Biological Control 74 (2014) 1–5

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Biological Control

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Management of white mold in processing tomatoes by Trichoderma spp.and chemical fungicides applied by drip irrigation

http://dx.doi.org/10.1016/j.biocontrol.2014.03.0091049-9644/� 2014 Elsevier Inc. All rights reserved.

⇑ Corresponding author. Fax: +55 62 3533 2100.E-mail addresses: renatalvesufg@yahoo.com.br (R.A. de Aguiar), mgc@agro.ufg.br

(M.G. da Cunha), murillo.lobo@embrapa.br (M. Lobo Junior).

Renata Alves de Aguiar a, Marcos Gomes da Cunha a, Murillo Lobo Junior b,⇑a College of Agronomy, Federal University of Goiás, Campus Samambaia, Rodovia GO-462 km 0, 74690-900 Goiânia, GO, Brazilb Embrapa Rice and Beans, Rodovia GO-462 km 12, 75375-000 Santo Antônio de Goiás, GO, Brazil

h i g h l i g h t s

�White mold on processing tomatowas controlled by Trichoderma spp.� Control was achieved by chemigation

in a drip-irrigated field, in 2009 and2010.� White mold control was not

improved by fungicides applied viachemigation.� The use of Trichoderma spp. increased

processing tomato yields in up to25 t ha�1.� Biological control increased pulp

yield from 1.0 (2009) to 7.0 t ha�1 in2010.

g r a p h i c a l a b s t r a c t

a r t i c l e i n f o

Article history:Received 18 January 2013Accepted 12 March 2014Available online 27 March 2014

Keywords:Trichoderma harzianumTrichoderma virideSclerotinia sclerotiorumFluazinamProcimidoneAntagonist delivery

a b s t r a c t

Field trials were carried out to evaluate six treatments combining biological agents and chemical fungi-cides applied via chemigation against white mold (Sclerotinia sclerotiorum) on processing tomatoes. Theexperiment was performed in Goiânia, Brazil, with tomato hybrid Heinz 7155 in 2009 and 2010 in a fieldpreviously infested with S. sclerotiorum sclerotia. Treatments were arranged in a randomized completeblock design in a 2 � 3 factorial structure (with and without Trichoderma spp. 1.0 � 109 viable conidiamL�1 ha�1) � fluazinam (1.0 L ha�1), procimidone (1.5 L ha�1) and control, applied by drip irrigation.Treatments were applied three times 10 days apart, starting one month after transplanting. Each treat-ment consisted of plots with three 72-meter rows with four plants m�1 and 1.5 m spacing between rows,with three replications. Based on disease incidence evaluated weekly, the area under the disease progresscurve (AUDPC) was obtained. Yield and its components were evaluated in addition to fruit pH and �Brix.Results were subjected to ANOVA, Scott-Knott (5%), and regression analysis. Biocontrol using Trichodermaspp. via chemigation singly or in combination with synthetic fungicides fluazinam and procimidonereduced AUDPC and increased fruit yield up to 25 t ha�1. The best treatment for controlling white moldalso increased pulp yield around 1.0 and 7.0 t ha�1 in 2009 and 2010, respectively. The present workdemonstrated the advantages of white mold biological control in processing tomato crops, where dripirrigation favored Trichoderma spp. delivery close to the plants and to the inoculum source.

� 2014 Elsevier Inc. All rights reserved.

1. Introduction

Brazil ranks ninth in the world in tomato (Solanum lycopersicumL.) production. The majority of the crop is intended for industry,where transformation into value-added products renders this

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species the most economically important vegetable in the BrazilianCentral-West Region. Approximately 80% of the irrigated process-ing tomato crop is concentrated in the states of Minas Gerais andGoiás, which is the largest producer, averaging yields of 92 t ha�1.To attain such high yields, however, large amounts of inputs arenecessary, which elevate production costs (FAEG/GETEC, 2010).

Disease incidence figures among the many factors limiting to-mato production and fungicide utilization account for 17% of thetotal costs of producing a crop (FAEG/GETEC, 2010). Among the rel-evant pathogens causing damage to processing tomato crops, Scle-rotinia sclerotiorum (Lib.) De Bary stands out as a soil-borne fungusthat causes white mold disease. Under mild temperatures and highsoil moisture content, environmental conditions commonly foundin tomato crops, S. sclerotiorum sclerotia germinate in the infestedsoil, producing hyphae, which may directly infect hosts or, in mostcases, apothecia, which in turn release ascospores colonizingsenescent flowers (Jones et al., 1991). Affected shoots present acotton-like white mycelium, which is easily broken later on, andoriginate numerous black sclerotia, structures used for long-termsurvival in the soil, externally and/or within the stem.

Since the pathogen is polyphagous and considering the absenceof resistance in tomato hybrids, chemical control has been themost common method employed for disease management. Despiteaerial plant protection, fungicides rarely impact sclerotia in thesoil, leaving an ample source of initial inoculum for the next hostcrop. For this reason, infested areas depend annually on severalspraying operations to control disease and limit pathogen multipli-cation. In areas subjected to drip irrigation, it is possible thatdifficulties in reaching the pathogen structures in the soil may beovercome using fungicides via irrigation water, known aschemigation.

Specifically for white mold control, chemigation may presentthe advantage of reaching the soil surface and the first 5 cm soildepth, considered the maximum depth for carpogenic germinationof sclerotia (Abawi and Grogan, 1975), directly affecting sclerotia,mycelia, and apothecia. Chemigation is also economically recom-mended over conventional chemical applications because it re-duces hand labor and time in addition to preventing soilcompaction caused by tractors that may negatively affect cropyield (Pinto, 1994). However, its practicability and efficacy havenot yet been estimated for white mold in processing tomato crops.

Fungicide application via irrigation has been beneficial for dis-ease management in many pathosystems, including tomato earlyblight (Alternaria solani) (Tolentino Júnior et al., 2011), late blight(Phytophthora infestans), gray mold (Botrytis cinerea) in potatoes,Cercospora leaf spot (Cercospora beticola), and Rhizoctonia crownrot (Rhizoctonia solani) in beet roots, among others (Johnsonet al., 1986). However, reduction in disease severity and yield gainshave usually been obtained using synthetic fungicides by sprin-kling, as reported by Vieira et al. (2003), who worked with whitemold in dry beans. Biological control may be used as an alternativeto chemical utilization for white mold management because itreduces inoculum density in the soil and prevents selection ofresistant isolates, such as reported for S. sclerotiorum in canolaand alfalfa (Gossen and Rimmer, 2001) and in horticultural crops(Porter et al., 2002).

Besides its larger spectrum, biological control uses differentmethods of reaching the target, restricting the chances of selectingfungicide-resistant lines (Fravel, 2005). In 90% of the antagonistsused in plant disease biological control, there is participation of dif-ferent species of the genus Trichoderma, as reported by Benítezet al. (2004). Trichoderma species, necrotrophic mycoparasites eas-ily isolated from the soil, are efficient in controlling plant patho-gens, especially those with resistance structures such as sclerotiaor chlamidospores, because they act through several antagonismmechanisms such as antibiosis, antibiotic production, competition,

and induction of resistance in addition to growth promotion ofsome plants (Howell, 2003).

Many reports describe the efficiency of Trichoderma spp. to con-trol sclerotia from S. sclerotiorum. Clarkson et al. (2004) demon-strated that two isolates of Trichoderma viride and one of T.pseudokoningii degraded up to 80% of sclerotia from four isolatesof Sclerotium cepivorum in a silty clay soil and up to 60% of sclerotiain three other different soil types. Clarkson et al. (2002) also veri-fied up to 60% sclerotia degradation in soil using T. viride; they alsoobserved a significant reduction of white rot in garlic seedlings.

The suitability of application of antagonists and synthetic fungi-cides to control white mold has never been demonstrated before inareas under drip irrigation; therefore, the objective of this workwas to evaluate biological control of white mold using Trichodermaspp., associated or not with chemical control, in drip-irrigatedprocessing tomatoes via chemigation.

2. Materials and methods

Trials were conducted at an experimental farm (altitude 816 m16� 430 07.100 S and 49� 240 37.900 W) in Goiânia, (Goiás State, Brazil)from April to September 2009 and from April to August 2010, in amedium-texture soil. The hybrid used was Heinz 7155 (HeinzCompany), drip irrigated, transplanted on 2009 April 27 and2010 April 26. The irrigation equipment (Plastro Brasil) used hydroPC water emitters ND, model 16/45, adjusted for 1.35 L h�1 flowand spaced 0.40 m.

Experiments were initiated by transplanting 30-day-old seed-lings produced in substrate for vegetable production (Silva et al.,2003) and carried out according to technical crop recommenda-tions for the Brazilian Central-West Region. Soil tillage was per-formed with disc harrow and subsoiler; soil was amended with1300 kg ha�1 of lime and 1500 kg ha�1 fertilizer formula 04-30-16 + 0.5% boron. Seedlings were sprayed with thiametoxam(450 g ha�1) + metalaxyl + mancozeb (3 g L�1) before manualtransplanting; irrigation was started just before transplanting tofacilitate crop establishment.

The climate from May to September is dry with mild night tem-peratures averaging 22.2 �C and average precipitation of 22.3 mm(Freemeteo, 2009). These factors, in addition to moisture suppliedby irrigation, provide adequate conditions for white mold occur-rence. The experimental area was previously infested with patho-gen sclerotia obtained from soybean residue on grain cleaningunits, with a completely randomized block design. To facilitatetreatment applications via irrigation (chemigation), treatmentswere arranged in a 2 � 3 factorial combination of biological andchemical treatments, with three replications. Biological treatmentswere conducted with or without a Trichoderma spp. formulation(1 � 109 CFU mL�1, three applications of 1.0 L ha�1) and combinedor not with chemical treatments (fluazinam 1.0 L ha�1 or procimi-done 1.5 kg ha�1 used singly) and the control. The biological treat-ment was based on three distinct isolates of Trichoderma spp.,comprising two (T10 and T11) of Trichoderma harzianum and one(T9) of T. viride. Each plot consisted of three rows of 72 m longspaced 1.5 m, containing four plants m�1. Trichoderma spp. treat-ments consisted of three applications performed at 10-day inter-vals, with the first taking place 30 days after transplanting (dat).Their matching applications of fluazinam or procimidone weredone the following day after application of the antagonist.

Treatment assessment started when the first white mold symp-toms were observed. The procedure was carefully performed, sinceit is necessary to observe plant’s lower third portion covered by thecanopy as the crop develops. The rate of diseased plants was eval-uated weekly in the central plot rows by recording every plantwith symptoms. From these evaluations, the areas under the

R.A. de Aguiar et al. / Biological Control 74 (2014) 1–5 3

disease progress curve (AUDPC) were also estimated according toShaner and Finney (1977).

To calculate yield, commercially produced fruits were harvestedby hand in 10 replicates of 1.5 m2. Yield losses were estimated bythe weight differences between unripe and rotten fruits as well asby the differences of pH and �Brix between them. Thirty fruits perreplicate were gridded in a blender before measuring pH and �Brix,with a pH meter pH51 Milwaukee Waterproof (Milwaukee Instru-ments) and a portable digital refractometer Atago, model PR-1(Atago CO, Ltd.). To accelerate the fruit ripening period, irrigationwas stopped at 110 dat.

Pulp yield was obtained using formula P (t ha�1 pulp) = [(yieldin t ha�1) ⁄ 0.95 ⁄ �Brix]/28, according to Silva and Giordano(2000), where 0.95 corresponds to yield in percentage (5% is loss),and 28 corresponds to standard �Brix. For data analysis, the seasonof trial was considered the main plot, while biological and syn-thetic fungicides were labeled as factorial treatments for a split-plot analysis. The results obtained were submitted to ANOVA andto Scott-Knott (5%) tests with a joint analysis performed to com-pare the 2009 and 2010 results. Regression analyses were also per-formed to verify the differences in disease progress along the cropcycle, according to the different treatments. All analyses were per-formed by Sisvar software (Universidade Federal de Lavras, Lavras,Brazil).

3. Results and discussion

White mold was successfully established in both years of study,with a general difference in disease incidence between years andinteraction between application of biological control and year oftrial (p < 0.0001). Chemical treatments did not differ from the con-trol (p < 0.19) in both years and were considered inefficientwhether Trichoderma spp. was used or not. In the two years ofexperimentation, the disease progressed linearly in all treatments(Fig. 1), which were grouped according to the presence or absenceof Trichoderma spp. (p < 0.0001). All white mold progress curveswere well adjusted by simple linear models with R2 values rangingfrom 0.88 to 0.99. There was a lower incidence of disease wherebiological control was applied and, in contrast, the disease pro-gressed more rapidly and a greater AUDPC occurred in the absenceof the antagonist, as chemical fungicides did not affect white mold

Fig. 1. White mold (Sclerotinia sclerotiorum) progress on ‘Heinz 7155’ processing tomharzianum + T. viride at 1 � 109 CFU mL�1) associated or not with chemical fungicides (fltreatments, recorded in 2009 and 2010. Goiânia, GO, Brazil.

development. Therefore, the use of Trichoderma spp. via chemiga-tion singly reduced the disease progress curve in both years, whencompared with the control and fungicides used with and withoutthe antagonist (Fig. 1).

AUDPC on plots under application of Trichoderma spp. via che-migation ranged from 79% to 85% of that recorded on the controlplots in 2009 (p < 0.0003). AUDPC was not affected by fluazinamor procimidone applications without the antagonist and was simi-lar to the control (Fig. 2). The same behavior was observed in 2010,when Trichoderma reduced AUDPC by 80% (p < 0.0001); syntheticfungicides fluazinam and procimidone again did not differ fromthe control. The underperforming chemical fungicides singly tocontrol white mold could have been the result of the inefficacy ofthose products applied via chemigation on the miceliogenic germi-nation of sclerotia, despite Costa and Costa (2004) reporting thatthe use of fluazinam in the soil affected apothecia production. Fun-gicide degradation under field conditions probably occurred andcontributed to the poor performance of those treatments. Never-theless, chemical control did not harm the performance of biolog-ical control agents.

Several authors have reported the effect of white mold controlwith Trichoderma species, but in horticultural crops these studiesare concentrated mostly in seedlings or seeds, without coveringthe entire crop cycle and yield. Under greenhouse conditions,Abdullah et al. (2008) verified satisfactory control of S. sclerotiorumwhen using various sources of T. harzianum in tomato, pumpkin,and eggplant; achieving over 80% white mold control in thosethree crops. Trichoderma harzianum not only protected the plantsagainst infection but provided better seedling growth as well,especially in tomatoes. Lack of field results makes its efficacy ques-tionable, however (Budge and Whipps, 1991).

The present work, in turn, demonstrated the advantages of thebiological method to control white mold in processing tomatocrops. Positive results should also be credited to the applicationmethod used, which enabled distribution of the antagonist closeto the plants and to the inoculum source in an environment favor-able to Trichoderma spp. proliferation. Moreover, the chemigationmethod overcomes a relevant demand concerning delivery of bio-control agents, as pointed out by Glare et al. (2012) as a majorobstacle to successful biopesticide use.

Fungicide application through irrigation water is usuallyperformed by sprinkling, but in the case of diseases caused by

atoes, according to treatments with or without biological control (Trichodermauazinam 1.0 L ha�1 or procimidone 1.5 kg L ha�1 used singly) and control with no

Fig. 2. Percentage reduction of white mold (Sclerotinia sclerotiorum) area under the disease progress curve (AUPDC) after using Trichoderma harzianum + T. viride (1 � 109

CFU mL�1) via drip irrigation in three applications of 1 L ha�1, associated or not with fungicides fluazinam (1.0 L ha�1) and procimidone (1.5 kg L ha�1) and control treatments,on in processing tomato ‘Heinz 7155’ in 2009 and 2010, compared to control. Goiânia, GO, Brazil.

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soil-borne pathogens, applications by dripping might be more effi-cient. Browne et al. (2002) compared applications of methane so-dium by drip and sprinkle irrigation to control Sclerotium rolfsiiin potatoes and found that dripping applications were moreefficient, killing all sclerotia up to a 46 cm row depth. In this sense,the present work is the first to report on white mold control intomato crops in field conditions using Trichoderma spp. associatedor not with synthetic fungicides via chemigation.

Regardless of year, the association between the antagonist andthe pathogen was decisive to achieve marked reductions in AUDPC,as observed in the association of Trichoderma with fluazinam,respectively 85% and 80% lower than the control in 2009 and2010 (Fig. 2).

Although the density of S. sclerotiorum inoculum was not eval-uated in this work, it is known that synergisms between the ac-tions of biological and chemical fungicides may exist in whichthe effects of one treatment favor the other (Wilson et al., 2008).Nevertheless, it may be possible to develop further arrangementsbetween antagonists and chemical fungicides or improved strate-gies that will enhance white mold control and increase the deathrate of sclerotia in soil, with benefits to producing crops in areas in-fested by S. sclerotiorum.

The use of Trichoderma may also influence yield by promotingplant growth, and for this reason it may also be associated withhigher pulp yields (Table 1). Increases in yield of many speciesby Trichoderma have been reported by authors such as Görgenet al. (2009) in soybeans and Gravel et al. (2007) in tomatoes.

Table 1Effect of biological control with Trichoderma harzianum + T. viride (1 � 109 CFU mL�1), assocyield and its components of processing tomato hybrid Heinz 7155, in 2009 and 2010. Goi

Treatment Total yield (t ha�1) Yield loss (t ha�1)

2009 2010 2009 2010

Trichoderma 121.7 aA 151.1 aA 12.1NS A 2.9NS BTrichoderma + Fluazinam 120.6 aA 170.8 aA 13.4 A 2.8 BTrichoderma + Procimidone 126.5 aB 152.9 aA 12.1 A 3.0 BControl 104.8 bB 126.1 bA 10.5 A 3.2 BFluazinam 135.5 aB 122.4 bA 9.5 A 2.6 BProcimidone 100.1 bB 98.2 cA 11.9 A 4.8 BWithout Trichoderma 113.5NS 115.6 b 10.6 b 3.5NS

With Trichoderma 122.9 158.2 a 12.5 a 2.9Average 118.2 B 136.9 A 11.6 A 3.2 BCV (%) 18.22 47.03

Means followed by the same small letter in the columns and capital letters in the rowsNS Not significant at 5% probability.

In 2010, treatments with Trichoderma spp. singly or associatedwith synthetic fungicides were also verified as superior to othertreatments regarding yield (Table 1). Procimidone applied singlypresented the lowest pulp yield. As described above, the superior-ity of Trichoderma spp. was observed to be associated with fluazi-nam, followed by Trichoderma spp. singly, even thoughassociation with procimidone did not differ between them com-pared to the control and to fungicides applied singly. Besides pro-viding greater efficiency for disease control, Trichoderma spp. alsoincreased crop yield and consequently pulp yield, which, in turn,is a characteristic of much interest for the industry, sufficient tocompensate lower soluble solid contents (Table 1). The lowest sol-uble solid contents (�Brix) were observed when Trichoderma andprocimidone were used individually, whereas the remaining treat-ments did not differ among them. These differences in soluble sol-ids, however, are within standards accepted by the processingindustry and do not necessarily indicate undesired losses in indus-trial yield. There were no differences among treatments regardingpH and yield losses.

This is apparently the first report on white mold control withchemigation by dripping using biological control agents. The re-sults presented here endorse the success of Trichoderma utilizationto control soil-borne pathogens regardless of chemical inputs byproviding adequate conditions for the antagonist make use of itshigh reproductive capability and soil survival ability and to actagainst plant pathogenic fungi. The best results were obtainedvia chemigation when Trichoderma spp. was used singly for white

iated or not with fungicides fluazinam and procimidone, applied by drip irrigation onânia, GO, Brazil.

Pulp yield (t ha�1) �Brix pH

2009 2010 2009 2010 2009 2010

17.8 aA 26.3 bA 4.3 bB 5.1 bA 4.3NS B 6.9NS A18.3 aA 30.6 aA 4.4 aB 5.3 aA 4.3 B 6.8 A19.0 aB 25.9 bA 4.4 aB 5.0 bA 4.3 B 6.9 A16.0 bB 22.8 cA 4.5 aB 5.4 aA 4.4 B 6.9 A21.3 aB 22.4 cA 4.6 aB 5.4 aA 4.3 B 6.9 A14.4 bB 17.0 dA 4.2 bB 5.1 bA 4.4 B 6.9 A17.2NS 20.8 b 4.4NS 5.3 a 4.4 a 6.9NS

18.4 27.6 a 4.4 5.1 b 4.3 b 6.917.8 B 24.2 A 4.4 B 5.2 A 4.3 B 6.9 A19.82 5.45 1.02

are not different by the Scott-Knott test at 5% probability.

R.A. de Aguiar et al. / Biological Control 74 (2014) 1–5 5

mold control and for yield improvement, despite its associationwith synthetic fungicides fluazinam and procimidone, with subse-quent positive results in terms of fruit quality and pulp yields. Theassociation of methods of control may increase the efficiency ofwhite mold management with subsequent yield increases, demon-strating its suitability and efficacy to manage the disease. Knowingthat many other horticultural species are grown using drip irriga-tion and are also hosts of S. sclerotiorum, it is possible that theapplication of Trichoderma spp. in the soil, either under field orgreenhouse conditions, may reduce white mold severity in otherhosts, providing better yields.

4. Conclusions

White mold biological control with the use of Trichoderma spp.singly via chemigation reduced AUDPC and increased processingtomato yields in up to 25 t ha�1 on average. Biocontrol perfor-mance was not affected when associated with synthetic fungicidesfluazinam and procimidone. Treatments under biological controlincreased pulp yield from 1.0 to 7.0 t ha�1 in 2009 and 2010,respectively.

Acknowledgments

To CNPq and Capes for the financial support granted to the firstand to the third author (Grant 578604/2008-6). To Unilever S/A, fortheir kindly support on field operations and yield analysis.

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