Variation in the aggressiveness of Xanthomonas citri subsp. citri pathotypes A and A* on three Citrus species, and epiphytic growth on some citrus weeds
Zohreh Ebrahimi A , Rasool Rezaei A C , Asad Masoumi-Asl B and Habiballah Charehgani AA Department of Plant Protection, College of Agriculture, Yasouj University, Yasouj, Iran.
B Department of Agronomy and Plant Breeding, College of Agriculture, Yasouj University, Yasouj, Iran.
C Corresponding author. Email: rrezaei@yu.ac.ir
Crop and Pasture Science 71(3) 260-267 https://doi.org/10.1071/CP19448
Submitted: 25 October 2019 Accepted: 20 January 2020 Published: 1 April 2020
Abstract
Citrus bacterial canker, caused by Xanthomonas citri subsp. citri (Xcc), is a widespread disease in citrus-producing areas of the tropics and subtropics. It is a serious threat to most commercial citrus cultivars and species. In this study, aggressiveness of different isolates of Xcc was determined on leaves of Citrus aurantiifolia, Citrus limon ‘Eureka’ and Citrus sinensis, and the population dynamics of isolates of two Xcc pathotypes (A and A*) was evaluated on eight plant species considered weeds of citrus, including Amaranthus caudatus, Medicago sativa, Sorghum halepense, Xanthium strumarium, Portulaca oleracea, Avena ludoviciana, Plantago lanceolata and Chenopodium album under greenhouse conditions. Isolates varied from aggressive to weakly aggressive on the basis of the intensity and persistence of water soaking and the development of necrosis 12 days post-inoculation. Both Xcc pathotypes multiplied on all plant species tested except Portulaca oleracea up to 20 days post-inoculation under greenhouse conditions. A high bacterial growth rate was observed on Medicago sativa and Plantago lanceolata. Strains of the A* pathotype successfully proliferated on all weeds except Portulaca oleracea, attaining a population density even higher than that of the A pathotype. The results clearly suggest that weed management is an important strategy in controlling canker disease in citrus-growing areas.
Additional keywords: citrus canker, virulence.
References
Al-Saleh MA, Widyawan A, Saleh AA, Ibrahim YE (2014) Distribution and pathotypes identification of Xanthomonas citri subsp. citri recovered from south western region of Saudi Arabia. African Journal of Microbiological Research 8, 673–679.| Distribution and pathotypes identification of Xanthomonas citri subsp. citri recovered from south western region of Saudi Arabia.Crossref | GoogleScholarGoogle Scholar |
Behlau F, Scandelai L, Junior G, Lanza F (2017) Soluble and insoluble copper formulations and metallic copper rate for control of citrus canker on sweet orange trees. Crop Protection 94, 185–191.
| Soluble and insoluble copper formulations and metallic copper rate for control of citrus canker on sweet orange trees.Crossref | GoogleScholarGoogle Scholar |
Brunings AM, Gabriel DW (2003) Xanthomonas citri: breaking the surface. Molecular Plant Pathology 4, 141–157.
| Xanthomonas citri: breaking the surface.Crossref | GoogleScholarGoogle Scholar | 20569374PubMed |
Cafati CR, Saettler AW (1980) Role of non-host species as alternate inoculum sources of Xanthomonas phaseoli. Plant Disease 64, 194–196.
| Role of non-host species as alternate inoculum sources of Xanthomonas phaseoli.Crossref | GoogleScholarGoogle Scholar |
Christiano RSC, Dalla Pria M, Jesus WC, Parra JRP, Amorim L, Bergamin A (2007) Effect of citrus leaf-miner damage, mechanical damage and inoculum concentration on severity of symptoms of Asiatic citrus canker in Tahiti lime. Crop Protection 26, 59–65.
| Effect of citrus leaf-miner damage, mechanical damage and inoculum concentration on severity of symptoms of Asiatic citrus canker in Tahiti lime.Crossref | GoogleScholarGoogle Scholar |
Ercolani GL, Hagedorn DH, Kelman A, Rand RE (1974) Epiphytic survival of Pseudomonas syringae on hairy vetch in relation to epidemiology of bacterial brown spot of bean in Wisconsin. Phytopathology 64, 1330–1339.
| Epiphytic survival of Pseudomonas syringae on hairy vetch in relation to epidemiology of bacterial brown spot of bean in Wisconsin.Crossref | GoogleScholarGoogle Scholar |
Ference CM, Gochez AM, Behlau F, Wang N, Graham JH, Jones JB (2018) Recent advances in the understanding of Xanthomonas citri subsp. citri pathogenesis and citrus canker disease management. Molecular Plant Pathology 19, 1302–1318.
| Recent advances in the understanding of Xanthomonas citri subsp. citri pathogenesis and citrus canker disease management.Crossref | GoogleScholarGoogle Scholar | 29105297PubMed |
Fernández-Sanz AM, Rodicio MR, González AJ (2016) Pseudomonas syringae pv. phaseolicola isolated from weeds in bean crop fields. Letters in Applied Microbiology 62, 344–348.
| Pseudomonas syringae pv. phaseolicola isolated from weeds in bean crop fields.Crossref | GoogleScholarGoogle Scholar | 26880144PubMed |
Francis M, Peña A, Graham JH (2010) Detached leaf inoculation of germplasm for rapid screening of resistance to citrus canker and citrus bacterial spot. European Journal of Plant Pathology 127, 571–578.
| Detached leaf inoculation of germplasm for rapid screening of resistance to citrus canker and citrus bacterial spot.Crossref | GoogleScholarGoogle Scholar |
Gabriel DW, Kingsley MT, Hunter JE, Gottwald T (1989) Reinstatement of Xanthomonas citri (ex Hasse) and X. phaseoli (ex Smith) to species and reclassification of all X. campestris pv. citri strains. International Journal of Systematic Bacteriology 39, 14–22.
| Reinstatement of Xanthomonas citri (ex Hasse) and X. phaseoli (ex Smith) to species and reclassification of all X. campestris pv. citri strains.Crossref | GoogleScholarGoogle Scholar |
Gent DH, Lang JM, Schwartz HF (2005) Epiphytic survival of Xanthomonas axonopodis pv. allii and Xanthomonas axonopodis pv. phaseoli on leguminous hosts and onion. Plant Disease 89, 558–564.
| Epiphytic survival of Xanthomonas axonopodis pv. allii and Xanthomonas axonopodis pv. phaseoli on leguminous hosts and onion.Crossref | GoogleScholarGoogle Scholar | 30795378PubMed |
Goto M, Ohta K, Okabe N (1975) Studies on saprophytic survival of Xanthomonas citri (Hasse) Dowson: longevity and survival density of the bacterium on artificially infested weeds, plant residues and soils. Annals of the Phytopathological Society of Japan 41, 141–147.
| Studies on saprophytic survival of Xanthomonas citri (Hasse) Dowson: longevity and survival density of the bacterium on artificially infested weeds, plant residues and soils.Crossref | GoogleScholarGoogle Scholar |
Goto M, Takahashi T, Messina MA (1980) A comparative study of strains of Xanthomonas axonopodis pv. citri isolated from citrus canker in Japan and cancerosis B in Argentina. Annals of the Phytopathological Society of Japan 46, 329–338.
| A comparative study of strains of Xanthomonas axonopodis pv. citri isolated from citrus canker in Japan and cancerosis B in Argentina.Crossref | GoogleScholarGoogle Scholar |
Gottwald TR, Graham JH, Civerolo EL, Barret HC, Hearn CJ (1993) Differential host range reaction of citrus and citrus relatives to citrus canker and citrus bacterial spot determined by leaf mesophyll susceptibility. Plant Disease 77, 1004–1009.
| Differential host range reaction of citrus and citrus relatives to citrus canker and citrus bacterial spot determined by leaf mesophyll susceptibility.Crossref | GoogleScholarGoogle Scholar |
Gottwald TR, Graham JH, Bock CH, Bonn G, Civerolo E, Irey M, Leite RP, Lopez M, McCollum G, Parker P, Ramallo J, Riley T, Schubert T, Stein B, Taylor E (2009) The epidemiological significance of post-packinghouse survival of Xanthomonas citri ssp citri for dissemination of Asiatic citrus canker via infected fruit. Crop Protection 28, 508–524.
| The epidemiological significance of post-packinghouse survival of Xanthomonas citri ssp citri for dissemination of Asiatic citrus canker via infected fruit.Crossref | GoogleScholarGoogle Scholar |
Graham JH, Gottwald TR (1990) Variation in aggressiveness of Xanthomonas campestris pv. citrumelo associated with citrus bacterial spot in Florida citrus nurseries. Phytopathology 80, 190–196.
| Variation in aggressiveness of Xanthomonas campestris pv. citrumelo associated with citrus bacterial spot in Florida citrus nurseries.Crossref | GoogleScholarGoogle Scholar |
Katkar M, Raghuwanshi KS, Chimote VP, Borkar SG (2016) Pathological, bio-chemical and molecular diversity amongst the isolates of Xanthomonas axonopodis pv. citri causing citrus canker in acid lime from different agro-climatic region of India. International Journal of Environment Agriculture and Biotechnology 1, 302–315.
| Pathological, bio-chemical and molecular diversity amongst the isolates of Xanthomonas axonopodis pv. citri causing citrus canker in acid lime from different agro-climatic region of India.Crossref | GoogleScholarGoogle Scholar |
Khodakaramian G, Swings J (2011) Genetic diversity and pathogenicity of Xanthomonas axonopodis strains inducing citrus canker disease in Iran and South Korea. Indian Journal of Microbiology 51, 194–199.
| Genetic diversity and pathogenicity of Xanthomonas axonopodis strains inducing citrus canker disease in Iran and South Korea.Crossref | GoogleScholarGoogle Scholar | 22654164PubMed |
Kinkel LL, Wilson M, Lindow SE (2000) Plant species and plant incubation conditions influences variability in epiphytic bacterial population size. Microbial Ecology 39, 1–11.
| Plant species and plant incubation conditions influences variability in epiphytic bacterial population size.Crossref | GoogleScholarGoogle Scholar | 10790512PubMed |
Koizumi M (1979) Ultrastructural changes in susceptible and resistant plants of citrus following artificial isolation with Xanthomonas citri (Hasse) Dowson. Annals of the Phytopathological Society of Japan 45, 635–644.
| Ultrastructural changes in susceptible and resistant plants of citrus following artificial isolation with Xanthomonas citri (Hasse) Dowson.Crossref | GoogleScholarGoogle Scholar |
Koupaei FY, Taghavi SM, Shiotani H, Tesuyumu S (2014) A PCR-based assay for differentiating A and A* type strains of Xanthomonas citri subsp. citri, the causal agent of Asiatic citrus canker. Journal of General Plant Pathology 80, 85–89.
| A PCR-based assay for differentiating A and A* type strains of Xanthomonas citri subsp. citri, the causal agent of Asiatic citrus canker.Crossref | GoogleScholarGoogle Scholar |
Lamichhane JR (2014) Xanthomonas arboricola disease of stone fruit, almond, and walnut trees: progress toward understanding and management. Plant Disease 98, 1600–1610.
| Xanthomonas arboricola disease of stone fruit, almond, and walnut trees: progress toward understanding and management.Crossref | GoogleScholarGoogle Scholar | 30703892PubMed |
Mohammadi M, Mirzaee MR, Rahimian H (2001) Physiological and biochemical characteristics of Iranian strains of Xanthomonas axonopodis pv. citri, the causal agent of citrus bacterial canker disease. Journal of Phytopathology 149, 65–75.
| Physiological and biochemical characteristics of Iranian strains of Xanthomonas axonopodis pv. citri, the causal agent of citrus bacterial canker disease.Crossref | GoogleScholarGoogle Scholar |
Osdaghi E, Taghavi SM, Hamzehzarghani H, Fazliarab A, Harveson RM, Tegli S, Lamichhane JR (2018) Epiphytic Curtobacterium flaccumfaciens strains isolated from symptomless solanaceous vegetables are pathogenic on leguminous but not on solanaceous plants. Plant Pathology 67, 388–398.
| Epiphytic Curtobacterium flaccumfaciens strains isolated from symptomless solanaceous vegetables are pathogenic on leguminous but not on solanaceous plants.Crossref | GoogleScholarGoogle Scholar |
Pruvost O, Goodarzi T, Boyer K, Soltaninejad H, Escalon A, Alavi SM, Javegny S, Boyer C, Cottyn B, Gagnevin L, Vernière C (2015) Genetic structure analysis of strains causing citrus canker in Iran reveals the presence of two different lineages of Xanthomonas citri pv. citri pathotype A*. Plant Pathology 64, 776–784.
| Genetic structure analysis of strains causing citrus canker in Iran reveals the presence of two different lineages of Xanthomonas citri pv. citri pathotype A*.Crossref | GoogleScholarGoogle Scholar |
Samavi S, Hassanzadeh N, Faghihi MM, Rezaee-Danesh Y (2009) Effects of thyme (Zaatar) essential oil and some chemical compounds in the control of citrus bacterial canker in Iran. Journal of Plant Pathology 91, 691–696.
Schubert TS, Rizvi SA, Xiaoan S, Gottwald TR, Graham JH, Dixon WN (2001) Meeting the challenge of eradicating citrus canker in Florida-Again. Plant Disease 85, 340–356.
| Meeting the challenge of eradicating citrus canker in Florida-Again.Crossref | GoogleScholarGoogle Scholar | 30831965PubMed |
Silva C, Regasini LO, Petrônio MS, Silva DHS, Bolzani VS, Belasque J, Sacramentod LVS, Ferreira H (2013) Antibacterial activity of alkyl gallates against Xanthomonas citri subsp. citri. Journal of Bacteriology 195, 85–94.
| Antibacterial activity of alkyl gallates against Xanthomonas citri subsp. citri.Crossref | GoogleScholarGoogle Scholar |
Sun X, Stall RE, Jones JB, Cubero J, Gottwald TR, Graham JH, Dixon WD, Schubert TS, Chaloux PH, Stromberg VK, Lacy GH, Sutton BD (2004) Detection and characterization of a new strain of citrus canker bacteria from Key/Mexican lime and alemow in South Florida. Plant Disease 88, 1179–1188.
| Detection and characterization of a new strain of citrus canker bacteria from Key/Mexican lime and alemow in South Florida.Crossref | GoogleScholarGoogle Scholar | 30795311PubMed |
Thompson DC, Schaad NW, Forster RL (1989) New perennial hosts of epiphytic populations of Xanthomonas campestris pv. translucens. Phytopathology 79, 1168
Zarei S, Taghavi SM, Hamzehzarghani H, Osdaghi E, Lamichhane JR (2018) Epiphytic growth of Xanthomonas arboricola and Xanthomonas citri on non-host plants. Plant Pathology 67, 660–670.
| Epiphytic growth of Xanthomonas arboricola and Xanthomonas citri on non-host plants.Crossref | GoogleScholarGoogle Scholar |