TRANSMISSION OF CELERY-YELLOW-SPOT VIRUS BY THE HONEYS'UCKLE APHID, RHOPALOSIPHU;M CONII (DVD.) JULIUS H. FREITAG AND HENRY H. P.
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2 TRANSMISSION OF CELERY-YELLOW-SPOT VIRUS BY THE HONEYS'UCKLE APHID, RHOPALOSIPHU;M CONII (DVD.) JULIUS H. FREITAG AND HENRY H. P. SEVERIN
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4 TRANSMISSION OF CELERY-YELLO'V-SPOT VIRUS BY THE HONEYSUCKLE APHID, RHOPALOSIPHUMCONII (DVD.)l JULIUS H. FREITAG AND HENRY H. P. SE~RIN3 CELERY YELLOW SPOT was first bserved during the summer f 934 in the Santa Clara Valley near Milpitas and has since been fund in the celery fields near San Jse, Hllister, Salinas, and Sacrament. Symptms have been briefly described (Severin and Freitag, 938),' and results f insect-transmissin experiments (Freitag and Severin, 939) presented, in previus papers. The disease causes n appreciable lss t celery grwers, althugh 40 per cent f the plants were infected in sme fields. Because the plants are nly slightly stunted and because the sptted uter leaves are nrmally discarded in the harvesting f celery fr the 'market, the disease is f small ecnmic imprtance. In 935 an investigatin was undertaken t study the symptms and hst range f celery-yellw-spt virus. Attempts were made t transmit the virus by means f different aphid species and by mechanical inculatins. Virus transmissin by single specimens f winged and mature wingless aphids and retentin by the aphid vectr were the subject f experiment. SYMPTOMS Usually the first symptm nticed in the greenhuse, abut 4 days after inculatin f celery plants by the hneysuckle aphid, Rhpalsiphum cnii (Dvd.) [R. melliferum (Httes)], was the irregular pale green areas r spts and stripes, which rapidly became yellw (plate, B). This yellw sptting is the mst characteristic sign f the disease. The spts and stripes are mstly alng the veins (plate, Cj plate, A), but are als scattered irregularly ver the leaflets (plate, E j plate, E). The yellw areas are irregular in shape and variable in size (plate, D] plate, B, C). The spts alng the veins are ften elngate (plate, C j plate, E) and smetimes ccur at the basal prtin f veinlets, where the latter jin the main and lateral veins (plate, A). Sme f the yellw spts are rund and frm small circular chlrtic areas (plate, D). The chlrtic spts may be numerus (plate, D) and may result in a. general yellwing f the leaflet (plate, E). In advanced stages f the disease the small chlrtic spts may calesce, frming enlarged spts (plate, D j plate, B, D) and mttled areas (plate, F). Their yellw clr gradually fades and may becme white as the leaf matures. 'I'he petiles f naturally infected celery plants develp circular white sptting (fig. ). When the epidermis is remved frm these areas, brwn specks may be seen alng the veins f the celery stalk (plate, F). Received fr publicatin March 7, 944. Assistant Prfessr f Entmlgy- and Assistant Entmlgist in the Experiment Statin. 3 Entmlgist in the Experiment Statin. 4:See "Literature Cited" fr cmplete data n citatins, referred t in the text by authr and date f publicatin. [ 375 ]
5 376 Hagardw [Vl. 6, N.8 Fig. I.-Petiles frm celery plants: left, petile frm a healthy plant; right, three petiles frm celery naturally infected with yellw spt, shwing white sptting. (Milpitas, Octber 7, 935.) HOST RANGE Natural Infectin.-Celery (Apium gravelens L. var. dulce DC.), pisn hemlck (Onium macula tum L.), and parsnip (Pastinaca sativa L.) are the nly plants that were fund t be naturally infected with celery yellw spt. Virus was recvered, by the hneysuckle aphid, frm naturally infected parsnip and pisn hemlck. Althugh the virus has nt yet been recvered frm celery either by aphids r by mechanical inculatin (see p. 380), the symptms n naturally infected celery are identical with thse n celery experimentally infected by the hneysuckle aphid frm infected pisn hemlck and parsnip.
6 March,945] Freitag-Severin: Transmissin f Celery-Yellw-Spt Virus 377 Naturally infected parsnip plants, fund at Stcktn, shwed a mild mttling f the leaves, whereas pisn hemlck prved t be a symptmless carrier. Experimental Infectin f Celery.-Experiments were cnducted t infect celery with yellw spt. Flwer clusters frm pisn-hemlck plants heavily infested with hneysuckle aphids were cllected frm several lcalities. Nne f the plants frm which the aphids were taken manifested yellw-spt symptms. Pisn hemlck that shwed mttling, sptting, chlrtic rings, and line patterns was always demnstrated t be infected with the pisnhemlck-ringspt virus (Freitag and Severin, 945). Plants, hwever, rarely suffered frm a virus cmplex f ringspt and yellw spt. The pisn-hemlck flwer clusters infested with aphids were cut s that each piece had 50 t 00 aphids n it. Frm 5 t 0 pieces were cut frm a single infested plant; then each piece was placed in a cage with a healthy celery plant. As the flwer clusters wilted and dried, the aphids wuld 'mve t the healthy celery leaves. There they fed fr t 5 days, after which they were fumigated with Nic-fume tbacc paper. Samples were taken near Alvarad, Sacrament, San Pabl, and San Jse frm 5 pisn-hemlck plants which prved t be naturally infected. The results btained were as fllws: Lcality and pisnhemlck plant n. San Pabl N. 0 N. 0 N.3 0 San Jse N.4 0 Sacrament N.5 5 N.6 5 N.7 5 N.8 5 N.9 5 Alvarad N.0 0 N. 0 N. 0 N.3 0 N. 4 0 N. 5 0 N.6 0 N.7 0 N.8 0 N.9 0 N.0 0 N. 0 N. 5 N.3 5 N.4 5 N.5 5 Celery plants inculated Celery plants infected Ttals' 05 6
7 378 Hilgardia [Vl. 6, N.8 These data shw that the aphids infected 6 f 05 celery plants, r 6.5 per cent. Transmissin by aphids was erratic; the number f plants infected ranged frm 0 t 00 per cent. This variatin may have resulted frm differences in virus cncentratin in the infected plants; r perhaps the aphids varied greatly in their ability t acquire and transmit the virus. Experimental. Infectin f Pisn Hemlck and Celery.-Since pisn hemlck is a symptmless carrier f the yellw-spt virus, celery plants were inculated in these experiments t serve as indicatrs f the presence f the virus. The hneysuckle aphids used fr this purpse came frm the same surce as thse used t infect the pisn hemlck. They were cllected n TABLE EXPER,IMENTAL INFECTION OF CELERY AND POISON HEMLOCK WITH CELERY-YELLOW-SPOT VIRUS BY HONEYSUCKLE APHIDS FRO~I NATURAL,LY INFECTEn POISON HEMLOCK Naturally infected pisn hemlck n. Celery plants "Pisn-hemlck plants Inculated Infected Inculated Infected* Ttal Percentage S.. fs.9 As determined by recvery f the virus by aphids and transfer t healthy celery plants. naturally infected pisn hemlck, and thse frm each plant were transferred t frm t 0 healthy pisn hemlck and 5 t 0 healthy celery plants. Abut a mnth after the celery had develped symptms, nninfective hneysuckle aphids were taken t the inculated pisn hemlck, where they were allwed t feed fr abut a week. Then they were mved t 5 healthy celery plants. Infectin f ne r mre celery plants was cnsidered prf that the pisn hemlck was infected, althugh the latter displayed n symptms. As table shws, the aphids were apparently able t infect celery mre readily than pisn hemlck. In each f trials cnducted, they infected t 7 celery plants, whereas ther aphids frm the same surces infected pisn hemlck in nly 6 f trials. A ttal f 37 f 85, r 43.5 per cent, f the celery plants and 4 f 54, r 5.9 per cent, f the pisn-hemlck plants became infected. I
8 March,945] Freitag-Severin: Transmissin f Celery-Yellw-Spt Virus 379 I~ECOVERY OF VIRUS FROM POISON HEMLOCK AFTER INOCULATION Experiments were cnducted t test pisn hemlck as a surce f virus. Inculatins were made in the usual way by transferring hneysuckle aphids Pisn-hemlck plant n. and da te f recvery test N. (inculated June 8) ; recvery f virus n: July 8. August 6. N. (inculated June 8) ; recvery f virus n: July 5 ~. August 7. Octber 0. Nvember 5. December 9. December. January 0. N.3 (inculated June 8) ; recvery f virus n: July 8. August 7. N.4 (inculated June 8) ; recvery f virus n: July 5. August 9. Octber December 9. December. N.5 (inculated June 8) ; recvery f virus n: July 5. August 7. N.6 (inculated June 8) ; recvery f virus n: July 5. August 7. N.7 (inculated June 8) ; recvery f virus n: July 5. August 7. N.8 (inculated September 4) ; recvery f virus n: January 4. February. March. April 3. N.9 (inculated August 8) ; recvery f virus n: September. September. Octber 6. N. 0 (inculated August 8) ; recvery f virus n: September. September. Octber 6. Celery plants infected, 0 f 5 inculated Ttal 3 Percentage 9. 5 Out f 0 celery plants inculated
9 380 Hilgardia [Vl. 6, N.8 frm naturally infected plants t healthy plants grwn frm seeds. These plants, as in previus experiments, failed t develp symptms. The first recvery tests were cnducted 4 days after the inculatin. Additinal recvery tests were made at irregular intervals. The results were as shwn n the preceding page. The data indicate that experimentally infected pisn hemlck is a pr surce f the virus. In 6 f 0 tests the aphids recvered the virus frm pisn hemlck the first mnth after inculatin, but failed t recver it thereafter. The aphids infected nly 3 f 65 celery plants, r 9.4 per cent. The lw percentage f transmissin btained by using experimentally infected pisn hemlck as a surce f virus made it difficult t cnduct many experiments. Why the aphids are unable t recver the virus readily frm experimentally infected pisn hemlck, whereas they were far mre successful in acquiring it frm naturally infected plants, is nt understd. FAILURE TO RECOVER VIRUS FROM CELERY Nine species f aphids (listed in table ) were reared n celery that shwed symptms f yellw spt. The aphids frm each infected plant were transferred in lts f 5 t each f 5 healthy celery plants. After this transfer, the juice f the infected plants was extracted by crushing the leaves in a mrtar with a pestle and pressing the juice thrugh cheeseclth by hand. Five healthy celery plants were then inculated by dusting the leaves with pwdered carbrundum and lightly rubbing the leaves with absrbent cttn that had been dipped in the extracted juice accrding t the methd described by Rawlins and Tmpkins (936). -The transmissin results with aphids and with mechanical inculatins are summarized in table. As this experiment cnclusively demnstrates, the aphids were nt able t recver virus frm 66 infected celery plants and cnsequently did nt infect any f the 330 celery plants t which they were transferred. Mechanical inculatin f 85 celery plants with the juice frm plants used as a surce f virus fr the aphid tests resulted in n infectins. TRANSMISSION OF VIRUS BY SINGLE APHIDS A cmparisn was made f the transmissin f yellw-spt virus by single specimens f winged and mature wingless hneysuckle aphids reared n naturally infected pisn hemlck. The aphids were cllected at Alvarad n pisn-hemlck plants f this kind. Each was transferred singly, by means f a camel's-hair brush, t healthy celery and fed fr day. The winged hneysuckle aphids prved t be mre efficient vectrs than the mature wingless nes. The frmer infected 0 ut f 50 celery plants; the latter nly 6 ut f 50. RETENTION OF VIRUS BY APHIDS Sme plant viruses transmitted by aphids are retained, whereas thers are lst sn after the aphids leave the infected plants. Experiments were cnducted t determine hw lng the hneysuckle aphids retained the yellwspt virus. The aphids were cllected n naturally infected pisn hemlck and transferred with a camel's-hair brush t successive healthy celery plants
10 March, 945] Freitag-Severin: Transmissin. f Celery-Yellw-Spt Virus 38 daily fr 6 t 3 days. Five experiments were perfrmed; and in each, frm 0 t 5 lts f 5 aphids were transferred daily t healthy celery, a ttal f 85 lts being used. Every day, when the aphids were thus transferred, several wuld die, s that after 0 days nly a few remained alive. TABLE ATTEMPTS TO TRANSMIT CELE,RY-YELLOW-SPOT VIRUS FROM CELERY TO CELERY BY APHIDS AND BY MECHANICAL INOCULATION Aphid Number f Aphid transmissin Mechanical inculatin infected celery plants Plants Plants Plants Plants tested inculated infected inculated infected Celery aphid, Aphis apigravelens Essig Celery aphid, Aphis apii The Rusty-banded aphid, Aphis Ierruinea-etriata Essig Cttn r meln aphid, Aphis gssypii Glver Erigern rt aphid, Aphis middletnii Ths Yellw willw aphid, Cavariella capreae (Fab.) Lily aphid, Myzus circumfiexu«(buck.) Fxglve aphid, Myzus cnvlvuli (Kalt.) Hneysuckle aphid, Rhpalsiphum cnii (Dvd.) Ttal TABLE 3 RETENTION OF CELERY-YELLOW-SPOT VIRUS BY LOTS OF 5 NATURALLY INFECTED HONEYSUCKLE APHIDS TRANSFERRED TO SUCCESSIVE HEALTHY CELERY PLANTS DAILY Experiment Experiment Experiment 3 Experiment 4 Experiment 5 Number f days after transfer f aphids frm infected plants Plants Plants Plants Plants Plants incu- Plants incu- Plants incu- Plants incu- Plants incu- Plants lated infected lated infected lated infected lated infected lated infected I " " * 0 Cntinued fr 3 days; but n infectins resulted after twelfth day. The results, shwn in table 3, indicate that the aphids retain the virus fr sme time. Apparently, therefre, the mde f transmissin differs frm that bserved fr mst aphid-transmitted viruses; 'mst aphid vectrs fail t transmit after the first day. The hneysuckle aphid retained the virus 5 t days
11 38 Hi~gardia [Vl. 6, N.8 after being remved frm infected pisn hemlck. The pssibility f aphids' reacquiring virus frm plants n which they were allwed t feed fr 4 hurs was eliminated, since all tests s far cnducted with aphids r with mechanical inculatins have failed t recver the virus frm infected celery. DISCUSSION Judging frm the results presented, hneysuckle aphids that have acquired the yellw-spt virus may retain it fr days. Sn after being remved frm an infected plant, mst aphids lse the capacity t prduce infectin. Several species f them, hwever, retain viruses fr 3 t 9 days. Smith (99,93) and Elze (97) have shwn that the green peacli aphid, Myzus persicae (Sulzer), the vectr f ptat-leafrll virus, can feed n immune plants such as cabbage and spinach fr 7 t 0 days and then infect healthy ptates. Bennett (97) has demnstrated that the raspberry-leaf-curl virus remains active fr weeks in the bdy f the aphid vectr, Aphis rubiphila, Patch. Osbrn (935, 938) fund that the pea-msaic virus was retained by the pea aphid, Macrsiphum nbrachis (B. d. F.) (M. pisi Kalt.), fr 9 days and by the ptat aphid, M. slaniflii (Ashm.) fr days. In the experiment f Rland (939) and Watsn (940) the green peach aphid when transmitting the sugar-beet-yellws virus prduced infectin n successive healthy plants fr a perid f 3 days. Why the aphids were nt able t acquire virus frm celery plants infected with yellw spt is difficult t explain. A pssible reasn might be lw virus cncentratin in the celery plant, r plant-tissue relatins that make it impssible fr aphids t acquire the virus. Hggan (99, 93, 934) fund that aphids did nt transmit the tbacc-msaic virus frm ne tbacc plant t anther, but culd acquire it regularly frm tmat and transmit it t tbacc. The results btained with the yellw-spt virus indicate a smewhat similar situatin. Recvery f virus frm sme hst plants infected with aster yellws has als prved difficult. Severin and Hassis (934) were able t infect ptat plants with aster-yellws virus by means f the aster leafhpper, Macrsteles divisus (UhI.), but nt t recver the virus subsequently frm thse plants. Mre recently, hwever, Severin (940) reprts that aster-yellws virus was recvered frm naturally infected ptat plants by means f the lng-winged aster leafhpper. SUMl\iARY Celery (Apium gravelens L. var. dulce DC.), pisn hemlck (Cnium maculatum L.), and parsnip (Pastinaca sativa, L.) were fund t be naturally infected with the celery-yellw-spt virus. The symptms n celery are irregular areas r spts; r stripes at first pale green, later yellw, and finally white. These spts ccur alng the veins and scattered ver the leaflets. The virus was recvered frm 5 naturally infected pisn-hemlck plants, which were symptmless carriers f the disease, and was transmitted by means f the hneysuckle aphid, Rhpa.lsiphum cnii (Dvd.), t 6 f 05 celery plants, r 6.5 per cent. Attempts t transmit the virus frm infected pisnhemlck plants t healthy plants by mechanical inculatin were unsuccessful. Attempts t transmit the virus frm celery t celery by means f 9 species
12 March, 945] Freitag-Severin: Transmissin f CeZery-YeZZw-Spt Virus 383 f aphids and by mechanical inculatin failed t prduce infectin in 65 celery plants tested. Hneysuckle aphids cllected n naturally infected pisn hemlck transmitted the disease t 37 f 85 celery plants, r 43.5 per cent; and 4 f 54 pisn-hemlck plants, r 5.9 per cent. Experimentally infected pisn hemlck prved t be a pr surce f virus fr aphid-transmissin experiments, especially if recvery was attempted after the plant had been diseased fr mre than a mnth. Single specimens f winged hneysuckle aphids prved t be mre efficient vectrs than mature wingless aphids. Hneysuckle aphids cllected n naturally infected pisn-hemlck plants and transferred t successive healthy celery plants daily were able t infect plants fr a perid f days.
13 384 Hilgardia [Vl. 6, N.8 LITERATURE CITED BENNETT, C. W. 97. Virus diseases f raspberries. Michigan Agr. Exp. Sta. Tech. Bul. 80 :-38. ELZE, D. L. 97. De verspreiding van virusziekten van de aardappel (Blaaun» tubersum L.) dr insecten. [Wageningen] Landbushgesch. (Meded.) 3:-90. FREITAG, J. H., and H. H. P. SEVERIN Additinal celery virses. (Abstract.) Phytpathlgy 9 : Pisn-hemlck-ringspt virus and its transmissin by aphids t celery. Hilgardia 6(8) : HOGGAN, IsMEA. 99. The peach aphid, Myzus persicae (Sulzer), as an agent in virus transmissin. Phytpathlgy 9: Further studies n aphid transmissin f plant viruses. Phytpathlgy : Transmissibility by aphids f the tbacc msaic virus frm different hsts. Jur. Agr. Research 49 :35-4. OSBORN, H. T Incubatin perid f pea msaic in the aphid Macrsiphum pisi. Phytpathlgy 35: Incubatin perid f pea virus in the aphid Macrsiphum slaniflii. Phytpathlgy 38 : RAWLINS, T. E., and C. M. TOMPKINS Studies n the effects f carbrundum as an abrasive in plant virus inculatins. Phytpathlgy 6 : ROLAND, G nderzekingen verricht in 937 ver de vergelingsziekte en enkele minerale gebreken bij biet en de spinazie. 'I'ijdschr, ver Plantenziekten 45() :-. SEVERIN, H. H. P Ptat naturally infected with Califrnia aster yellws. Phytpathlgy 30 : SEVERIN, H. H. P., and J. H. FREITAG Western celery msaic. Hilgardia (9) : SEVERIN, H. H. P., and F. A. HASSIS Transmissin f Califrnia aster yellws t ptat by Cicadula divisa. Hilgardia 8 (0) : SMITH, K. M. 99. Studies n ptat virus diseases. V. Insect transmissin f ptat leafrll. Ann. Appl, BiI. 6: Studies n ptat virus diseases. IX. Sme further experiments n insect transmissin f ptat leafrll. Ann. Appl. BiI. 8:4-57. WATSON, M. A Studiesn the transmissin f sugar-beet-yellws virus by the aphis, Myzus persicae (Sulz.). Ry. Sc. Lndn Prc., Ser. B. 8:535-5.
14 HILGARDIA. VOL. 6. NO.8 [ F R E I T A G-S EV E R I N ] PLATE c D -- E... F P lat e.-a. Health y celery leaflet. B t P, symptms f celery yellw sp t n lea flets f celery plants experi mentally infected by the hnevsu ckle aphid, Rhpal.viph.lrn cnii ( Dvd. ) : B, early stage with nl y a few chlrtic spts between the veins a nd a few 'I't narrw chlrtic stripes alng th e veins ; C, elue nted yell w st ri pes alng the veins a nd chlrtic sptting ; D, enlarged chlr tic spts, the result f the cal escing f smaller nes; E, numerus chlrtic spts wit h gene ral yellw ing f basal prtin f lea flets; P, calescing f chlrt ic spts t frm enla rged yellw area s.
15 H [FREITAG-SEVERIN] PLATE D E F Plat e.- Sym pt ms f ce ler y ye llw sp t n leaflets a n d petiles f celery tak en frm n a tura lly in fected pl ants : Lt, yellw sp ts an d stri pes a lng the veins, mstly at basal prtin f veinl ets whe re they jin main and la teral vein s ; B, irreg-ularly shaped chlrtic spt s, man y the result f smaller spts ca les ci ng; 0, small chlrti c spt s and stri pes alng the vein s ; D, num eru s small chlr tic spts, sme f wh ich are cir cul ar ; basal prtin f leaflet shws e nla rged chlrti c sp ts frmed by the calesci ng f s malle r n es ; E, chlr tic s p tti ng a n d el ng-ated strip es a lng th e veins ; F, ep idermis r emved frm three pet iles, s h w ing brwn s pec ks alng the veins. (Milpit a s, Nv ember 8, 9 34; curtesy M, W. Gardner.) HILGARDIA. VOL. 6. NO.8
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