Printed in Great B,iJain Geminivirus transmission and...

311 Ann appl Bioi (1994) 125311-325 Printed in Great BiJain

Geminivirus transmission and biological characterisation of Bemisia tabaci (Gennadius) biotypes from different

geographic regions

By I D BEDFORDl R W BRIDDON J K BROWN R C ROSELL and P G MARKHAM

Department of Virus Research John Innes Institute John Innes Centre for Plant Science Research Colney Lane Norwich NR47UH UK

Department of Plant Sciences University of Arizona Tucson Arizona 85721 USA

(Accepted 19 April 1994)

Summary Eighteen populations of Bemisia tabaci collected from different geographic

locations (North amp Central America the Caribbean Africa the Middle East Asia and Europe) were studied to identify and compare biological and genetic characteristics that can be used to differentiate biotypes The morphology of the fourth instarpupal stage and compound eye structures of adults were investigated using scanning electron microscopy and found to be typical of the species among all biotypes and populations studied Setae and spines of B tabaci larval scales from the same colony were highly variable depending on the host plant species or leaf surface characteristics The location and the morphology of caudal setae characteristic of all B tabaci studied to date were present in all colonies However differences in adult body lengths and in the ability to induce phytotoxic disorders in certain plant species were found between biotypes or populations The recently identified B biotype characterised by a diagnostic esterase banding pattern and by its ability to induce phytotoxic responses in squash honeysuckle and nightshade was readily distinguished from non-B biotype populations None of the non-B biotypes studied were found to induce phytotoxic responses Nine populations examined showed typical B biotype characteristics regardless of country of origin All tested populations detershymined as B or B-like biotypes successfully mated with other B biotype colonies from different geographic areas Non-B biotype colonies did not interbreed with other biotypes

The B tabaci populations were tested for their ability to transmit 15 whiteflyshytransmitted geminiviruses (WTGs) from different geographic areas with a wide range of symptom types All WTGs were transmitted by the B biotype colonies and by most non-B biotype colonies with the exception of three viruses found in ornamental plants which were non-transmissible by any colony Some nonshyB biotypes would not transmit certain geminiviruses and some geminiviruses were more efficiently transmitted than were others

Key words Bemisia tabaci biotypes whitefly-transmitted geminiviruses physhytotoxic responses host plant adaptation mating studies

To whom correspondence should be addressed

copy 1994 Association of Applied Biologists

312 I D BEDFORD ET AL

Introduction

Bemisia tabaci (Gennadius) the cotton tobacco or sweetpotato whitefly has recently become very important to world agriculture as a pest and as a virus vector In many of the warmer parts of the world populations are increasing and severe crop losses have been experienced in some areas Evidence has accumulated that populations have different biological characteristics and that some recent devastating outbreaks of B tabaci parshyticularly in areas where it was previously unimportant are linked to the appearance of a new biotype strain or possibly species of B tabaci

B tabaci is indigenous to the tropical and sub-tropical regions of the world and has long been a pest and virus vector associated with certain crop and weed species It was previously reported to have a composite host range of around 300 species within 63 families (Mound amp Halsey 1978) and caused localised losses to crops such as cassava in Africa (Bock Guthrie amp Meredith 1978) and cotton in the Sudan (Nour amp Nour 1964) through feeding damage and plant virus transmission Over the past decade however severe outbreaks of B tabaci have become more frequent and crops colonised by B tabaci have suffered major losses with yield reductions ranging from 20 to 100 (Brown amp Bird 1992) Watermelon crops in the Yemen have been decimated since 1989 (Bedford et al 1994) and the southern states of North America experienced an estimated $500 million loss in the 1991 cotton and vegetable harvest (Perring et al 1993a) The cotton crop in Pakistan is likewise threatened by a whitefly-transmitted virus (Mansoor et al 1993) In Mexico the Caribbean Basin and Central America cotton melon tobacco and tomato crops have been subjected to losses as a result of whitefly feeding and whitefly-transmitted virus infection (Brown amp Bird 1992) Previously B tabaci had been a sporadic controllable pest in these areas New presently uncharacterised whitefly-transmitted viruses have occurred in some crops (Brown 1990 Brown amp Bird 1992) and phytotoxic disorders such as squash silverleaf (SSL) (Yokomi Hoelmer amp Osbourne 1990) pumpkin white stems (Costa amp Brown 1991) white streaking in cole crops (Brown Costa amp Laemmlen 1992a) uneven ripening of tomato (Maynard amp Cantliffe 1989) and reduced growth yellowing and stem blanching in lettuce and kai choy (Costa Ullman Johnson amp Tabashnik 1993) have been observed To-date only certain populations of B tabaci are known to induce these phytotoxic responses and they are linked to some of the most agriculturally devastating outbreaks worldwide Symptoms similar to squash silverleaf were first reported in Israel in the 1960s (Paris Stoffella amp Powell 1993) and more recently in Florida (Maynard amp Cantliffe 1989 Simons Stoffella Shuler amp Raid 1988) Arizona (Brown et al 1992a) California (Cohen Duffus amp Liu 1992) and southern France (Villevieille amp Lecoq 1992) These same populations have been reported to have an increased fecundity (Bethke Paine amp Nuessly 1991) a strong resistance to carbamate and organophosphorus based pesticides (Byrne amp Devonshire 1993 Costa Brown Sivshyasupramaniam amp Bird 1993) and an extremely broad host range compared to other populations of B tabaci studied so far (Costa amp Russell 1975 Burban Fishpool Fargette amp Thouvenel 1992 Wool amp Greenberg 1990) Studies of non-specific esterases have produced a diagnostic test to identify the populations of B tabaci that induce phytotoxic disorders (Costa amp Brown 1991 Bedford et al 1992 1993 J K Brown S A Coats I D Bedford and P G Markham unpublished Byrne amp Devonshire 1993 Byrne Cahill Denholm amp Devonshire 1994) They all exhibit a highly polymorphic esterase banding pattern and have been tentatively termed the B biotype Two B tabaci populations which exhibited the characteristic B biotype esterase band also showed another distinct esterase band and have been termed B2 biotypes (J K Brown S A Coats I D Bedford and P G Markham unpublished) B biotype B tabaci have been identified within many areas of the horticultural industry even in northern Europe and the global spread of this insect is

313 Biotypes and geminivirus transmission by B tabaci

Table 1 Bemisia tabaci colonies kept in culture at the John Innes Institute showing colony code origin year of collection and culture host plant

Colony Biotype Origin Year Host plant

FN B Florida USA 1990 Nightshade (Solanum nigrum) CC B California USA 1991 Cotton (Gossypium hirsurum) ArP B Arizona USA 1990 Poinsettia (Euphorbia pulcherrima) ArPu A Arizona USA 1990 Pumpkin (Cucurbita pepo) GC G Guatemala 1988 Cotton (Gossypium hirsurum) MnC 0 Nicaragua 1991 Cotton (Gossypium hirsurwn) AnW B Antigua 1991 Watermelon (Cirulus lanaus) ABA E Benin Africa 1990 Asystasia (Asysasia gangeica) NI J Nigeria 1990 Ipomea (Ipomea congesla) SC L Sudan 1974 Cotton (Gossypium hirsurum) SAP B South Africa 1992 Potato (Solanum uberosum) IsC B Israel 1991 Cotton (Gossypium hirsuum) CyC B Cyprus 1991 Cotton (Gossypiwn hirsuum) TC M Turkey 1985 Cotton (Gossypium hirsuum) YC B Yemen 1990 Cotton (Gossypium hirsurum) YW B Yemen 1990 Watermelon (Cirulus lanaus) PC K Pakistan 1992 Cotton (Gossypium hirsuum) IW H India 1991 Watermelon (Cilrulus lanaus)

Biotype as defined by esterase banding patterns (Bedford el albull 19j12)

seemingly exacerbated by the transportation of infested ornamental plants such as poinsettias (Byrne amp Devonshire 1993)

In this study we recorded various morphological characteristics of 18 discrete populations of B tabaci and investigated whether different populations of whiteflies are able to transmit only the geminiviruses from their own locality

Materials and Methods

Origins and maintenance of whitefly colonies

Adult B tabaci were collected from various field locations throughout the world (Table 1) and used to start whitefly colonies B tabaci were cultured in perspex cages (90 cm x 45 cm x 45 cm) in growth rooms at 25degC (16 h daylength) and were maintained on the same or a closely related plant species as originally collected from in the field All colonies were tested for esterase profiles and their biotype defined (Bedford et al 1992 J K Brown et al unpublished) This data is summarised in Table 1

Scanning electron microscopy

To identify the species by reference to taxonomic keys (Martin 1987) morphological studies were performed on individual fourth instarpupal stages from B tabaci colonies with a particular emphasis on the morphology of the vasiform orifice Leaf pieces infested with larval scales were frozen in liquid nitrogen gold coated viewed and photographed at -180degC with a Cam Scan Series Four scanning electron microscope (SEM)

Ommatidial arrangements of the adult compound eyes were also examined with the SEM Adult B tabaci from different colonies were killed by freezing (-200C for 30 min) fixed


Table 2 Whitefly-transmitted gemini viruses tested their codes origins and maintenance histories

Provided Virus Code Origin Received by Maintained

Abutilon mosaic AbMV UK Unknown JlI (v) African cassava mosaic ACMYN Nigeria 1990 S Shoyinka (v) Ageratum yellow vein AgYYYS Singapore 1993 J Stanley (i) Asystasia golden mosaic AGMY Benin 1989 R Markham (i)(v) Bean calico mosaic BCMoV Arizona 1992 J K Brown (i) Benin legume BLV Benin 1991 R Markham (i) (v) Cotton leaf crumple CLCV Arizona 1990 J K Brown (v) Honeysuckle yellow vein

mosaic HYVMV UK Unknown P Markham (v) Pseuderanthemum yellow

vein PYVV Yemen 1989 P Jones (v)(g) Sida golden mosaic SiGMVmiddotC Costa Rica 1990 R Markham (i)(v) Sida golden mosaic SiGMYmiddotH Honduras 1990 R Markham (i) (v) Sida yellow vein SYVV Nigeria 1991 R Markham (i)(v) Squash leaf curl SLCY Arizona 1990 J K Brown (i) Tomato yellow leaf curl TYLCYmiddotY Yemen 1989 P Jones (i)(v)(g) Tobacco leaf curl TLCYmiddotY Yemen 1989 P Jones (i)(v)(g) Watermelon chlorotic

stunt WCSY Yemen 1989 P Jones (i) (g)

(i)-Insect transmitted (v)-Vegetative propagation (g)-Grafting

to the viewing stage of the scanning electron microscope using a piece of double-sided sticky tape and sputter coated with gold Whiteflies were viewed by SEM and photographed at room temperature A mjnimum of 20 insects were studied from each colony and compared to a taxonomic diagram of a typical B tabaci compound eye (Gill 1990)

Morphometries

Adult whiteflies from different populations were collected and killed by exposing to ethyl acetate fumes for five minutes Several parameters of 10 males and 10 females from each population were measured and evaluated as possibly useful morphometric criteria A binocular microscope with an eye-piece graticule was used to make measurements

Transmission of gemini viruses

Plants infected with whitefly-transmitted geminiviruses were either collected from the location where the virus is endemic or from other research centres (Table 2) Approximately 500 non-viruliferous B tabaci from each colony were placed on virus infected plants in perspex cages After a 24 h acquisition access period (AAP) on the infected plant it was replaced by three - five healthy test seedlings and the insects were allowed a 48 h inoculation access period (lAP) All whitefly adults were removed and the seedlings transferred to an insect proof glasshouse where they were fumigated with a carbamate-based insecticide (Propoxur Octavius Hunt Ltd) and twice weekly thereafter Any infested leaves were removed and plants were checked daily for virus symptoms Experiments were repeated three times

Transmission of viruses to test seedlings was confirmed by dot-blot hybridisation (Maule Hull amp Danson 1983) to radioactively labelled probes (Rigby Dieckmann Rhodes amp


Table 3 Virus transmission efficiencies ofgeminiviruses by the B biotype B tabaci colony (FN) showing number of infected plants over number of plants tested

Number of insects Virus 10 20 100 1000 2000 3000-5000

TLCV-Y 1260 6670 6060 1010 1010 TYLCV-Y 1590 88120 118120 1010 1010 WCSV 490 4070 3030 1010 1010 SLCV 210 810 1010 1010 1010 AGMV 210 610 910 1010 ACMV-N 010 010 010 010 010 38 36 12

010 010 010 010 010 36 1832 613 BCMoV 524 1824 2424 1010 1010 AgYVVmiddotS 024 024 224 724 1010 bull Transmissions were made from infected cassava to D slramonium Transmissions were made from infected cassava to N tabacum vaL Samson Not tested

Berg 1977) of African cassava mosaic virus DNA A (Stanley amp Gay 1983) watermelon chlorotic stunt virus DNA A (R W Briddon unpublished results) and asystasia golden mosaic virus DNA A (R W Briddon unpublished results)

Virus transmission efficiency

Groups of one five 10 20 and 100 B tabaci of B biotype colony FN were caged for a minimum 48 h AAP on a geminivirus infected plant and then placed onto individual healthy test seedlings of the same plant species (Table 3) The test seedlings were grown in individual 2 cm x 2 cm plastic pots and the viruliferous insects were caged on them by meshshyvented 150 ml sterilin jars After the 48 h lAP plants were fumigated transferred to an insect proof glasshouse and observed for symptom development as described above

In those cases where transmission was not achieved with 100 insects transmission experiments were repeated with approximately 1000 2000 and 3000-5000 insects caged in 10 cm x 20 cm vented clear plastic containers on seedlings grown in two litre plastic pots

Bioassay for phytotoxicity

The ability of colonies to induce a phytotoxic response in squash plants (Cucurbita pepo cv Fordhook) (Yokomi et al 1990 Costa amp Brown 1991) was tested by placing single seedlings of squash into an insect cage with adult whiteflies Honeysuckle (Lonicera japonica) and nightshade (Solanum nigrum) were also used as diagnostic indicators of phytotoxicity resulting from feeding by whitefly larvae (Bedford et al 1993)

Host plant adaptation

Groups of 30 individual B tabaci from B biotype and non_B biotype colonies were caged on single plants of a selected host range (Table 4) and kept in a growthroom at 25degC with a 16 h daylength After 24 hand 48 h the number of individuals still alive was recorded (Table 4) Each test was repeated three times

Mating studies

Leaves hosting fourth instarpuparium stages of different B tabaci colonies already established on cotton (Gossypium hirsutum cv Delta Pine 16) were removed from the stock


Table 4 Mean adult survival of three replicates of30 Bemisia tabaci per test after 24 h and 48 h when caged on various lest plants

Colony () CC(B) IsC(B) YW(B) SC(L) MnC(D) ABA(E) PC(K)

Test plant 24 h 48h 24 h 48h 24 h 48h 24 h 48h 24h 48 h 24 h 48h 24h 48h

Phaseolus vulgaris 30 28 29 28 27 23 25 17 26 17 8 4 18 12

Lycopersicon esculemum 27 22 28 24 28 24 23 20 26 25 0 14 8

Nicoliana abacum 26 22 28 23 24 22 19 12 25 7 3 19 7

Daura stramonium 30 28 30 29 29 28 25 23 24 23 5 3 15 12

Gossypium hirsutum 30 29 30 29 28 25 20 15 28 27 16 7 29 28 CucurbiJa

pepo 26 24 27 26 27 25 19 10 24 19 8 4 25 16 Capsicum

annaheim 28 26 27 24 28 25 25 24 26 20 10 6 23 18 Asyslasia

gangelica NT NT 25 22 NT NT NT NT NT NT 24 22 NT NT

(--Biotype as defined by esterase banding patterns (Bedford el al 1992) NT-Not tested

ANDVAR (by Genstat) for a comparison of all biotypes based on angular transformed data from Table 4

Source of variation df MS VR

Plant species 6 166847 4323 Time 1 826083 21404 Biotypes 6 1418963 35837 Within B biotypes 1 1552 039 Within nonmiddotB biotypes 5 1702446 42997 Plant x time 6 11624 301 Plant x biotypes 36 33464 845 Plant x B biotypes 6 42 16 106 Plant x nonmiddotB biotypes 30 39314 993 Time x biotypes 5 6119 159 Plant x time x biotypes 30 6027 156 Residual 210 3860 TOlal 293

SED Plant species = 137 Time = 073 Biotypes = 137 Plant x Time = 194 Plant x Biotypes = 36 Time x Biotype = 194 Plant x Time x Biotype = 513 Level of significance

cages and placed in 9 cm plastic Petri dishes after ensuring that all adults had been removed As virgin adults emerged in the Petri dishes they were segregated into males and females Twenty males from one colony and 20 females from another colony were placed on two four-leaf stage seedlings of G hirsutum cv Delta Pine 16 grown in a two litre plastic pot and caged with a vented clear plastic cage Reciprocal mating experiments were also set up Experiments were performed in a growthroom at 25degC with a 16 h daylength and


repeated three times After seven days all remaining adults were removed and any progeny allowed to develop on the caged cotton plants

Results

Morphology

Results of morphological studies indicated that B tabaci from all colonies studied here have features typical of the species (Martin 1987) Specific studies of the vasiform orifice region of larval fourth instarpuparium stages showed no differences between any of the colonies nor did the ommatidial arrangement of adult eyes Differences were detected in the setae and spines of larvae within the same population depending on the leaf surface morphology Larvae cultured on glabrous-leaved plants developed fewer setae and spines compared to those cultured on plants with hirsute leaves (Fig 1) This difference was also observed when larvae from the same colony developed on the smooth upper leaf epidermis compared to the hairy lower leaf surface of certain plants such as poinsettia (Euphorbia pulcherrima) and tobacco (Nicotiana tabacum cv Samsun)

M orphometrics

The most easily measurable parameter and that having the least variability among adults of the same colony was length from tip of head to tip of abdomen Some colonies showed significantly smaller adult body lengths these were all non-UB biotypes The non-uB colony ABA reared on Asystasia gangetica had the smallest males measuring an average 0641 mm (SE 0014) in length and the smallest females measuring an average 0704 mm (SE 0016) in length The largest whiteflies were a uB biotype colony FN reared on nightshade where males averaged 0851 mm (SE 0023) and females 1107 mm (SE 0014) Although differences were found between different UB biotype colonies they were all significantly larger than the non-uB biotype colonies studied (Table 5) UB biotype males averaged 0840 mm (SE 0017) in length with non-uB males averaging 0771 mm (SE 0021) and B biotype females averaged 0976 mm (SE 0036) with non-uB females averaging 0854 mm (SE 0023)

Geminivirus transmission

All colonies were shown to transmit at least one geminivirus (Table 6) The uB biotype colonies and most non-uB biotype colonies transmitted at least 12 of the 15 gemini viruses tested although differences were found in the efficiencies (Table 3) ACMV could not be transmitted to its original host cassava (Manihot esculenta) (over 30000 insects failed to transmit to 16 rooted cassava cuttings) but successful transmissions were made from infected M esculenta to N tabacum cv Samsun and Datura stramonium (Table 3)

Three geminiviruses shown to be still infectious by grafting infected scions onto healthy plants (data not shown) could not be transmitted by any of the colonies (Table 6) even though cross-hybridisation tests confirmed homology to other transmissible WTGs such as ACMV (data not shown) These viruses are present in ornamental plants grown specifically for their virus-induced leaf patterns and are abutilon mosaic virus (AbMV) in Abutilon pictum var Thomsonii honeysuckle yellow vein mosaic virus (HYVMV) on Lonicera japonica aureoreticuiata and pseuderanthemum yellow vein virus (PYVV) in Pseushyderanthemum sp

Asystasia golden mosaic virus (AGMV) could not be transmitted by the non-B biotype colonies NI GC and TC and the two uB colonies YW and yc The non-B colony

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319 Biotypes and geminioirus transmission by B tahaci

Table 5 Characteristics of B tabaci colonies (i) biotype as defined by diagnostic esterase fgtunding pattern (ii) abilityinability to induce a phytotoxic response in squash plants and

(iii) mean (adult) body length of 10 males lind TO females

Phytotoxic Adult body kngth (mm(plusmnsEraquo Colony symptom

code Biotype inuuction Male Female

FN B + ORSI (0023) 1107 (0014) CC B + 0844 (0017) 0999 (0tJ20) ArP 13 + 01l94 (0020) 0935 (0014) ArPu A O7H9 (0017) 0856 (0018) GC G 0763 (0011) 0846 (0009) MnC D OS37 (0011) 0911 (0010) AnW B + NT NT ABA E 0641 (0014) 0704 (0016) NI J NT NT SC L 0749 (0007) 0853 (0010) SAP B + NT NT IsC B + NT NT eyC 13 + NT NT TC M 0783 (0012) 0R94 (0014) YC 13 + 0818 (0(J20) 0918 (0017) YW B + 0794 (0012) 0921 (0014) PC K 0791 (0017) 0886 (0021) IW H 0816 (0023) 0885 (0017)

-Biotype as defined by esterase banding patterns (Bedford el al 1992) sE-Standard error NT-Not tested

ABA would only colonise A gangetica the host plant from which it originated and oniy transmitted AGMV the virus associated with that plant species The non-H8 hiotype NI was an inefficient vector of all viruses tested (Tnble 6)


Nine of the 18 colonies tested induced a phytotoxic response in squash (c pepo cv Fordhook) honeysuckle (L japonica) and nightshade (S nigrum) (Table 5) This directly (orrelated with the nine colonies that exhibited a 8 or B2bullbull biotype esterase banding pattern (Bedford et al 1992 J K Brown et al unpublished) Silverleaf symptoms were induced in the squash plants and a yellow vein clearing response was observed in honeysuckle and nightshade


All HB hiotype colonies of B tabaci readily adapted to the plant species tested with minimal mortality although theB2 colony YW did not adapt as well as the B biotypes Non-B biotypes had a higher mortality on all test plants compared to the B and B2 colonies except when transferred to a plant of the same species as the culture originated (Table 4) Colony ABA had the highest mortality level of all colonies tested when transferred to alternative hosts yet had greatly reduced mortality when transferred to a plant of its original host plant species A gangelica Phaseolus vulgaris Datura stramonium Gossypium hirsUlum and Capsicum annaheim were significantly better host plants for all B tabaci colonies tested than Nicotiana tabacum Cucurbita pepo and Lycopersicon esculelllum B

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Table 7 Results of mating between B tabaci colonies M indicates male and F indicates female progeny

Female Colony (Biotype) CC(B) IsC(B) CyC(B) YC(B) PC(K) TC(M) MnC(O)

CC(B) MampF MampF MampF MampF M M M IsC(B) MampF MampF MampF MampF M M M CyC(B) MampF MampF MampF MampF M M M YC(B) MampF MampF MampF MampF M M M PC(K) M M M M MampF M M TC(M) M M M M M MampF M MnC(O) M M M M M M MampF

-Biotype as defined by esterase banding patterns (Bedford el al 1992)

biotypes were also found to swarm (towards the light source at the top of culture cages) when populations reached a high density This phenomenon was not observed in non-B biotype colonies one such colony TC having been cultured for 8 years

Mating studies

B biotype colonies of B tabaci readily interbred with all other B and B2 biotypes tested resulting in the appearance of males and females in the following generation However all non-B biotypes tested would not interbreed with any other biotype based on the appearance of only male progeny (Table 7)

Discussion

We have shown that different populations of B tabaci exist in distinct geographic locations worldwide Populations of whitefly collected from a variety of world locations and host plants have morphological features typical of the genus Bemisia and can be ascribed to the species B tabaci as described by Martin (1987) Scanning electron microscopy and light microscopy revealed that some characters specifically ommatidial arrangements and caudal setae were more stable than others such as thoracic abdominal and cephalic setae Adult body length was the most obvious parameter which varied between populations collected from different locales andor host plants but in general adults from populations identified as B and B2 biotypes were larger than non-B biotypes Biological assays were used as a test to differentiate B and B2 biotypes from the non-B biotypes Mating studies established that individuals from B biotype colonies could interbreed with other B and B2 types but that non-B biotypes did not interbreed with any other biotype under these conditions

Biotypes of B tabaci are defined at present using diagnostic esterase banding patterns (Bedford et al 1992 1993 Brown et al 1992b Byrne amp Devonshire 1993) or by RAPD DNA fingerprinting (Brown et al 1992b Perring et al 1993a Bedford el al 1993) As esterases are a phenotypic phenomenon which can be induced by agrochemicals they may not be an ideal long term taxonomic tool and should not be taken in isolation Suggestions that the B biotype should be recognised as a new species based on the above criteria and limited interbreeding experiments (Perring et al 1993a Perring Farrar Cooper amp Bellows 1993b) are premature (Campbell Duffus amp Baumann 1993 Bartlett amp Gawel


1993) Until the whole genus has been examined and definitive data on experimental conditions required for crossing experiments are obtained together with provision to reshyname all non-interbreeding populations such arbitrary decisions are unhelpful

B and B2 biotype populations were readily established on alternative hosts and could change hosts with lower mortality rates than the non-S biotypes however certain plant species were clearly shown to be better hosts than others for all biotypes tested A small but significant difference was shown between the B and B colonies tested where the S2 colony YW was less successful at alternative host adaptation than the S colonies This could have been due to the differing original host plant species and requires further investigation into the influence of original host species on further host adaptation before definite conclusions can be drawn Bz colonies were also shown to be different to B biotypes in their failure to transmit the virus AGMV a virus that some of the non-B biotypes failed to transmit The ability of B and B2 biotype populations to interbreed may facilitate future investigations into the differences between certain biotypes in transshymitting this virus The swarming behaviour of the B biotype colonies could have serious implications for virus transmissions in the field For non-B biotypes in cases of poor host acceptance it is possible that population numbers in the field decrease sharply following senescence of the host crop that has supported reproduction and that adaptations or host specialisation may occur among some individuals on alternative hosts all year round This adaptive ability and host sampling feeding behaviour may play an important role in transmission and dispersion of WTGs The dispersal of the S biotype into new areas such as the Caribbean Basin North Central and South America has probably occurred as a result of its ability to adapt and colonise a broad spectrum of plant hosts and may be associated with the worldwide movement of plants within the horticultural industry It is now a major pest and virus vector to food and fibre crops and weed hosts previously unaffected by WTGs There are still areas where the B biotype has not yet appeared such as most of Africa and Asia where WTGs are already endemic and are transmitted by indigenous B tabaci populations within specific ecosystems These areas are now under the greatest threat from the B biotype

All populations of B tabaci were able to transmit the field derived WTGs except for the non-B colonies ABA and NI which did not adapt well to alternative hosts and were also inefficient vectors of most viruses tested However ABA whiteflies were highly efficient in transmitting AGMV which infected its primary host plant A gangetica Our results suggest that the transmission efficiency is not biotype specific since the S biotype colony FN transmitted different viruses with different efficiencies At least 200-1000 times more insects were required to achieve the same transmission efficiencies of ACMV from cassava to tobacco compared to SLCV from squash to squash Virus distribution within the plant and vector feeding behaviour may contribute to vector transmission efficiencies

We conclude that geminiviruses present in areas colonised by non-B biotypes have host ranges restricted by the vector host range The recent introduction of the B biotype which has an extremely wide host range compared to nonS biotype populations has added a new selection pressure by expanding the host ranges of WTGs and creates the possibility of mixtures and recombinants of these viruses occurring We already know that dual infections can occur and subsequently still maintain distinct infections (Bedford et ai 1994) However pseudorecombinants (DNA A and B of bipartite WTGs in different combinations) are probably only infectious when strains of the same virus are used (Stanley Townsend amp Curson 1985 Von Arnim amp Stanley 1992) The appearance of new viruses in areas colonised by the B biotype is probably a direct result of the extended host range of the B biotype

Host preference cannot account for the failure to transmit the three geminiviruses from


ornamental plants Whiteflies were unable to transmit the viruses even though they were shown to be members of the WTG group by cross-hybridisation to transmissible WTGs and in the case of AbMV by the published nucleotide sequence (Frischmuth Zimmat amp Jeske 1990) All three were however still transmissible by grafting Some change(s) may have occurred in these viruses such that they can no longer be transmitted by the whitefly vector The fact that these plants have been vegetatively propagated as ornamentals for decades may offer one explanation for loss of transmissibility Additional studies are being carried out to clarify these issues in both biological and molecular terms

Acknowledgements We thank Mrs P Glanfield for technical assistance Dr James K Brown and Mr Mike

Ambrose for statistical advice Dr Frank Byrne Matt Cahill and Dr Ian Denholm (IACR Harpenden) for supplying colonies of B tabaci from Guatemala Cyprus Israel and Sudan and Professor J W Davies for reading this manuscript

The work was carried out under the Plant Pests (Great Britain) Order 1987 licence Ndeg PHF 1185A56(1l0)

References Bartlett A C Gawel N J 1993 Determining whitefly species Science (Technical comments) 2611333-shy

1334 Bedford I D Briddon R W Jones P Alkaff N Markham P G 1994 Differentiation of three whiteftyshy

transmitted gemini viruses from the Republic of Yemen European Journal of Plant Pathology (In press)

Bedford I D Briddon R W Markham P G Brown J K Rosell R C 1992 Bemisia tabaci - Biotype characterisation and the threat of this whitefly species to agriculture Proceedings 1992 British Crop Protection Conference - Pests and Diseases 31235-1240

Bedford I D Briddon R W Markham P G Brown J K Rosell R C 1993 A new species of Bemisia or biotype of Bemisia tabaci (Genn) as a future pest of European agriculture Plant Health and the European Single Market BCPC Monograph 54381-386

Bethke J A Paine T D Nuessly G S 1991 Comparative biology morphometrics and development of 2 populations of Bemisia tabaci (Homoptera Aleyrodidae) on cotton and poinsettia Annals of the Entomological Society of America 84401

Bock K R Guthrie E J Meredith G 1978 Distribution host range properties and purification of cassava latent virus a geminivirus Annals of Applied Biology 90361-367

Brown J K 1990 An update on the whitefly-transmitted geminiviruses in the Americas and the Caribbean Basin FAO Bulletin 395-23

Brown J K Bird J 1992 Whitefly-transmitted gemini viruses and associated disorders in the Americas and the Caribbean Basin Plant Disease 76220-225

Brown J K Costa H S Laemmlen F 1992a First incidence of whitefly-associated squash silverleaf disorder of Cucurbita in Arizona and of white-stem streaking disorder of Brassica species in Arizona and California Plant Disease 76426 (Abstract)

Brown J K Coats S A Bedford I D Markham P G Bird J 1992b Biotypical characterisation of Bemisia tabaci populations based on esterase profiles DNA fingerprinting virus transmission and bioassay to key host plant species Phytopathology 82 1104

Burban C Fishpool L D C Fargette D Thouvenel J C 1992 Host-associated biotypes within West African populations of the whitefly Bemisia tabaci (Genn) (Hom Aleyrodidae) Journal ofApplied Entomology 113416-423

324 I D BEDFORD E1 AL

Byrne F J Devonshire A L 1993 Insensitive acetylcholinesterase and esterase polymorphism in susceptible and resistant populations of the tobacco whitefly Bemisia tabaci (Genn) Pesticide Biochemistry and Physiology 4534-42

Byrne F J Cahill M Denholm I Devonshire A L 1994 A biochemical and toxicological study of the role of insensitive acetylcholinesterase in organophosphorus resistant Bemisia tabaci from Israel Bulletin of Entomological Research 84 179--184

Campbell B C Duffus J E Baumann P 1993 Determining whitefly species Science (Technical comments) 261 1333

Cohen S Duffus J E Liu H Y 1992 A new Bemisia tabaci biotype in the southwestern United States and its role in silverleaf of squash and transmission of lettuce infectious yellows virus Phytopathology 8286-90

Costa H S Brown J K 1991 Variation in biological characteristics and esterase patterns among populations of Bemisia tabaci and the association of one population with silverleaf induction Entomologia experimentalis et applicata 61 211

Costa H S Russell L M 1975 Failure of Bemisia tabaci to breed on cassava plants in Brazil (Homoptera AJeyrodidae) Ciencia e Cultura (Sao Paulo) 27388-390

Costa H S Brown J K Sivasupramaniam S Bird J 1993 Regional distribution insecticide resistance and reciprocal crosses between A and B biotypes of Bemisia tabaci Genn Insect Science and its Application 14 127-138

Costa H S Ullman D E Johnson M W Tabashnik B E 1993 Association between Bemisia tabaci density and reduced growth yellowing and stem blanching of lettuce and kai choy Plant Disease 77969--972

Frischmuth T Zimmat G Jeske H 1990 The nucleotide sequence of abutilon mosaic virus reveals prokaryotic as well as eukaryotic features Virology 178461-468

Gill R J 1990 The morphology of whiteflies In Whiteflies their Bionomics Pest Status and Manageshyment Ch 2 pp 13-44 Hampshire UK Intercept Ltd

Mansoor S Bedford I Pinner M Stanley J Markham P G 1993 A whitefly-transmitted geminivirus associated with cotton leaf curl disease in Pakistan Pakistan Journal of Botany 25105-107

Martin J H 1987 An identification guide to common whitefly pest species of the world (Homoptera Aleyrodidae) Tropical Pest management 33(4)298-322

Maule A J Hull R Donson J 1983 The application of spot hybridisation to the detection of DNA and RNA viruses in plant tissues Journal of Virological Methods 6215-224

Maynard D N CantlitTe D J 1989 Squash silverleaf and tomato irregular ripening New vegetable disorders in Florida Vegetable Crops Fact Sheet VC-37 Florida Cooperative Extension Service University of Florida GainsviiJe

Mound L A Halsey S H 1978 Whitefly of the world A systematic catalogue of the Aleyrodidae (Homoptera) with host plant and natural enemy data New York Wiley 340 pp

Nour M A Nour J J 1964 Leaf curl viruses in the Sudan The Empire COllon Growing Review 4127shy37

Paris H S Stoffella P J Powell C A 1993 Sweetpotato whitefly drought stress and leaf silvering of squash HortScience 28157-158

Perring T M Farrar C A Cooper A D Bellows T S 1993b Determining whitefly species Science (Technical comments) 261 1334--1335

Perring T M Cooper A D Rodriguez R J Farrar C A Bellows T S 1993tl Identification of a whitefly species by genomic and behavioural studies Science 25974--77

Rigby P W J Dieckmann M Rhodes C Berg P 1977 Labelling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase Journal of Molecular Biology 113237shy251

Simons J N Stoffella P J Shuler K D Raid R N 1988 Silverleaf of squash in south Florida Proceedings of the Florida State Horticultural Society 101397-399

Stanley J Gay M R 1983 Nucleotide sequence of cassava latent virus DNA Nature 301260shy262

Stanley J Townsend R Curson S J 1985 Pseudorecombinants between cloned DNAs of two isolates of cassava latent virus Journal of General Virology 66 1055


Von Arnim A Stanley J 1992 Determinants of tomato golden mosaic virus symptom development located on DNA B Virology 186286-293

Villevieille M Lecoq H 1992 Largenta de la courgette und maladie nouvelle en France liee a un Aleurode Phytoma - La Defense des vegetaux 44035-36

Wool D Greenberg S 1990 Esterase activities in whiteflies (Bemisia tabaci) in Israel in relation to insecticide resistance Entomologia experimentalis et applicata 57 251

Yokoml R K Hoelmer K A Osbourne L S 1990 Relationships between the sweetpotato whitefly and the squash silver leaf disorder Phytopathology 10895-900

(Received 10 December 1993)


Introduction

Bemisia tabaci (Gennadius) the cotton tobacco or sweetpotato whitefly has recently become very important to world agriculture as a pest and as a virus vector In many of the warmer parts of the world populations are increasing and severe crop losses have been experienced in some areas Evidence has accumulated that populations have different biological characteristics and that some recent devastating outbreaks of B tabaci parshyticularly in areas where it was previously unimportant are linked to the appearance of a new biotype strain or possibly species of B tabaci

B tabaci is indigenous to the tropical and sub-tropical regions of the world and has long been a pest and virus vector associated with certain crop and weed species It was previously reported to have a composite host range of around 300 species within 63 families (Mound amp Halsey 1978) and caused localised losses to crops such as cassava in Africa (Bock Guthrie amp Meredith 1978) and cotton in the Sudan (Nour amp Nour 1964) through feeding damage and plant virus transmission Over the past decade however severe outbreaks of B tabaci have become more frequent and crops colonised by B tabaci have suffered major losses with yield reductions ranging from 20 to 100 (Brown amp Bird 1992) Watermelon crops in the Yemen have been decimated since 1989 (Bedford et al 1994) and the southern states of North America experienced an estimated $500 million loss in the 1991 cotton and vegetable harvest (Perring et al 1993a) The cotton crop in Pakistan is likewise threatened by a whitefly-transmitted virus (Mansoor et al 1993) In Mexico the Caribbean Basin and Central America cotton melon tobacco and tomato crops have been subjected to losses as a result of whitefly feeding and whitefly-transmitted virus infection (Brown amp Bird 1992) Previously B tabaci had been a sporadic controllable pest in these areas New presently uncharacterised whitefly-transmitted viruses have occurred in some crops (Brown 1990 Brown amp Bird 1992) and phytotoxic disorders such as squash silverleaf (SSL) (Yokomi Hoelmer amp Osbourne 1990) pumpkin white stems (Costa amp Brown 1991) white streaking in cole crops (Brown Costa amp Laemmlen 1992a) uneven ripening of tomato (Maynard amp Cantliffe 1989) and reduced growth yellowing and stem blanching in lettuce and kai choy (Costa Ullman Johnson amp Tabashnik 1993) have been observed To-date only certain populations of B tabaci are known to induce these phytotoxic responses and they are linked to some of the most agriculturally devastating outbreaks worldwide Symptoms similar to squash silverleaf were first reported in Israel in the 1960s (Paris Stoffella amp Powell 1993) and more recently in Florida (Maynard amp Cantliffe 1989 Simons Stoffella Shuler amp Raid 1988) Arizona (Brown et al 1992a) California (Cohen Duffus amp Liu 1992) and southern France (Villevieille amp Lecoq 1992) These same populations have been reported to have an increased fecundity (Bethke Paine amp Nuessly 1991) a strong resistance to carbamate and organophosphorus based pesticides (Byrne amp Devonshire 1993 Costa Brown Sivshyasupramaniam amp Bird 1993) and an extremely broad host range compared to other populations of B tabaci studied so far (Costa amp Russell 1975 Burban Fishpool Fargette amp Thouvenel 1992 Wool amp Greenberg 1990) Studies of non-specific esterases have produced a diagnostic test to identify the populations of B tabaci that induce phytotoxic disorders (Costa amp Brown 1991 Bedford et al 1992 1993 J K Brown S A Coats I D Bedford and P G Markham unpublished Byrne amp Devonshire 1993 Byrne Cahill Denholm amp Devonshire 1994) They all exhibit a highly polymorphic esterase banding pattern and have been tentatively termed the B biotype Two B tabaci populations which exhibited the characteristic B biotype esterase band also showed another distinct esterase band and have been termed B2 biotypes (J K Brown S A Coats I D Bedford and P G Markham unpublished) B biotype B tabaci have been identified within many areas of the horticultural industry even in northern Europe and the global spread of this insect is























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c ~

-

) shy

Fl-

1 F

ou

rth

1ns

t~lr

pUp

(lrl

Um

Irtg

e~ o

( B

(

thaC

i co

lon

y F

J s

ho

win

g d

orsa

l e

-Iac

m

d sp

ine

h

cn c

uJt

ured

on

hir

~ute J

eilmiddot

e

of Al~lfll

ol1

PfC

fltU

(a

)

dnd

no d

orsa

l ~t

l

IC l

ind

Sp

ll1t

~

whc

11 t

u lr

ule

d o

n t

he gla

brou

~ le

Jyes

of

cass

ava

lHa

mh

o(

rsc

ueJ

ua (

b)













w ~

Tab

le 6

A

bili

ty o

fB t

abac

i col

onie

s to

tra

nsm

it v

ario

us g

emin

ivir

uses

sho

win

g ge

ogra

phic

sou

rce

ofb

oth

whi

tefli

es a

nd v

irus

es

and

whi

tefly

bio

type

as

defi

ned

by e

ster

ase

band

ing

patt

erns

(B

edfo

rd e

t al

19

92)

CL

CV

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

S

LC

V

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

BC

MoV

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

0

S

GM

V-H

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

= tTl

SG

MV

-CR

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

0

TY

LC

VmiddotY

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

T1

0

TL

CV

-Y

+

+

+

+

+

+

+

+

+

+

-+ +

+

+

+

+

a 0

WC

SV

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

trJ

PY

VV

o

j

AC

MV

-N

+

+

+

+

+

+

+

+

+

) ~

BL

V

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

SY

VV

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

A

GM

V

+

+

+

+

+

+

+

+

+

+

+

+

+

+

HY

VM

V4(

j A

bMV

(Ij

Bio

type

B

B

B

A

G

D

B

E

L

B

B

B

M

B

B

K

H

+ =

suc

cess

fultr

ansm

issi

oD

-=

neg

ativ

e tr

ansm

issi

on

bull =

no

data

V

irus

ori

gina

ting

fro

m

-

he A

mer

icas

-

he M

iddl

e E

ast

-A

fric

a

-Eu

rop

e

-Far

Eas

t







Mating studies


Discussion


























































Results

Morphology


M orphometrics






00

w

m

]

~

c

c ~

-

) shy

Fl-

1 F

ou

rth

1ns

t~lr

pUp

(lrl

Um

Irtg

e~ o

( B

(

thaC

i co

lon

y F

J s

ho

win

g d

orsa

l e

-Iac

m

d sp

ine

h

cn c

uJt

ured

on

hir

~ute J

eilmiddot

e

of Al~lfll

ol1

PfC

fltU

(a

)

dnd

no d

orsa

l ~t

l

IC l

ind

Sp

ll1t

~

whc

11 t

u lr

ule

d o

n t

he gla

brou

~ le

Jyes

of

cass

ava

lHa

mh

o(

rsc

ueJ

ua (

b)













w ~

Tab

le 6

A

bili

ty o

fB t

abac

i col

onie

s to

tra

nsm

it v

ario

us g

emin

ivir

uses

sho

win

g ge

ogra

phic

sou

rce

ofb

oth

whi

tefli

es a

nd v

irus

es

and

whi

tefly

bio

type

as

defi

ned

by e

ster

ase

band

ing

patt

erns

(B

edfo

rd e

t al

19

92)

CL

CV

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

S

LC

V

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

BC

MoV

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

0

S

GM

V-H

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

= tTl

SG

MV

-CR

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

0

TY

LC

VmiddotY

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

T1

0

TL

CV

-Y

+

+

+

+

+

+

+

+

+

+

-+ +

+

+

+

+

a 0

WC

SV

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

trJ

PY

VV

o

j

AC

MV

-N

+

+

+

+

+

+

+

+

+

) ~

BL

V

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

SY

VV

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

A

GM

V

+

+

+

+

+

+

+

+

+

+

+

+

+

+

HY

VM

V4(

j A

bMV

(Ij

Bio

type

B

B

B

A

G

D

B

E

L

B

B

B

M

B

B

K

H

+ =

suc

cess

fultr

ansm

issi

oD

-=

neg

ativ

e tr

ansm

issi

on

bull =

no

data

V

irus

ori

gina

ting

fro

m

-

he A

mer

icas

-

he M

iddl

e E

ast

-A

fric

a

-Eu

rop

e

-Far

Eas

t







Mating studies


Discussion
























































00

w

m

]

~

c

c ~

-

) shy

Fl-

1 F

ou

rth

1ns

t~lr

pUp

(lrl

Um

Irtg

e~ o

( B

(

thaC

i co

lon

y F

J s

ho

win

g d

orsa

l e

-Iac

m

d sp

ine

h

cn c

uJt

ured

on

hir

~ute J

eilmiddot

e

of Al~lfll

ol1

PfC

fltU

(a

)

dnd

no d

orsa

l ~t

l

IC l

ind

Sp

ll1t

~

whc

11 t

u lr

ule

d o

n t

he gla

brou

~ le

Jyes

of

cass

ava

lHa

mh

o(

rsc

ueJ

ua (

b)













w ~

Tab

le 6

A

bili

ty o

fB t

abac

i col

onie

s to

tra

nsm

it v

ario

us g

emin

ivir

uses

sho

win

g ge

ogra

phic

sou

rce

ofb

oth

whi

tefli

es a

nd v

irus

es

and

whi

tefly

bio

type

as

defi

ned

by e

ster

ase

band

ing

patt

erns

(B

edfo

rd e

t al

19

92)

CL

CV

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

S

LC

V

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

BC

MoV

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

0

S

GM

V-H

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

= tTl

SG

MV

-CR

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

0

TY

LC

VmiddotY

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

T1

0

TL

CV

-Y

+

+

+

+

+

+

+

+

+

+

-+ +

+

+

+

+

a 0

WC

SV

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

trJ

PY

VV

o

j

AC

MV

-N

+

+

+

+

+

+

+

+

+

) ~

BL

V

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

SY

VV

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

A

GM

V

+

+

+

+

+

+

+

+

+

+

+

+

+

+

HY

VM

V4(

j A

bMV

(Ij

Bio

type

B

B

B

A

G

D

B

E

L

B

B

B

M

B

B

K

H

+ =

suc

cess

fultr

ansm

issi

oD

-=

neg

ativ

e tr

ansm

issi

on

bull =

no

data

V

irus

ori

gina

ting

fro

m

-

he A

mer

icas

-

he M

iddl

e E

ast

-A

fric

a

-Eu

rop

e

-Far

Eas

t







Mating studies


Discussion




































































w ~

Tab

le 6

A

bili

ty o

fB t

abac

i col

onie

s to

tra

nsm

it v

ario

us g

emin

ivir

uses

sho

win

g ge

ogra

phic

sou

rce

ofb

oth

whi

tefli

es a

nd v

irus

es

and

whi

tefly

bio

type

as

defi

ned

by e

ster

ase

band

ing

patt

erns

(B

edfo

rd e

t al

19

92)

CL

CV

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

S

LC

V

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

BC

MoV

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

0

S

GM

V-H

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

= tTl

SG

MV

-CR

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

0

TY

LC

VmiddotY

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

T1

0

TL

CV

-Y

+

+

+

+

+

+

+

+

+

+

-+ +

+

+

+

+

a 0

WC

SV

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

trJ

PY

VV

o

j

AC

MV

-N

+

+

+

+

+

+

+

+

+

) ~

BL

V

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

SY

VV

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

A

GM

V

+

+

+

+

+

+

+

+

+

+

+

+

+

+

HY

VM

V4(

j A

bMV

(Ij

Bio

type

B

B

B

A

G

D

B

E

L

B

B

B

M

B

B

K

H

+ =

suc

cess

fultr

ansm

issi

oD

-=

neg

ativ

e tr

ansm

issi

on

bull =

no

data

V

irus

ori

gina

ting

fro

m

-

he A

mer

icas

-

he M

iddl

e E

ast

-A

fric

a

-Eu

rop

e

-Far

Eas

t







Mating studies


Discussion






























































Mating studies


Discussion
























































Printed in Great B,iJain Geminivirus transmission and...

Documents

Transcript of Printed in Great B,iJain Geminivirus transmission and...