Revista Mexicana de Fitopatología

ISSN: 0185-3309

mrlegarreta@prodigy.net.mx

Sociedad Mexicana de Fitopatología, A.C.

México

Montes-García, Noé; Williams-Alanis, Héctor; Norman-Odvody, Gary; Kajac-Prom, Louis

Comparative Efficacy of Triazole Fungicides for Control of Claviceps africana Frederickson, Mantle,

and de Milliano in Sorghum [Sorghum bicolor (L.) Moench.] Seed Production of Northern Mexico

Revista Mexicana de Fitopatología, vol. 23, núm. 2, julio - diciembre, 2005, pp. 152-156

Sociedad Mexicana de Fitopatología, A.C.

Texcoco, México

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Comparative Efficacy of Triazole Fungicides for Control ofClaviceps africana Frederickson, Mantle, and de Milliano inSorghum [Sorghum bicolor (L.) Moench.] Seed Production of

Northern MexicoNoé Montes-García, Héctor Williams-Alanis, INIFAP, Campo Experimental Río Bravo,Apdo. Postal 172, Río Bravo, Tamaulipas, México CP 88900; Gary Norman-Odvody,TAMU Agricultural Research and Extension Center, Rt 2, Box 589, Corpus Christi, TX,USA 78406; and Louis Kajac-Prom, USDA-ARS, 2765 F&B Road, College Station,TX, USA 77845. Correspondence to: nmontes62@hotmail.com

Montes-García, N., Williams-Alanis, H., Norman-Odvody,G., and Kajac-Prom, L. 2005. Comparative efficacy of triazolefungicides for control of Claviceps africana Frederickson,Mantle and de Milliano in sorghum [Sorghum bicolor (L.)Moench.] seed production of northern Mexico. RevistaMexicana de Fitopatología 23:152-156.Abstract. A study was established to minimize the effect ofsorghum ergot caused by Claviceps africana in sorghum seedproduction fields. Efficacy of four triazole fungicides againstergot, was determined using the male-sterile sorghum lineATx635 under field conditions. Fungicide rates of 0 (control),31, 62, 125, and 250 µg ml-1 or µl ml-1 (ppm) were applied atbloom stage. The combined analysis showed that ergotseverity was significantly affected by fungicide brand andrates. Severity values observed on the different fungicide ratesshowed similar trends among years. The relationship betweenergot severity and fungicide rate was better represented byexponential decay regression models. According to themodels, triadimefon (Bayleton®) (y = 57.6356e-0.0448x) showedthe best control. The models for propiconazole (Tilt®) andtebuconazole (Folicur®) showed that at least 250 µl ml-1 arerequired to eliminate ergot infection. Meanwhile, C. africanainfection was reduced to zero at rates of less than 150 µg ml-

1 for triadimefon and about 200 µg ml-1 for acibenzolar-s-methyl (Actigard®). The area under the disease reductioncurve (AUDRC) analysis showed that propiconazole had thehighest value (3384), followed by tebuconazole with 2984;meanwhile, the lowest value of 1296 was provided bytriadimefon. If fungicides are applied using a ground method,a total of 100 ml ha-1 of Tilt® and 105 ml ha-1 of Folicur® arerequired to control ergot. Meanwhile, C. africana can becontrolled with only 36 g ha-1 of Bayleton® or with 56 g ha-

1 of Actigard®.

Additional keywords: Clavicep, ergot, area under the diseasereduction curve (AUDRC).

Resumen. Se estableció un estudio para minimizar el efectodel cornezuelo del sorgo causado por Claviceps africana enlotes de producción de semilla. La eficacia de cuatrofungicidas triazólicos sobre cornezuelo, se determinó usandola línea andro-estéril de sorgo ATx635 bajo condiciones decampo. Dosis de fungicidas de 0 (testigo), 31, 62, 125 y 250µg ml-1 ó µl ml-1 (ppm) se aplicaron durante la floración. Elanálisis combinado mostró que la severidad del cornezuelofue afectada significativamente por el tipo de fungicida y lasdosis. Los valores de severidad en las diferentes dosis defungicidas mostraron tendencias similares a través de los años.La relación entre severidad del cornezuelo y la dosis defungicida fue mejor representada por modelos de regresiónexponencial negativos. De acuerdo a los modelos, triadimefon(Bayleton®) (y = 57.6356e-0.0448x) mostró el mayor control.Los modelos para propiconazole (Tilt®) y tebuconazole(Folicur®) mostraron que se requieren al menos 250 µl ml-1

para eliminar la infección del cornezuelo. Mientras que lainfección por C. africana se redujo a cero con dosis menoresa 150 µg ml-1 con triadimefon y alrededor de 200 µg ml-1 conacibenzolar-s-methyl (Actigard®). El análisis del área bajola curva de reducción de la enfermedad (ABCRE), mostróque propiconazole tuvó el mayor valor (3384) seguido portebuconazole con 2984; mientras que el valor más bajo (1296)lo mostró triadimefon. Si los fungicidas se aplican usando unmétodo terrestre, se requiere de un total de 100 ml ha-1 deTilt® y 105 ml ha-1 de Folicur® para controlar el cornezuelo,mientras que C. africana se puede controlar con sólo 36 gha-1 de Bayleton®, o con 56 g ha-1 de Actigard®.

Palabras clave adicionales: Claviceps, cornezuelo, área bajola curva de reducción de la enfermedad (ABCRE).

Since its introduction to the Americas in 1995 (Reis et al.,1996), sorghum ergot caused by Claviceps africanaFrederickson, Mantle and de Milliano is a serious threat to

(Received: March 28, 2005 Accepted: June 10, 2005)

152 / Volumen 23, Número 2, 2005

sorghum productivity. Ergot has been target to be controlledby triazole fungicides that have systemic activity and areabsorbed through the sorghum [Sorghum bicolor (L.)Moench.] head, and translocated within the plant through thexylem. The principal objective of these compounds is toinhibit the ergosterol synthesis beside the long protective andcurative activity against diseases caused by manyascomycetes, imperfect fungi and basidiomycetes (Agrios,1997). The fungus C. africana only attacks unfertilizedovaries, infecting and forming a fungal structure called asphacelium that contains hyphae, macroconidia, andmicroconidia. Male-sterile sorghum lines are highlysusceptible to ergot infection, because they depend on pollenfrom other plants to be fertilized, and this situation can beaggravated when weather conditions are favorable for pollensterility (Montes et al., 2002b) on the pollinator plants, orwhen they can restrict the period when pollen is available forfertilization (Bandyopadhyay et al., 1998). Because of thissituation, sorghum ergot has been considered a major threatto the main sorghum hybrid seed production areas of theworld. Recent research on chemical control of C. africanahas been focused on the use of systemic fungicides. Acollaborative research program was developed during 1995in Brazil to control the disease using triazole fungicidesapplied alone and in combinations (De Almeida et al., 1997).Using a male-sterile sorghum line inoculated with a local C.africana isolate, tebuconazole at 375 ppm a.i. ha-1 (Folicur®

3.6E, Bayer), and propiconazole applied at 250 ppm a.i. ha-

1 (Tilt®, Syngenta), were effective in controlling the disease.They also noticed toxicity to sorghum heads (reduced seedgermination) as a result of the application of triadimenol,despite its good control of the disease. They found a non-curative effect of the fungicides due to the higher values ofdisease severity observed on plots that were artificially ornaturally inoculated before the fungicide application. In thespring of 1997, sorghum ergot was reported in Mexico(Aguirre et al., 1997), and Texas (Isakeit et al., 1998), andthe economic impact of the disease was felt immediately.According to Dahlberg (1997), emergency exemptionsdefined by the Animal and Plant Health Inspection Service(APHIS) of the United States, were sought and granted touse the systemic triazole fungicide propiconazole on nurseriesand seed production fields to control and prevent the disease.In Zimbabwe, Frederickson and Leuschner (1997) noticedthat treatment with benomyl or thiram was ineffective ifapplied when the plants already had the disease symptoms.Meanwhile, the application at flowering stage or stigmaexsertion reduced drastically the disease severity with a 0.2%a.i. of benlate. In other studies, McLaren (1994) and Monteset al. (2002c) observed that triazole fungicides failed tocontrol the disease when they were applied once during theflowering period. Triadimefon has been used to control ergotin buffelgrass (Cenchrus ciliaris L.) with beneficial effectsof frequent applications of 150 µl ml-1 in the duration of theprotection against the fungus. The results obtained with

triadimefon in buffelgrass could be applicable to the problemof ergot in crops like barley (Hordeum vulgare L.), wheat(Triticum aestivum L.), pearl millet [Pennisetum glaucum (L.)R. Br.] and sorghum (Craig and Hignight, 1991). Montes etal. (2002c) conducted several studies at Corpus Christy,Texas, to identify the most effective fungicide to use in hybridseed production fields, and they found that infection by C.africana can be reduced by triazole fungicides that make goodcontact with the sorghum florets. Triadimefon (Bayleton®

50DF, Bayer AG) gave the best control of ergot.Propiconazole at 250 ppm provided control of ergot similarto lower rates (62 ppm) of triadimefon. In other study, Promand Isakeit (2003) observed in field evaluations that a singleapplication of propiconazole, tebuconazole, triadimefon,myclobutanil (Nova® 40G, Dow AgroSciences LLC,Indianapolis, IN) or azoxystrobin (Quadris® 2.08F, Syngenta,Greensboro, NC) at a rate of 25 µg ml-1 controlled ergotdisease on the sorghum male-sterile line ATx623. Theymentioned that results from field trials suggest that ergotcontrol, particularly under ergot conducive environments, mayrequire higher rates than the ones used in their study.Therefore, and because ergot is endemic in the northern partof Mexico, we established this study to minimize the effectof C. africana in sorghum seed production fields by observingthe effect of triazole fungicides on the disease, and identifythe best one that can control the disease at a lower cost. Thisinformation will benefit farmers and seed productioncompanies that are located in the area.

MATERIALS AND METHODSThree experiments were conducted during the spring of 1999,fall of 2000, and fall of 2002 at Rio Bravo INIFAP´sExperimental Station, located in northern Tamaulipas,Mexico. Triazole fungicides propiconazole, tebuconazole ,and triadimefon, and the systemic acquired resistancecompound acibenzolar-s-methyl (Actigard® 50WG-A,Syngenta) were applied at rates of 0 (control), 31, 62, 125,and 250 µg ml-1 or µl ml-1 (ppm) to sorghum heads of thecultivar ATx635 (Texas A&M University male-sterile line).Heads were bagged at bloom initiation with Lawson® paperbags until the end of anthesis (to ensure that all the stigmaswere exposed), after which they were treated. Each fungiciderate was applied to 10 random panicles by using a hand-heldsprayer until runoff. Each panicle was considered a replicate.Panicles treated with fungicides were allowed to dry and theninoculated with a suspension of Claviceps africana (1.6 x106 conidia ml-1) until runoff using a hand-held sprayer.Disease assessment was performed four to six days afterinoculation. Ergot severity based on the percentage ofdiseased florets on each head (showing sphacelia and/orhoneydew) was recorded.Statistical analysis. Data were transformed using thelogarithmic (log X + 1) function to be normally distributed.Analysis of variance (ANOVA) using Statistical AnalysisSystem 8e (SAS Institute, Cary, NC) was performed for a

Revista Mexicana de FITOPATOLOGIA/ 153

factorial experiment in a complete randomized design toevaluate the effect of fungicide, rate and the interaction. Chi-square (÷2) test was performed to determine if there washomogeneity of error variances among years. Comparison ofmeans (using transformed data; Tukey’s separation of means),and non-linear regression models (exponential decay models)were estimated using SAS procedures. The model used forthe exponential decay regression line was: y = becx, where: y= estimated ergot severity (%); b = intercept; e = is a constant(2.711828); c = constant, and x = rate or fungicideconcentration (ppm). Also, to compare the effectiveness ofthe different fungicides, the area under the disease progresscurve (AUDPC) was calculated with modifications. TheAUDPC has been used to describe an epidemic due tofluctuations in disease rates over time (Shaner and Finney,1977). In our case, AUDPC was modified to describefluctuations in disease rates over fungicide doses. The nameof AUDPC is related to the increase in the epidemics,therefore, in our study, we call it area under disease reductioncurve (AUDRC) due to the nature of the obtained exponentialdecay regression models. The applied formula was:

indicated that there was indeed homogeneity of variances,and therefore the data of the three years were combined. Thecombined analysis showed that ergot severity on the male-sterile line ATx635 was significantly affected by fungicide,rates and by the fungicide-rate interaction (Table 1). Ergotseverity values observed on the different fungicide rates,showed similar trends among years. Statistically, triadimefonprovided at all rates the best ergot control over the otherfungicides. The relationship between ergot severity andfungicide rate was better represented by exponential decayregression models. All fungicides showed similar trends intheir ergot control; nevertheless, according to the models,triadimefon (y = 57.6356 e-0.0448x ; r2 = 0.86, P < .0001) showedthe best C. africana control over the others. The model foracibenzolar-s-methyl (y = 54.9670 e-0.0307x ; r2 = 0.84, P <.0001) was similar to the one provided by triadimefon.Tebuconazole (y = 61.7459 e-0.0206x ; r2 = 0.82, P < .0001) andpropiconazole (y = 59.9058 e-0.0175x ; r2 = 0.82, P < .0001)models showed similarities in their control. The models forpropiconazole and tebuconazole showed that at least 250 µlml-1 are required to eliminate ergot infection. Meanwhile, C.africana infection was reduced to zero at rates lower than150 µg ml-1 for triadimefon, and about 200 µg ml-1 foracibenzolar-s-methyl. According to the models, for every unitof triadimefon applied to the sorghum florets, there was 1.5,1.2, and 0.5 times better control of ergot than the onesprovided by propiconazole, tebuconazole, and acibenzolar-s-methyl, respectively. Also, for every unit of tebuconazoleapplied, there was 0.2 times better control than propiconazole,and 0.33 times less than acibenzolar-s-methyl (Fig. 1). Withthe data provided by the exponential decay regression models,an AUDRC analysis was performed. Propiconazole showedthe highest value (3384) followed by tebuconazole with 2984.The lowest value of 1296 was provided by triadimefon almostsimilar to the value of 1796 by acibenzolar-s-methyl. Thisanalysis determine that triadimefon gave the lowest AUDRCand that it can perform 1.6 and 1.3 times better thanpropiconazole and tebuconazole, respectively. Also,triadimefon gave 0.39 more effectiveness than acibenzolar-s-methyl. The differences (total of 2088 units) between the

Ó((ãi + ãi+1)/2) (Ãi+1 - Ãi)i

n-1AUDRC =

Where: n = Number of assessment times; AUDRC has unitsof concentration rates; ãi = Disease severity observed in the(Ãi) concentration; ãi+1 = Disease severity observed in the (Ãi+1)concentration; Ãi+1 = Value of the (Ãi+1) concentration; Ãi =Value of the (Ãi) concentration.

RESULTSErgot severity on ATx635 line was significantly affected bythe year factor. Differences in the amount of disease amongyears were significant. On the Spring of 1999, an average of28% ergot severity was recorded, while, during 2000, ergotwas observed near the 12% value, statistically different fromthe 18% severity observed during the fall of 2002. A test ofhomogeneity of error variances of the three-year data

Year 2 35.2120 17.6060 379.07** <.0001Fungicide 3 8.3845 2.7948 60.17** <.0001Rate 4 158.6077 39.6519 853.73** <.0001Year*Fungicide 6 14.2155 2.3693 51.01** <.0001Fungicide*rate 12 3.0775 0.2564 5.52** <.0001Year*rate 8 11.2003 1.4000 30.14** <.0001Year*Fung*rate 24 14.5659 0.6069 13.07** <.0001Error 540 25.0806 0.0464

Source Df Sum of Mean F value Prob > F squares square

Table 1. Combined analysis of variance for Claviceps africana severityobserved in a male-sterile sorghum (Sorghum bicolor) line at Rio Bravo,Mexico, treated with triazole fungicides.

154 / Volumen 23, Número 2, 2005

fertilization.

CONCLUSIONTriadimefon was the best triazole fungicide that reduced C.africana infection to zero at rates lower than 150 µg ml-1.Complete coverage of sorghum heads with triadimefon at lowapplication rates might be an economical and efficientmanagement strategy for C. africana control in seedproduction areas of northern Mexico, where the disease hasbeen endemic for the past five years.

Acknowledgments. We thank William L. Rooney forproviding the genetic material used in this study, and alsoThomas Isakeit for providing some of the fungicides used.We also want to express our gratitude to Lauro Macias,Francisco Garcia, Ciro Longoria, and Daniel Alvarado fortheir technical assistance during the course of this study. Thisresearch was developed between INIFAP, TAMU, and theUSDA, and was funded in part by the USDA/FAS/ICD/RSEDgrants 58-3148-7-026 and 586202-1-F151 to developresearch on sorghum ergot.

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