karna Raf. IVIA-242 44343 + Citrus latifolia Tan. (cv Bearrs) IVIA-124 1 0 1 4 4 + Citrus limon L. Burm f. (cv. Verna) IVIA-50 42232 — Citrus macroptera Montr. IVIA-279 1 2 0 3 2 — Citrus madurensis Lour. IVIA- 135 41244 — Citrus meyeri Y. Tan. (cv. Meyer) IVIA-145 0 2 2 4 4 + Citrus myrtifolia Raf. (Hoja G) IVIA-136 13343 — Citrus myrtifolia Raf. (Hoja P) IVIA-137 12344 — Citrus pyriformis Hassk. (cv. Ponderosa) IVIA-268 31333 + Citrus shunkokan Hort. ex Tan. IVIA-241 0 1 0 4 0 — Citrus sunki Hort. ex Tan. IVIA- 239 12222 — Citrus tachibana (Mak.) Tan. IVIA-237 11221 — Citrus temple Hort. ex Y.Tan. IVIA-81 33244 — Citrus unshiu (Mak.) Marc. (cv. Clausellina) IVIA-19 0 1 1 1 0 — Citrus webberi Wester IVIA-234 12233 — Atalantia citroides Pierre ex Guill IVIA-180 0 0 0 0 0 — Fortunella crassifolia Swing. IVIA-280 1 0 1 2 1 — Fortunella margarita Lour. Swing. IVIA-138 0 2 3 4 4 — zViroids were detected by sPAGE and molecular hybridization analysis of bark tissue samples. Viroid titers were rated accordingly with the intensity of the sPAGE bands and the hybridization signal: (0) not detected, (1) sPAGE negative and very weak hybridization signal, (2) sPAGE positive and weak hybridization signal, (3) sPAGE positive and intense hybridization signal, (4) sPAGE positive and very intense hybridization signal. 265 266 TABLE 1 (CONTINUED) DETECTION OF CITRUS VIROIDS ON INOCULATED SPECIES OF CITRUS AND CITRUS RELATIVES Viroid detection and titerz Accession Citrus and citrus relatives number CEVd CVd-I CVd-II CVd-III CVd-IV Symptoms Fortunella obovata Tan. IVIA-312 0 2 2 4 4 — Microcitrus australis (Planch.) Swing. IVIA-313 0 0 0 0 0 — Microcitrus australasica (F. Muell.) Swing. IVIA-150 1 0 1 1 0 — Microcitrus warburgiana (F.M. Bail.) Tan. IVIA-315 0 2 2 4 3 — M. australis × M. australasica IVIA-378 32222 — Fifteenth IOCVConference,2002—Viroids Pleiospermium sp. Engl. Swing. IVIA-389 0 3 2 4 2 — Severinia buxifolia Poir. Tenore IVIA-147 11111 — zViroids were detected by sPAGE and molecular hybridization analysis of bark tissue samples. Viroid titers were rated accordingly with the intensity of the sPAGE bands and the hybridization signal: (0) not detected, (1) sPAGE negative and very weak hybridization signal, (2) sPAGE positive and weak hybridization signal, (3) sPAGE positive and intense hybridization signal, (4) sPAGE positive and very intense hybridization signal. Fifteenth IOCV Conference, 2002—Viroids 267 molecular hybridization analysis of phatase-anti-DIG Fab fragment con- bark samples from the inoculated jugate and visualized with the plants. In some cases viroid infec- chemiluminescence substrate CSPD tion was confirmed by inoculation on (Boehringer Mannheim). Etrog citron (three bark-grafts/ Viroid titers were visually rated plant) followed by nucleic acid anal- from 0 to 4 according to the inten- ysis 3 mo after inoculation. sity of the silver stained sPAGE Viroid detection. Bark or leaf bands and the molecular hybridiza- (with petiole and mid-rib removed) tion signals. samples (5 g) were homogenized in 5 ml of extraction buffer (Tris-HCl 0.4 RESULTS AND DISCUSSION M, pH 8.9; SDS 1% (w/v); EDTA 5 mM, pH 7.0; mercaptoethanol 4% (v/ Infectivity. The five viroid spe- v) and 15 ml of water saturated phe- cies (CEVd, CVd-I, CVd-II, CVd-III nol (25). The total nucleic acids were and CVd-IV) were detected directly partitioned in 2M LiCl and the solu- from bark tissues in 17 of the 32 ble fraction was concentrated by genotypes studied. None of the inoc- ethanol precipitation and resuspen- ulated viroids could be detected from sion in TKM buffer (Tris-HCl 10 tissues of Atalantia citroides and mM; KCl 10 mM; MgCl2 0.1 mM; pH Microcitrus australis. In the remain- 7.4) (24). These preparations were ing 13 accessions, at least one of the subjected to sPAGE and slot-blot viroids was undetectable: CEVd (C. hybridization analysis using specific meyeri, C. shunkokan, C. unshiu, viroid probes. For some specific Fortunella margarita, F. obovata, M. viroid-host combinations, the recov- waburgiana and Pleiospermium ery of viroids from bark versus leaf sp.), CVd-I (C. hystrix, C. latifolia, F. lamina tissues were compared. crassifolia and M. australasica), For sPAGE (5%, 39:1) analysis, CVd-II (C. ichangensis, C. mac- 20 µl aliquots of the nucleic acid roptera and C. shunkokan), and preparations equivalent to 300 mg of CVd-IV (C. shunkokan, C. unshiu fresh tissue were subjected to elec- and M. australasica) (shown shaded trophoresis under non-denaturing in Table 1). These plants were graft- conditions (2 h, 60 mA) and 8M urea inoculated on Etrog citron and the denaturing conditions (4 h, 18 mA) inoculated citrons were subjected to (19). Circular forms of viroids were sPAGE and molecular hybridization visualized by silver staining (10). analysis to determine their infection For slot-blot hybridization, ali- status. In all instances the graft sur- quots (10 µl equivalent to 150 mg of vived and the results suggest that fresh tissue) were pre-treated with 11 of these 15 species may be truly 6×SSC and 8% formaldehyde for 15 resistant to one or more of the inocu- min at 60°C and blotted onto posi- lated viroids (Table 2). These results tively charged Nylon membranes should be further confirmed to avoid (Boehringer Mannheim®) using an an erroneous interpretation due to Hybri-slot filtration manifold (BRL®), uneven viroid distribution as immobilized by UV cross-linking and already reported for satsuma and hybridized with DIG-labeled DNA Navelina sweet orange (6). probes. DIG-labelled viroid specific The detection results rated 1 probes were synthesized by PCR from (Table 1) should be considered with plasmid templates containing full- caution since the hybridization sig- length viroid cDNAs as described by nal was only slightly above back- Palacio et al.
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