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Editor» EditorinChief: Dagmar Hanold SUBMIT BACK NEXT 1/10RESEARCH ARTICLE
Searching for resistance sources to Verticillium
wilt of cotton in seedlings from
Gossypium spp.
Mehmet Erhan Göre1&Oktay Erdoğan2
&Nedim Altın3
Received: 25 April 2016 / Accepted: 7 December 2016 / Published online: 19 December 2016 # Sociedade Brasileira de Fitopatologia 2016
Abstract Verticillium dahliae is a major wilt pathogen impacting cotton production in Turkey. Isolates of V. dahliae can be characterized as defoliating (D) or nondefoliating (ND) pathotypes based on symptom expression in cotton. Currently there are no fungicides identified that can manage this patho-gen. Host resistance is the most economical and environmen-tally friendly means to manage this disease. Cotton genotypes, comprising the main cultivars and some breeding lines avail-able in Turkey, were evaluated under controlled conditions for resistance to verticillium wilt. To establish adequate condi-tions for resistance expression, experiments examining isolate pathogenicity and the most appropriate inoculum concentra-tion were carried out first. Based on the obtained data, 10 cultivars were then inoculated with D and ND pathotypes by the“pot immersion” method at 106conidia/mL inoculum con-centration and the plants were evaluated considering both in-ternal and exin-ternal disease symptoms. Plants were scored on a 0 to 4 scale for above-ground symptoms (0 = healthy; 4 = dead plant) ca. two weeks after inoculation. Significant differences in resistance level were observed among the genotypes (p < 0.05). The cultivar Maydos Yerlisi had the lowest level of wilt, with a mean rating of 1.0. The cultivar Nazilli NDT-15 had the strongest wilt, with a mean rating of 3.3. These results
suggest that‘Maydos Yerlisi’ can be used in cotton breeding programs to develop resistant varieties to V. dahliae.
Keywords Defoliating and non-defoliating pathotypes . Resistant rootstock . Root-dip inoculation . Verticillium wilt
Introduction
Cotton (Gossypium spp.) is the most widely cultivated fiber crop in the world, with upland cotton (G. hirsutum L.) as the predominant type. Verticillium wilt, a fungal disease caused by Verticillium dahliae Kleb., has become one of the main constraints in cotton production. The disease caused 0.5– 3.5% yield loss nationwide in the US (Blasingame and Patel
2005) and as high as 7% in Turkey (Karademir et al.2012).
Verticillium wilt also significantly reduces fiber quality, in-cluding fiber length and micronaire (Göre et al.2009). Many methods, such as crop rotation, chemical fumigation and soil amendments, have been applied to control this disease, but none are effective due to the wide host range of the pathogen, long-term persistence of its resting structure (microsclerotia), and the inability of fungicides to affect the pathogen once the plants are infected (Lüders et al.2008).
The most efficient and cost-effective method of controlling the disease is the use of resistant cotton cultivars. Identifying sources of resistance has been successful to improve verticillium wilt resistance in other crop species (Göre et al.
2011,2014). For example, the resistance gene Ve, which
con-fers resistance to some isolates of V. dahliae, has been cloned in tomato, Solanum lycopersicum L. (Diwan et al.1999). Of the four cultivated cotton species (G. hirsutum, G. barbadense L., G. arboretum L., and G. herbaceum L.), only G. barbadense, known as Pima cotton in the US, has a higher level of resistance against verticillium wilt (Wilhelm et al. Section Editor: Rosana Rodrigues
* Mehmet Erhan Göre egore@ibu.edu.tr
1
Department of Plant Protection, Abant Izzet Baysal University, Bolu, Turkey
2
Department of Biosystem Engineering, Nevsehir Haci Bektas Veli University, Nevsehir, Turkey
3 Department of Plant Protection, Duzce University, Duzce, Turkey Trop. plant pathol. (2017) 42:28–31
1974). However, it is planted in very limited areas in California, as well as in the arid regions of Arizona, New Mexico and southwest Texas (USDA-ERS 2013). Resistance from Pima cotton has not been successfully trans-ferred into commercial upland cotton (Zhang et al.2012). Since the 1930s, Acala cultivars, thought to be derived from Pima cotton germplasm, have been released in California and New Mexico for cotton production (Zhang et al.2005). Due to high yield, good fiber quality and resistance to verticillium wilt, these Acala cultivars have been used to control verticillium wilt. However, Zhang et al. (2012) reported that only some Acala cotton conferred resistance to the disease.
Upland cotton is widely planted throughout Turkey, ac-counting for about 97% of the annual cotton crop (Harem 2014). However, highly resistant cultivars to verticillium wilt are lacking and no source of heritable immunity has been found in upland cotton (Wilhelm et al.1974). Great efforts have been made to improve the resistance of upland cotton against verticillium wilt worldwide. Zhang et al. (2012) re-ported that the verticillium wilt resistance in Pima was suc-cessfully transferred to upland cotton lines by advanced backcrossing and selfing. Fang et al. (2013) have mapped two quantitative trait loci (QTL) for verticillium wilt resis-tance in an interspecific backcross inbred line population and 21 QTLs associated with verticillium wilt resistance in an introgressed inbred line population. However, whether verticillium wilt resistance can be transferred from Pima to upland cotton through pedigree selection is currently un-known. Information on levels of resistance against verticillium wilt worldwide is lacking for most commercial cultivars, most of which were developed under non-verticillium wilt conditions. The same is true for advanced breeding lines developed from public cotton breeding pro-grams in Turkey. Verticillium wilt disease resistance genes may have been randomly fixed during the selection process. The objective of this study was to evaluate verticillium wilt resistance in commercial cotton cultivars and breeding lines under controlled conditions.
Material and methods
In this study, the effects of different amounts (100, 150, 200 mL) and concentrations (104, 105, 106conidia/mL) of the D pathotype of V. dahliae on disease development in the cultivar Deltapine 15–21 (reference control) was firstly inves-tigated, and 200 mL of a 106conidia/mL suspension was selected for further studies (Table1).
Ten cotton cultivars were evaluated for resistance to V. dahliae in two experiments in controlled conditions in a growth chamber, with eight replications per experiment. The cultivars were BA-119, Carmen, Çukurova-1518, Giza-45, Gosspolsuz Nazilli, Maydos Yerlisi, Nazilli 84-S, Nazilli
NDT-15, Sayar-314 and SG-125. Plant material was obtained from the Cotton Research Institute, Aydın, Turkey. Plants were inoculated with isolates I/22 (VCG2B) and Mn/8 (VCG1) of V. dahliae, from the collection of the Plant Pathology Laboratory, Plant Protection Research Institute, Izmir, Turkey. Isolate I/22 represents a mildly virulent, cotton ND pathotype, and Mn/8 a highly virulent, cotton D pathotype (Göre2007). Both isolates maintain the same differential path-ogenicity in cotton (Göre2007). The experiments were con-ducted in a randomized block design. The seeds were planted in 4-in plastic pots with 3 seeds per pot. The pots were filled with potting soil (Scott 450, Scotts Co.) mixed with slow release Osmocote fertilizer (Scotts Co.). After emergence, seedlings were thinned to 1 plant per pot. Plants were grown in a growth chamber under fluorescent illumination of 216– 270μE/m2/s, 14:10 light:dark. Temperature and relative hu-midity, respectively, were 24–27°C and 50–70% during the light period, and 18–22°C and 60–80% during the dark period.
Both isolates were cultured in Czapek-Dox broth at 24°C and 140 rpm on a rotary shaker for two weeks. The conidial suspension was passed through a double-layer of cheesecloth to separate spores (conidia) from mycelia. Concentration of conidia was adjusted with a haemocytometer. When seedlings were at the 3–4 true leaf stage, root inoculation was made by pouring 200 mL of a 4 × 106conidia/mL suspension on the soil surface of each pot. Control plants were treated similarly with sterile distilled water. Assessment of the leaf severity of wilt symptoms was done 15 days after inoculation (DAI). A scale of 0 to 4 was used according to the percentage of foliage affected by chlorotic, necrotic and wilt symptoms and/or de-foliation, in an acropetal progression (0 = no symptoms; 1 = 1– 33% foliage affected; 2 = 34–66% foliage affected; 3 = 67– 100% foliage affected; 4 = dead plants) (Bejarano-Alcázar et al. 1996). Data were statistically analyzed according to standard procedures for analysis of variance (general linear Table 1 Effect of the concentration and amount of the Verticillium dahliae defoliating (D) isolate Mn/8 on disease development in the upland cotton (G. hirsutum) cultivar Deltapine 15–21
Concentration of inoculum (conidia/mL)
Amount (mL) Mean disease severity index 104 100 1.58 150 2.00 200 1.79 105 100 1.50 150 2.18 200 2.35 106 100 2.29 150 2.42 200 3.38
model) and mean separation (least significant difference) (SAS Institute). All differences referred to in the text were significant at 5% probability.
Results
Symptoms ranging from sudden wilt to severe chlorosis of leaves and stunting were observed in plants inoculated with both the D and ND V. dahliae pathotypes. Chlorosis was the most common symptom, observed within 10 days after inoc-ulation when the ND pathotype was used. Leaves became necrotic but remained attached to the stems. In plants inocu-lated with the D pathotype, chlorosis was associated with cul-tivars showing a certain level of resistance and defoliation was also common. Defoliation occurred in the absence of chlorosis in most of the susceptible cultivars inoculated with the D pathotype, starting at 7 days and intensifying from the tenth day after inoculation. Defoliation ranged from intensive in susceptible cultivars such as BA-119, Carmen, Çukurova-1518, NDT-15 and Sayar-314, to slight and restricted to the middle of the main shoots in moderately susceptible cultivars such as Giza-45, Gossypolsuz Nazilli, Nazilli-84-S and SG-125. The D pathotype induced a higher incidence of disease and symptom severity than the ND pathotype and earlier death of plants. The D pathotype caused between 13 and 63% mor-tality in seven out of the 10 cultivars inoculated, whereas mortality was only observed in five of them when the ND pathotype was used (Table2). From the thirteenth day after inoculation, only one cultivar, Nazilli 84 S, showed recovery from the disease, expressed as a reduction in disease severity. This phenomenon was not observed in cultivars inoculated with the ND pathotype (Table2). Cultivars were classified into resistance categories, with most of them being more sus-ceptible to the D pathotype than to the ND pathotype (Table2). Eight of the 10 cultivars were susceptible or ex-tremely susceptible to both pathotypes of V. dahliae. This group includes the most important Turkish commercial culti-vars, such as BA-119, SG-125 and Nazilli-84-S. Only one cultivar, Maydos Yerlisi, was found to be resistant to both pathotypes, showing only slight chlorosis when inoculated with both the D and ND pathotypes which began to diminish from 10 days after inoculating with either pathotype, reaching medium final values of symptom severity. This result suggests that this cultivar can be used in cotton breeding programs to develop varieties with good agronomic characteristics.
In the analysis of V. dahliae pathotypes over cotton culti-vars, the D pathotype was significantly different from the ND pathotype in terms of disease symptoms and damage to the plants. The LSD tests comparing mean values of cultivars inoculated with D and ND V. dahliae pathotypes (Table2) showed that BA-119, NDT-15 and Sayar-314 had the highest mean disease index values, while the average mean value for
Çukurova 1518 (reference control) was lower than those for these cultivars.
Discussion
Our method proved to be adequate for testing cultivar resis-tance to Verticillium wilt. The disease reaction showed by the reference cultivar, Çukurova 1518, was effectively differenti-ated in our inoculations by the mean disease index values and PDP, and consistent with those observed in the field (Korolev et al.2001). Isolation of the fungus from affected plants during the experiments demonstrated that plants were consistently infected, irrespective of the cultivar, pathotype and resistance level (Garber and Houston1967).
Table 2 Mean disease severity index (DSI), percentage of dead plants (PDP) and susceptibility of cotton cultivars inoculated with isolates belonging to defoliating (D) and non-defoliating (ND) pathotypes of Verticillium dahliae
Cultivar Resistance source Mean DSI1 PDP Score2 Defoliating isolate
BA-119 G. hirsutum 3.4ab 50 ES Carmen G. hirsutum 3.0abc 37.5 S Çukurova-1518 G. hirsutum 2.9abc 37.5 S Giza-45 G. barbadense 3.0abc – S Gossypolsuz Nazilli G. hirsutum 2.9abc 12.5 S Maydos Yerlisi G. herbaceum 1.0d – R Nazilli-84-S G. hirsutum 2.6bc 25 S Nazilli NDT-15 G. hirsutum 3.5a 62.5 ES Sayar-314 G. hirsutum 3.1abc 37.5 ES SG-125 G. hirsutum 2.5c – S Nondefoliating isolate BA-119 G. hirsutum 2.6A 25 S Carmen G. hirsutum 1.6B 12.5 MS Çukurova-1518 G. hirsutum 2.5A – S Giza-45 G. barbadense 2.6A – S Gossypolsuz Nazilli G. hirsutum 2.4A – S Maydos Yerlisi G. herbaceum 1.0B – R Nazilli-84-S G. hirsutum 2.9A 12.5 S Nazilli NDT-15 G. hirsutum 3.1A 37.5 ES Sayar-314 G. hirsutum 2.9A 37.5 S SG-125 G. hirsutum 2.5A – S Four-week-old cotton plants were inoculated with isolates belonging to the ND or D pathotypes of V. dahliae. Assessment of the severity of wilt symptoms was carried out at 15 days after inoculation
1
Mean values followed by the same lowercase letter (for the D isolate) and uppercase letter (for the ND isolate) are not significantly different at 5% probability according to the LSD test
2
R, resistant; MS, Moderately susceptible; S, susceptible; ES, extremely susceptible; Categories correspond to the following interval of values of mean DSI: R = 0−1; MS = 1+−2; S = 2+−3; ES = 3+−4
Almost all the evaluated cultivars have been catalogued as susceptible or extremely susceptible to both pathotypes of V. dahliae, including the most important Turkish cultivars (Table2). Moreover, all the cultivars were more susceptible and showed a higher frequency of positive isolation of the pathogen from affected plant tissues when they were inocu-lated with the D rather than with the ND pathotype. These results agree with studies of Schnathorst and Mathre (1966), Schnathorst et al. (1975) and Bejarano-Alcázar et al. (1996).
We have also demonstrated that BA-119, NDT-15 and SG-125 cultivars, widely used nowadays in Turkey, show the same susceptibility as Çukurova-1518 (Table2). Also, culti-vars Giza-45, Gossypolsuz Nazilli and Nazilli-84-S were as susceptible as Sayar-314 to both pathotypes (Table 2). Cultivar Carmen was susceptible to the D, but resistant to the ND pathotype (Table2). This differential reaction could be used to test‘Carmen’ in soil infested with low inoculum densities of ND isolates of V. dahliae. ‘Maydos Yerlisi’ was resistant to the both pathotypes and this makes it promising for use in breeding programs.
In conclusion, the present study demonstrated that the most commonly cultivated cultivars in Turkey are highly suscepti-ble to both the D and ND pathotypes of V. dahliae under our experimental inoculation conditions. The best resistance sources were‘Carmen’ and ‘Maydos Yerlisi’. Consequently, there is a need to pursue the search for resistance sources in additional cotton genotypes and closely related species. Acknowledgements We thank Ercan Gül for providing the V. dahlie isolates of the D and ND pathotypes, and for laboratory support.
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