Screening and breeding for resistance to leafminer (Liriomyza langei) in lettuce and spinach

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1 Sreening and reeding for resistane to leafminer (Liriomyza langei) in lettue and spinah Beiquan Mou and Edward J. Ryder Agriultural Researh Servie, U.S. Dept. of Agriulture, 1636 East Alisal Street, Salinas, CA 93905, USA. Contat: Tel (+1) Astrat: Leafminer (Liriomyza langei Frik) is a major pest that auses onsiderale damage to a wide variety of vegetale rops inluding lettue and spinah. Forty-eight lettue ultivars and introdution lines and 338 spinah aessions were sreened in an inset age for leafminer resistane. Signifiant geneti variation for leafminer stings per unit leaf area was oserved among genotypes tested. Resistant lines with fewer leafminer stings were found in ultivated lettue and spinah, Latua saligna, L. serriola, and L. virosa. The resistane in lettue was onfirmed in a field experiment. Crosses were made to omine leafminer resistane and superior hortiultural traits in risphead, green leaf, red leaf, romaine, and utterhead lettues. Leaf miner resistant plants were seleted in F 2 progenies of suh rosses, and were akrossed to restore hortiultural type. A phenotypi reurrent seletion method was used to inrease the level of leafminer resistane in spinah. Keywords: Latua sativa, L. serriola, L. saligna, L. virosa, Spinaia oleraea, S. tetrandra, S. turkestania, inset resistane Introdution Leafminers are major inset pests of many important agriultural rops inluding lettue and spinah (Parrella, 1987). Adult sting and larval mining of leaves redue photosyntheti apaity, render leaves unmarketale, and provide an entrane for disease organisms (University of California, 1992; LeStrange et al., 1999). The prinipal leafminer speies affeting vegetales inlude Liriomyza rassiae, L. sativae, L. trifolii, L. huidorensis, and L. langei. Sheffer and o-workers (2001) identified the leafminers in entral California as L. langei y using polymerase hain reation (PCR) amplifiation of mitohondrial DNA. Few studies on leafminer resistane in vegetales have een reported. Larval (L. trifolii) antiiosis was found in four interspeifi hyrids of Lyopersion pennellii, L. heesmanii, and L. hirsutum, and adult antiiosis and antixenosis for feeding was partially a result of the tomato plant s trihome exudates (Er et al., 1993). No resistane to leafminers (L. trifolii) has een oserved in ultivated elery, ut an aession from a wild speies, Apium prostratum, was found to e pratially immune (Trumle and Quiros, 1988). No feeding or oviposition was oserved in this speies. It has een used in a akross program in an attempt to develop leafminer-resistant elery lines (Quiros, 1993). In addition, an aession from another wild speies, A. nodiflorum, demonstrated sustantial inset toxiity; few mines were oserved and no larvae survived to the pupal stage (Trumle et al., 1990). In lettue, signifiant differenes among four romaine ultivars were found in the numer of pupae produed and in the total numers of stipples when exposed to leafminers (L. trifolii), ut these differenes resulted from differenes in adult survival. Female leafminers survived signifiantly longer and produed more pupae on the ultivar Tall Guzmaine than on three other ultivars (Nuessly and Nagata, 1994; Nagata et al., 1998). Lettue and spinah ultivars highly resistant to leafminers are not presently availale. The geneti variation of leafminer resistane in the germplasm of lettue and spinah, inluding the wild speies, has not een fully explored. The purposes of the present study CGN Euarpia Leafy Vegetales 2003 (eds. Th.J.L. van Hintum, A. Leeda, D. Pink, J.W. Shut) 43

2 were to evaluate differenes in leafminer resistane among lettue and spinah genotypes and to inorporate the resistane into elite ultivars. Material and methods Lettue The experiments were onduted at the Agriultural Researh Station of the U.S. Department of Agriulture, Salinas, California in Forty-eight genotypes from the lettue germplasm olletion maintained at the station were studied in an inset age. They inlude ultivated lettue (Latua sativa), and the wild speies L. serriola, L. saligna, and L. virosa from different geographi areas of the world. Three weeks after planting, 8 plants of eah genotype were transplanted individually into plasti pots (10 x 10 x 10-m) with soil. Plants were plaed in a field age (2 m high y 4 m wide y 8 m deep) made of polypropylene shade loth and were arranged in a randomized omplete lok with a single plant as the experimental unit and 8 repliations. Lettue leaves with leafminer mines were olleted from newly harvested fields around Salinas and leafminer larvae were allowed to emerge from the leaves and pupate. Pupae were olleted and put in plasti ontainers to allow the adult flies to emerge. Aout 2,800 flies were released in the field age. The leaf with the most leafminer stings on eah plant was ounted for the numer of stings per 20-m 2 leaf area with the aid of an optial glass inoular magnifier (OptiVisor, Donegan Optial Co., Lenexa, Kansas, USA) 7 days after the introdution of leafminer flies in the age. Fifty-four genotypes were also transplanted in a field on the station in summer. Eah plot onsisted of eight plants, with 30 m etween plants and 35 m etween rows on doule-row eds with 1-m enters. The experimental design was a randomized omplete lok with 8 repliations. The leaf with the most leafminer stings on eah plant was ounted for the numer of stings per 20-m 2 leaf area when plants reahed maturity. Data were analyzed statistially, using Analysis of Variane (ANOVA) with Mirosoft Exel (Offie 2001, Mirosoft Co., Redmond, Washington, USA). The per plant values were averaged and the analysis was onduted on the asis of plot means for the field experiment. Means of different lettue genotypes were ompared with t tests (Petersen, 1985). Spinah We sreened the spinah aessions from the USDA olletion (maintained at Iowa State University, Ames, Iowa, USA) for leafminer resistane at our researh station in 2001 in a preliminary study. The olletion inludes 332 aessions of ultivated spinah (Spinaia oleraea), 4 aessions of S. turkestania, and 2 aessions of S. tetrandra. Aout 16 seeds from eah aession were planted in a pot (10 x 10 x 10-m) with sand: soil 2: 1 in the greenhouse, and thinned to 10 plants per pot. Plants were moved into a field age (as desried aove) for sreening three weeks after planting. Lettue leaves with mines were olleted from fields near Salinas and larvae were allowed to pupate and eome adults. The adult (aout 3,500) flies were then released in the age to feed on the spinah plants. After 10 days, the numer of stings per unit area was ounted on the leaf with most leafminer stings on eah plant, using an optial glass inoular magnifier (OptiVisor), and the numer of plants with mines for eah aession was reorded. Results and disussion Signifiant differenes among lettue genotypes were found for the numer of stings per unit leaf area, and the nine genotypes with fewest stings from the age experiment are shown in 44

3 Fig. 1. Five L. saligna lines (PI , PI , PI , PI , and PI ), two L. serriola lines (PI and PI ), and a L. virosa line (PI ) had the least leafminer stings among genotypes tested. Among the ultivated lettues (L. sativa), PI showed fewer leafminer stings per unit leaf area than other lines. Ieerg registered the most sting damage among the genotypes tested. These results demonstrate the existene of large geneti variaility in leafminer resistane in different lettue speies. However, all genotypes had at least a few stings, indiating that none of the genotypes tested was immune to leafminers e Stings / 20 m d 50 0 a a a a a a PI PI PI PI PI PI PI PI PI Salinas 88 Margarita Ieerg Figure 1. Mean and standard errors of leafminer stings per 20-m 2 leaf area of seleted lettue genotypes tested in an inset age. Means with same letters are not signifiantly different at P = 0.05 level. The results from the age test were onfirmed in the field experiment (Fig. 2). Although the plants in the age experiment and in the field trial were at different ages and were sujeted to different environments and leafminer pressures, genotypes with fewer stings per unit leaf area in the inset age also had fewer stings in the field. These similarities in performane suggest that differenes in resistane were stale and a age test an e used to sreen lettue plants for leafminer resistane. We are attempting to inorporate the leafminer resistane into elite lettue ultivars in a reeding program. Resistant soures were rossed to ultivars of risphead, green leaf, red leaf, romaine, and utterhead type of lettues, and the progenies were seleted y the pedigree method. Sine some resistant soures are from wild speies, it may e neessary to akross to the adapted ultivars a few times to restore the hortiultural traits. The progenies of the rosses an also e used to study the inheritane of leafminer resistane. Crosses were also made among the resistant soures, and their progenies are eing seleted to elevate the level of resistane. The 20 spinah aessions with the least leafminer stings and the 4 lines with the most stipples are listed in Tale 1. There is muh geneti variation in mean leafminer stings per m 2 leaf area, ranging from 1.1 for PI to 13.4 for PI Perent of plants with 45

4 mines varied from 0 to 100 for different aessions. These results demonstrated that partial resistane to leafminer exists in spinah germplasm, whih may serve as the foundation for a reeding program to inrease the level of resistane and to transfer the resistane into elite spinah varieties. 250 f 200 f Stings / 20 m d e 50 0 a a a a PI PI PI Shining Star PI Lolla Rossa La Brillante Merlot Salinas Ieerg Margarita Da Ye Wo Sun Figure 2. Mean and standard errors of leafminer stings per 20-m 2 leaf area of seleted lettue genotypes tested in the field. Means with same letters are not signifiantly different at P = 0.05 level. Tale 1. Mean numer of stings per m 2 leaf area and perent of plants with mines for seleted spinah aessions from the USDA olletion at Iowa State University. Aession Mean stings % Plants / m 2 with mines PI PI PI PI PI PI PI PI PI PI PI PI Aession Mean stings % Plants / m 2 with mines PI PI PI PI PI NSL NSL PI PI PI PI PI We are using a phenotypi reurrent seletion method to inrease the level of leafminer resistane in spinah. Plants with fewer leafminer stings and/or mines were seleted from 46

5 resistant aessions and plaed in glass isolators on the station to open-pollinate with eah other. Seed harvested from these plants were planted in the field next season. Leafminerresistant plants were again seleted for another yle of hyridization. This yle will ontinue until a satisfatory level of resistane is reahed. The method has een suessfully used at the University of Arkansas to reed for white rust disease resistane in spinah (Goode et al., 1988). Starting with 27 yellow lover aphid-resistant plants seleted from a wide diversity of germplasm, Gorz and o-workers (1979) used phenotypi reurrent seletion to improve resistane to aphids in red lover. Through five yles of testing and seletion for yellow lover aphid resistane and three suh yles for pea aphid resistane, a syntheti variety ( N-2 ) was developed that had a high level of resistane to oth aphids. In summary, a wide range of geneti variation of leafminer resistane was found in different types and speies of lettue and spinah. Coupled with the staility of the trait, geneti improvement of oth rops for leafminer resistane seems feasile. We are urrently inorporating the resistane soures found in this study into elite ultivars in a reeding program. Aknowledgements We would like to thank JoAnn Tanaka, Yong-Biao Liu, William Chaney, and Franklin Dlott for their tehnial assistane. This researh was supported in part y a grant from the California Lettue Researh Board. Referenes Er, W.A., Lindquist, R.K., Flikinger, N.J. and Casey, M.L Resistane of seleted interspeifi Lyopersion hyrids to Liriomyza trifolii (Diptera:Agromyzidae). J. Eon. Entomol. 86: Goode, M.J., Morelok, T.E., and Bowers, J.L Fall Green spinah. HortSiene 23: 931. Gorz, H.J., Manglitz, G.R., and Haskins, F.A Seletion for yellow lover aphid and pea aphid resistane in red lover. Crop Siene 19: LeStrange, M., Koike, S., Valenia, J. and Chaney, W Spinah prodution in California. Univ. of Calif., Div. of Agr. and Natural Resoures, Pul. 7212, p Nagata, R.T., Wilkinson, L.M. and Nuessly, G.S Longevity, feundity, and leaf stippling of Liriomyza trifolii (Diptera: Agromyzidae) as affeted y lettue ultivar and supplemental feeding. J. Eon. Entomol. 91: Nuessly, G.S. and Nagata, R.T Differential proing response of Serpentine leafminer, Liriomyza trifolii (Burgess), on os lettue. J. Entomol. Si. 29: Parrella, M.P Biology of Liriomyza. Annu. Rev. Entomol. 32: Petersen, R. G Design and analysis of experiments. Marel Dekker, New York. Quiros, C.F Celery reeding program at the department of vegetale rops, University of California, Davis. HortSiene 28: 250. Sheffer, S.J., Wijesekara, A., Visser, D. and Hallett, R.H Polymerase hain reation-restrition fragment-length polymorphism method to distinguish Liriomyza huidorensis from L. langei (Diptera: Agromyzidae) applied to three reent leafminer invasions. J. Eon. Entomol. 94: Trumle, J.T. and Quiros, C.F Antixenoti and antiioti resistane in Apium speies to Liriomyza trifolii (Diptera: Agromyzidae). J. Eon. Entomol. 81: Trumle, J.T., Derks, W., Quiros, C.F. and Beier, R.C Host plant resistane and linear furanooumarin ontent of Apium aessions. J. Eon. Entomol. 83: University of California Integrated pest management for ole rops and lettue. Insets. Statewide Integrated Pest Management Projet, Div. of Agr. and Natur. Res., Pul. 3307, p