Rust disease continues to threaten California crop

Steven T. Koike u Richard F. Smith u R. Michael Davis u J. Joe Nunez u Ron E. Voss

In 1998, following the very wet El Niiio weather event, a devastating outbreak of rust disease severely damaged the garlic crop in Califor- nia. The disease also occurred in 1999 and 2000, indicating that rust may have developed into an annual problem. We identified the patho- gen as allii. In our study, it infected allium crops such as gar- lic, and chives, but not leek, elephant garlic or shallot. Currently registered materials did not control the disease, but tebuconazole (Folicur) and azoxystrobin (Quadris) provided good protection against garlic rust. Based on our work, a Section 18 emergency ex- emption for tebuconazole was approved by state pesticide regulators. We tested 34 UC and Possibly present in California for many industry garlic varieties and found years at low levels, garlic rust has recently become a significant crop that none were completely resistant disease. Rust causes distinctive orange to garlic rust. and black pustules to form on garlic .

roximately 84% of the com- A mercial garlic grown in the United States is produced in California. Of the total 37,100 acres grown here, about 60% to 65Y0 is grown for dehydrated products, while the rest is sold fresh (CASS 2000). California garlic can be grouped into early (planted early to late October) and late (planted late October to early December) crops that are har- California. During this year, El Nifio in many fields. An estimated 54% vested in mid-June to early July and late weather conditions, with record-high (20,015 acres) of California garlic acre- July, respectively. The majority of the rainfall and long periods of cool tem- age was affected. Average yields state’s garlic is grown in the inland San peratures, favored the development of dropped from 9.50 tons per acre to Joaquin Valley (Fresno and Kern coun- rust. The disease was widespread and 4.74 tons per acre, a 50% reduction in ties) and the coastal Salinas Valley severe in both growing regions. It was expected yields. The 1998 average gross (Monterey County). first observed in early spring (Febru- value per acre was $3,214, or 73% of nor- In 1998, a devastating outbreak of ary and March); later on (May and mal; bulb weights were 25% to 60% of rust disease affected garlic throughout June), 100% of the plants were infected normal. In addition, the quality of

CALIFORNIA AGRICULTURE, SEPTEMBER-OCTOBER 2001 35 that the pathogen currently causing rust in California is Puccinia allii and fully characterized California isolates for the first time (Jennings et al. 1990; Laundon and Waterston 1965). Infection on allium crops To determine the allium host range of the California garlic rust pathogen, we collected isolates from three loca- tions (Soledad, King City and Hollister) for use in inoculation experi- ments. For each isolate, we prepared suspensions and then sprayed them onto potted, 2-month-old plants of several cultivars of the following al- lium plants: garlic, onion, chives, leek, the crop was severely affected; soluble study was to characterize the rust elephant garlic and shallot. Immedi- solids were reduced 15%,and diseased pathogen and find means of managing ately after inoculating them, we placed bulbs lacked the protective dry outer the disease. the plants in a dew chamber for 48 skins. This caused the garlic to shatter hours, then grew them in a green- when it was harvested mechanically, Identifying the rust species house. We examined plants weekly for resulting in loose cloves that were left Because bulbous crops in the genus signs of rust disease. This inoculation in the fields. Growers were forced to Allium can be infected by several dif- experiment was repeated once. use hand labor to retrieve the bulbs, ferent rust pathogens, we collected Light to moderate rust developed and harvest costs were three to five samples of diseased garlic and onion on all inoculated garlic plants after 4 times higher than usual. from various locations in 1998 and to 5 weeks. All four onion cultivars The earliest symptom of rust dis- 1999 to identify the rust species. Doz- were susceptible to the P. allii isolates ease is small (less than one-eighth ens of samples of garlic were collected from garlic. However, disease severity inch), circular to elongate white flecks from Monterey, San Benito and Kern on onion was consistently lower than that occur on both sides of leaves. As counties. During the course of this on garlic. Chives were susceptible, the disease progresses, these small study, rust occurred sporadically and while shallots developed a very small spots expand, and the tissue cov- at low severity on onion; hence, only amount of rust. Leek and elephant gar ering the lesions ruptures. Masses of one sample was collected from onion lic failed to develop any rust. There the characteristic orange, powdery (Monterey County). For each sample, were no significant differences in dis- () of a rust fun- we microscopically examined the ease severity between the Soledad, gus then become visible as pustules. urediniospores and and King City and Hollister rust isolates, Severely infected leaves are almost en- compared them with previously pub- and results from the two experiments tirely covered with pustules, resulting lished descriptions of various garlic were similar (Koike et al. 2001). in extensive yellowing, wilting and rust fungi. drying of leaves. Teliospores, a second Rust samples from all locations and Evaluating fungicides type of spore formed by many rust years were similar. While the orange We conducted field evaluations of species, later develop on the same urediniospores can be used to identify fungicides to control rust in commercial leaves, resulting in black pustules. The rust species, the dark stage and experimental fields in 1998,1999 severity of the rust was so extreme in is usually more distinctive. Telio- and 2000, in Monterey, San Benito and 1998 that entire fields turned prema- spores on garlic leaves were two- Kern counties. For most trials, we used turely yellow and then brown. celled and borne on fragile, short experimental designs of completely ran- While rust on garlic was reported in stalks. The teliospores developed in- domized blocks with four replications. California as early as 1934 (Gardner side leaf pustules that were divided up Plots generally measured 20 feet long by 1940), the disease has never been eco- into cavities or compartments due to two beds wide and contained two garlic nomically important. The 1998 rust the presence of fused fungal structures seed rows per bed. We added a nonionic outbreak was an unprecedented and called paraphyses. Based on the char- surfactant to the sprays and applied damaging event for California agricul- acteristics of the urediniospores, telio- treatments with a carbon dioxide back- ture. The purpose of this multiyear spores and paraphyses, we confirmed pack sprayer.

36 CALIFORNIA AGRICULTURE, VOLUME 55, NUMBER 5 eight plants per plot and Kern counties), tebuconazole and derived a mean value for azoxystrobin provided the best control each plot. We determined of garlic rust disease because they re- plot yields by harvesting sulted in the lowest disease severity garlic from a 10-foot ratings and highest number of viable length in the middle two leaves. Most of the other materials rows of each plot. We gave rust control that was significantly trimmed harvested bulbs less effective (table 1).Likewise, according to standard tebuconazole and azoxystrobin treat- The 1998 outbreak of garlic rust, facilitated by the El Niiio weather svstern. caused entire fields to turn commercial practice and ments resulted in the highest yields brown. Yields ire sianificantlv reduced and mechanical weighed them. We deter- and percent soluble solid readings harvesting becornes-difficult.- mined percent soluble (Koike et al. 2001). solids (a measure of sug- In the Monterey County trials, re- The initial field trials (San Benito ars in the cloves) for 20 bulbs per plot sults were similar at both locations and Kern counties) tested a wide with a refractometer. (table 2). When we sprayed the plants range of fungicides and included: un- For the Kern County experiment, at 10-day intervals, tebuconazole and treated control, propiconazole (Tilt we assessed treatment effects on azoxystrobin treatments at either rate 3.6E), myclobutanil (Rally 40W), plants in a 3-foot length from the cen- gave excellent rust control (low dis- azoxystrobin (Quadris 2.0SSC), ter bed of each plot. Because of the se- ease severity, high number of viable chlorothalonil (Bravo 720, Bravo vere disease that occurred at this loca- leaves and high yields); such control Weather Stik 6F), iprodione (Rovral tion, only the youngest leaves could be was significantly better than untreated 4F), tebuconazole (Folicur 3.6F), evaluated. We randomly sampled 15 controls and all other treatments maneb (Maneb 75 DF, Manex), of the youngest leaves per plot and (Koike et al. 2001). metalaxyl/mancozeb (Ridomil MZ), rated them for percent leaf surface sulfur (Thiolux) and copper hydroxide covered with lesions. We harvested Resistant garlic cultivars (Kocide DF). Most fungicide treat- garlic bulbs from a 3-foot length in the To evaluate various garlic cultivars ments consisted of four applications center bed of each plot and trimmed and breeding lines for resistance to made at 7- to 10-day intervals. and weighed them. We then calculated rust, we planted a field trial in We designed two subsequent trials mean bulb weight. Monterey County in November 1999. in Monterey County, based on the re- In the initial trials (San Benito and The experimental design was a ran- sults generated by the initial trials. We focused on the two best-performing fungicides, tebuconazole and azoxy- strobin, sprayed at two rates and at 10- or 20-day intervals. Other treatments included untreated control, mancozeb (Manzate 200) and benzo-thiadiazole carbothioic acid (Actigard). For the San Benito and Monterey county experiments, we evaluated rust near crop maturity by assessing dis- ease on the third, fourth and fifth youngest leaves. We estimated disease severity using a scale in which 0 signi- fied that 0% of the leaf surface was covered with pustules, 1 meant 1%to 10% was covered, 2 meant 11%to 25%, 3 meant 26% to 50%, 4 meant 51% to 75%, and 5 meant 76% to 100%. As an

, additional measurement of rust im- pact, we counted the total number of viable leaves per plant (viable mean- ing that more than 75% of the leaf re- tained healthy tissue).We evaluated

CALIFORNIA AGRICULTURE, SEPTEMBER-OCTOBER 2001 37 domized, complete block with five practices. In the spring, we evaluated group ratings for the fifth leaf were 3.5 replications each of 34 garlic selections the plants for disease severity, as well (early), 3.3 (medium) and 3.4 (late). from university and industry sources. as maturity and vigor characteristics. Cultivars that possessed the greatest Each plot measured 10 feet long by There were significant differences tolerance to garlic rust, as measured one bed wide and contained two garlic among the cultivars in rust severity on by disease severity on the fourth and seed rows per bed. To provide inocu- the third, fourth and fifth leaves, as fifth leaves, included W6-8413, lum, dried garlic leaves that were in- well as the total number of viable W6-2308, W6-8418 and PI-540380. fected by rust and collected the previ- leaves per plant (table 3). Included in These garlic lines are not used com- ous fall were spread on the ground in the trial were 11 early, 11 medium- mercially at this time. Other cultivars February 2000 between the plant rows. and 12 late-season cultivars. These ma- possessed intermediate tolerance or We sprinklejrrigated the plots and turity groups did not differ in disease were highly susceptible. Significant grew them according to commercial resistance. For example, the mean differences existed among cultivars when the number of total viable leaves was considered, though no differences were found among maturity groups. However, the total number of leaves produced and the number of viable leaves at any given growth stage natu- rally varied among cultivars. Garlic rust in California Though garlic rust was reported in California in 1934 and again in 1940 (Gardner 1940; Yanvood and Gardner 1941), our multiyear project is the first to fully characterize garlic rust in the state and to document that P. allii caused the disease outbreak. Prior to 1998, this dis- ease occurred sporadically and errati- cally in California, and the industry did not experience economic damage. P. allii reportedly infects 20 differ- ent species in the allium group, in- cluding commercial crops such as chives, garlic, Japanese bunching or Welsh onion, leek, onion and shallot. In our inoculation experiments, our garlic rust isolates infected garlic, on- ion and chives, but were unable to cause disease in leek, elephant garlic or shallot. This inability to infect leek is notable because P. allii as it occurs in Europe is an extremely damaging leek pathogen. Distinct strains of the rust exist in different regions of the world. The source of initial inoculum for the current rust problem is unknown. The may always be present at ex- tremely low levels in California. Managing rust In the fungicide trials, tebucon- azole and azoxystrobin consistently provided the best control of rust and the highest garlic yields. Because of our efficacy data, California pesticide regulators" first "granted a Section 18

38 CALIFORNIA AGRICULTURE, VOLUME 55, NUMBER 5 S.T. Koike is Plant Pathology Farm Advi- sor and R.F. Smith is Vegetable and Weed Farm Advisor, UC Cooperative Extension (UCCE),Monterey and Santa Cruz coun- ties; R.M. Davis is Specialist, Depart- ment of Plant Pathology, UC Davis; J.J. Nunez is Farm Advisor, UCCE Kern County; and R.E. Voss is Specialist, De- partment of Vegetable Crops, UC Davis. This research was supported in part by the American Dehydrated Onion and Garlic Association. The authors thank the followingfor assistance with this project: Basic Vegetables, Christopher Ranch, Em- pire Research, Gilroy Foods, Rogers Certain fungicide treatments provided excellent control of rust in field trials Foods, Western Farm Service, Carol (tebuconazole-treated plants, right; untreated control, left). Adams, Mike Brautovich, Kevin Brink, Fred Crowe, Bob Ehn, Mike Hardoy, Kris emergency exemption for tebucon- reduced. At one King City site, 50 bulbs Headley, Kathy Kosta, Ed Kurtz, Mac azole use in garlic in 1999. (Federal harvested from tebuconazole plots Learned, Mike Mantelli, Steve Moss, Section 18 registrations allow grow- weighed 8.3 pounds and 50 bulbs har- Herb Phillips, Gail Pierleoni, Jerry Rava, ers to use an unregistered chemical vested from untreated plots weighed 4.3 Heather Scheck, Dora Tabancay, Tim for specific uses that are deemed pounds. However, in the interior San Tidwell, Rick Yraceburu, and technicians critical.) Our trials demonstrated Joaquin Valley, while many garlic fields Steve Bout y,Teo Gonzales, Luis how optimum control can be did not receive tebuconazole treatments Guerrero, David Haviland, Patrick achieved if these fungicides are de- in 1999 and 2000, rust failed to develop Headley, Diana Henderson, Devin Kile, ployed as protectants and applied to levels that might cause economic David Miltz and Kevin Simonin. We prior to significant rust develop- damage. This indicates that environ- thank Hartnell College of Salinas for the ment. Azoxystrobin is still used un- mental factors strongly influence the de- use of its East Campus facility. der an annually renewed Section 18 velopment of garlic rust in various re- registration. gions of California. References With the Section 18 registration for Variability in garlic rust severity as [CASS] California Agricultural Statistics tebuconazole, commercial garlic was seen in the cultivar trial is encourag- Service. 2000. County Agricultural Commis- sioners’ Data. Sacramento, CA. sufficiently protected during the 1999 ing; however, none of the varieties in www.nass.usda.gov/cdbul/agcom/ and 2000 seasons. However, to deter- this trial were completely resistant to indexcachtm. mine whether the garlic rust pathogen the disease. The varieties that pos- Gardner MW. 1940. Garlic rust in Califor- could cause significant damage in a year sessed the greatest tolerance to garlic nia. Plant Dis Rep 24:298-9. Jennings DM, Ford-Lloyd BV, Butler GM. in which wet and cool El Niiio weather rust are not commercially available in 1990. Morphological analysis of spores from conditions did not exist, in 1999 and the United States, for a variety of rea- different allium rust populations... Mycol Res 2000 we arranged for some growers in sons primarily related to growing fac- 94:83-93. Koike ST, Smith RF, Davis, et al. 2001. coastal California to omit tebuconazole tors Other than disease resistance‘ Be- Characterization and control of garlic rust in applications in large experimental plots cause the P. allii pathogen may have California. plant ~i~85:585-91.

~ ~~ Laundon GF. Waterston JM. 1965. in commercial fields. Interestingly, the become____~~ established in various 1Darts of severity of the garlic rust in these plots the state, effective fungicide treat- fuccinia allii. CMI Descriptions of Patho- genic Fungi and Bacteria No 52. Common- was comparable to those during the merits may be needed in Some regions wealth Mycological Institute, Engham, UK. 1998 El Niiio year, and garlic yields until resistant cultivars are found and Yarwood CE. Gardner MW. 1941. Garlic from these plots were likewise severely developed for market. rust infects onion. Plant Dis Rep 25:202.

CALIFORNIA AGRICULTURE, SEPTEMBER-OCTOBER 2001 39