TRANSMISSION OF PLANT DISEASES BY

George N. Agrios University of Florida Gainesville, Florida, USA

Plant diseases appear as pathogenic organism (some fungi, some necrotic areas, usually spots of various bacteria, some nematodes, all protozoa shapes and sizes on leaves, shoots, causing disease in plants, and many and fruit; as cankers on stems; as ) depends on for transmission blights, wilts, and necrosis of shoots, from one plant to another, and on which branches and entire plants; as some pathogens depend on for survival discolorations, malformations, galls, and (Fig. 1). root rots, etc. Regardless of their The importance of appearance, plant diseases interfere transmission of plant diseases has with one or more of the physiological generally been overlooked and greatly functions of the plant (absorption and underestimated. Many plant diseases in translocation of water and nutrients from the field or in harvested plant produce the soil, photosynthesis, etc.), and become much more serious and thereby reduce the ability of the plant to damaging in the presence of specific or grow and produce the product for which non-specific insect vectors that spread it is cultivated. Plant diseases are the pathogen to new hosts. Many generally caused by microscopic insects facilitate the entry of a pathogen organisms such as fungi, bacteria, into its host through the wounds the nematodes, protozoa, and parasitic insects make on aboveground or green algae, that penetrate, infect, and belowground plant organs. In some feed off one or more types of host cases, insects help the survival of the plants; submicroscopic organisms such pathogen by allowing it to overseason in as viruses and viroids that enter, infect, the body of the insect. Finally, in many spread systemically and affect the cases, insects make possible the growth of their host plants; parasitic existence of a plant disease by higher plants which range from about an obtaining, carrying, and delivering into inch to several feet in size and penetrate host plants pathogens that, in the and feed off their host plants. Plant absence of the insect, would have been diseases are also caused by abiotic, unable to spread, and thereby unable to environmental factors such as nutrient cause disease. It is offered as a guess deficiencies, extremes in temperature that 30-40% of the damage and losses and soil moisture, etc. that affect the caused by plant diseases is due to the normal growth and survival of affected direct or indirect effects of transmission plants. and facilitation of pathogens by insects. Of the aforementioned causes of Insects and related organisms, disease, many of the microscopic such as mites, are frequently involved in organisms and of the viruses are the transmission of plant pathogens transmitted by insects either accidentally from one plant organ, or one plant, to (several fungi and bacteria) or by a another on which then the pathogens specific insect vector on which the cause disease. Equally important is that insects can and do transmit pathogens pathogen with the plant sap they eat. among plants from one field to another, Subsequently, the pathogen circulates in many cases even when the fields are through the body of the insect until, with several to many miles apart. Almost all or without further multiplication in the types of pathogens, that is, fungi, insect, the pathogen reaches the bacteria, viruses, nematodes, and salivary glands and the mouthparts of protozoa, can be transmitted by insects. the insect through which it is injected Insects transmit pathogens, such as into the next plant on which the insect many fungi and bacteria, mostly feeds (Fig. 3). externally on their legs, mouthparts, and bodies. Almost all plant pathogenic Role of insects in bacterial diseases viruses, all phytoplasmas, xylem- and of plants phloem-inhabiting fungi and bacteria, In most plant diseases caused by some protozoa, and some nematodes plant pathogenic bacteria (especially in are also transmitted by insects, and they those that cause spots, cankers, blights, are usually carried by the insect galls, or soft rots, bacteria), which are internally. The insects that transmit fungi produced within or between plant cells, and bacteria externally on their bodies escape to the surface of their host and legs belong to many orders of plants as droplets or masses of sticky insects. On the contrary, the insects that exudates (ooze). The bacteria exudates transmit the other pathogens listed are released through cracks or wounds above internally are very specialized in the infected area, or through natural and specific for the pathogen they openings such as stomata, transmit and belong to a certain species nectarthodes, hydathodes, and or of insects (Fig. 2). sometimes through lenticells, present in Insects transmit pathogens in the infected area. Such bacteria are three main ways. 1) Many insects then likely to stick on the legs and transmit bacteria and fungal spores bodies of all sorts of insects, such as passively by feeding in or walking , aphids, ants, beetles, whiteflies, through an infected plant area that has etc., that land on the plant and come in on its surface plant pathogenic bacteria contact with the bacterial exudates. or fungal spores as a result of the Many of these insects are actually infection. The bacteria and spores are attracted by the sugars contained in the often sticky, cling to the insect as it bacterial exudate and feed on it, thereby moves about, and are carried by it to further smearing their body and other plants or parts of the same plant mouthparts with the bacteria-containing where they may start a new infection. 2) exudate. When such bacteria-smeared Some insects transmit certain bacteria, insects move to other parts of the plant fungi, and viruses by feeding on infected or to other susceptible host plants, they plant tissues and carrying the pathogen carry on their body numerous bacteria. If on their mouthparts as they visit and the insects happen to land on a fresh feed on other plants or plant parts. 3) wound or on an open natural opening, Several insects transmit specific viruses, and there is enough moisture on the phytoplasmas, protozoa, nematodes, plant surface, the bacteria may multiply, and xylem- and phloem-inhabiting move into the plant, and begin a new bacteria by ingesting (sucking) the infection. The same happens if the insects happen to create a fresh wound Bacterial soft rots on the plant. Bacterial soft rots cause The type of insect transmission of tremendous losses worldwide, bacteria is probably quite common and particularly in the warmer climates and widespread among bacterial diseases of the tropics. They are caused primarily plants, but it is passive and haphazard, by the bacterium Erwinia carotovora pv. depending a great deal on the carotovora, to some extent by availability of wounds or moisture on the Pseudomonas fluorescens and Ps. plant surface. In any case, there are few chrysanthemi, and, occasionally, by data on how frequently such species of Bacillus and Clostridium. The transmission occurs, and many last two genera of bacteria cause rotting conclusions about it are the result of of potatoes and of cut fleshy leaves in conjecture. A further point that has been storage while Pseudomonas fluorescens made is that insects which, whether and Ps. chrysanthemi cause soft rots of above or below ground, wound the host many fleshy fruits and fleshy plant organs (roots, shoots, fruit, etc.) by vegetables. The species E. c. pv. feeding or by ovipositing in them, carotovora causes the vast majority of increase the probability of transmission soft rots on fleshy plant organs of any of plant pathogenic bacteria. This occurs type (leave, blossoms, fruit, stems, or because such insects place the roots), especially in storage and under bacteria, with their mouthparts or the cover or in plastic bags. Affected fleshy ovipositor, in or around wounded plant fruits are, for example, strawberries and cells, where they are surrounded by a other berries, cantaloupes, peaches, suspension of nutrients (plant cell sap) pears, etc.; vegetables, for example, in the absence of active host defenses tomatoes, potatoes, spinach, celery, and where they can multiply rapidly and onions, cabbage, etc.; and ornamentals, subsequently infect adjacent healthy for example, cyclamen, iris, lily, etc. tissues. Nearly all fleshy vegetables are subject Numerous plant diseases could to bacterial soft rots. The soft rot be listed among those in which bacteria bacteria enter the plant organ through a are spread by insects passively as wound, sometimes in the field but more described above, for example, the commonly during storage, and there bacterial bean blights, of apple they multiply rapidly, secrete enzymes and pear, citrus canker, cotton boll rot, that separate the cells from each other crown gal, bacterial spot and canker of and macerate the plant cell walls, which stone fruits, etc. In several bacterial causes the tissues to become soft and diseases, however, the causal to rot. In many cases, these bacteria are bacterium has developed a special accompanied in the rotting tissues by symbiotic relationship with one or a few other saprophytic bacteria that further specific types of insects and depends a degrade the softened plant tissue and great deal on these insects for its cause it to give off a foul odor. In all spread from infected to healthy host cases, rotting tissues become soft and plants. Some of the better known watery, and slimy masses of bacteria bacterium - insect associations are ooze out from cracks in the tissues. described briefly below. The soft rotting bacteria survive in infected fleshy organs in storage and in the field, in plant debris, in infected Otitidae), the seedcorn maggot, and the roots and other plant parts of their hosts, onion bulb , Eumerus strigatus in ponds and streams from where (Fallen) (Diptera: Syrphidae) and the irrigation water is obtained, and to some soft rot of onion; and the iris borer, extent in the soil and in the pupae of onusta (Grote) several insects. The seedcorn maggot, (: ) and soft rot of platura (Meigen) (Diptera: iris. ), was shown to play an The exact relationship between important role in the dissemination and soft rot in each host and each specific development of bacterial soft rot in insect found to possibly be involved in potatoes both in storage and in the field. the transmission of soft rot bacteria from The soft rot bacteria are usually one organ or plant to another is not introduced into a field on infected clear. There is little doubt, however, that or contaminated seed pieces but they insect transmission of soft rot bacteria can also live in all stages of the insect, does occur, that insects help introduce including the pupae, and there they may the bacteria into wounds they open, and survive cold or dry weather conditions. that the presence of insects in soft- The insect larvae become contaminated rotting tissues inhibits the defense with the bacteria as they feed in, or reaction of the plants against the crawl about on, infected seed pieces; bacteria. The insects also, by carrying they also carry the bacteria to healthy the soft rot bacteria internally in their plants and there they deposit them into bodies, help the bacteria survive wounds they create. Even when the adverse environmental conditions. On plants or storage organs are resistant to the other hand, the bacteria seem to soft rot bacteria and can normally stop help their insect vectors by preparing for the advance of the bacteria by them a more nutritive substrate through developing a barrier of cork layers, the partial maceration of the host plant maggots destroy the cork layers as fast tissues. as they are formed and the soft rot continues to spread. Some other related Bacterial wilts of plants flies, for example, the bean seed In several bacterial diseases of maggot Delia florilega (Zetterstedt), plants, the bacteria enter the xylem Drosophila busckii Coquillett (Diptera: conductive system of the plant and there ), and probably others, they move, multiply, and clog up the seem to have analogous relationship to vessels. The clogging of the xylem the soft rot of potato and other fleshy vessels is further increased by organs. It has also been shown that substances released from cell walls by several other flies have similar bacterial enzymes and interferes with relationships with soft rot bacteria and the translocation of water through the the host plants on which they prefer to stems to the shoots of the plant. As a feed. Such relationships, for example, result of insufficient water, the leaves exist between the cabbage maggot, and shoots loose turgor, wilt, and Delia radicium (Linnaeus) and soft rot in eventually turn brown and die. In some the Brassicaceae; the onion maggot, bacterial wilts, the bacteria destroy and Delia antiqua (Meigen), the onion black dissolve parts of the xylem walls and fly, Tritoxa flexa (Weidman) (Diptera: move into the adjacent tissues where they form pockets full of bacteria from depends on these two vectors for its which the bacteria ooze out onto the transmission to and inoculation of new plant surface through cracks or natural plants. In the spring, striped cucumber openings. In other bacterial wilts, the beetles and, to a lesser extent, spotted bacteria remain confined in the xylem cucumber beetles, that carry bacteria, and do not reach the plant surface until feed and cause wounds on the leaves of the plant is killed by the disease. cucurbit plants. The insects deposit The wilt-causing bacteria bacteria in the wounds through their overwinter in plant debris in the soil, in feces and the bacteria enter the the seed, in vegetative propagative wounded xylem vessels in which they material, and in some cases, in their multiply rapidly and through which they insect vector. They enter plants through move to all parts of the plant. In the wounds, and they spread from plant to xylem, the bacteria excrete plant through the soil, through tools and polysaccharides, secrete enzymes that direct handling of plants, or through break down some of the cell wall insect vectors. The most important substances, and induce xylem bacterial wilts in which insects play a parenchyma cells to produce tyloses in significant role in the transmission of the the xylem. All of them together form gels bacteria from plant to plant are or gums that clog the vessels, especially described briefly below. at their end walls, thereby reducing the Bacterial wilt of cucurbits - upward flow of water in the xylem by up Bacterial wilt of cucurbits has been to 80% and causing the leaves and reported from most developed countries vines to wilt. Beetles feeding on infected but it probably occurs throughout the cucurbit plants pick up bacteria on their world. It affects many species of mouthparts and when they feed onto cucurbits, including cucumber, healthy plants they deposit the bacteria muskmelon, squash, and pumpkin. in the new wounds they have made. Watermelon is resistant or immune to Thus, the bacteria start a new infection. bacterial wilt. Diseased plants develop a Each contaminated beetle can infect sudden wilting of their foliage and vines several healthy plants after one feeding and eventually die. Diseased squash on an infected plant. It appears that a fruit develops a slimy rot in storage. relatively small percentage of beetles Losses from bacterial wilt vary from an become carriers of the bacteria through occasional wilted plant to destruction of the winter. Spotted cucumber beetles 75 to 95% of the crop (Fig. 4). transmit the wilt bacteria rather late in Bacterial wilt of cucurbits is the season, therefore they are caused by the bacterium Erwinia considered less important vectors of this tracheiphila. The bacterium survives in disease than the striped cucumber infected plant debris for a few weeks but beetles. it survives over winter in the intestines of Bacterial wilt of corn - This its two insect vectors, the striped disease is also known as Stewart’s wilt cucumber beetle (Acalymma vittatum of corn. It is caused by the bacterium [Fabricius]) and the spotted cucumber Pantoea (formerly Erwinia) stewartii. It beetle (Diabrotica undecimpunctata occurs in North and Central America Mannerheim [Coleoptera: and also in Europe and China. It is more Chrysomelidae]). The bacterium severe in the northern states. The bacterium invades the vascular tissues overwinter. The corn flea beetles but it also spreads into other tissues. overwinter as adults in the upper 2-3 cm When sweet corn plants are affected at of soil in grass sod. They are rather the seedling stage they may wilt rapidly sensitive to low temperatures, however. and may die, or they develop pale green In mild winters, when the sums of mean wavy streaks on the leaves, become temperatures for December, January, stunted, wilt, and may also die. If and February are above 3 to 4 C, large infected plants survive, they often tassel numbers of beetles survive. When the prematurely, the tassels become soil warms up to about 17 to 20 C, they bleached and may die, and produce begin to feed on corn seedlings, which deformed ears. Bacteria also enter the they infect with bacteria. Following mild stalk pith, which they macerate in places winters, bacterial wilt of corn is spread near the soil line and form cavities. rapidly by corn flea beetles, and corn From there the bacteria invade all losses can be quite severe. During cold vascular tissues and spread throughout winters that average temperatures the plant. Field corn is more resistant to below 0 C, many of the beetles do not early infection but becomes more survive and the incidence and spread of severely infected later in the season. bacterial wilt of corn the following spring Some hybrids are susceptible and their and summer are quite limited. symptoms parallel those of sweet corn. Southern bacterial wilt of Later infections, after tasseling, produce solanaceous and other crops - This irregular streaks on the leaves that vascular wilt is caused by the bacterium originate at feeding points of the corn Ralstonia solanacearum. It occurs in the flea beetle, Chaetocnema pulicaria warmer regions around the world and is Melsheimer. The corn wilt bacteria are particularly severe in the tropics. It is also transmitted by the toothed flea known by different names in different beetle (Chaetocnema denticulata Illiger), hosts, for example, southern wilt or the spotted cucumber beetle (Diabrotica brown rot in potato and tomato, undecimpunctata howarti Barber), and Granville wilt in tobacco, and Moko by the larvae of the seed corn maggot disease in banana. Insects, primarily (Delia platura Meigen), wheat wireworm bees (Trigona corvine Cockerell, (Agriotes mancus Say), and the May Hymenoptera: Apidae), wasps (Polybia beetle (Phyllophaga sp.). It appears, spp., Hymenoptera: Vespidae), and flies however, that overwintering and spread (Drosophila spp., Diptera: of the bacteria in the field is carried out Drosophilidae) have been implicated as primarily by the corn flea beetle. vectors. Because these and other These beetles cause direct insects visit infected stem wounds and damage to corn leaves and seedlings natural abscission sites oozing out but their main damage comes from bacteria, they are considered as playing harboring and transmitting the bacteria a role in the transmission of the bacteria from plant to plant. The beetles pick up to natural infection courts and in the bacteria when they feed on infected providing wounds for bacterial entry, but corn plants. The bacteria survive in the their importance as vectors has not digestive tract of the insect as long as been documented. the latter lives. The insects are also the Fire blight of pears, apples and main place where the bacteria other rosaceous plants - The disease is caused by the bacterium Erwinia beetles, flies, and ants, have been amylovora. Fire blight occurs in North shown to visit oozing cankers and America, Europe and countries healthy blossoms, although bees and surrounding the Mediterranean Sea, and wasps seem not to visit oozing cankers in New Zealand. It continues, however, routinely. Insects smeared with bacteria to spread into new countries. Fire blight oozing out at cankers carry the bacteria is the most devastating diseases to young shoots where they deposit affecting rosaceous plants. The them in existing wounds or in fresh symptoms consist of infected blossoms wounds they make upon feeding, or in and young shoots becoming discolored the nectar of the flowers. Once the fire and water-soaked, then being killed blight bacteria are transmitted to rapidly and appearing brown to black as blossoms by rain or insects, they enter though scorched by fire. The disease the flower tissues through nectarthodes spreads rapidly into larger twigs and or wounds, multiply rapidly in them, and branches, which it also kills, and parts of ooze out of them and commingle with or entire trees may be killed. At the base the nectar in the flower. The same kinds of twig or branch infections, cankers of insects apparently can transmit fire develop at the margins of which the blight bacteria from infected to healthy bacteria overwinter. Fruit also become flowers but flower to flower transmission infected and ooze droplets of bacteria. of fire blight bacteria is carried out so The bacteria kill and macerate the much more efficiently by pollinating contents of primarily parenchyma cells insects, namely bees, that the on flowers and in the bark of young contribution of other insects to that type shoots and twigs, but as they destroy of transmission seems to be relatively these cells they move on mass in the insignificant. As honeybees, wild bees, bark. The bacteria also enter the phloem bumblebees, wasps, and other insects and xylem vessels through which they visit pear, apple, and other flowers may move over relatively short infected with fire blight bacteria, their distances. mouthparts, legs, and other body parts The fire blight bacteria overwinter become smeared with the bacteria in at the margins of cankers of twigs and the nectar. The insects then carry the branches. In the spring, the bacteria bacteria and deposit them in the nectar around cankers multiply and their of healthy flowers they visit and there byproducts absorb water and build up the bacteria start new infections. The internal pressure. This results in bacteria, however, do not survive on or droplets of liquid containing masses of in the insects for more than a few days fire blight bacteria oozing out of the and do not appear to overwinter in cankers. The bacteria in the ooze are association with the insects. disseminated by splashing rain and also Olive knot - Olive knot is caused by flying and crawling insects, several of by the bacterium Pseudomonas which are attracted to the bacterial savastanoi. It occurs in the ooze, and their legs, bodies, and Mediterranean region, in California, and mouthparts become smeared with probably the other parts of the world bacteria. More than 200 species where olive trees grow. The disease belonging to many insect groups, occurs as rough galls of varying sizes including aphids, , psyllids, developing on leaves, branches, roots, on leaf and fruit petioles, and on wounds the insect for survival of the larvae and in tree branches and trunks. Sometimes for development of adults. the galls are so numerous on twigs that the twigs decline and may die back. The Insect transmission of xylem- galls are the result of growth regulators inhabiting bacteria being produced by the bacteria, which Quite a few important bacterial grow and multiply in the intercellular diseases of plants, primarily trees, are spaces of the outer cells of the galls. In caused by the fastidious bacterium California, the bacteria are spread by Xylella fastidiosa. These bacteria inhabit running and splashing rain water that the xylem of their host plants and are carries the bacteria to existing wounds, rather difficult to isolate and to grow on pruning wounds, and leaf scars. In other the usual culture media. The diseases parts of the world, however, such as the they cause differ from the vascular wilts Mediterranean region, the olive knot caused by conventional bacteria in that bacteria are also spread by the olive fly instead of wilt they cause infected plants or olive fruit fly, Bactrocera (formerly to decline, some of their twigs to die Dacus) oleae (Gmelin) (Diptera: back, and in some cases the whole Tephritidae), which is the most plant to die. The xylem-inhabiting destructive pest of olive in its own right. fastidious bacteria are transmitted in The bacterium and the olive fly nature only by xylem-feeding insects, have developed a close symbiotic such as sharpshooter leafhoppers relationship that contributes to the (Cicadellidae: Cicadellinae) and transmission of the olive knot bacteria spittlebugs (Cercopidae). Xylella from tree to tree. The bacteria are bacteria seem to be distributed in carried by all stages (larvae, pupae, and tropical and semitropical areas adults) of the olive fly. The adult olive worldwide. Among the most important flies, and related fly species, have diseases caused by Xylella are Pierce’s specialized structures along their disease of grape and citrus variegated digestive tract that are filled with chlorosis. Other diseases caused by bacteria. There is even a connection of xylem-inhabiting bacteria include phony the digestive tract with the oviduct that peach, plum leaf scald, almond leaf insures contamination of the eggs scorch, bacterial leaf scorch of coffee, before oviposition. Transmission of the oak leaf scorch, and leaf scorch bacteria by the insect takes place during diseases of oleander, pear, maple, feeding and oviposition into olive mulberry, elm, sycamore, and tissues. The bacteria actually penetrate miscellaneous ornamentals, as well as the egg through the micropyle, thereby the alfalfa dwarf disease (Fig. 5). ensuring that when the larvae hatch Pierce’s disease of grape - they are contaminated with the bacteria. Pierce’s disease is a devastating It appears that while the olive fly plays a disease of European-type grapevines significant role in the transmission of the (Vitis vinifera). It is caused by the xylem- olive knot bacteria, the bacteria inhabiting bacterium Xylella fastidiosa. It contribute to the insect by hydrolyzing occurs in the Southern United States proteins and making available to the and in California, in Central America, insect certain amino acids needed by and parts of northwestern South America. The presence of Pierce’s disease in an area precludes the transmitted from plant to plant through production of European-type grapes in vegetative propagation, such as that area but some muscadine grapes cuttings, budding, and grafting, and by and hybrids of European grapes with one or more of several closely related American wild grapes are tolerant or insects. The known vectors of Xylella resistant to Pierce’s disease. The fastidiosa are sharpshooter leafhoppers Pierce’s disease bacterium moves and (family Cicadellidae, subfamily multiplies in the water-conducting Cicadellinae) or spittlebugs (family (xylem) vessels of shoots and leaves, Cercopidae). It is possible that other or some of which become filled with all sucking insects that feed on xylem bacteria and reduce the flow of water sap, for example, the cicadas (family through them. Leaves beyond such Cicadidae), are also vectors of Xylella blocked vessels become stressed from fastidiosa. In California, there are at lack of sufficient water and develop least four important sharpshooter yellowing and then drying or scorching vectors of Xylella: The blue- along their margins. During the summer, green (Graphocephala atropunctata), the scorching continues to expand the green (Draeculacephala minerva), towards the center of the leaf, while the red-headed (Carneocephala some or the entire grape clusters begin fulgida), and the glassy-winged to wilt and dry up. Scorched leaves fall (Homalodisca coagulata) sharpshooters. off leaving their petioles still attached to The vectors may be different in other the vine, while the vines mature parts of the world. All vector insects unevenly and have patches of brown acquire the bacteria when they feed on (mature) and green bark. In the infected plants. Ingested bacteria seem following season(s), affected grapevines to adhere to the walls of the foregut of show delayed growth and stunting. The the insect and when the insect moves to leaves and vines repeat the symptoms and feeds on the next healthy plant, the of the first year and both, the top of the insect transmits the bacteria into the plant as well as the root system, decline xylem vessels of that plant where they and die back. multiply and cause a new infection. The bacterium that causes Once a vector acquires bacteria from a Pierce’s disease of grape is Xylella diseased plant, it remains infective fastidiosa. The bacterium apparently indefinitely. When, however, infective consists of various host specific strains. insects shed their external skeleton by The strain that causes Pierce’s disease molting, they loose the bacteria and of grape also causes alfalfa dwarf must feed on a diseased plant again disease and almond leaf scorch. before they can transmit the bacteria to Apparently related but different strains healthy plants. of the bacterium cause citrus variegation chlorosis, the other related leaf scorch Insect transmission of phloem- diseases of fruit and forest trees and of inhabiting bacteria ornamental trees and shrubs. The At least four plant diseases are identity and , as well as the caused by bacteria that inhabit only the host range and vector preference of the phloem of their host plants. These possible strains of Xylella fastidiosa, are diseases include the destructive citrus unknown. In all cases, the bacterium is greening disease, the severe papaya bunchy top disease, the cucurbit yellow the disease. Diseased fruit is also quite vine disease, and the infrequent clover bitter. club leaf disease. The bacteria causing Citrus greening is spread by these diseases have not yet been grown vegetative propagation with buds and on nutrient media and so far many of grafts, and by at least two citrus psyllids: their properties remain unknown. All of Diaphorina citri Kuwayama, which is the them, however, are transmitted from principal vector of the more severe and plant to plant only by specific insect more destructive Asian form of the citrus vectors. The citrus greening bacterium greening bacterium that occurs at higher is transmitted by a psyllid, while the temperatures (30 to 35ºC), commonly papaya bunchy top disease bacterium found at lower elevations; and Trioza and the clover club leaf bacterium are erytreae Del Guercio, which is the transmitted by leafhoppers, and the principal vector of the milder, less cucurbit yellow vine disease bacterium severe, lower temperature (27 C) is transmitted by the squash bug. In the African form of the bacterium, which is psyllid and leafhopper vectors, the normally found at higher elevations. bacterium also multiplies in and is Both vectors, however, can transmit passed from the mother insect to its both forms of the bacterium. Asian offspring through the eggs (transovarial psyllids acquire the bacterium within 30 transmission). It is not known what minutes of feeding while African psyllids happens to the bacteria transmitted by require 24 hours. The bacterium the squash bug. apparently multiplies in the vector and Citrus greening disease - Citrus can be transmitted within 8 to 12 days greening is a very destructive disease of from acquisition. all types of citrus. It occurs in most citrus Infected plants and vectors have producing areas of Asia, including the been introduced into several citrus- Arabian Peninsula, and in Africa. The producing countries but in most cases it disease is caused by the bacterium was eradicated before it could become Liberobacter asiaticum in Asia, and L. established. The vector of the greening africanum in Africa. Both bacteria are bacterium Diaphorina citri was limited to the phloem of the host plants, introduced in Brazil in the early 1980s and have yet to be cultured. The and in Florida in 1998 but, so far, the disease first appears as a chlorosis and causal bacteria apparently have not leaf mottling on one shoot or branch, been introduced and no trees have been which it has given it the name found in either place to be infected with “huanglongbing”, or “yellow shoot”, in citrus greening. Chinese. Later on, entire trees become Bunchy top of papaya disease chlorotic as though they are suffering - Bunchy top is a devastating disease of from zinc deficiency, their twigs die papaya. It occurs in most or all islands back, and the trees decline rapidly and of the Caribbean Basin and, probably, become non-productive. Fruit on also in Central America and in the diseased trees is small, lopsided, and northern part of South America. Young does not color uniformly as it ripens but leaves of infected plants show mottling, large parts of it remain green even when then chlorosis and marginal necrosis, mature, thereby the “greening” name of and become rigid. Internodes become progressively shorter, further apical growth stops, and the plant develops a pathogenic mollicutes are generally “bunchy” top. Older leaves may fall off, classified as belonging to the genus any fruits that are set are bitter, and the Phytoplasma. Most phytoplasmas have entire plant may die. an irregular spherical to elongated Bunchy top of papaya is caused shape and have been obtained and by a rickettsia-like phloem-limited maintained on complex nutrient media, bacterium that moves and multiplies in although they do not readily grow or the phloem elements of the plant. The multiply on them. A few plant pathogenic bunchy top bacteria are transmitted from mollicutes typically have spiral diseased to healthy papaya plants by morphology and belong to the genus the leafhoppers Empoasca papayae Spiroplasma. Spiroplasmas grow and Oman and E. stevensi Young. multiply readily on specialized nutrient Symptoms appear 30-45 days after media. Plant diseases caused by inoculation. mollicutes appear as yellowing of Cucurbit yellow vine disease - leaves, proliferation of shoots (witches’ Yellow vine disease affects watermelon, brooms) and of roots, stunting of shoots melon, squash, and pumpkin. It was first and whole plants, greening of flowers, reported in the Texas-Oklahoma area abortion of flowers and fruit, dieback of and has since been found in twigs, and decline and death of trees. Massachusetts, New York, and Numerous important diseases of annual Tennessee. Affected plants show vines crops are caused by mollicutes, mostly with yellow leaves, the phloem of leaves phytoplasmas, for example, aster and vines becomes discolored, and the yellows of vegetables and ornamentals, leaves and vines collapse and die. The tomato big bud (stolbur), corn stunt, etc. disease has been severe in the Texas Phytoplasmas cause even more, and and Oklahoma areas where it annually more severe, diseases on trees, destroys thousands of acres of cucurbits including X-disease of peach, peach costing millions of dollars. yellows, apple proliferation, elm yellows, Cucurbit yellow vine disease is pear decline, and lethal yellowing of caused by a phloem-limited bacterium coconut palms. Spiroplasmas also that has been placed in the species cause severe diseases, for example, Serratia marcescens and its properties corn stunt, and citrus stubborn disease. are still being characterized. The All mollicutes, that is, bacterium is most probably transmitted phytoplasmas and spiroplasmas, are by insect vectors. The squash bug, spread from plant to plant through Anasa tristis, is considered to be a vegetative propagation and, in nature, vector of this bacterium, but its these pathogens depend for their involvement in transmitting this transmission on phloem-feeding, sap- bacterium has been questioned. sucking insects, mainly leafhoppers, planthoppers, and psyllids. These Insect transmission of plant diseases insects can acquire the pathogen after caused by mollicutes feeding on appropriate infected plants Mollicutes are prokaryotes for several hours or days, or if they are (bacteria) that lack cell walls. In nature, artificially injected with extracts from plant pathogenic mollicutes are limited infected plants or insects. More insects to the phloem of their host plants. Plant become vectors when they feed on young leaves and stems of infected crops, mostly vegetables and plants than on older ones. The insect ornamentals, for example, tomato, vector cannot transmit the pathogen lettuce, carrot, onion, potato, immediately after feeding on the chrysanthemum, aster, and many infected plant but it begins to transmit it others, on which it causes severe after an incubation period of 10 to 45 symptoms and serious losses, in some days, depending on the temperature. crops amounting to 10-25% of the crop The quickest transmission (10 days) and occasionally up to 80-90% of the occurs at about 30 C, while the slowest crop. Plants infected with aster yellows (45 days) takes place at about 10 C. develop general chlorosis (yellowing) The reason for the incubation and dwarfing of the whole plant, period is that the acquired phytoplasmas abnormal production of shoots and, or spiroplasmas must first multiply in the sometimes, roots, sterility of flowers, intestinal cells of the insect vector and malformation of organs, and a general then move through the insect by passing reduction in the quantity and quality of into the hemolymph, then infect internal yield. The aster yellows phytoplasma is organs and the brain, and finally reach transmitted by several leafhoppers, one and multiply in the salivary glands. of which is the aster leafhopper When the concentration of the pathogen Macrosteles fascifrons. The various in the salivary glands reaches a certain leafhopper vectors have a wide host level, the insect begins to transmit the range, as does the aster yellows pathogen to new plants and continues to phytoplasma. The phytoplasmas survive transmit it with more or less the same in perennial ornamental, vegetable, and efficiency for the rest of its life. Insect weed plants. The vector leafhopper vectors are not generally affected acquires the phytoplasmas while adversely by the phytoplasmas or feeding by inserting its stylet into the spiroplasmas multiplying in their cells, phloem of infected plants and but in some cases they show severe withdrawing the phytoplasmas with the pathological symptoms. Phytoplasmas plant sap. After an incubation period, and spiroplasmas can be acquired as when the insect feeds on healthy plants readily or better by nymphs than by it injects the phytoplasmas through the adult leafhoppers, etc., and they survive stylet into the phloem of the healthy through subsequent molts of the insect. plants where they establish a new The pathogens, however, are not infection and multiply. The passed from the adults to the eggs and phytoplasmas move out of the leaf and to the next generation. For this reason, spread throughout the plant causing the young insects of any stage must feed on symptoms characteristic of the host infected plants in order to become plant. infective vectors. Tomato big bud - The disease Some of the most important plant occurs in many parts of the world but diseases caused by mollicutes and their except for a few areas, it is of little insect vectors are described briefly economic importance. It affects most below. Solanaceous vegetables and lettuce. Aster yellows - Aster yellows is The symptoms include small, distorted, caused by phytoplasmas and occurs yellowish green leaves and production worldwide. It affects numerous annual of numerous thickened, stiff, and erect apical stems that have short internodes. transmit the phytoplasmas into healthy The flower buds are excessively big, apple trees. The time between green, and abnormal looking, and fail to inoculation and appearance of set fruit. Fruit present when infection symptoms varies with the size of the takes place becomes deformed. inoculated tree. Young nursery trees Tomato big bud is caused by a may develop symptoms within a year phytoplasma that is transmitted by while large established trees may do so several leafhoppers, the main one of two or three years after inoculation. which is the Pear decline - It is a serious argentatus. The insect feeds disease of pear resulting in significant and breeds on infected weed hosts and crop losses and also in stunting and when they become undesirable the death of affected pear trees grown on insects move into tomato or other crops certain rootstocks. The disease, which is bringing with them the big bud caused by a phytoplasma, occurs in phytoplasmas. North America and in Europe, and Apple proliferation - It is the probably in many other parts of the most important insect transmitted world where pears are grown. The disease of apple in most of Europe. It symptoms of pear decline may develop may also occur in South Asia and South as a quick decline, that is, sudden wilt Africa. Depending on prevalence in an and death of a tree within a few days or orchard, apple proliferation may cause weeks, with or without first showing economic losses of 10-80% due to reddening of leaves, or a slow decline. reduction in fruit size, total yield, and Quick decline usually develops on trees vigor of trees. The most conspicuous propagated on certain hypersensitive symptoms of apple proliferation are the rootstocks in which a brown necrotic line production of witches’ brooms or of leaf develops at the graft union of the tree. rosettes, and of enlarged stipules at the Slow decline also occurs on trees base of leaves. Affected trees leaf out grafted on the same or other rootstocks, earlier in the spring but flowering is and appears as a progressive delayed. The leaves, fruit, and entire weakening of the tree of varying trees are smaller, and fruit color and severity. Slow declining trees have taste are also poor. Proliferating shoots reduced or no terminal growth, have are often infected with powdery mildew. few, small, leathery, light green leaves Apple proliferation is caused by a whose margins are slightly rolled up and phytoplasma that also infects other wild may be yellow or red in the autumn. and ornamental apple species, and Such trees may or may not die a few possibly pear and apricot. The years after infection. Some infected pear phytoplasma is spread in nature by trees, however, show primarily a several leafhoppers, including Philaenus reddening of the leaves in late summer spumarius, Aphrophora alni, Lepyronia or early autumn, and mild reduction in coleoptrata, Artianus interstitialis, and vigor. Fieberiella florii. The leafhopper vectors The pear decline phytoplasma is acquire the phytoplasmas when they transmitted from tree to tree by grafting feed on the phloem elements of young and by the pear psylla (Psylla pyricola leaves and shoots of infected apple Forster) and in Europe, probably by P. trees and, after an incubation period, pyri and P. pyrisuga. Pear psylla acquires the phytoplasma after feeding vector acquires the phytoplasma while on infected trees for a few hours and sucking juice off the phloem of palm leaf remains infective for several weeks. veins, the phytoplasma multiplies in the Young trees inoculated with vector during an incubation period, and phytoplasma by the insect show the insect then transmits the symptoms the same or the next year, phytoplasma when it visits and feeds on while older trees may take longer. The leaf veins of healthy palm trees. phytoplasma is sensitive to low Corn stunt - Corn stunt causes temperatures and dies out in the above- severe losses where it occurs although ground parts of the tree but survives in losses vary from year to year. It occurs the tree roots. In the spring, the in the southern United States, Central phytoplasma recolonizes the stem, America, and northern South America. branches and shoots and from the latter Symptoms consist of yellow streaks in it can be acquired and transmitted again young leaves followed by yellowing and by the insect vectors. reddening of leaves, shortening of Lethal yellowing of coconut internodes, stunting of the whole plant, palms - Lethal yellowing is a blight that and sterile tassels and ears. kills coconut and some other palm trees Corn stunt is caused by the within 3 to 6 months from the time the spiroplasma Spiroplasma kunkelii. The trees show the first symptoms. It occurs spiroplasma invades phloem cells from in Florida, Texas, Mexico, most where it is acquired by its leafhopper Caribbean islands, in West Africa, and vectors Dalbulus maidis, Dalbulus elsewhere. The disease appeared for eliminatus, and other leafhoppers after the first time in Florida in 1971 and killed feeding on infected plants for several 15,000 coconut palm trees the first two days. The vectors transmit the years, 40,000 by the third year, and by spiroplasma after an incubation period the fourth year (1975), 75% of the of 2 to 3 weeks, during which the coconut palms in the Miami area were spiroplasma moves and multiplies in the dead or dying from lethal yellowing. The insect. disease appears as a premature drop of Citrus stubborn disease - It is coconuts followed by blackening and present and severe in hot and dry areas death of the male flowers. such as the Mediterranean countries, Subsequently, first the lower and then the southwestern United States, Brazil, the other leaves turn yellow and then Australia, and elsewhere. It is one of the brown and die, as does the vegetative most serious diseases of sweet orange bud, and the entire top of the tree falls and grapefruit. It is hard to diagnose but off leaving the palm trunk looking like a reduces yield, quality, and marketability telephone pole. of fruit dramatically. Infected trees grow Lethal yellowing is caused by a upright but are stunted. There is less phytoplasma that lives and multiplies in fruit and it is smaller, lopsided, green, the phloem elements of the plant. The and sour, bitter, and unpleasant. main means of spread of lethal Citrus stubborn disease is yellowing from tree to tree is through the caused by the spiroplasma Spiroplasma planthopper Myndus crudus, although citri, which is found in the phloem of other vectors are also possible. As with affected orange trees. It is transmitted the other phytoplasma diseases, the by budding and grafting and, in nature, by several leafhoppers such as Anacentrus deplanatus, by the Hessian Circulifer tenellus, Scaphytopius fly Phytophaga destructor, and by the nitrides, and Neoaliturus haemoceps. southern and northern corn root worms Role of insects on fungal diseases of Diabrotica undecimpunctata howardii plants and Diabrotica longicornis, respectively. As with bacteria, many insects In the black stain root disease of pines, are involved in the transmission of hemlock, and Douglas fir is caused by numerous plant pathogenic fungi from the fungus Leptographium wageneri, the diseased to healthy plants. Insects are teliomorph of which is Ophiostoma also involved in plant diseases by wageneri, and is transmitted by the root- breaking the epidermis and other feeding bark beetle Hilastes nigrinus protective tissues of plants with their and two root and crown weevils, mouthparts or with their ovipositor and Steremnius carinatus and Pissodes thereby allowing the fungus to enter. fasciatus. Most of the insect transmissions of fungi Stalk or stem-infecting fungi - are accidental, that is, they occur Many fungi infecting stalks or stems, for because the insects happen to become example Gibberella, Fusarium, and externally or internally contaminated Diplodia in corn, are apparently aided by with the fungus or its spores when they various insects, for example, the visit infected plants and then carry the widespread European corn borer, spores with them to the plants or plant Pyrausta nubilalis. parts they visit next. In some cases, Trunk and branch canker- insect transmission of a fungus occurs causing fungi - Many fungi, such as as the insect visits blossoms during species of Neofabrea, Nectria, pollination, in others it occurs while Leucostoma (Cytospora), Ceratocystis, wounding plants during oviposition, and and Leptosphaeria, causing tree in other and most frequent cases, cankers, are apparently also often transmission occurs while wounding the associated with and assisted by insects plant during feeding. In relatively few in the initiation and development of the cases, the insect and the fungus it cankers. The insects involved vary with transmits develop a symbiotic the particular host and fungus. For relationship in which each benefit from example, the fungus Neofabrea its association with the other. perennans (Gloeosporium perennans), Root-infecting fungi - It should the cause of the perennial canker of be pointed out that there are apple, is transmitted by the wooly aphid innumerable cases for which there is Eriosoma lanigerum. The woolly aphids circumstantial evidence that insects are feed on the bark at the base of the trunk apparently involved in the transmission where they cause the formation of galls of many plant pathogenic fungi and in within which they multiply. In early the development of disease by them, spring the galls burst, the aphids come but this has not been proven out and the fungus attacks the injured experimentally. In this category belong, tissue and from it advances into healthy for example, root infections by fungi tissue and produces a canker. In the such as Pythium, Fusarium, and summer, the apple tree produces callus Sclerotium, being facilitated by billbugs tissue and seals off the fungus and the such as Calendra parvula and spread of the canker stops. The aphids, however, grow into the callus tissue and and/or Botryodiplodia theobromae enter form a new gall, and the process is the twigs through wounds created by the repeated. feeding of the insects The spittlebug Aphrophora Sahlbergella singularis and Distantiella saratogensis seems to be involved in theobroma. In isolated infections the the Nectria canker of pines, the nitidulid tree defenses take over, isolate the beetle Carpophilus freemani and the fungus, and its further spread stops. In drosophilid fly Chymomyza trees massively infested with the insect, procnemoides in the Ceratocystis however, the fungus develops cankers of stone fruit trees, while the unchecked in the insect-infested tissues tree cricket Oecanthus niveus and the and causes a chronic dieback of twigs. raspberry midge Thomasianna theobaldi Control of the insects also halts the are involved in the tree cricket canker of invasion by the fungus and the tree apple and the midge canker of recovers. raspberry, respectively. Many more In mango malformation disease, such insect-pathogen associations could presumably caused by the fungus be mentioned. Fusarium moniliforme, the fungus is In the beech bark canker, caused transmitted by the eriophyid mite Aceria by the fungus Nectria coccinea var. mangifera, while other fungi seem to be faginata, the fungus is transmitted to carried in the digestive tract of certain some extent by the scale insect termites. Cryptococcus fagi but the main effect of Sooty molds - These are black- the insect is in weakening the tree and colored fungi that grow on the surfaces reducing its defenses to the fungus. of mostly leaves of plants, especially in Thus, after beech trees have been the tropics and subtropics. Sooty mold heavily infested by scale insects for fungi do not penetrate and infect plants about three to five years, the fungus but cause disease by blocking the light invades and kills the bark and the tree from reaching the leaves. Sooty mold forms a canker that may girdle the tree fungi do not parasitize plants but feed partially or completely and may kill it. off the honeydew excreted by insects In the birch constriction disease, such as whiteflies, scales, mealybugs, the lower parts of shoots become aphids, etc. The sooty mold fungi are constricted at the point where the apical disseminated through their spores being birch woodwasp (Pseudoxiphydria blown about by wind. However, they are betulae Ensl.) feeds on the shoots. The also spread by the honeydew-producing leaves above the constriction wither and insects and, also, by several other types die but cling to the twigs past the of insects such as flies, wasps, bees, autumn. Almost all (92%) of the and ladybug beetles, all of which seek constrictions are also infected with the honeydew as a source of food and in anthracnose fungus Melanconium the process become smeared with bicolor. fungus spores which they carry about. A similar case in which twig Wood rots - Rotting of wood is canker initiation and development are carried out primarily by wood-rotting facilitated by insects is the cacao basidiomycete fungi. The shelf or conk- dieback disease in which the fungi shaped fruiting bodies of many of these Calonectria (Fusarium) rigidiuscula fungi are visited routinely by many types of insects and it is believed that many of isolated from the infected wood and are these insects act as vectors of the carried by the same insects both wood-rotting fungi. Insects and mites externally and internally. A similarly have also been implicated in the spread complex association seems to occur in of some pine rust diseases, while at spruce attacked by Dendroctonus least three common scolytid beetles engelmani, followed by the fungi have been shown to be involved in the Leptographium sp., Endoconidiophora transmission of the scleroderis canker of sp., or Ophiostoma sp. infecting the pine and spruce. wood and causing a gray stain in the Wood-stain diseases - Wood sapwood of the infected trees. stain or wood discoloration diseases occur in conifer trees and felled timber. Vascular wilts They are caused by the so-called blue- Several vascular wilts affect trees stain fungi, of which the most common and some of them cause extensive are species of Ceratocystis and death of trees, because the fungus Ophiostoma. The blue-stain fungi are responsible for the disease is associated with several species of bark transmitted from diseased to healthy beetles, such as Dendroctonus trees by specific insect vectors. The ponderosae, Ips pini, etc., which serve spores produced by the causal fungi are as vectors of the fungi and provide them sticky and are produced primarily inside with wounds for penetration. On the the tree, therefore, they can be spread other hand, the fungi reduce the water by no other means but only by certain content of the tree and otherwise insects closely associated with the improve the microenvironment for the disease. These vascular wilts include: 1) developing brood of insects. Such a persimmon wilt, a devastating disease fungus-insect relationship is described caused by the fungus Cephalosporium as true mutualistic symbiosis. In other diospyri which enters through all kinds blue-stain diseases, like the ones of wounds but is also transmitted by the caused by the fungi Trachosporium powder-post beetle Xylobiops basilaris tingens and T. t. var. macrosporum, the and the twig girdler beetle Oncider fungi are constantly associated with cingulatus, and 2) mango wilts, one their bark-beetle vectors Myelophilus caused by the fungus Diplodia recifensis (Blastophagus) minor and Ips and transmitted by the beetle Xyleborus acuminatus, respectively, and are found affinis, and another caused by the regularly in the breeding places of the fungus Ceratocystis fimbriata and insects in pine stems. Such fungal- transmitted by the scolytid beetle insect associations are known as Hypocryphalus mangiferae. The other symbiotic ambrosia cultures. two vascular wilts are oak wilt and the In the Southern United States, Dutch elm disease and will be discussed attacks of short-leaf pines by beetles in some detail below. like Dendroctonus frontalis are quickly Oak wilt - It is caused by the followed by heavy fungus infection soon fungus Ceratocystis fimbriata and is one after the beetles tunnel through the bark of the most important diseases of forest and outer wood. Several fungi, including trees. The fungus enters the xylem Ceratocystis pini, Saccharomyces pini, vessels of trees through fresh wounds to Dacryomyces sp. and Monilia sp. can be which it is carried by air or insects, and through natural root grafts. Tree parts in the Netherlands in 1921, found in beyond the point of infection wilt, turn Ohio and New York in the 1930s, and brown and die while newly infected has since spread throughout the United wood shows dark streaks. The fungus is States and much of the rest of the world. spread to healthy trees by nitidulid It kills elm tree twigs, branches and beetles such as Carpophilus lugubris, whole trees by clogging their xylem Colopterus niger, Cryptarcha ample, vessels and blocking movement of and several species of Glischrochilus. water from the roots to these parts. These fungi breed in the mycelial mats Dutch elm disease has been particularly of the fungus between the bark and devastating in the United States where wood and carry the fungus both the native elm tree Ulmus americana is externally on their bodies and internally extremely susceptible to the pathogen. through their digestive tract. In addition The disease has killed almost all trees in to the nitidulid beetles, several scolytid its path, especially elm trees planted beetles, such as Monarthrum fasciatum along streets and parks. Elm trees in and Pseudopityophthorus minutissimus, forests have also been killed but many the brentid beetle Arrhenodes minuta, of them have escaped infection so far the buprestid Agrillus bilineatus, the flat- (Fig. 6). headed borer Chrysobothrys femorata, The fungus causing Dutch elm and others, have been shown to carry disease is spread from diseased to the spores of the fungus, both externally healthy trees by the European elm bark and internally, when they emerge from beetle Scolytus multistriatus and the the tunnels in diseased trees in which native elm bark beetle Hylurgopinus they breed and overwinter and to carry rufipes, and by natural root grafts. The them to susceptible trees in the spring. fungus overwinters in the bark of dying Transmission of the oak wilt fungus by or dead elm trees and logs as mycelium insects not only spreads the fungus and and spores. The elm bark beetles lay the disease to new trees and into new their eggs in galleries they make in the areas, it also increases the ability of the intersurface between bark and wood of fungus to produce new variants and new weakened or dead elm trees. If the tree races more virulent than the existing is already infected with the Dutch elm ones. This is accomplished by the disease or if the insects carry with them insects bringing together in the same spores of the fungus, the fungus grows tree the compatible self-sterile mating and produces new spores in the tunnels. types which results in the production of After the eggs hatch, the larvae make perithecia containing the sexual spores tunnels perpendicular to that made by ascospores. The latter express any new the adult female and pupate. The adults characteristics brought together during emerge, carrying thousands of fungal the formation of the spores, some of the spores on their body. The emerging characteristics possibly being increased adults prefer to feed on young twigs of virulence. trees and the crotch of small branches. Dutch elm disease - It is caused As the beetles burrow into the bark and by the fungus Ophiostoma ulmi and the wood for sap, the spores they carry on most recent variant Ophiostoma novo- their body are deposited in the wounded ulmi, which is replacing the earlier moist tissues of the tree. There the species. The disease was first described spores germinate and grow into the injured bark and wood and the fungus appendages that cling to the legs or reaches the xylem vessels of the tree in other body parts of such insects and are which it grows producing mycelium and carried by them to other plants or plant spores. The latter are carried upward by parts they visit next. A few examples of the sap stream where they can start foliar diseases in which insect new infections. Shoots beyond the transmission of the fungal pathogen has infected areas turn brown, wilt, and die, been shown to occur are described and as their number increases the tree briefly below. shows more browning and more wilted Powdery mildews - These are branches. Eventually large parts of or diseases that affect most annual and entire trees wilt and die, while the perennial plants. They are characterized fungus continues to grow and spread in by white superficial mycelial growth and the dead tree. Such trees are then sporulation by a small group of fungi visited by adult female beetles that lay that cause symptoms on leaves, shoots, their eggs in them and the cycle is blossoms and fruit of their host plants. repeated. Powdery mildews serve as food for In Dutch elm disease there is a many mycophagous fungi and produce clear dependency of each organism, the large numbers of loosely attached fungus and the insect, on the other. spores. Such spores become attached Probably more than 99% of the elm tree to, and are disseminated by, insects infections are caused by the fungus with which they come in contact. being carried to the elm trees by the elm Examples include the feeding of thrips bark beetles. On the other hand, the elm on and the transmission of spores of the bark beetles depend on the fungus for fungi Sphaerotheca panosa and causing many elm trees to weaken and Uncinula necator that cause powdery die, thereby becoming available as mildew on rose and grape, respectively. breeding grounds for the two species of Although these fungi are disseminated elm bark beetles that transmit the readily by wind, it is likely that fungus. The interdependence of the two transmission is aided by insects. organisms has provided the most Rust diseases - Most rust effective means of managing the Dutch diseases produce several types of elm disease by burning or debarking superficial spores on their host plants dead elm trees and logs, thereby that, like those of the powdery mildews, denying the insects the breeding ground are easily disseminated by air currents they need and, through the reduced but are also visited, eaten, and number of insects produced, reducing transported by a wide variety of insects. the number of elm trees to which they Furthermore, many rust fungi produce spread the disease. spermatia and receptive hyphae in the same spermagonium but they are self- Foliar diseases sterile. Many insects, when visiting such Many foliar diseases are probably spermagonia become smeared with spread by various insects visiting and sticky spermatia. When the insects visit moving about on leaf surfaces that are successive spermagonia, they transfer exhibiting infections by spore-producing to the receptive hyphae spermatia from fungi. Spores or the spore containers of the opposite, compatible type. These many such fungi are sticky or have spermatia can fertilize the receptive hypha which then produces dikaryotic leafhopper Graphocephala coccinea; mycelium and spores that contain two bud rot disease of carnations caused by nuclei. These dikaryotic spores have the fungus Fusarium poae and aided by entirely different properties. For the mite Siteroptes graminum. example, they can infect an entirely Several diseases of blossoms different host plant from the plant on have been associated with insect which they were produced. The vectors. In most cases, transmission of involvement of insects in rust diseases the fungus by the insect is related to the is, therefore, important in both the activities of the insect during pollination. dissemination of the spores to new Some of the better-known examples hosts and, more importantly, in the include: fertilization of the fungus and, thereby, Anther smut of carnations - in increasing the potential of the fungus This is caused by the fungus Ustilago to produce more new and possibly more violacea. In this disease, the pollen is virulent races. replaced by the teliospores of the Some other examples of foliar fungus but the petals remain unaffected diseases in which insects have been and continue to attract insects. The shown to play a role in their visiting insects become smeared with transmission include: red pine needle the smut spores, which they transfer to blight caused by the fungus Pullularia previously healthy flowers. pullulans and transmitted and aided in Blossom blight of red clover - penetration of pine needles by a This is caused by the fungus Botrytis cecidomyiid midge; cucurbit anthophila and is transmitted primarily anthracnose, caused by the fungus by pollinating bees. Colletotrichum lagenarium and Ergot of cereals and grasses - transmitted and aided in penetration by This is caused by the fungus Claviceps the spotted cucumber beetle Diabrotica purpurea, which develops in the flowers undecimpunctata; oil palm leaf spot, and produces spores that are contained caused by the fungus Pestalotiopsis in a sweet and sticky substance. That palmarum and transmitted and aided in substance is attractive to many insects, penetration by the oviposition punctures particularly flies and beetles. The of a tinged of the genus Gargaphia. insects feed on the spores and also become smeared with them externally Diseases of buds and blossoms and carry them, externally and through Insects often overwinter in buds their feces, to healthy flowers. Although of plants and many also visit blossoms primary infections by the ergot fungus to feed on the nectar they produce. are primarily from ascospores produced Buds also often contain mycelium and by sclerotia overwintering on the ground spores of plant pathogenic fungi, and and carried via air currents, insect blossoms are often the first plant organ transmission of conidia is important for such fungi attack in the spring. secondary transmission of the disease Examples of bud infections in which and for transmission over long insects have been implicated to play a distances. Some beetles, however, feed role include: bud-blast disease of on ergot sclerotia on the ground and rhododendron, caused by the fungus may carry mycelium and ascospores on Pycnostyamus azalea and aided by the their bodies to healthy plants and through them may cause primary Rots of fleshy fruits infections. Fig rots - Several kinds of fungi Anthracnose disease of Musa attack figs and cause rotting of fruits in balsamiana - This is caused by the the field. In most such cases, certain fungus Gloeosporium musarum and is types of insects play a more or less transmitted by the hymenopterans important role in the transmission and Polybia occidentalis, Synoeca surinama, introduction of the fungus into the fig. and Trigona sp. The fungus infects the Endosepsis of figs - This is floral parts of the plant but these are caused by the fungus Fusarium dropped while still producing conidia moniliforme, and results in the entire and sweet exudate. The insects are fruit content turning into a pulp. The attracted to the exudate on the fallen fungus is transmitted from fruit to fruit by flowers and there they become smeared the fig wasp Blastophaga psenes, which wit conidia, which they subsequently also plays a crucial role in the pollination carry to healthy flowers, which the of figs. Fig trees, being dioecious, have spores infect. male trees that produce staminate Flower spot of azalea - This is flowers around the opening and gall caused by the fungus Ovulina azaleae flowers in the cavity, and female trees and is transmitted by several species of that produce only pistilate flowers. The bees, thrips, and ants. The insects carry fig wasp lays its eggs in the ovules of spores on their bodies and drop them off the gall flowers of male plants, which on healthy flowers they visit which, in are thereby stimulated to grow. The addition, may injure directly and eggs hatch and the larvae parasitize the facilitate penetration and infection by the galls until they pupate. The adults fungus. emerge from the pupae and the females are fertilized while still in the male fig. Diseases of fruit and seeds in the When they come out of the fig, the field females brush against the staminate Fruits and seeds are the source flowers that surround the opening and of food and the breeding grounds of become smeared with pollen. The many insects. Insects puncture fruit and female wasps carry the pollen to male seeds to obtain food and to lay their and female flowers they subsequently eggs in them. Although insects often visit for oviposition. In female flowers, cause direct damage to fruits and seeds however, because of the length of that make them unsalable, the damage styles, oviposition fails but pollination is increases manifold when the insects nevertheless successful and the fruit also carry to the fruits and seeds fungi develop into edible figs. If, however, as that infect and cause these organs to rot the female wasp visits some infected or to develop other symptoms. figs it becomes smeared with spores of Numerous examples of fruit-insect- the fungus, it transmits the spores to pathogen interactions could be cited, male and female figs it visits, and the although in many cases no hard data of fungus then causes endosepsis of the such interactions exist. Some of the female figs. better-studied cases are described Souring of figs - This is caused briefly below. by yeast fungi that cause fermentation, and appears as discoloration and wateriness of the fig contents which be increased by the wounds made on then exude from the fig opening. Such them by the larvae of the lepidopterans figs shrivel, dry, and cling to the tree. Argyrotaenia pulchellana and Lobesia The fermenting yeasts are transmitted to botrana. figs externally and internally on the Black pod of cacao - This is bodies of the two most common visitors caused by the fungus Phytophthora of figs still in the tree, the sap beetle palmivora and results in devastating Carpophilus hemipterus and the fruit fly losses of yield. Insects of several Drosophila melanogaster. different families play a role in the Fig smuts and molds - These are transmission of this disease. At least ten caused by the black mycelium and species of ants, especially spores of Aspergillus niger and the Crematogaster striatula and to a lesser variously colored growths of other fungi. extent Camponotus acvapimensis and These fungi are carried into green figs Pheidole megacephala, appear to on the bodies of predatory mites and, to spread the fungus vertically within the a lesser extent, by thrips. tree, especially during the rainy season, Brown rot of stone and pome when they carry spore-containing soil fruits - This is caused by the three particles up the cacao tree for nesting related fungi Monilinia fructicola, M. purposes. Certain coleoptera, such as fructigena, and M. laxa and affects all the nitidulid beetle Brachypeplus the stone fruits and, to a lesser extent, pilosellus, and certain dipterans, such the pome fruits. The fungi are aided in as the fly Chaetonarius latifemur, their penetration of the fruit by the colonize black pods in the field and may feeding and oviposition wounds made carry the fungus internally or externally by the insects plum curculio on their bodies to healthy pods. (Conotrachelus nenuphar) and the Because of their large numbers on oriental fruit (Grapholitha molesta), cocoa trees, their habit of visiting and the feeding wounds of the dried fruit wounded pods, and their proven beetle (Carpophilus hemipterus) and efficiency to transmit the fungus, these two nitidulid beetles (Carpophilus insects are considered the main vectors mutilatus and Haptonchus luteolus). The of the fungus locally and over long insects also become smeared with distance. spores of the brown rot fungi which they Boll rots of cotton - These are carry on their bodies and deposit at the caused by several fungi including wounds they make on the fruits they Fusarium moniliforme, Alternaria tenuis, visit. In pome fruits, the fungus is Aspergillus flavus, and Rhizopus facilitated in penetrating the fruit by the nigricans. Various insects are feeding holes made by the earwig apparently involved in the transmission Forficula auricularia at the beginning of of these fungi and they seem to use ripening of the fruit, at which time they different mechanisms of transmission. are susceptible to brown rot. Thus, in boll rot due to Fusarium and Gray mold of grapes - This is Alternaria, the fungi penetrate cotton caused by the fungus Botrytis cinerea. bolls through feeding and oviposition The fungus spores are generally spread wounds made by the boll weevil by air currents. Penetration of the (Anthonomus grandis), the cotton grapes and shoots, however, seem to bollworm (Heliothis zeae), and the tarnished plant bug, Lygus lineolaris, or large berries and if they carry the fungus they are brought to and penetrate the latter causes infection of the bean. through the nectarines by nectar feeding The number of infected berries is flies such as Drosophila and cabbage proportional to the number of insects, looper, Trichoplusia ni. In boll rots approximately 300 insects per tree caused by Aspergillus flavus and other resulting in infection of all the berries on aflatoxin-producing species, the fungus the tree. is primarily wind disseminated but is also carried internally and externally by Molds and decays of grains and insects, such as the lygus bug Lygus legumes hesperus and the stink bug Chlorochroa Numerous decays and molds sayi, that frequently visit cotton bolls. affect the various grains and legumes The latter fungus, however, seems to while still in the field and their frequency depend for entrance on the presence of and severity increase as the number of large wounds like the large exit holes insects infesting the crops, and feeding made by the mature larvae of the pink on the seeds, increases. In corn, for bollworm, Pectinophora gossypiella. On example, seed rots can be caused by the other hand, boll rots by Rhizopus species of the fungi Fusarium, stolonifer occur when wounds made by Gibberella, Diplodia, Cephalosporium, the bollworm Earias insulana and by the Nigrospora, Physalospora, pink bollworm are available. In the lint Cladosporium, Penicillium, Aspergillus, rot of cotton, caused by the fungus Rhizopus, Trichoderma, and others. The Nigrospora oryzae, the fungus is insects most commonly involved in transmitted very efficiently by the mite transmitting and facilitating infection of Siteroptes reniformis. In corn kernels by these fungi are the corn Stigmatomycosis or internal boll earworm, Heliothis zea, and the disease, caused by the fungus European corn borer, Pyrausta nubilalis, Nematospora gossypol, the cotton fibers but other borers and other insects also are stained in the absence of external play important roles as vectors and, symptoms. This disease is associated most importantly, as facilitators of with the feeding of several species of infection by these fungi by creating plant bugs primarily of the genus wounds that allow the fungus to enter Dysdercus, often referred to as cotton the seed. In seed infections by stainers. The insects carry the fungus Aspergillus and by Fusarium there is the spores externally on the mouthparts and added adverse effect of production of internally in their deep stylet pouches debilitating mycotoxins. Similar, and introduce it via their proboscis although less studied situations have through the wall of young cotton bolls. been reported for rice infections by Coffee bean rot - This is caused fungi, e.g., Nematospora corylii, by the related fungi Nematospora corylii transmitted and facilitated by wounds and N. gossypii, which cause berries to made by the rice stinkbug Oebalus turn black and subsequently to rot. The pugnax; wheat and corn infections by fungi are introduced into the berries Nigrospora sp. and Fusarium poae, through the feeding wounds made by transmitted by large numbers of the insects Antestia lineaticolis and A. Peliculopsis mites feeding on and faceta. The insects feed on small and transporting spores of the fungus in their abdominal sacs; and in various legume involved in transmission and facilitation infections by the fungi Nematospora, of infection of fleshy organs after Cladosporium, Aureobasidium, etc. harvest include larvae and adults of transmitted and facilitated in their various Lepidoptera such as the oriental penetration and infection of the seeds fruit moth, Grapholitha molesta, Diptera by the stinkbugs Acrosternum hilare and such as the apple maggot, Rhagoletis Thyanta custator, the lygaeid pomonella, the Mediterranean fruit fly, Spilostethus pandurus, by thrips, Ceratitis capitata, the house fly, and aphids, and other insects. others. The insects involved in the transmission and facilitation of infection Molds and decays of harvested fruits by fungi causing molds and decays of and seeds grains and legumes are the larvae and Generally little is known adults of various Coleoptera such as the definitively about the roles of specific rice weevil Sitophilus oryzae, the insects on the transmission and granary weevil Sitophilus granarius, and facilitation of rots of specific fruits and the confused grain beetle, Tribolium vegetables, and of molds and decays of confusum, and also Lepidoptera such as seeds of specific grains, legumes, or the Angoumois grain moth, Sitotroga nuts by specific fungi. It is generally cerealella, the European corn borer, accepted, however, that postharvest Pyrausta nubilalis, the ear cornworm, infections of plant products are greatly Heliothis zea, and other insects. increased in numbers and in severity if insects are also present in the same or Insect transmission of plant adjacent containers. There is agreement pathogenic nematodes that insects moving about among stored Two very serious plant diseases fruits, seeds, etc., transport externally caused by nematodes of the genus and internally on their bodies spores of Bursaphelenchus are transmitted by fungi infecting such fruits and seeds and insects. In both diseases there is a deposit such spores on the next fruit or symbiotic relationship between the seed they feed on. There is also fungal pathogen and the insect vector. agreement that by creating feeding or Pine wilt - This is a lethal oviposition wounds on harvested fruit disease of many species of pines and and seeds, the insects create openings other conifers. It is caused by the through which the fungi can penetrate nematode Bursaphelenchus xylophilus, and release sap and additional known as the pinewood nematode. The nutrients. The fungi then can grow and nematode is about 800 m long by 22 build momentum to eventually infect and m in diameter and it develops and rot the entire fruit or seed. multiplies rapidly, each female laying The fungi that cause most rots of about 80 eggs and completing a life fleshy fruits and vegetable after harvest cycle in as short as 4 days. The include Penicillium, Fusarium, Botrytis, nematode produces the four juvenile Rhizopus, Alternaria, Sclerotinia, stages and the adults. The juvenile Monilinia, and Colletotrichum, while the stages develop in the resin canals of molds and decays of grains and infected pine trees, feeding at first on legumes involve primarily Aspergillus, plant cells and later on fungi that invade Fusarium, and Penicillium. The insects the dying or dead tree. Later, the nematode produces special fourth-stage instar penetrates the wood where it dispersal juveniles that are adapted to undergoes the next molt and produces survive in the respiratory system of the the fourth instar, which overwinters cerambycid beetles Monochamus there. In early spring, the fourth instar carolinensis and M. alternatus by which digs a cavity in the wood where it they are transmitted to healthy pine pupates and to which numerous third- trees. stage nematode juveniles are attracted The pinewood nematode and congregate. The juvenile overwinters in the wood of infected dead nematodes undergo the next molt and trees, which also contain larvae of the produce the fourth-stage dispersal beetle vectors of the nematode. Early in juveniles, which by the thousands infect the spring, the larvae dig small cavities the tracheae of the adult insects as soon in the wood in which they pupate. As the as they emerge from the pupae and are adult beetles emerge from the pupae carried by them to healthy pine trees, later in the spring, large numbers of thus completing the cycle. fourth-stage juvenile nematodes enter Red ring of coconut palms - the beetles and almost fill the tracheae This disease kills coconut palm trees of the respiratory system of each insect from Mexico to Brazil and in the with about 15,000 to 20,000 juveniles. Caribbean islands. It is caused by the These nematode-carrying adult beetles nematode Bursaphelenchus cocophilus, emerge and fly to young branch tips of which is transmitted from palm to palm healthy pine trees where they feed for by the American palm weevil, several weeks. As the beetles strip the Rhynchophorus palmarum, the bark and reach the cambium, the sugarcane weevil, Metamasius sp., and nematode juveniles emerge from the probably other weevils. The nematodes insect and enter the pine tree through infect, discolor, and kill the palm tissues the wound. The juveniles in the tree in a ring 3 to 5 cm wide about 5 cm then undergo the final molt and produce inside the stem periphery over the adult nematodes. The latter migrate to length of the stem. the resin canals, feed on their cells and The nematode pathogen lays its cause their death, and then they move eggs and produces all its juvenile stages in the xylem and in the cortex where thy and the adults inside infected palm reproduce quickly and build enormous trees, completing a life cycle in about 9 populations of nematodes and kill twigs, to 10 days. Female weevil vectors are branches and entire trees. attracted to red ring-diseased trees but After the adult Monochamus they also lay eggs on healthy or beetles, the vector of the pine wilt wounded palm trees. If the female nematode, have fed on young twigs for carries red ring nematodes, it deposits about a month, they are ready to breed them in its feeding wounds at bases of and look for stressed and dead pine leaves or at internodes. The nematodes trees, including trees showing then enter the palm tissues and undergo symptoms or dying from infection by the repeated life cycles and spread pinewood nematode. The female intercellularly in the parenchyma cells of beetles deposit their eggs under the the petioles, stem, and roots, where the bark of such trees where the first two cells break down and form a flaky, instars develop and feed. The third orange to red discolored tissue with cavities. Red ring nematodes do not (Pentatomidae) such as the genera invade xylem and phloem tissues but Lincus and Oclenus, and possibly cause tyloses to develop in xylem others. vessels within the red ring that block the upward movement of water and Insect transmission of plant nutrients. In the meantime, the weevil pathogenic viruses larvae of the insect vector feed on the Plant viruses cause many and red ring tissue and swallow several severe diseases of plants, their number hundred thousand nematode third-stage and importance being second only to juveniles. Of these, however, only a few fungal diseases of plants. Most viruses hundred of the nematodes survive and infect their host plants systemically, that pass through the molt, internally or is, the multiplies internally externally, to the next stage weevil throughout the plant. Almost all viruses larvae and to the adult weevil. As weevil enter and multiply in phloem and in females emerge from rotted palms, a parenchyma cells. Viruses do not small percentage of them carry with produce spores, nor do they come to the them third-stage juveniles of the surface of the plant. All plant viruses are nematodes. Nematode populations transmitted to new plants that are increase rapidly at first but later they propagated from infected plants decline and about 3 to 5 months after vegetatively (that is, by grafting or infection there are hardly any red ring budding, by cuttings, by bulbs, corms, nematodes or their eggs left in roots, tubers, etc.), and many can be decomposed stem tissue of infected, transmitted artificially by mechanical dead palm trees. The nematodes, inoculation, that is, by rubbing sap from however, survive in newly infected palm infected plants onto leaves of healthy trees and, briefly, in their insect vector. plants. Some plant viruses can be transmitted from diseased to healthy Insect transmission of plant plants by pollen or seed produced by pathogenic protozoa infected plants, some by the parasitic Three plant diseases: phloem higher plant dodder when it is infecting necrosis of coffee, heartrot of coconut both virus-infected and healthy plants, palms, and sudden wilt of oil palms, are and some plant viruses are transmitted caused by flagellate protozoa of the from plant to plant by certain plant genus Phytomonas. In all three pathogenic fungi, nematodes, or certain diseases, protozoa invade the phloem mites. More than half of the plant elements of infected plants and multiply viruses, numbering more than 400, are in them, reaching populations of varying transmitted from diseased to healthy densities. Some of the sieve tubes plants by insects. become plugged by protozoa. The number of insect groups that Generally, the more severe the are vectors of plant viruses is relatively symptoms of infected plants, the higher small. The most important vector the populations of protozoa in their groups, with the number of vector phloem. The pathogen is transmitted species and viruses transmitted, are from infected to healthy plants listed below. , which includes occasionally through natural root grafts, the aphids (Aphididae, 192 species, 275 and primarily by stink bugs viruses), leafhoppers (Cicadellidae, 49 species, 31 viruses), the planthoppers primary and alternate species of host (Fulgoroidea, 28 species, 24 viruses), plants. the whiteflies (Aleurodidae, 3 species, Aphids have mouthparts that 43 viruses), the mealybugs consist of two pairs of flexible stylets (Pseudococcidae, 19 species, 10 held within a groove of the labium. viruses), and some treehoppers During feeding, the stylets are extended (Membracidae, 1 species, 1 virus), from the labium and, through a drop of contain by far the largest number and gelling saliva, the stylets rapidly the most important insect vectors of penetrate the epidermis. Penetration plant viruses, but the true bugs may stop at the epidermis or it may (Hemiptera, 4 species), the thrips continue into the middle layers of leaf (Thysanoptera, 10 species, 11 viruses) cells with a sheath of saliva forming and the beetles (Coleoptera, 60 species, around the stylets. The stylets move 42 viruses) also are implicated. between the cells until they reach and Grasshoppers (Orthoptera, 27 species) enter a phloem sieve tube from which seem to occasionally carry and transmit the aphids obtain their food. Individual a few viruses. Unquestionably, the most aphids vary in their ability to transmit the important virus vectors are the aphids, virus to individual plants. Infection of a leafhoppers, whiteflies, and thrips. plant with a virus often makes the plant These and the other groups of more attractive for aphids to grow on Hemiptera have piercing and sucking and to reproduce. Both acquisition and mouthparts, although several thrips transmission of virus by aphids are have rasping, sucking ones. Beetles and affected by temperature, humidity and grasshoppers have chewing light. mouthparts, but many beetles are quite effective vectors of certain viruses. Virus-vector relationships Generally, viruses transmitted by one Insect vectors that have sucking type of vector are not transmitted by any mouthparts carry plant viruses on their other type of vector. stylets, and such viruses are known as stylet-borne, externally borne, or non- Aphids and aphid-transmitted viruses circulative, because they do not pass to Aphids have evolved as the most the vector’s interior. The remaining successful exploiters of plants as a food viruses are taken up internally within the source, particularly in the temperate vector and are called internally borne regions. Many species of aphids persistent circulative or persistent alternate between a primary and a propagative viruses. secondary host, although there are Stylet-borne non-persistent many variations of aphid life cycles transmission - Most externally borne depending on the aphid species and on viruses can be transmitted in the typical climate. Some aphids overwinter as stylet-borne non-persistent manner. In parthenogenetic viviparous forms while such a transmission the virus is assisted others go through their life cycle on one in its transmission by a specific host species or on several related configuration of its coat protein or by a species. On the other hand, there are non-structural virus-encoded protein. several aphid species, such as Myzus The insect acquires the virus from the persicae, that have as many as 50 plant by feeding on it for only seconds or, at most, minutes. The insect can appears that saliva alone may carry out transmit the virus immediately after the this function. acquisition feeding, that is, without any Semi-persistent viruses - Some incubation period required for externally borne non-persistent viruses transmission. The insect retains the are known as semi-persistent because virus and is usually able to transmit it for they reach but do not seem to go past only a few minutes after it acquired it. the foregut of the vector; the vector must Most of the nearly 300 known aphid- feed on an infected plant (acquisition borne plant viruses are stylet-borne non- period) for several minutes or hours persistent. Some of the most important before it can transmit the virus; and the groups of plant viruses, such as those in vector can then retain (retention time) the genera Potyvirus, Cucumovirus, and transmit the virus to healthy plants Alfamovirus, and the Caulimovirus for several hours. Semi-persistent transmitted by Myzus persicae are viruses are also assisted in their stylet-borne non-persistent viruses. In transmission by a transmission helper the few seconds in which aphids acquire protein or coat protein configuration. the virus, the aphid stylet usually The best known semi-persistent viruses penetrates only the epidermal cell. are caulimoviruses, which occur in most Actually, deeper penetration of the stylet cell types, and the closteroviruses beet into leaf tissues reduces the ability of yellows virus and curly top virus, which aphids to transmit the virus. Aphids vary are found primarily in phloem cells. In greatly in their ability to transmit viruses, several of the semi-persistent viruses, a each particular virus being transmitted helper component seems to be involved by one or a few species of aphids. in their transmission. In cauliflower Sometimes, certain virus strains are , the helper component transmitted by distinct aphid species. consists of two non-capsid proteins, one Also, even individual aphids in a of which is associated with the virus population vary in their ability to transmit particles and the other has two binding the same virus, some of them being domains that interact strongly with incapable of transmitting the virus. microtubules. In some cases, certain All non-persistently transmitted viruses can be transmitted only in the viruses have simple structures of presence of a second virus which acts elongated or isometric particles with the as the helper virus. nucleic acid encapsidated by one or Persistent viruses - Internally more kinds of coat proteins. In some borne viruses are either persistent viruses, the coat protein interacts circulative or persistent propagative. directly with the binding site of virus Persistent circulative viruses are retention in the aphid. In other viruses, acquired from the plant by the vector the virus encodes a non-structural after an acquisition feeding period of protein which interacts with the aphid- several hours to several days, and then virus retention binding site and forms a they are retained by the insect vector bridge between the virus and the aphid and can be transmitted by it for several stylet. However viruses are bound to the days or weeks. Persistent circulative aphid stylet, there must also be a viruses require a latent period of several mechanism for release of the virus when hours to several days beyond the the aphid feeds on the next plant. It acquisition time before they can be transmitted by the insect vector, they produced via a read-through of the coat reach the hemolymph of the vector, and protein stop code if they are to advance pass through the various stages of the beyond the hemocoel. Some persistent insect, but not through the ovaries to the circulative viruses also require a helper egg. Persistent propagative viruses are virus to be present for them to be acquired by the insect after a feeding transmitted by their aphid vector. period of several hours to several days, Persistent propagative viruses - are retained by the vector for several Propagative viruses are transmitted weeks to several months, they multiply primarily by leafhoppers and in the vector, they have a latent period planthoppers but several members of of a few to several weeks, and can pass the multiply in and are through the various stages of the insect, transmitted by their aphid vector. These including transovarial passage to the bacilliform viruses replicate in the egg. Persistent viruses are generally nucleus and the cytoplasm of cells in the transmitted by one or a few species of brain, salivary glands, ovaries, and aphids and cause symptoms muscle of the insect vector. The virus characterized by leaf yellowing and leaf goes through the egg to about 1% of the rolling. nymphs. Infection of aphids with Persistent circulative viruses - rhabdoviruses results in increased These include primarily the luteoviruses, mortality of the aphids. such as barley yellow dwarf virus, and the nanoviruses, such as banana Leafhoppers and planthoppers, and bunchy top virus. The luteoviruses are transmission of plant viruses acquired after a feeding period as short Leafhoppers lay eggs that hatch as 5 minutes but it usually takes 12 to nymphs which pass through several hours. After an incubation period of an molts before becoming adults. Some of additional 12 hours, the vector can them overwinter as eggs, some as transmit the virus within a 10 to 30 adults, and some as immature forms. minute inoculation feeding and can They all feed by sucking sap from continue transmitting it for several days phloem elements of plants. Their or a few weeks. In the vector, the virus feeding behavior is similar to that of particles seem to associate only with the aphids in that the mouthparts, hind gut of the aphid, entering its cells surrounded by the salivary sheath, by endocytosis into coated pits and penetrate the phloem of host plants. vesicles and accumulating in tubular vesicles and lysosomes. Virus particles Virus-vector relationships are then released into the hemolymph All hopper-transmitted viruses are by fusion of the vesicles with the persistent circulative or persistent plasmodesmata and enter the salivary propagative, and are transmitted by only glands of the aphid via invaginations one or by a few closely related species with two plasma membranes on the of the hopper vectors. Only two of the hemocoel side of the salivary gland 60 sub-families of leafhoppers accessory cells. It appears that (Cicadellidae) contain species that are persistent circulative viruses do not vectors of viruses: the Agalliinae feed on require a non-capsid protein for helper herbaceous dicotyledonous hosts and component but they require a protein the that feed on monocots. Of the 20 planthopper viruses that infect , and their families (Fulgoroidea), only one, the virus members that infect plants have Delphacidae, have species that are been considered as viruses that vectors of viruses all of which infect infect plants. The propagative viruses monocotyledonous plants and many of have a latent period of about two weeks. them cause severe diseases on cereal During this period the virus replicates crops such as rice, wheat, and corn. and invades most tissues of the insect Semi-persistent transmission - vector. When the virus reaches the Two viruses, maize chlorotic dwarf virus salivary glands of the vector, the latter (MCDV) and rice tungro spherical virus can transmit the virus to new plants and (RTSV), are acquired by their vectors can continue to transmit it for the rest of (Graminella nigrifrons and Nephotettix their life. Only a small percentage of the virescens, respectively) from their hosts hoppers feeding on infected plants within about 15 minutes and are become vectors and of these only about retained by their vectors for one to a few 1% pass the virus through their eggs to days. MCDV particles have been seen the next generation. Various capsid in the foregut and a few other tissues proteins seem to be necessary for but not beyond. Hoppers egest material passage of viruses through the organs from the foregut once in a while during of the vector and are required for feeding and it is thought that transmission. transmission occurs during this The two genera that have ingestion-egestion process. propagative viruses are Tenuivirus, Persistent transmission - This members of which are transmitted by involves the internal movement of the delphacid planthoppers, and virus obtained from the plant to the Marafivirus, which is vectored by the salivary glands of the insect vector. leafhopper Dalbulus maydis. These Some of these viruses are circulative viruses have an acquisition feeding while others are propagative. period of 15 minutes to 4 hours, a latent Circulative viruses - Only two period of 4-31 days, inoculation periods genera of geminiviruses ( as short as 30 seconds, and can and Curtovirus) are transmitted by transmit the virus for as long as they leafhoppers in the persistent circular live. Almost all of these viruses are manner. The viruses are acquired by the transmitted transovarially to the egg. vector after feeding for a few seconds to an hour. There is a latent period of Whitefly transmission of plant about a day, presumably for the virus to viruses reach the salivary glands. The internal Whiteflies transmit the viruses in movement of these viruses is the genus Begomovirus of the family determined by the viral coat protein and , and all the viruses in the by receptor-mediated endocytosis. genus Crinivirus and some in the genus Propagative viruses - There are Closterovirus of the family four families and genera of plant viruses . Whitefly adults are that replicate within the cells of their winged but only the first instar among insect vectors as well as the cells of the larvae is mobile. Whiteflies produce their host plants. Two of these families, many generations in a year and reach Rhabdoviridae and , contain high populations. Only a few species of whiteflies transmit viruses, mostly in the the other genera are transmitted in the tropics and subtropics, but the viruses pollen carried by the thrips vectors and they transmit cause very severe by mechanical damage during feeding diseases. Begomoviruses are of the vector. transmitted by Bemisia tabaci whiteflies, By far the most important thrips- while the criniviruses and the whitefly- transmitted viruses are the tospoviruses, transmitted closteroviruses are vectored which include the widespread and by the whiteflies Trialeuroides severe tomato spotted wilt virus and the vaporariorum, T. abutilonea, B. tabaci, impatience necrotic spot virus. In and the type B of B. tabaci (also referred tospoviruses, only the larvae but not the to as B. argentifolii). Whitefly mouthparts adults can acquire the virus, and their and feeding behavior resemble those of ability to acquire it decreases with age. aphids. Larvae sometimes acquire the virus Begomoviruses are bipartite after feeding on a diseased plant for as geminiviruses and are transmitted by little as 5 minutes, but usually they must whiteflies in the persistent circulative feed for more than an hour both in manner. A helper factor coded by the acquiring and in inoculating the virus. virus seems to be involved in the There is a latent period of 3-4 days transmission. The whitefly-transmitted before the larvae can transmit the virus. monopartite closteroviruses and the The virus is passed from the larvae to bipartite criniviruses reach only the the adults which can transmit it, foregut of the vector and are transmitted although erratically, for as long as they in the semi-persistent manner. These live. These viruses appear to multiply in viruses are retained in the vector for the vector but are not passed through about 3-9 days. Two capsid proteins the egg. Several structural proteins of help the virus in its transmission by the the virus seam to be associated with the vector. acquisition, passage through, and inoculation of the virus by its larval and Thrips transmission of plant viruses adult insect vector. About 10 species of thrips of the family Thripidae are the vectors of about Mealybug and other bug a dozen viruses belonging to four transmission of plant viruses genera (Carmovirus, Ilarvirus, Mealybugs are important as virus Sobemovirus, and Tospovirus) of four vectors primarily on some perennial families. Thrips are polyphagous insects plants in the tropics and subtropics. that have many hosts. Some of the They move slowly on plants and vector species reproduce mainly therefore are not as efficient virus parthenogenetically. The larvae are vectors as those discussed previously. rather inactive but the adults have wings They move from plant to plant, mostly and are very active. Thrips adults feed as crawling nymphs, through leaves of by sucking the contents of subepidermal adjacent plants being in contact with cells. Adults live up to 3 weeks and each other; by ants tending the there may be as many as 20 mealybugs and moving them from one generations per year. The tospoviruses plant to the other; and occasionally by are transmitted in the persistent wind. propagative manner, while the viruses of Mealybugs feed on the phloem can also be translocated through the and they are vectors of the xylem of the plant. Beetles can acquire badnaviruses, such as the cacao and can transmit the virus after feeding swollen shoot virus (CSSV), several for a few seconds and they can retain closteroviruses, such as grapevine the virus from 1 to 10 days. leafroll associated viruses and the pineapple mealybug wilt associated Virus transmission by mites virus, and the trichoviruses, such as Several members of the mite grape viruses A and B. Mealybugs family Eriophyidae transmit viruses of acquire the viruses after feeding on the genus Rymovirus which cause many diseased plants for only a few, about 20, serious diseases in grain crops. Two minutes and retain the virus for a few, mite species of the family Tetranychidae up to 24 hours, so the transmission transmit two plant viruses, one of them resembles the non-persistent or semi- transmitting the peach mosaic virus. All persistent mechanism of transmission mites in these families feed by piercing by aphids. plant cells and sucking their contents. Other bugs that transmit plant Eriophyid mites are small (0.2 viruses include the mirid bugs, which mm long), move little by themselves transmit some sobemoviruses in and, instead, they are spread by wind. manners that have characteristics of They have two nymphal instars followed non-persistent, semi-persistent, and by a resting pseudopupa. They beetle-like transmission, and the complete a life cycle within two weeks. piesmatid bugs, which transmit beet leaf Mites can acquire virus from infected curl virus in a persistent propagative host plants within 15 minutes from the manner. start of feeding and can transmit it to healthy plant within a similar duration. Virus transmission by insects that Mites acquire the virus as nymphs but have biting/chewing mouthparts not as adults. They carry the virus Although there are a few vectors through molts and remain infective for 6 in the orders Orthoptera and to 9 days. Dermaptera, there are more than 60 Tetranychid mites are larger (0.8 vector species in the order Coleoptera mm long). Pre-adult mites readily (beetles), 30 of them in the family acquire the virus and they, as well as Chrysomelidae. Most beetle vectors the adults, transmit the virus efficiently. tend to eat plant cells between the leaf veins and regurgitate during feeding, Virus transmission by pollinating thereby bathing their mouthparts with insects sap and virus. Virus transmission by Honey bees and other pollinating beetles, however, is specific between insects seem to play a role in each virus and its vector. Beetle- distributing virus-infected pollen from transmitted viruses belong to the genera infected plants to healthy ones. It Tymovirus, Comovirus, Bromovirus, and appears, however, that no special Sobemovirus. Most of these viruses are mechanisms or involvement of the small (25 to 30 nm in diameter), stable, insect are present in such virus reach high concentrations, and are transmission. easily transmitted by sap. These viruses Summary by the insect feeding on the pathogen Insects play various roles in the growing in the cavities made by its transmission of plant pathogens, and in insect vector. Also, while in most cases the initiation and development of the pathogen does not affect its insect disease in plants. In some diseases, the vector directly, there are several plant insects incidentally carry pathogens on viruses and mollicutes that multiply in their bodies or in their feces and deposit the insect vector as well as in their plant them on healthy plants where they host, and such vector insects often cause disease, without developing any show histopathological symptoms, special relationships with the pathogens. reduced reproduction, and shorter life In several cases, the insects weaken the span. Most of the insect/pathogen plants on which they feed and make associations are highly specific and them much more susceptible to attack involve sophisticated molecular by pathogens. In other cases, the mechanisms that regulate the uptake, pathogens depend on the insects to retention, and transmission of the carry them to healthy plants and to pathogen by its insect vector. deposit them on fresh wounds through See also, Plant Viruses and which they penetrate and infect the Insects, Management of Insect-Vectored plants. While pathogens seem to be the Pathogens of Plants, Transmission of beneficiaries of these actions, insects Xylella Fastidiosa Bateria by Xylem- also derive advantages by the pathogen Feeding Insects, Vectors of making the diseased plant more Phytoplasmas. attractive to the insect for feeding or breeding purposes, and in some cases,

References Agrios, G. N. 1997. Plant pathology (4th ed.). Academic Press, San Diego, California. Anonymous. Compendium of Diseases of… A series of books on diseases of individual crops published periodically by APS Press, St. Paul, Minnesota. Capinera, J.L. 2001. Handbook of vegetable pests. Academic Press, San Diego, California. Hull, R. 2001. Matthews’ plant virology (4th ed.). Academic Press, San Diego, California. Harris, K.F., and K. Maramorosch. 1980. Vectors of plant pathogens. Academic Press, San Diego, California. Hiruki, C. (ed.). 1988. Tree mycoplasmas and mycoplasma diseases. University of Alberta Press, Edmonton, Alberta, Canada. Nault, L.R. 1997. transmission of plant viruses: a new synthesis. Annals of the Entomological Society of America 90: 521-541. Schowalter, T.D., and G.M. Filip (eds.). 1993. Beetle-pathogen interactions in conifer forests. Academic Press, San Diego, California.

Figure 1. Schematic representation of the basic functions in a plant (left)and the interference with these functions (right) caused by some common types of plant diseases. (From Agrios, G.N. 1997. Plant pathology (4th ed.). Academic Press, San Diego, California.)

Figure 2. Schematic diagram of the shapes and sizes of certain plant pathogens in relation to a plant cell. (From Agrios, G.N. 1997. Plant pathology (4th ed.). Academic Press, San Diego, California.)

Figure 3. Morphology and multiplication of some of the groups of plant pathogens. (From Agrios, G.N. 1997. Plant pathology (4th ed.). Academic Press, San Diego, California.)

Figure 4. Disease cycle of bacterial wilt of cucurbits caused by Erwinia tracheiphila and transmitted by the striped cucumber beetle (Acalymma vittatum). (From Agrios, G.N. 1997. Plant pathology (4th ed.). Academic Press, San Diego, California.)

Figure 5. Sequence of events in the overwintering, acquisition, and transmission of plant viruses, mollicutes, and fastidious bacteria by leafhoppers. (From Agrios, G.N. 1997. Plant pathology (4th ed.). Academic Press, San Diego, California.)

Figure 6. Disease cycle of Dutch elm disease caused by the fungus Ophiostoma ulmi and transmitted by the European and the American elm bark beetles. (From Agrios, G.N. 1997. Plant pathology (4th ed.). Academic Press, San Diego, California.)