Abstract
This chapter deals with major endemic and emerging fungal diseases of citrus as well as with exotic fungal pathogens potentially harmful for citrus industry in the Mediterranean region, with particular emphasis on diseases reported in Italy and Maghreb countries. The aim is to provide an update of both the taxonomy of the causal agents and their ecology based on a molecular approach, as a preliminary step towards developing or upgrading integrated and sustainable disease management strategies. Potential or actual problems related to the intensification of new plantings, introduction of new citrus cultivars and substitution of sour orange with other rootstocks, globalization of commerce and climate changes are discussed. Fungal pathogens causing vascular, foliar, fruit, trunk and root diseases in commercial citrus orchards are reported, including Plenodomus tracheiphilus, Colletotrichum spp., Alternaria spp., Mycosphaerellaceae, Botryosphaeriaceae, Guignardia citricarpa and lignicolous basidiomycetes. Diseases caused by Phytophthora spp. (oomycetes) are also included as these pathogens have many biological, ecological and epidemiological features in common with the true fungi (eumycetes).
Keywords
- Plenodomus tracheiphilus
- Colletotrichum spp.
- Alternaria spp.
- greasy spot
- Mycosphaerellaceae
- Botryosphaeriaceae
- Guignardia citricarpa
- Basidiomycetes
- Phytophthora spp
1. Introduction
Citrus are among the ten most important crops in terms of total fruit yield worldwide and rank first in international fruit trade in terms of value. More than seven million hectares are planted with citrus throughout the world. The term “citrus” indicates a complex of species and hybrids of the genera
2. General considerations
Any rational disease management strategy is based on accurate diagnosis and prevention. Fungal diseases of citrus showing specific symptoms can be easily diagnosed visually, while for diseases with no typical symptoms, laboratory tests are needed. A limit of symptomatic diagnosis is that some symptoms are visible only at certain times of the year or appear on organs distinct from those colonized by the pathogen. Moreover, secondary parasites or opportunistic pathogens can overgrow primary pathogens or colonize senescent or necrotic tissues. Typical examples are
The most effective control method of fungal diseases is prevention, especially for diseases caused by soil-borne pathogens. Most of the rootstocks used in commercial citrus orchards, e.g. are resistant to
Mediterranean climate is not conducive to epidemic infections of fungal diseases of the tree canopy, and as a consequence, chemical control of these diseases in the Mediterranean region is economically justified only in few cases. The choice of fungicides is restricted to active ingredients registered for citrus. In Italy, only copper derivatives (oxychloride, hydroxide and sulphate tribasic) are allowed for field treatments against fungal diseases. Systemic fungicides, metalaxyl M and ethyl-phosphytes (Al ethyl-phosphite and K ethyl-phosphite) are available for chemical control of diseases caused by
Hereafter we illustrate major fungal diseases of citrus already established or potentially harmful for the citrus industry in the Mediterranean region. Two quarantine fungal pathogens of citrus presently are included in the A1 list of the European and Mediterranean Plant Protection Organization (EPPO),
3. Mal secco
The mal secco, an Italian name meaning “dry disease”, is a vascular wilt disease (Figure 1) caused by the mitosporic fungus
Alemow (
The mal secco fungus was originally classified among the Deuteromycota as
Recent molecular phylogenetic studies on the genus
Infection occurs between 14 and 28°C, whereas at temperatures above 28°C, fungal growth ceases and symptoms are not expressed. As a consequence disease progress is temporarily inhibited during the hot or cold temperature extremes.
While in Sicily most infections occur from autumn to early spring; in Israel, mid-November to mid-April was the most conducive time for infection, coinciding with the rainy season, although no correlation was found between the amount of rain, the number of rainy days and the percentage of infected plants. No infection was observed after the rain ceased, so it appears that the rain affects inoculum dissemination rather than infection [20]. Length of the incubation period varies according to season, and in young trees, it ranges between 2 and 7 months, whereas it can last several years in the “mal nero” form of the disease because this chronic infection could remain confined to the heartwood over a long time. Expression of symptoms is therefore a poor selection criterion for phytosanitary inspection of propagation material. This aspect has practical relevance as the use of disease-free propagation material helps to reduce the dissemination of mal secco and its introduction into disease-free areas.
Like for other tracheomycoses, fungicide treatments are not effective against mal secco, and research of newly resistant genotypes remains the only effective strategy to control this disease. Lemon cultivars with various degrees of resistance to mal secco, such as ‘Monachello’, ‘Interdonato’, ‘Feminello Zagara Bianca’, ‘Femminello Continella’ and ‘Cerza’, have been selected in Sicily. However, ‘Monachello’ has a poor yield, ‘Interdonato’ does not bloom several times, and its juice has low acidity, and the tolerance to mal secco of the other cultivars is not comparable to that of ‘Monachello’. Two new cultivars with high yield potential, ‘Femminello Siracusano 2Kr’, a mutant nucellar clone obtained with cobalt γ-radiation, and the triploid hybrid ‘Lemox’ (European patent number 20040073), have been included in the official list of lemon cultivars whose use is recommended in Italy for new plantings. However they proved to be extremely susceptible to mal secco disease. The goal of obtaining tolerant cultivars with competitive yields and satisfactory bio-agronomic characteristics remains one of the primary objectives of lemon-breeding programmes in the Mediterranean region. Additional and more detailed information on mal secco disease can be found in two recent comprehensive reviews [20, 21].
4. Emerging and endemic foliar and fruit diseases
Despite the Mediterranean climate is not conducive to epidemic outbreaks of fungal diseases of the canopy of citrus trees, being characterized by long periods of drought and high temperatures in summer as well as cool winters, in the last years, some citrus-growing areas of the Mediterranean region have experienced the emergence or resurgence of new and endemic fungal diseases of leaves and fruit.
4.1. Alternaria brown spot
Alternaria brown spot (ABS) is one of the most important diseases of tangerines and their hybrids worldwide. It is caused by the tangerine pathotype of the fungus
ABS is prevalent in citrus production areas with a Mediterranean climate, characterized by cool, humid winters and hot, arid summers. It was first reported on ‘Emperor’ mandarin in Australia in 1903, and subsequently it was detected in the Americas, the Mediterranean basin, South Africa, Iran and China affecting mainly ‘Fortune’ and ‘Nova’ mandarin hybrids [22, 29, 30]. In Europe, it has been reported in Greece, Italy and Spain. Its appearance in Italy coincided with the diffusion of the mandarin ‘Fortune’. Warm temperatures and prolonged wetness are required for infection. However the disease causes severe epidemics in both humid areas and semi-arid regions provided a susceptible citrus variety is present. Fruits can get infected in all development stages but are more susceptible during the first four months following petal fall. Spring infections on young fruits may lead to premature fruit drop. Early fruit drop is common, especially if infection has occurred shortly after petal fall. Symptoms on fruits are necrotic brown circular lesions that may vary in size (Figures 6 and 7). Mature lesions have a corky appearance, and in older lesions, the centre may dislodge leaving tan-coloured pockmarks. Brown to black lesions surrounded by yellow halos and veinal necrosis appear on young leaves, which often are deformed due to necrosis of the margin. On highly susceptible cultivars abundant defoliation, abscission of young shoots and twig dieback may occur. Conditions of persistent humidity (fog or dew), which provide a wetting period of 8–12 h, are conducive for the development of infections; the optimum temperature is 20–27°C, but infections can occur between 17 and 32°C. The disease incubation period is 16–36 h. Conidia are produced on necrotic lesions in young leaves but not on fruits and are dispersed by air currents and rain splash. The presence of the disease is a limiting factor for the diffusion of highly susceptible mandarin or tangerine-like cultivars such as ‘Fortune’, ‘Dancy’, ‘Minneola’, ‘Orlando’, ‘Nova’, ‘Guillermina’, ‘Clemenpons’, ‘Esbal’, ‘Page’, ‘Lee’, ‘Sunburst’, ‘Encore’, ‘Murcott’, ‘Michal’, ‘Winola’, ‘Ponkan’, ‘Emperor’, ‘Tangfang’ and ‘Primosole’. Even some varieties of pomelo are susceptible, while orange cultivars, with very few exceptions, are resistant.
Lemon and lime cultivars are not susceptible, with the exception of Mexican lime (
Generally speaking, hybrids with ‘Dancy’ and ‘King’ mandarins as a parent are very susceptible. In many countries, such as Italy, Israel, Spain and the USA, ABS is a strong concern for triploid breeding programmes aiming at producing seedless mandarin cultivars. From diploid progeny analysis, it has been proposed that the inheritance of ABS susceptibility in citrus is controlled by a single gene with two alleles, one dominant (S) and the other recessive (r) which transmit susceptibility and resistance, respectively [31]. Therefore, resistant cultivars are considered to be recessive homozygous for this locus, whereas susceptible cultivars could be heterozygous or homozygous dominant. Cultivars like ‘Minneola’ and ‘Dancy’, which are homozygous (SS), transmit susceptibility to all the descendants. Most susceptible commercial cultivars like ‘Fortune’, ‘Nova’ and ‘Murcott’ are heterozygous, and both resistant and susceptible hybrids can be found in their progeny.
Resistant oranges, mandarins and clementines are recessive homozygous (rr), so when they breed with each other, all descendants are resistant. The single-locus dominant inheritance of susceptibility was corroborated by the analysis of triploid progenies. Recently, in Spain two new ABS-resistant hybrids of ‘Fortune’, ‘Garbi’ (‘Murcott’ × ‘Fortune’) and ‘Safor’ (‘Kara’ × ‘Fortune’) have been released.
Currently on susceptible cultivars, ABS control is based on the application of fungicides [32, 33]. Sprays must be scheduled to protect susceptible organs during the critical period for infection. Depending on the climate and the susceptibility of the cultivar, between four and ten fungicide sprays per year may be needed to produce quality fruit for the fresh market. On susceptible cultivars, foliar applications with copper fungicides are requested every 10–15 days in periods of high susceptibility. Despite this large number of sprays, disease control is not always satisfactory, and cultivation of very susceptible cultivars such as ‘Fortune’ in Mediterranean countries and ‘Minneola’ in Florida has declined significantly.
An integrated approach can reduce the risk of ABS infections and the disease severity [22]. In the nursery, it is recommended to grow susceptible citrus cultivars indoors, to avoid infections on young shoots and prevent inoculum dissemination in new commercial citrus plantings. New plantings of susceptible cultivars should be established in ventilated sites where environmental conditions are unfavourable for infections and sporulation of the causal agent on young leaves. Similarly, dense planting is not recommended for susceptible cultivars. Orchards of susceptible cultivars should be monitored frequently to detect the presence and prevent epidemic outbreaks of the disease.
4.2. Septoria spot
Septoria spot is more severe in years when rainfall levels are high and temperature fluctuates. The causal agent survives in infected orchards as a saprobe. Inoculum is constituted by pycnidia forming on dead twigs and leaves. Conidia, the infective propagules, are dispersed by water splash. Infections usually occur during cool, damp weather in late summer or autumn and when the fruits are still green. They may remain latent for up to six months, and fruit symptoms generally appear as the fruit starts ripening in late winter and early spring, after cool, frosty or cold windy weather. The susceptibility of fruits is related to the maturity of the rind at the time of infection. Management practices to prevent or reduce the disease incidence and severity include tree skirting and canopy pruning to improve air circulation, early fruit harvesting and the removal of withered twigs from the tree canopy and fallen leaves from the soil under the tree canopy to reduce the amount of inoculum. Copper sprays in late fall or early winter to control fruit brown rot caused by
The traditional taxonomy of
4.3. Greasy spot and other cercosporoid diseases
Several species of cercosporoid fungi have been associated with leaf and fruit spot diseases of
Symptoms of greasy spot appear as yellow to dark brown to black lesions occurring first on the underside of mature citrus leaves. As the lesions develop on the underside of the leaves, they become darker, and a corresponding chlorotic spot appears on the upper leaf surface. Symptoms differ among citrus species. On highly susceptible species, such as lemon, spots are diffuse and tend to remain yellow, while on grapefruit, which is somewhat less susceptible, lesions are less diffuse, more raised and darker. On mandarins and ‘Valencia’ oranges, which are much more tolerant, lesions are smaller, brown to black and much more raised. Affected leaves fall prematurely from the tree during the fall and winter, resulting in reduced tree vigour and yield. Beside defoliation, the disease causes a rind blemish on fruit which has been referred to as greasy spot rind blotch. Greasy spot rind blotch significantly reduces the marketability of fruit for fresh consumption and is a serious problem especially on grapefruit but can also occur on oranges and other citrus. Greasy spot was first reported in Florida and is now endemic in all citrus-growing areas of the Caribbean Basin [37]. It also occurs in Texas but does not cause serious damage, probably because of a drier climate. Similar diseases of citrus have been observed in Argentina, Australia, China, Brazil, Egypt, Japan, Korea, Morocco, Spain and Italy. However the causal agent is not always
During the last years, an epidemic outbreak of a foliar disease closely resembling greasy spot has been observed in some citrus-growing areas of western Sicily (Italy). Symptoms appear on mature leaves and range from those typical of greasy spot (Figures 9 and 10) to black dots. Premature leaf drop occurs and causes heavy defoliation of the tree.
The analysis of the fungal community using an amplicon metagenomic approach has revealed that Mycosphaerellaceae were the dominant group of fungi, in both symptomatic and asymptomatic leaves, and were represented by the genera
5. Bleeding cankers caused by Botryosphaeriaceae and Phomopsis /Diaporthe
Botryosphaeriaceae and
On citrus trees, cankers are found prevalently on trunk and main branches. The canker exudes a reddish gum, giving it a bleeding, water-soaked appearance. Symptoms may also include wilt of shoots and branches, sometimes with dead leaves still attached. Two types of fruiting bodies (perithecia and pycnidia) can be found on cankers, which are the sexual and asexual stage of these fungi, respectively. They produce the infective spores and appear as tiny black bumps protruding from the bark. Pycnidial spores that are far more frequently observed in nature than perithecial spores ooze out in a ribbon-like gelatinous matrix and are usually disseminated by rain splash. Botryosphaeriaceae and
Species of Botryosphaeriaceae (
Biochemical and genetic stimuli, resulting from environmental changes inside the hosts (changes in host physiological conditions or microbial equilibrium) or outside the host (climatic changes or extreme environmental events), trigger these fungi to change their lifestyle from endophytic to pathogenic. Therefore these fungi can be regarded as opportunistic fungal pathogens, and the management of diseases they cause is based essentially on preventing environmental stresses. In particular, an agronomical means to prevent the disease is to avoid water stress by reducing the time intervals between irrigations. Surgical removal of infected bark does not restrict the expansion of cankers, and copper treatments are only partially effective to reduce the inoculum on the tree. They can be recommended to protect top-worked stumps and prevent shoot blight.
6. Wood rots
Wood rots are caused by a wide variety of wood-degrading microorganisms and are characterized by decay and discoloration of wood of the trunk, large branches and main roots. Most wood-degrading fungi are Basidiomycetes that on living trees can cause two major kinds of decay: brown and white rots. Although wood-decay fungi play an ecologically important role as primary biotic decomposers of wood in forest ecosystems, they can cause economic losses in cultivated orchards by contributing to the premature ageing and the structural failure of the trees. It can also affect young trees as a result of abiotic stress, such as severe frosts and sun burning of branches exposed by heavy pruning. Most wood-decay fungi penetrate through wounds, although a few of the root-infecting species can enter the unwounded surface directly.
Citrus wood rot is a chronic disease occurring endemically on old trees in most citrus-growing areas of the world. Although this disease is not a major constraint for the citrus industry, it can contribute to the deterioration of orchards because affected trees show a premature ageing, a progressive decline in vigour and reduced productivity. A direct effect of wood decay is the breakage of scaffold branches due to loss of wood strength. Moreover trees show symptoms of leaf chlorosis and twig dieback. The incidence of the disease is high in more than 40-year-old orchards, and its severity depends on environmental conditions and susceptibility of the citrus species and cultivars. In particular, lemon trees are significantly more susceptible to wood decay than other types of citrus, including orange, grapefruit and tangelo. In addition, the disease incidence seems to be correlated with the intensity and pattern of precipitations. As far as the Mediterranean region is concerned,
7. Phytophthora diseases
The all-inclusive term “
At least ten species of
Recently,
Interestingly, however, genetic analyses of a worldwide collection of
Temperature is a major ecological factor affecting seasonal fluctuations of
Sporangia produced in the most superficial soil layer (0 to about 30 cm depth), on contact with air, are the main source of inoculum. Natural infections are most frequently caused by zoospores and occasionally by direct or indirect germination of sporangia through a germ tube or by releasing zoospores, respectively. Production and germination of sporangia are influenced by temperature and soil water potential. Their dissemination is mostly by water splash and occasionally by wind, within water droplets. The zoospores are motile and can swim short distances by flagellar movement or can be carried over longer distances by soil water. They swim towards roots, as they are attracted by root exudates, and encyst upon contact, germinate and penetrate fruits, leaves, shoots and green twigs directly.
Grafting on resistant rootstocks, such as sour orange, is the most practical and widely used means to control
Brown rot is both a preharvest and postharvest decay of citrus fruit. Infected fruit shows a typical leathery brown rot with indistinct edges and has a characteristic rancid smell. With high moisture in the environment, white furry mould forms on the fruit surface. Infections cause the fruit to drop prematurely and occur especially on fruits hanging in the lower part of the tree canopy, with rain splash. Epidemic explosions are more frequent in citrus orchards where trunk gummosis is endemic. The incubation period of the disease is 7–10 days at 10°C but may be longer with lower temperatures. Asymptomatic infected fruits can infect healthy fruits even after harvesting, during transportation and storage.
Two major breakthroughs in the implementation of integrated management strategies of
8. Concluding remarks
Over the last decade, there have been a number of publications dealing with molecular studies on fungal pathogens of citrus, focusing particularly on their identification and genetic diversity. In particular, new species of
References
- 1.
Damm U, Cannon PF, Woudenberg JHC, Johnston PR, Weir BS, Tan YP, Shivas RG, Crous PV. The Colletotrichum boninense species complex. Stud. Mycol. 2012; 73: 1–36. DOI: 10.3114/sim0002. Epub 2012 Feb 29 - 2.
Huang F, Chen GQ, Hou X, Fu YS, Cai L, Hyde KD, Li HY. Colletotrichum species associated with cultivated citrus in China. Fungal Divers. 2013; 61: 61–74. DOI:10.1007/s13225-013-0232-y - 3.
Schena L, Mosca S, Cacciola S, Faedda R, Sanzani SM, Agosteo GE, Sergeeva V, Magnano di San Lio G Species of the Colletotrichum gloeosporioides andC. boninense complexes associated with olive anthracnose. Plant Pathol. 2014; 63: 437–446. DOI: 10.1111/ppa.12110 - 4.
EPPO/OEPP (European and Mediterranean Plant Protection Organization). Standards: diagnostic protocols for regulated pests: PM7/17(2). Guignardia citricarpa . Bull. OEPP/EPPO Bull. 2009; 39: 318–327. 10.1111/j.1365-2338.2009.02315.x - 5.
Lillie SH, Hanlon E Jr, Kelly JM, Rayburn BB. Army Knowledge Online. 2005. Available from: www.us.army.mil - 6.
Perrotta G, Graniti A. Phoma tracheiphila (Petri) Kanchaveli & Gikashvili. In: Smith IM, Dunez J, Lelliott RA, Phillips DH, Archer SA, editors. European Handbook of Plant Diseases. Blackwell Scientific Publications, Oxford; 1988. pp. 396–398. DOI: 10.1002/9781444314199 - 7.
Boerema GH, de Gruyter J, van Kesteren HA. Contributions towards a monograph of Phoma (Coelomycetes)–III. I. SectionPlenodomus: taxa often with aLeptosphaeria teleomorph. Persoonia. 1994; 15: 431–487 - 8.
Boerema GH, de Gruyter J, Noordeloos ME, Hamers MEC. Phoma identification manual. Differentiation of specific and infra-specific taxa in culture. CABI Publishing, Wallingford, UK; 2004. 448 p. DOI: 10.1079/9780851997438.0000 - 9.
Balmas V, Scherm B, Ghignone S, Salem OM, Cacciola SO, Migheli Q. Characterisation of Phoma tracheiphila by RAPD-PCR, microsatellite-primed PCR and ITS rDNA sequencing and development of specific primers forin planta PCR detection. Eur. J. Plant Pathol. 2005; 111: 235–247. DOI:10.1007/s10658-004-4173-x - 10.
De Gruyter J, Aveskamp MM, Woudenberg JHC, Verkley GJM, Groenewald JZ, Crous PW. Molecular phylogeny of Phoma and allied anamorph genera: towards a reclassification of thePhoma complex. Mycol. Res. 2009; 113: 508–519. DOI: 10.1016/j.mycres.2009.01.002 - 11.
Aveskamp MM, de Gruyter J, Woudenberg JHC, Verkley GJM, Crous PW. Highlights of the Didymellaceae polyphasic approach to characterise Phoma and related pleosporalean genera. Stud. Mycol. 2010; 65: 1–60. DOI: 10.3114/sim.2010.65.01 - 12.
De Gruyter J, Woudenberg JHC, Aveskamp MM, Verkley GJM, Groenewald JZ, Crous PW. Redisposition of Phoma -like anamorphs in Pleosporales. Stud. Mycol. 2013; 75: 1–36. DOI: 10.3114/sim0004 - 13.
EPPO/OEPP (European and Mediterranean Plant Protection Organization). Standards: diagnostic protocols for regulated pests: PM7/048 (3). Plenodomus tracheiphilus (formerlyPhoma tracheiphila ). Bull. OEPP/EPPO Bull. 2015; 45: 183–192. DOI: 10.1111/epp.12218 - 14.
Licciardello G, Grasso FM, Bella P, Cirvilleri G, Grimaldi V, Catara V. Identification and detection of Phoma tracheiphila , causal agent of mal secco disease, by real-time polymerase chain reaction. Plant Dis. 2006; 90: 1523–1530. DOI: http://dx.doi.org/10.1094/PD-90-1523 - 15.
Ezra D, Kroitor T, Sadowski A. Molecular characterization of Phoma tracheiphila , causal agent of mal secco disease of citrus, in Israel. Eur. J. Plant Pathol. 2007; 118:183–191. DOI:10.1007/s10658-007-9128-6 - 16.
Kalai L, Mnari-Hattab M, Hajlaoui MR. Molecular diagnostic to assess the progression of Phoma tracheiphila inCitrus aurantium seedlings and analysis of genetic diversity of isolates recovered from different citrus species in Tunisia. J. Plant Pathol. 2010; 92:3. DOI: 10.4454/jpp.v92i3.307 - 17.
Demontis MA, Cacciola SO, Orrù M, Balmas V, Chessa V, Maserti BE, Mascia L, Raudino F, Magnano di San Lio G, Migheli Q. Development of real-time PCR systems based on SYBR® Green1 and Taqman® technologies for specific quantitative detection of Phoma tracheiphila in infectedCitrus . Eur. J. Plant Pathol. 2008; 120: 339–351. DOI:10.1007/s10658-007-9222-9 - 18.
Raimondo F, Raudino F, Cacciola SO, Salleo S, LoGullo MA. Impairment of leaf hydraulics in young plants of Citrus aurantium (sour orange) infected byPhoma tracheiphila . Funct. Plant Biol. 2007; 34: 720–729. DOI: 10.1071/FP07065 - 19.
Raimondo F, Nardini A, Salleo S, Cacciola SO, Assunta Lo Gullo M. A tracheomycosis as a tool for studying the impact of stem xylem dysfunction on leaf water status and gas exchange in Citrus aurantium L. Trees. 2010; 24:2. DOI: 10.1007/s00468-009-0402-4 - 20.
Migheli Q, Cacciola SO, Balmas V, Pane A, Ezra D, Magnano di San Lio G, Mal secco disease caused by Phoma tracheiphila : a potential threat to lemon production worldwide. Plant Dis. 2009; 93: 853–867. DOI: 10.1094/PDIS-93-9-0852 - 21.
Nigro F, Ippolito A, Salerno M. Mal secco disease of citrus, a journey through a century of research. J. Plant Pathol. 2011; 93: 523–560. DOI: 10.4454/jpp.v93i3.3637 - 22.
Timmer LW, Peever TL, Solel ZVI, Akimitsu K. Alternaria diseases of citrus-novel pathosystems. Phytopathol. Mediterr. 2003; 42: 99–112. DOI: http://dx.doi.org/10.14601/Phytopathol_Mediterr-1710 - 23.
Peever TL, Su G, Carpenter-Boggs L, Timmer LW. Molecular systematic of citrus-associated Alternaria spp. Mycologia. 2004; 96: 119–134. DOI: 10.2307/3761993 - 24.
Woudenberg JHC, Seidi MF, Groenewald E, de Vries M,Stielow B, Thomma BJ et al. Alternaria sectionAlternaria : Species, formae specials or pathotypes. Stud. Mycol. 2015; 82: 1–21. DOI: 10.1016/j.simyco.2015.07.001 - 25.
Ohtani K, Fukumoto T, Nishimura S, Miyamoto Y, Gomi K, Akimitsu K. Alternaria pathosystems for study of citrus diseases. Tree For. Sci. Biotechnol. 2009; 3 (special issue 2): 108–115 - 26.
Tsuge T, Harimoto Y, Akimitsu Y, Ohtani K, Kodama M, Akagi Y et al.. Host-selective toxins produced by the plant pathogenic fungus Alternaria alternata . FEMS Microbiol. Rev. 2013; 37: 44–66. DOI: 10.1111/j.1574-6976.2012.00350.x - 27.
Ajiro N, Miyamoto Y, Masunaka A, Tsuge T, Yamamoto M, Ohtani K et al. Role of the host-selective ACT-toxin synthesis gene ACTTS2 encoding an enoyl-reductase in pathogenicity of the tangerine pathotype of Alternaria alternata. Phytopathology. 2010; 100:120–126. DOI: 10.1094/PHYTO-100-2-1120 - 28.
Garganese F, Schena L, Siciliano I, Prigigallo MI, Spadaro D, De Grassi A, Ippolito A, Sanzani SM. Characterization of citrus-associated Alternaria species in Mediterranean areas. PLoS One. 2016; 11: e0163255. DOI: 10.1371/journal.pone.0163255 - 29.
Elena K. Alternaria brown spot of Minneola in Greece; evaluation of citrus species susceptibility. Eur. J. Plant Pathol. 2006; 115:259–262. DOI:10.1007/s10658-006-9005-8 - 30.
Kakvan N, Zamanizadeh H, Morid B, Hajmansor S, Taeri H. Evaluation of citrus cultivars resistance to Alternaria alternata , the causal agent of brown spot disease, using RAPD-PCR. J. Res. Agric. Sci. 2012; 8: 69–76 - 31.
Cuenca J, Aleza P, Vicent A, Brunel D, Ollitrault P, Navarro L. Genetically based location from triploid populations and gene ontology of a 3.3-Mb genome region linked to Alternaria brown spot resistance in citrus reveal clusters of resistance genes. PLoS One. 2013; 8: e76755. DOI: 10.1371/journal.pone.0076755 - 32.
Peres NA, Timmer LW. Evaluation of the Alter-Rater model for spray timing for control of Alternaria brown spot on Murcott tangor in Brasil. Crop Prot. 2006; 25: 454–460. DOI: 10.1016/j.cropro.2005.07.010 - 33.
Vicent A, Armengol J, Garcia-Jimenez J. Protectant activity of reduced concentration copper sprays against Alternaria brown spot on ‘Fortune’ mandarin fruit in Spain. Crop Prot. 2009; 28: 1–6. DOI: 10.1016/j.cropro.2008.07.004 - 34.
Menge JA. Septoria spot. In: Timmer LW, Garnsey SM, Graham JH, editors. Compendium of Citrus Diseases. 2nd ed. The American Phytopathological Society, St Paul, MN; 2000.pp. 32–33 - 35.
Verkley GJM, Quaedvlieg W, Shin HD, Crous PW. A new approach to species delimitation in Septoria . Stud. Mycol. 2013; 75: 213–305. DOI 10.3114/sim0018 - 36.
Quaedvlieg W, Verkley GJM, Shin HD, Barreto RW, Alfenas AC, Swart WJ, Groenewald JZ, Crous PW. Sizing up Septoria. Stud. Mycol. 2013; 75: 307–390. DOI: 10.3114./sim0017 - 37.
Mondal SN, Timmer LW. Greasy spot, a serious endemic problem for citrus production in the Caribbean basin. Plant Dis. 2006; 90:532–538. DOI: 10.1094/PD-90-0532 - 38.
Huang F, Groenewald JZ, Zhu L, Crous PW, Li H. Cercosporoid diseases of citrus. Mycologia. 2015; 107: 1151–1171. DOI: 10.3852/15-059 - 39.
Abdelfattah H, Cacciola SO, Mosca S, Zappia R, Schena L. Analysis of the fungal diversity in citrus leaves with greasy spot symtoms. Microbial Ecol. Doi:10.1007/s00248-016-0874-x - 40.
Chethana TKW, Li X, Zhang W, Hyde KD, Yan J. Trail of decryption of molecular research on Botryosphaeriaceae in woody plants. Phytopathol. Mediterr. 2016; 55: 147–171. DOI: 10.14601/Phytopathol_Mediterr-16230 - 41.
Huang F, Hou X, Dewdney MM, Fu Y, Chen G, Hyde KD, Li H. Diaporthe species occurring on citrus in China. Fungal Divers. 2013; 61:237–250. DOI 10.1007/s13225-013-0245-6 - 42.
Huang F, Udayanga D, Wang X, Hou X, Mei X, Fu Y, Hyde KD, Li H. Endophytic Diaporthe associated with citrus: a phylogenetic reassessment with seven new species from China. Fungal Biol. 2015; 119: 331–347. DOI: 10.1016/j.funbio.2015.02.06 - 43.
Polizzi G, Aiello D, Vitale A, Giuffrida F, Groenewald JZ, Crous PW. First report of shoot blight, cancer and gummosis caused by Neoscytalidium dimidiatum on citrus in Italy. Plant Dis. 2009; 93: 1215. DOI: 10.1094/PDIS-93-11-1215 - 44.
Elena K, Fischer M, Dimou D, Dimou DM. Fomitiporia mediterranea infecting citrus trees in Greece. Phytopathol. Mediterr. 2006; 45:35–39. DOI: 10.14601/Phytopathol_Mediterr-1813 - 45.
Roccotelli A, Schena L, Sanzani SM, Cacciola SO, Mosca S, Faedda R, Ippolito A, Magnano di San Lio G. Characterization of Basidiomycetes associated with wood rot of citrus in southern Italy. Phytopathology. 2014; 104: 851–858. DOI: 10.1094/PHYTO-10-13-0272-R - 46.
González V, Tuset JJ, Hinarejos R. Fungi associated with wood decay (caries) of citrus. Levante Agríc. 2007; 384: 60–65 - 47.
Roccotelli A, Schena L, Sanzani SM, Cacciola SO, Ippolito A. Fomitopsis sp. causing brown rot in wood of living citrus trees reported for first time in southern Italy. New Dis. Rep. 2010; 22: 13. DOI: 10.5197/j.2044-0588.2010.022.013. - 48.
Cacciola SO, Magnano di San Lio G. Management of citrus diseases caused by Phytophthora spp. In: Ciancio A, Muekerji K G, editors. Integrated Management of Diseases Caused by Fungi, Phytoplasma and Bacteria. Springer Sciences Business Media B.V.,the Netherlands; 2008. pp. 61–84. ISBN: 978-1-4020-8570-3 - 49.
Prigigallo MI, Mosca S, Cacciola SO, Cooke DEL, Schena L. Molecular analysis of Phytophthora diversity in nursery-grown-ornamental and fruit plants. Plant Pathol. 2015; 64: 1308–1319. DOI: 10.1111/ppa.12362 - 50.
Prigigallo MI, Abdelfattah A, Cacciola SO, Faedda R, Sanzani SM, Cooke DEL, Schena L. Metabarcoding analysis of Phytophthora diversity using genus-specific primers and 454 pyrosequencing. Plant Dis. 2016; 106: 305–313. DOI: 10.1094/PHYTO-07-15-0167-R - 51.
Mammella MA, Cacciola SO, Martin F, Schena L. Genetic characterization of Phytophthora nicotianae by the analysis of polymorphic regions of the mitochondrial DNA. Fungal Biol. 2011; 115: 432–442. DOI: 10.1016/j.funbio.2011.02.018 - 52.
Mammella MA, Martin FN, Cacciola SO, Coffey MD, Faedda R, Schena L. Analyses of the population structure in a global collection of Phytophthora nicotianae isolates inferred from mitochondrial and nuclear DNA sequences. Phytopathology. 2013; 103: 610–622. DOI: 10.1094/PHYTO-10-12-0263-R - 53.
Biasi A, Martin FN, Cacciola SO, Magnano di San Lio G, Grunwald N, Schena L. Genetic analysis of Phytophthora nicotianae populations from different hosts using microsatellite markers. Phytopathology. 2016; DOI: 10.1094/PHYTO-11-15-0299-R - 54.
Farih A, Menge JA, Tsao PH, Ohr HD. Metalaxyl and efosite aluminium for control of Phytophthora gummosis and root rot of citrus. Plant Dis. 1981; 65: 654–657. DOI: 10.1094/PD-65-654 - 55.
Timmer LW and Castle WS. Effectiveness of metalaxyl and fosetyl-Al against Phytophthora parasitica on sweet orange. Plant Dis. 1985; 69: 741–743. DOI: 10.1094/PD-69-741 - 56.
Matheron ME and Matejka JC. Persistence of systemic activity for fungicides applied to citrus trunks to control Phytophthora gummosis. Plant Dis. 1988; 72: 170–174. DOI: 10.1094/PD-72-0170 - 57.
Matheron ME, Porchas M, Matejk JC. Distribution and seasonal population dynamics of Phytophthora citrophthora andP. parasitica in Arizona citrus orchards and effect of fungicides on tree health. Plant Dis.1997; 81: 1384–1390. DOI: 10.1094/PDIS.1997.81.12.1384 - 58.
Matheron ME, Porchas M. Comparative ability of six fungicides to inhibit development of Phytophthora gummosis on citrus. Plant Dis. 2002; 86: 687–690. DOI: 10.1094/PDIS.2002.86.6.687 - 59.
Timmer LW, Sandler HA, Graham JH, Zitko LE. Sampling citrus orchards in Florida to estimate populations of Phytophthora parasitica . Phytopathology. 1988; 78: 940–944. DOI:10.1094/Phyto-78-940 - 60.
Timmer LW, Zitko LE, Sandler HA, Graham JH. Seasonal and spatial analysis of populations of Phytophthora parasitica in citrus orchards in Florida. Plant Dis. 1989; 73: 810–813. DOI: 10.1094/PD-73-0810 - 61.
Magnano di San Lio G, Messina F, Greco G, Perrotta G. Effect of irrigation on the dynamics of Phytophthora citrophthora populations in soil of citrus orchards. Bull. OEPP/EPPO Bull. 1990; 20: 83–89. DOI: 10.1111/j.1365-2338.1990.tb01182.x - 62.
Agostini JP, Timmer LW, Castle WS. Effect of citrus rootstocks on soil populations of Phytophthora parasitica . Plant Dis. 1991; 75:296–300. DOI: 10.1094/PD-75-0296 - 63.
Ippolito A, Schena L, Nigro F, Soleti Ligorio, Yaseen T. Real-time detection of Phytophthora nicotianae andP. citrophthora citrus roots and soil. Eur. J. Plant Pathol. 2006; 110: 833–843. DOI: 10.1007/s10658-004-5571-9 - 64.
Klotz LJ. Fungal, bacterial and non-parasitic diseases and injuries originating in the seedbed, nursery and orchard. In: Reuther W, Calavan EC, Carman GF, editors. The Citrus Industry. Vol. 4, Crop Protection. University of California Agricultural Sciences Publications, Richmond, USA; 1978. pp. 1–66. ISBN: 0-931876-24-9 - 65.
Graham JH and Menge JA. Phytophthora-Induced diseases. In: Timmer LW, Garnsey SM, Graham JH, editors. Compendium of Citrus Diseases. 2nd ed. The American Phytopathological Society, Minnesota; 2000. pp. 12–15 - 66.
Magnano di San Lio G. Fungal diseases. In: Tribulato E, Inglese P, editors. Citrus. Bayer CropScience, Ed. Script, Bologna; 2012. pp. 246–265. ISBN: 978-88-6614-856-2