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Disease Control and Pest Management Trichoderma harzianum: A Biocontrol Agent Effective Against Sclerotium rolfsii and Rhizoctonia solani Y. Elad, I. Chet, and J. Katan Research assistant, professor, and associate professor, respectively, Department of Plant Pathology and Microbiology, Faculty of Agriculture, The Hebrew University, Rehovot, Israel. This work was supported by a grant from Der Niedersachsische Minister fur Wissenschaft und Kunst, G6ttingen, W. Germany. The authors express their appreciation to Y. Henis, Y. Hadar, A. Grinstein, Hadas Harshemesh, and Rumia Govrin from the Hebrew University of Jerusalem; to 0. Zeydan from the Ministry of Agriculture for help and cooperation; and to A. Hiittermann from G1ittingen University for helpful suggestions. Accepted for publication 22 August 1979. ABSTRACT ELAD, Y., 1. CHET, and J. KATAN. 1980. Trichoderma harzianum: A biocontrol agent effective against Sclerotium rolfsii and Rhizocionia solani. Phytopathology 70:119-121. An isolate of Trichoderma harzianum capable of lysing mycelia of The wheat bran preparation of T. harzianum increased growth of bean Sclerotium rolfsii and Rhizoctonia solani was isolated from a soil naturally plants in a noninfested soil and it controlled S. rolfsii more efficiently than a infested with those pathogens. In culture, T. harzianum grew better than S. conidial suspension of the same antagonist. An uninoculated wheat bran rolfsii and invaded its mycelium under growth conditions adverse to the preparation increased disease incidence. In naturally infested soils, wheat pathogen; eg, high pentachloronitrobenzene concentrations, high pH bran preparations of T harzianum inoculum significantly decreased levels, or low temperatures. Under greenhouse conditions, incorporation of diseases caused by S. rolfsii or R. solani in three field experiments with the wheat-bran inoculum preparation of T harzianum in pathogen-infested beans, cotton, or tomatoes, and they significantly increased the yield of soil significantly reduced bean diseases caused by S. rolfsii, R. solani, or beans. both, but its biocontrol capacity was inversely correlated with temperature. Additional key words: integrated control, PCNB. Biological control of soilborne plant pathogens by the addition vertisol soil (30% sand, 17.5% silt, 52% clay, and 0.5% organic of antagonistic microorganisms to the soil is a potential matter; pH 7.95) either artificially or naturally infested with S. nonchemical means for plant disease control. The species of rolfsii. Trichoderma capable of hvperparasitizing pathogenic fungi, are Artificial infestation of soil was accomplished by adding S. rolfsii highly efficient antagonists (2,5). Weindling (12) reported the sclerotia from a 10-day-old dried SM-agar culture. Unless parasitism of Trichoderma lignorum (Tode) Harz on Sclerotium otherwise stated, final sclerotial concentration was 0.1 g (dry rolfsii Sacc. and Rhizoctonia solani Kiihn. This effect was also wt)/kg soil. shown, under field conditions, by Wells et al (13) using T. The antagonistic fungus was grown on a wheat bran: sawdust: harzianum grown on ryegrass. Similarly, Backman and Rodriguez- tap water mixture (3:1:4, v/v) autoclaved for 1 hr at 121 C, on 2 Kabana (1) controlled S. rolfsii in peanuts by using molasses- successive days. Autoclavable plastic bags, containing this enriched clay granules as a food base for T. harzianum. Recently, medium, were inoculated with T. harzianum and incubated in Hadar et al (6) found that T. harzianum directly attacked R. solani illuminated chambers for 14 days at 30 C. The T. harzianum mycelium. Wheat-bran-grown cultures of this antagonist added to preparation (65% moisture), at various concentrations, was mixed soil in greenhouse plantings reduced damping-off caused by R. with the soil before planting. Experiments with beans (Phaseolus solani in beans, tomatoes, and eggplants. The efficiency of vulgaris L. 'Brittle Wax') were carried out in plastic boxes (9 X 9 X Trichoderma was improved when integrated with pentachloro- 10 cm) each containing 500 g of soil. Greenhouse temperatures were nitrobenzene (PCNB) at sublethal doses (3). kept at 23-30 C and treatments in all experiments were replicated In the present study, an antagonistic strain of T. harzianum six times in randomized blocks. capable of controlling both S. rolfsii and R. solani was isolated Conidial suspension was prepared from an SM-agar-grown from pathogen-infested soil and its behavior was studied under culture of Trichoderma. Numbers of conidia (haemocytometer laboratory, greenhouse, and field conditions. count) were adjusted to those of the wheat-bran T. harzianum preparations. MATERIALS AND METHODS Field experiments. The wheat-bran preparation of T. harzianum inoculum was mixed with the soil to a depth of 7-10 cm with a Fungi were isolated from the soil on Martin's agar medium as rotary hoe. Three experiments were conducted, all in a naturally described (8). Their antagonistic activity towards pathogens was infested alluvial soil and in a six-replicate, randomized block design. determined according to the method of Dennis and Webster (4), In the first experiment (T. harzianum preparation concentration but using a solidified synthetic medium (SM) (10). Different pH 150 g [fr wt]/m ) beans (cultivar Tender green) were sown on 21 levels were obtained by the addition of 0.1 N NaOH or 0.1 N HC1 to September 1978, in three 12-m rows. In the second experiment (7T. the medium before sterilization. PCNB as Terraclor (75% a.i. Olin harzianum inoculum preparation concentration 30 g [fr wt]/ m of Chemicals, Little Rock, AR 72200) was added to SM agar before row), cotton (Gossypium hirsutum L. 'SJ- ') was sown 2 June 1978 sterilization. in a 5-m row in a commercial cotton field. The percentage of Greenhouse experiments. These were carried out in an alluvial diseased plants was recorded on 1 July 1978. In the third experiment (T harzianum preparation concentration 50 g [fr wt]/_M_2), tomatoes (Lycopersicon esculentun Mill 'VF 317') were 0031-979X/80/02011903/$03.00/0 sown 20 April 1978, in a 10 X 3.6-m plot and the percentage of 01980 The American Phytopathological Society diseased plants was recorded on 20 August 1978. Analysis of Vol. 70, No. 2,1980 119

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Page 1: Trichoderma harzianum: Biocontrol Agent Effective … 2. Effect of a wheat bran preparation of Trichoderma harzianum ¥7 I I 1 1 1 1 I.(TH) or uninoculated wheat bran (WB) (both added

Disease Control and Pest Management

Trichoderma harzianum: A Biocontrol Agent Effective AgainstSclerotium rolfsii and Rhizoctonia solani

Y. Elad, I. Chet, and J. Katan

Research assistant, professor, and associate professor, respectively, Department of Plant Pathology and Microbiology, Faculty ofAgriculture, The Hebrew University, Rehovot, Israel.

This work was supported by a grant from Der Niedersachsische Minister fur Wissenschaft und Kunst, G6ttingen, W. Germany.The authors express their appreciation to Y. Henis, Y. Hadar, A. Grinstein, Hadas Harshemesh, and Rumia Govrin from the Hebrew

University of Jerusalem; to 0. Zeydan from the Ministry of Agriculture for help and cooperation; and to A. Hiittermann from G1ittingenUniversity for helpful suggestions.

Accepted for publication 22 August 1979.

ABSTRACT

ELAD, Y., 1. CHET, and J. KATAN. 1980. Trichoderma harzianum: A biocontrol agent effective against Sclerotium rolfsii and Rhizocionia solani.Phytopathology 70:119-121.

An isolate of Trichoderma harzianum capable of lysing mycelia of The wheat bran preparation of T. harzianum increased growth of beanSclerotium rolfsii and Rhizoctonia solani was isolated from a soil naturally plants in a noninfested soil and it controlled S. rolfsii more efficiently than ainfested with those pathogens. In culture, T. harzianum grew better than S. conidial suspension of the same antagonist. An uninoculated wheat branrolfsii and invaded its mycelium under growth conditions adverse to the preparation increased disease incidence. In naturally infested soils, wheatpathogen; eg, high pentachloronitrobenzene concentrations, high pH bran preparations of T harzianum inoculum significantly decreasedlevels, or low temperatures. Under greenhouse conditions, incorporation of diseases caused by S. rolfsii or R. solani in three field experiments withthe wheat-bran inoculum preparation of T harzianum in pathogen-infested beans, cotton, or tomatoes, and they significantly increased the yield ofsoil significantly reduced bean diseases caused by S. rolfsii, R. solani, or beans.both, but its biocontrol capacity was inversely correlated with temperature.

Additional key words: integrated control, PCNB.

Biological control of soilborne plant pathogens by the addition vertisol soil (30% sand, 17.5% silt, 52% clay, and 0.5% organicof antagonistic microorganisms to the soil is a potential matter; pH 7.95) either artificially or naturally infested with S.nonchemical means for plant disease control. The species of rolfsii.Trichoderma capable of hvperparasitizing pathogenic fungi, are Artificial infestation of soil was accomplished by adding S. rolfsiihighly efficient antagonists (2,5). Weindling (12) reported the sclerotia from a 10-day-old dried SM-agar culture. Unlessparasitism of Trichoderma lignorum (Tode) Harz on Sclerotium otherwise stated, final sclerotial concentration was 0.1 g (dryrolfsii Sacc. and Rhizoctonia solani Kiihn. This effect was also wt)/kg soil.shown, under field conditions, by Wells et al (13) using T. The antagonistic fungus was grown on a wheat bran: sawdust:harzianum grown on ryegrass. Similarly, Backman and Rodriguez- tap water mixture (3:1:4, v/v) autoclaved for 1 hr at 121 C, on 2Kabana (1) controlled S. rolfsii in peanuts by using molasses- successive days. Autoclavable plastic bags, containing thisenriched clay granules as a food base for T. harzianum. Recently, medium, were inoculated with T. harzianum and incubated inHadar et al (6) found that T. harzianum directly attacked R. solani illuminated chambers for 14 days at 30 C. The T. harzianummycelium. Wheat-bran-grown cultures of this antagonist added to preparation (65% moisture), at various concentrations, was mixedsoil in greenhouse plantings reduced damping-off caused by R. with the soil before planting. Experiments with beans (Phaseolussolani in beans, tomatoes, and eggplants. The efficiency of vulgaris L. 'Brittle Wax') were carried out in plastic boxes (9 X 9 XTrichoderma was improved when integrated with pentachloro- 10 cm) each containing 500 g of soil. Greenhouse temperatures werenitrobenzene (PCNB) at sublethal doses (3). kept at 23-30 C and treatments in all experiments were replicated

In the present study, an antagonistic strain of T. harzianum six times in randomized blocks.capable of controlling both S. rolfsii and R. solani was isolated Conidial suspension was prepared from an SM-agar-grownfrom pathogen-infested soil and its behavior was studied under culture of Trichoderma. Numbers of conidia (haemocytometerlaboratory, greenhouse, and field conditions. count) were adjusted to those of the wheat-bran T. harzianum

preparations.MATERIALS AND METHODS Field experiments. The wheat-bran preparation of T. harzianum

inoculum was mixed with the soil to a depth of 7-10 cm with aFungi were isolated from the soil on Martin's agar medium as rotary hoe. Three experiments were conducted, all in a naturally

described (8). Their antagonistic activity towards pathogens was infested alluvial soil and in a six-replicate, randomized block design.determined according to the method of Dennis and Webster (4), In the first experiment (T. harzianum preparation concentrationbut using a solidified synthetic medium (SM) (10). Different pH 150 g [fr wt]/m ) beans (cultivar Tender green) were sown on 21levels were obtained by the addition of 0.1 N NaOH or 0.1 N HC1 to September 1978, in three 12-m rows. In the second experiment (7T.the medium before sterilization. PCNB as Terraclor (75% a.i. Olin harzianum inoculum preparation concentration 30 g [fr wt]/ m ofChemicals, Little Rock, AR 72200) was added to SM agar before row), cotton (Gossypium hirsutum L. 'SJ- ') was sown 2 June 1978sterilization. in a 5-m row in a commercial cotton field. The percentage of

Greenhouse experiments. These were carried out in an alluvial diseased plants was recorded on 1 July 1978. In the thirdexperiment (T harzianum preparation concentration 50 g [frwt]/_M_2), tomatoes (Lycopersicon esculentun Mill 'VF 317') were

0031-979X/80/02011903/$03.00/0 sown 20 April 1978, in a 10 X 3.6-m plot and the percentage of01980 The American Phytopathological Society diseased plants was recorded on 20 August 1978. Analysis of

Vol. 70, No. 2,1980 119

Page 2: Trichoderma harzianum: Biocontrol Agent Effective … 2. Effect of a wheat bran preparation of Trichoderma harzianum ¥7 I I 1 1 1 1 I.(TH) or uninoculated wheat bran (WB) (both added

variance was used for statistical analysis. The significance level of culture media. A disc of mycelium from the zone where S. rolfsiiP = 0.05 was used throughout. grew was therefore removed daily at various distances from the

meeting line of the two fungi, and transferred to SM agar in orderRESULTS to determine the presence of T harzianum. T. harzianum

progressed faster through the S. rolfsii mycelium at lowerAntagonistic activity. Fungi were isolated from a field soil temperatures (<27 C) and at high PCNB concentrations or high pH

naturally infested with both S. rolfsii and R. solani. Of the 150 levels which were more favorable for growth of T. harzianum.isolates tested, it was mainly the Trichoderma spp. that were Greenhouse studies. A wheat bran inoculum preparation of T.antagonistic to S. rolfsii, and usually this was expressed as a strong harzianum was added to S. rolfsii-inoculated soil sown with beans.lysis of the mycelium. A more efficient biological control of the pathogen was achieved at

One isolate, identified as T. harzianum Rifai aggr. (11) was used higher concentrations of the T harzianum preparation and lowerthroughout this study. Its spectrum of antagonism, tested in concentrations of the S. rolfsii inoculum in the soil (Fig. 1).culture, was found to include R. solani and Pythiumr In another experiment, T harzianum (3 g/kg) was added to soilaphanidermatum Edson (Fitz), but not Fusarium oxysporum f. sp. naturally infested with pathogens capable of inducing damping-off.vasinfesctum, Sclerotium bataticola Taub, Sclerotinia sclerotiorum Thereafter, beans were sown in this soil. The proportion of plants(Lib.) de Bary, Dematophora necatrix Hartig, Verticillium dahliae attacked by S. rolfsii in the control and the Trichoderma-treatedKleb., or a Phytophthora sp. This isolate of T. harzianum, soils were 47 and 8%, respectively; the corresponding data fortherefore, differs from the one used by Hadar et al (8), its plants attacked by R. solani were 42 and 18%, respectively. In bothantagonistic ability extends in addition to R. solani, P. cases, the differences between the treatments were statisticallyaphanidermatum, and S. rolfsii. significant. The efficiency of S. rolfsii control by T harzianum

The growth rate of T. harzianum in culture was greater than that declined with the increase in temperatures (Fig. 2).of S. rolfsii at high PCNB concentrations (10-30 Ag/g culture Biological control by T harzianum depended on the type ofmedium) or pH levels (7.0--8.5), or at low temperatures. inoculum and the time of soil inoculation (Table 1). The wheat bran

T. harzianum invaded S. rolfsii mycelium in encounters on agar preparation was much more efficient than the conidial suspension,especially in a delayed sowing. In contrast, autoclaved wheat bran,with or without autoclaved T. harzianum, increased the incidence

TABLE 1. Effect of type of Trichoderma harzianum inoculum and time of of disease, caused by S. rolfsiiin beans by 21-46%, and wheat bran,application on biological control of a bean disease caused by Sclerotium inoculated with a mixture of microorganisms from a natural soil,rolfsii did not affect disease incidence at all. When the Trichoderma

Diseased plants ( preparation was mixed with autoclaved wheat bran (1:3, w/w) itsefficiency remained unimpaired. When applied to noninfested soil,Inoculum type the wheat bran preparation of T harzianum significantly increased

Time of sowingy Not Conidial Wheat bran both the size and weight of bean plants (Table 2). Uninoculated(days) inoculated suspension preparation wheat bran, however, had no significant effect on the plants.

0 64 bz 45 c 20 e Field studies. Beans were sown in a soil naturally infested with S.15 40 c 28 d 19 e rolfsiiand R. solani. Throughout the growth period, dead seedlings30 80 a 43 c 4 f with typical symptoms of damping-off caused by either S. rolfsii or

'Number of days between T. harzianum application to soil and sowing. R. solani, were recorded. T harzianum significantly delayed thezNumbers followed by the same letter are not significantly different (P = progress and incidence of both diseases for 9 wk (Fig. 3). Eleven

0.05). There were six replications.

100

80 \_ 80 CONTROL

Q S. ROLFSII-• CONCN.

(mg / kg) u 60 - DISEASE60 - 300 z REDUCTION

• ,,, uJ 40 T.w) < T.< 40 -U

-.. HARZIANUM

255

20 -2 2000

5- 0 20

0 1 3 5 7 22 26 30 34T. HARZIANUM CONCN. (g/kg) SOIL TEMPERATURE (°C)

Fig. 1. Effect of inoculum concentrations of fungal antagonist Trichoderma Fig. 2. Effect of soil temperature on the incidence of bean disease caused byharzianum and pathogen Sclerotium rolfsii on the incidence of bean disease Sclerotium rolfsii and on its biological control by fungal antagonistcaused by S. rolfsii, 14 days after inoculation. Each number represents the Trichoderma harzianum. Plants were grown in pots placed in Wisconsin-mean of at least six replications. type controlled-temperature tanks, at six replications.

120 PHYTOPATHOLOGY

Page 3: Trichoderma harzianum: Biocontrol Agent Effective … 2. Effect of a wheat bran preparation of Trichoderma harzianum ¥7 I I 1 1 1 1 I.(TH) or uninoculated wheat bran (WB) (both added

TABLE 2. Effect of a wheat bran preparation of Trichoderma harzianum ¥7 I I 1 1 1 1 1 I.

(TH) or uninoculated wheat bran (WB) (both added to soil at 3 g [fr wt]/ kg)on the growth of bean seedlings, 25 days after sowing SIR

Preparation 20-

Parameter TH WB None

Plant height (cm) 28.1 Aa 23.9 B 22.8 BNo. of leaves per plant 4.0 A 3.1 B 2.7 B *

Wet weight (grams per plant) 2.8 A 2.1 AB 1.3 B 15 -Dry weight (grams per plant) 0.33 A 0.28 AB 0.23 B RSaNumbers followed by the same letter in each row are not significantly -

different (P= 0.05). There were six replications and 20 plants were sampled a.

in each replication. W SR. TH

Inweeks after sowing, plants were removed and disease index (on a R -scale of 0-4, in which 0 = healthy plants and 4 = completely girdled RS.THones) for R. solani was determined. Indices in the untreated and T 5harzianum-treated plots were 1. 12 and 0.87, respectively. The greenpod yield of the T. harzianum-treated plots increased 20% (to 5,570kg/ha) compared with the control.

A second field experiment'was carried out with cotton in a soilnaturally infested with R. solani. Twenty-nine days after planting, 12 16 20 24 28 32 36 40 44 48

the proportions of diseased plants in the untreated and T. DAYS AFTER PLANTINGharzianum-treated plots were 44 and 23%, respectively.

A third field experiment was carried out with tomatoes sown in Fig. 3. Effect of fungal antagonist Trichoderma harzianum (TH) added in asoi natuiraly finfestd wxperimenth was carfiOnehued out oan e twentwheat-bran inoculum preparation (1,500 kg[fr wt]/ ha) on the percentage of

soil naturally infested with S. rolfsii. One hundred and twenty-three bean plants diseased by Sclerotium rolfsii(SR) or Rhizoctonia solani(RS)days after planting, T harzianum had significantly (P = 0.05) in a field experiment. Data are the averages of six replications.reduced the percentage of diseased plants by 20%.

DISCUSSION control. The T. harzianum preparation used actually improvedplant growth (Table 2)--an additional advantage over pesticides

Trichoderma harzianum was found to be an effective biological which frequently cause some phytotoxicity.control agent for protecting a number of crop plants from damageinduced by S. rolfsiiand R. solani under both greenhouse and field LITERATURE CITEDconditions. The T. harzianum isolate used in this study wasobtained from a soil naturally infested with both S. rolfsii and R. 1. BACKMAN, P. A., and R. RODRIGUEZ-KABANA. 1975. A system

solani. It was capable of directly attacking and lysing both for the growth and delivery of biological control agents to the soil.

pathogens in culture. The ability of Trichoderma to attack different Phytopathology 65:819-821.

fungi was shown by Durrell (5). 2. BARNETT, H. L., and F. L. BINDER. 1973. The fungal host-parasiterelationship. Annu. Rev. Phytopathol. 11:273-292.

Growth rates of T harzianum and S. rolfsii as well as 3. CHET, I., Y. HADAR, Y. ELAD, J. KATAN, and Y. HENIS. 1979.antagonistic activity in culture were higher at high PCNB dosages Biological control of soilborne plant pathogens by Trichoderma

and pH levels or low temperatures. Similarly, biological control in harzianum. Pages 585-591 in: B Schippers and W. Gams, eds. Soil

soil was more efficient at low temperatures (Fig. 2), which Borne Plant Pathogens. Academic Press. London.correlated with the influence of temperature on the comparative 4. DENNIS, L., and J. WEBSTER. 1971. Antagonistic properties of

growth rates of T. harzianum and S. rolfsii. The improved species-groups of Trichoderma. III. Hyphal interaction. Trans. Br.

antagonism under conditions adverse for the pathogen emphasizes Mycol. Soc. 57:363-369.

the potential of integrating various means of control; eg, a 5. DURRELL, L. W. 1968. Hyphal invasion by Trichoderma viride.

combination of PCNB at sublethal doses and T. harzianum as Mycopathol. et Mycol. Appl. 35:138-144.6. HADAR, Y., I. CHET, and Y. HENIS. 1979. Biological control of

recently shown (3,6). Similarly, Munnecke et al (9) found that Rhizoctonia solani damping off with wheat bran culture of

Trichoderma is more tolerant than is Armillaria mellea to methyl Trichoderma harzianum. Phytopathology 69:64-68.bromide and carbon disulfide. 7. KELLEY, W. D. 1976. Evaluation of Trichoderma harzianum-

In greenhouse experiments, biological control of S. rolfsii (up to Impregnated clay granules as a biocontrol for Phytophthora

97% reduction of disease incidence in bean seedlings) and R. solani cinnamomi causing damping-off of pine seedlings. Phytopathology

(57% reduction of disease incidence in bean seedlings) was achieved 66:1023-1027.

in soil naturally and artifically infested with both pathogens. The 8. MARTIN, J. P. 1950. Use of acid, rose bengal and streptomycin in the

efficiency of the biological control correlated positively with the plate method for estimating soil fungi. Soil Sci. 69:215-232.

rate of T. harzianum wheat bran preparation applied to the soil and 9. MUNNECKE, D. E., M. J. KOLBEZEN, and W. D. WILBUR. 1973.Effect of methyl bromide or carbon disulfide on Armillaria and

negatively with the level of infestation by the pathogen. Trichoderma growing on agar medium and relations to survival ofAs also shown elsewhere (1,6,13), efficient biological control Armillaria in soil following fumigation. Phytopathology 63:1352-1357.

depends, among other things, on the presence of living cells of T. 10. OKON, Y., I. CHET, and Y. HENIS. 1973. Effect of lactose,

harzianum and the presence of a food base (Table 1). Uninoculated ethanol and cycloheximide on the translocation pattern of radioactivewheat bran even increased disease incidence; this was reported by compounds and of sclerotium formation in Sclerotium rolfsii. J. Gen.

Kelley (7) who used molasses as a food base for Phytophthora Microbiol. 74:251-258.

cinnamomi. 11. RIFAI, M. 1969. A revision of the genus Trichoderma. Mycol. Pap.

Under field conditions, T. harzianum significantly increased the 116. Commonw. Mycol. Inst., Assoc. Appl. Biologists, Kew, Surrey,

yield and decreased disease incidence, although less efficiently than England.unde grenhose ondtion. Iproed mthos fr aplyig T 12. WEINDLING, R. 1934. Studies on a lethal principle effective in the

under greenhouse conditions. Improved methods for applying t. parasitic action of Trichoderma lignorum on Rhizoctonia solani and

harzianum in the field may produce better results. However, in this other soil fungi. Phytopathology 24:1153-1179.study the field results obtained from three different locations, with 13. WELLS, H. D., D. K. BELL, and C. A. JAWORSKI. 1972. Efficacy of

three plant species and two pathogens (which frequently coexist), Trichoderma harzianum as a biological control for Sclerotium rolfsii.point to the high potential and reproducibility of biological Phytopathology 62:442-447.

Vol. 70, No. 2, 1980 121