Infection Cycle of Watermelon Mosaic Virus
By TAKASHI YAMAMOTO*
Agronomy Division, Shikoku National Agricultural Experiment Station (Senyucho, Zentsuji, Kagawa, 765 Japan)
Among the viruses occurring in cucurbits transmission. As to other vectors, many of in Japan, the most prevalent ones are water them showed low parasitism to cucurbits and melon mosaic virus (WMV) and cucumber low ability of transmitting WMV, so that their mosaic virus (CMV) . Of them, WMV occurs role for the spread of WMV in the field was mainly in the summer season in the Kanto not clear. A survey conducted in fields of region and westward. The WMV diseases in cucurbits in 1981 spring to know the kinds of cucurbits cause not only systemic symptoms aphids which fly to the cucurbits at the initial such as mosaic, dwarf, etc. but also fruit mal incidence of WMV showed that more than a formation, thus giving severe damage to crops. half of the aphid species sampled were vector In addition, the control of WMV is quite dif species (Table 2). The initial incidence of ficult as the virus is transmitted by aphids WMV occurs usually in the period from mid and that carried by plant sap is also infectious. May to early-June at the survey site (west Thus, WMV is one of the greatest obstacles part of Kagawa Prefecture), and this period to the production of cucurbits. coincides with the period of abundant appear The infection cycle of the WMV, including ance of aphids. In this period, vector species the routes of transmission of the virus by less parasitic to cucurbits also flew in plenty aphids, which is the most important in con to cucurbits. It is inferred that these aphids trolling the virus is briefly presented in this may take part greatly in the primary in paper, based on the research results reported fection of WMV, namely, the infection to in the "Epidemiological studies of watermelon cucurbi ts from wintered hosts (virus-source mosaic virus".rn> plants) .
Species of the vector aphids Wintered host plants as the source of the first infection of WMV The main route of infection with WMV is through aphids. As shown in Table 1, many The range of WMV hosts is limited: mainly kinds of aphids transmit the virus in a non Cucurbitaceae, and few other plants such as persistent manner. Of them, 23 species have those of Pedaliaceae, Leguminosae, Chenopo been reported as vectors in Japan. Further diaceae, and Amaranthaceae. In areas where more, by adding several species distributed in cucurbits are cultivated throughout the year Japan, the total number reaches as many as under structures.;.;,~. in Shikoku, Kyushu, and nearly 30. Among them, Avhis gossyvii and other regions, WMV is transferred from Myzus persicae are highly capable of trans cucurbits to cucurbits. Namely, the winter mitting WMV. 18 > Particularly, Avhis gossypii ing infection-source plants are cucurbits. occurs abundantly on cucurbits, and is re However, in the regions of the open culture garded to play a principal role for the virus where no cucurbits are grown in winter, it has not been fully clarified that ·what kind Presented address: of plant serves as the wintering host. Major ,:, Toyama Vegetable and Ornamental Crops Research Station ""inter crops which are infected with (Goromaru, Tonami, Toyama, 939-13 Japan) ,:.. ; Glasshouses or vinylhouses 260 JARQ Vol. 19, No. 4, 1986
Table 1. Aphid s1>ecies reported to be vectors of WMV-2 (1982)
Species References
Acyrthosiphon kondoi Shinji et Kondo Wyman, 197910> A. lactucae (Passerini) Coubriet, 19624> 13 A. pismn (Harris) Swift, 1949 ' Aphis cit?·icola van der Goot Adlerz, 19782> ,,,., A. cleroclenci?•i Matsumura Yonaha et al., 197920> ** A. crciccivora Koch Greber, 1969"> A. fa.bae Scopoli Molnar & Schmelzer, 196411> A. frangulae beccabunuae Koch Karl & Proesler, 19768> ** A. ul1wines Matsumura Yamamoto et al., 198zts> ,;,:, A. r;ossypii Glover Lindberg et al., 195610> Komuro, 1956°> A. 1niddletonii Thomas Adlerz, 19782> A. na.stu,rt.ii Kaltenbach Karl & Schmelzer, 1971" "'* A. ne1-ii Boyer de Fonscolombe Tewari, 19761r,> ** A. ri,1nicis Linne Yamamoto & Ishii, 198017> * A. sanbuci Linne Karl & Schmelzer, 19717 > ,:,* Aidacorthwni rna.gnoliae (Essig et Kuwana) Yamamoto et al., 198218> ** A . nipponicurn (Essig et Kuwana) Yamamoto et al., 1982181 7 ** A. solani (Kaltenbach) Karl & Schmelzer, 1971 ' " A. (Neomyzus) circumfiexumi (Buckton) Karl & Schmelzer, 197171 Brachycaudi,s (Acai,dus) ca1·dui (Linne) Karl & Schmelzer, 19717> *"' Brevicoryne bra.ssicae (Linne) Coubriet, 19621> 7 C1yvto11iyziis 1·ibis ( Linne) Karl & Schmelzer, 1971 ' Dysavhis crataegi (Kaltenbach) Karl & Schmelzer, 19717 > ,., Hyalopterus 1w1.mi (Geoffory) Karl & Schmelzer, 197171 * Hysteroneura seta1-iae (Thomas) Coubriet, 19624> "* Livavh:is e1ysinii (Kaltenbach) Adlerz, 19741> *" ./1,focrosivhwm euvhorbiae (Thomas) Greber, 1969''> * Macrosivhoniella sanborni (Gillette) Karl & Schmelzer, 197171 Myzus cera,s·i (Fabricius) Karl & Schmelzer, 19717 i *'' M. (Nectarosiphon) persicae (Sulzer) Anderson, 1954:P Phorodon lmmiili (Schrank) Karl & Schmelzer, 197171 *" P. hu11ml-i javonensis Takahashi Yamamoto et al., 1982181 ,..,;. Rhodobimn porosiwi (Sanderson) Yamamoto et al., 198210 ,,,;. Rhopalosiphurn maiclis (Fitch) Coubriet, 1962<1> ,:,* R. padi (Linne) Karl & Schmelzer, 19717> Semiaphis ,i, Aphid species ooccurring in Japan. "* Aphid species reported to be vectors of WMV in Japan. ( Sako et al., 197712>; Tanaka et al., 19791<1>) 261 Table 2. Aphid species collected from the cucumber and pumpkin fields during the approximate p-eriod of first infection of WMV in Kagawa (1981) Cucumber field (May 2, 9, 16, 23, 30)11> Pumpkin field (May 20, 27, June 3, 7)"> No. of aphid No. of aphid Aphid speciesc> collected Aphid speciesc> collected (% of total) (% of total) * Acyrthosiphon 1>isum 1 ( 0.4) * Acyrthosiphon 1>isurn 6 ( 1.0) Aphis c'it1'icolct 2 ( 0.9) * A7>his citricolct 9 ( 1.5) ,:, A. craccivora 5 ( 2.2) ,:, A. craccivora 63 (10.3) '' A. gossypii 30 ( 13.1) A . gossypii 123 (20.1) A. odorikonis 64 (28.0) A . oclorikonis 316 (51.7) A. sp. 1 ( 0.4) A. Sp. 3 ( 0.5) '' A iilacorthu1n m.agnoliae 3 ( 1.3) ,:, A ulacorthimi nipponicmn 1 ( 0.2) * A. solani 31 (13.6) ,) A . solani 14 ( 2.3) "' B1·evicoryne brassicae 5 ( 2.2) •) Brevico1·yne brassicae 2 ( 0.3) ,:, Macrosiphwm euphorbiae 33 (14.5) Capitophorus hippophaes M egou.ra c1·assic(tuda. 7 ( 3.1) javanicits 4 ( 0.7) * Myzus (Nect.) prwsicae 30 (13.1) Ei,myzus i??ipatiensae 2 ( 0.3) * Rho1>alosiphimi 1nafrlis 3 ( 1.3) M egoura crassicauda 8 ( 1.3) "' R. pacli 7 ( 3.1) * Myzus (Nect.) persicae 35 ( 5.7) R. 11tfiabdorninalis 5 ( 2.2) * Phorodon humuli japonensis 1 ( 0.2) * Sitobion akebiae 1 ( 0.4) PleotrichophoritS glandulosus 1 ( 0.2) Total 228 Rhopalosiphurn nym1>haeae 9 ( 1.5) * R. padi 6 ( 1.0) Semiaphis heraclei 1 ( 0.2) * Sitobion akebiae 1 ( 0.2) S. ibarae 1 ( 0.2) Total 609 a) First incidence of WMV in the field; June 4. b) First incidence of WMV in the field; May 27. c) * : Vector aphid of WMV Table 3. Reciprocal transmission of WMV between cucumber and wintering cro1>s by a r>h id species Aphid species Transmission* Acyrthosi7>hon pismn Garden pea - Cucumber Aphis craccivora Broadbean } ~Cucumber Garden pea ~ Aphis gossypii Broadbean Garden pea - - ~ Cucumber Spinach Sweet pea - Myzus (Nect.) persicae Spinach --~ Cucumber <- - ,:, Arrows indicate direction of transmimission. 262 JARQ Vol. 19, No. 4, 1986 Table 4. WMV-transmission efficiency of Aphis gossgpii Factor Optimum condition Mot·ph, Age No significant difference Host plants Cucumber> Taro, Sweet pepper > Egg p lant, Pokeweecl Cucumber> Okra, Loquat, Weeds Pre-acquisition fasting period 1-2 hr Acquisition feeding period 1-2 min (5 sec) 1noculation feeding period > 1 hr (5 sec) Transmission by groups P= l-Q" Virus retention period Starved >4hr Released on plant > 15 min Serial transmission by single aphid 2-5 plants Temperature 2s 0 c WMV are spinach, garden pea, broad bean, Secondary infection etc.. 1•,1~> As garden pea plants with natural infection of WMV were collected every Although the number of diseased plants where,6,19> garden pea can be t·egarded as the caused by the first infection of WMV is not major wintering SOlU'Ce of infection of WMV. necessarily large, the disease spreads rapidly Since broad bean and spinach are also culti after the first incidence through the vector, vated abundantly like garden pea and their A. goss11pii and by the infection through plant growth duration overlaps with that of cucur sap, occurring during crop management prac bits of outdoor culture for certain periods in tices. Particularly, the role of A. goss11pii autumn and spring, and WMV is reciprocally seems to be very large. transmitted between cucumber and these crops As shown in Table 4, A. gossypii is able to by aphids as shown in Table 3, it is highly pos acquire and transmit WMV quite easily. The sible that these crops also serve as the win viruriferous insects maintain stable transmis tering source of WMV. sibility for many hours. Many of them can As given in Table 2, the first incidence of cause the disease in several seedlings of cu WMV occurs 1-2 weeks after the peak emer cumber by one insect. The large number of gence of aphids in spring, i.e. from mid-May A. gossypii emerged on cucurbits can explain to eal'ly-June. This time is later by more than how rapid is the spread of secondary infec one month than the time of incidence of CMV tion. It is considered that highly movable a late which is also transmitted by aphids like WMV. insects spread WMV to a wider extent, but Furthermore, the number of hills which show apterous-form insects play an important role the first incidence of WMV is quite few in to spread WMV within the fields. Therefore, the neld. These facts suggest that even in it is extremely important to suppress the em areas where WMV prevails, wintering host ergence of aphids in the field from the stand plants (infection source) of the virus are ex point of preventing the infection within the tremely few, with limited kinds and quantity. fields and of the large area control of WMV It seems to show that viruriferous aphids do disease. not emerge unless the aphid population in In addition to the high virus transmis creases to a considerably high level and the sibility of fl. gossypii, other factor for the number of viruriferous aphids reaching cu severe occurrence of WMV seems to be that curbits is also small. many of cucurbits infected with WMV serve as good virus-source plants. As shown in Table 5, WMV is transmitted through aphids 263 Table 5. WMV transmission by Aphis gossgpii from diseased plants to cucumber seedlings Transmission rate ( % ) •> Virus source plant (var.) I II Cucumis sativus ( Sagami-hajiro) 64 72 C. -melo (Earl's Favourite) 52 72 C. melo ?nakuwa (Shunka) 40 32 C. melo conomon (Katsura-ohshil'ouri) 64 40 Cuctwbita maxima ( Chikanari-ebisu) 64 80 C. 11toschata ( Heian-kogiku) 52 72 Citrullus vulgaris (Shinyamato 2) 44 28 Lagenaria sice?·a1-ia (Sakigake) 8 12 Lagena?·ia sice1·a?"ia (Hyo-tan) 20 24 Li,ffa cylincl1·ica 32 40 Sesamum indici,1n ( Suigen-kuro) 5 Sesa1ni,1n inclicimi (Birooclo) 5 Go1nphrea globosab> 4 Spinacia oleracea (King of Denmark) 43 ------a) Test plant: Each 25 seedlings, 2 aphids were placed on each test plant. b) Inoculum: Inoculated leaves. at a high rate from many kinds of cucurbit Infection cycle of WMV crops infected with WMV. In cucumber, even from resistant cultivars which do not show On the basis of the above-mentioned results, symptoms, WMV is transmitted at a high rate the infection cycle of WMV is summarized as similar to that of susceptible cultivars. Weeds follows: of Cucu1'bitaceae infected with WMV are con 1) Transmission of WMV from wintering sidered to serve as virus-source plants, like host plants (virus source plants) to cucurbit15 diseased cucurbits. As these weeds and cu (the primary infection, i.e., the initial inci curbits in home gardens remain growing until dence of WMV in the fields). late autumn, they are rega.rded important as 2) The secondary infection due to mutual the virus-source for wintering host plants. infection among cucurbit plants. As mentioned above, WMV can spread 3) Transmission of WMV from diseased rapidly among cucurbits by an efficient mutual crops to wintering plants. infection through aphids, and spread to wider Based on the growing season of major areas by repeating it, resulting in severe out crops which are liable to be suffered from break of WMV disease. Particularly during WMV and the occurrence pattern of WMV the period from summer to autumn, there are in Kagawa Prefecture (Fig. 1), the infection infection-source plants everywhere, so that cycle of the virus was drawn schematically cucurbit crops in the fields are always ex in Fig. 2. In a word, WMV is transmitted posed to the infection with WMV. In autumn, through its vector aphids from wintering host WMV is transmitted by aphids from diseased plants to cucurbits in spring, and conversely cucurbit crops to plants which are going to from the cucurbits to wintering plants in winter outdoors or cucurbit crops under struc autumn. Accordingly, the method of con ture. These plants and crops infected in trolling the virus should be based on such autumn become the sources of WMV for the infection routes. The control of WMV. ap succeeding year. pears to be extremely difficult because W~V is carried by many kinds of aphids. How ever, its host range is so limited that the 264 JARQ Vol. 19, No. 4, 1986 _:z ...... \ 1-:_-7 ...... ; .;::::;=:::=::;\ Cucumber L_'""_ ~ -Z..:-::::{{:::::::::::::\ A?}:;:;:}=:;:~?~N:\ ?\}>,, £ ...... · .·\. Pumpkin Weeds or C'ucurbit:,cc:tc G:mlcn pea Brn.1dbca11 Jan . Feb . Mar. A1>r. May June Jul. Aug. Sep1. Oc1. Nov. Dec. Mouth AES\ · Occurrcucc ofWMV Fig. 1. Croping pattern of host plants of WMV and occur rence of the virus Cucurbits of semi-forcing culture, spring cropping 0~ Cucurhits of 11rokctcd cropping Garden pea Cucm·bits of summer cropping Oroad bca11 Q Cncurbitaccous weeds Spinad1 0 0/ Cucurbits of summcr~..i utumn. autumn cropping Cucurbilaccous weeds Winier hos1 Summer hosl Fig. 2. Schematic presentation of infection cycle of WMV in western Japan 265 interruption of the infection cycle will be by watermelon mosaic virus. Ber. Ohara possible. For the culture under structures, Inst. Lmulw. Biol., 12, 133- 143 (1964). 7) Karl, E. & Schmelzer, K. C.: Unter- prevention of aphids entering into structures, suchungen zur -Obertragbarkeit von Wasser early removal of infection-source plants, pre melonenmosaik-Viren duch Blattlausarten. vention of sap transmission, etc. are effective Ar ch. Pflanz enscluttz, 7, 3-11 ( 1971) . in reducing the WMV occunence. In the fields, 8) Karl, E. & Proeseler, G.: Befahigung von control of aphids and prevention of aphids Aphis fra..ngi,lae beccabimuae Koch zur 'Ober ti-agung nichtpersistenter Viren. Arch. Phy from flying to crops, together with early re topathol. i1.. Pflanz enschutz, 12, 135-140 moval of virus-source plants in large areas and (1976). avoiding the overlapping of growing seasons 9) Komuro, Y.: Studies on a mosaic disease of of cucurbits and wintering host plants, etc. squash in Japan. 1. Its symptoms, host range may be able to suppress WMV occurrence to and transmission. Ann. Phytovathol. Soc. Jvn., 21, 162-166 (1956) (In Japanese with a considerable extent. In addition, the use of Eng·lish summary]. resistant cultivars is an important practice for 10) Lindberg, G. D., Hall, D. H. & Walker, J.C.: cucumber. A study of squash and melon mosaic virus. Phytopathol., 46, 18 (1956) . 11) Molnar, A. & Schmelzer, K. C.: Beitrage zur Acknowledgement Kenntnis des Wassermelonenmosaikvirus. Ph11toviithol. Z., 51, 361-384 (1964). The study presented in this paper was car 1.2) Sako, N., Okumura, T. & Nonaka, F.: Aphid ried out as a cooperative research with Dr. transmission of watermelon mosaic virus. Masayoshi Ishii of Vegetable and Ornamental Bull. Fae. Agr. Sagci U11:iv., 42, 1- 8 (1977) Crops Research Station, Dr. Toshihiro Katsube (In Japanese with English summary]. of Shikoku National Agricultural Experiment 13) Swift, J . E.: Vectors concerned in the trans mission of cantaloupe mosaic in the Imperial Station. Dr. Kan-ichi Ohata of National In valley. Plant Dis. Reptr., stipvl., 180, 4-5 stitute of Agro-Environmental Sciences, and (1949). Prof. Masato Sorin of Kogakukan University. 14) Tanaka, H., Kagi, T. & Kimura, H.: Per The author wishes to express his sincere sonal communication. (1979). thanks to· them. He also thanks Dr. T. Katsu 15) 'l'ewarii, J.P.: Transmission studies of wa termelon mosaic virus by aphids. Entomol, be for critical reading of the Japanese manu 1, 111- 114 (1976). script of this paper. 16) Wyman, J. A.: Acyrthosi1>hon lcondoi- a new vector of cucurbit viruses in southern Cali References fornia. Environ Ent., 8, 549- 551 (1979). 17) Yamamoto, T. & Ishii, M.: Aphid transmis sion of watermelon mosaic virus (WMV-2). 1) Adlerz, W. C. : Spring aphid flight and in Proc. Assoc. Plant Protec. Shikoki,, 15, 37- cidence of watermelon mosaic virus. Phyto 40 (1980) [In Japanese with English sum pcithol., 64, 350-353 (1974). mary]. 2) Adlerz, W. C.: Secondary spread of water 18) Yamamoto, T. et al.: Transmission of wa melon mosaic virus 2 by Anuraphis 1niclclle termelon mosaic virns by aphid species. }Jm. ton·ii. J. Econ. Entom..ol., 71, 531-533 (1978). J. appl. Ent. Zool., 26, 218- 223 (1982) [In 3) Anderson, C. W.: Two watermelon mosaic Japanese with English summary). virus strains from central Florida. Phyto 19) Yamamoto, T. et al.: Epidemiological studies pathol., 44. 198- 202 ( 1954) . of watermelon mosaic virus. Bull. Shikoku 4) Coubriet, D. L.: Efficiency of various insects Agr. Exv. Sta., 44, 26-140 (1984) [In Japa as vectors of cucumber mosaic and water nese with English summary]. melon mosaic virus in cantaloups. J. Econ. 20) Yonaha, T. 1 Kono, S. & Nishimura, T.: Entomol., 55, 519-520 ( 1962). Aphid transmission and disease symptoms of 5) Greber, R. S.: Viruses infecting· cucurbits in watermelon mosaic virus in pumpkin varie Queensland. Qcl. 26, 145- J. Agr. Anim. S ci., ties. Ann. Phytovathol. Soc. Jpn., 45, 567 177 (1969). ( 1979) [In Japanese]. 6) Inouye, T.: A virus disease of pea caused (Received fol' publication, August 24, 1985)