Symptomology, Agronomy, and Economic Considerations in Aster Yellows Management

Philip Northover, Manitoba Agriculture, Food and Rural Initiatives Crops Knowledge Centre, Box 1149 Carman MB R0G 0J0

E-mail: Philip.Northover@gov.mb.ca Abstract The aster yellows phytoplasma (formerly a mycoplasma like organism or MLO), is a single-celled prokaryotic microorganism, lacking a cell wall, capable of inciting disease in over 300 plant species. Vectored by the aster leafhopper (Macrosteles quadrilineatus Forbes =M. fascifrons), aster yellows (AY) symptoms, include proliferation, alteration of tissue pigments (red, orange, yellow, and purple), phyllody, and reduced palatability in food crops. Once a plant is infected, there is no curative treatment. Symptoms of AY often mimic other diseases or chemical damage making identification difficult. In 2007, aster yellows diseases were observed in a wide range of crops in Manitoba raising concerns among many producers. A survey of canola fields in 2007 determined aster yellows levels at 80% of fields compared to 3% in 2006, with mean incidence levels of 5.3% in 2007 compared to 1.0% incidence levels in 2006. Aster leafhoppers were monitored in Manitoba carrot fields in 2007 at levels that were seven times that of 2006, at the highest level recorded. The Aster Yellows Index (AYI) is a value that indicates when chemical application is warranted. In 2007, this level was exceeded for carrots on July 6th and reached levels as high as 35 times the economic threshold, in managed commercial fields. Incidence levels in four fields in September ranged from 10-13%, in one field, the incidence level exceeded 50%, a significant economic loss. Market considerations must be made for pest management, and management strategies employed in certain crops will not necessarily be feasible in others. The sporadic nature of AY in many field crops such as canola makes management difficult and is not an economically prudent option. In Manitoba, crops with significant economic returns (eg. carrots) in combination with regular AY outbreaks enable an integrated strategy implementing use of chemical inputs for AY management, to be employed. General Phytoplasma Biology Phytoplasmas (formerly referred to as mycoplasma like organisms or MLO’s), are highly modified bacterial plant pathogens, lacking a cell wall. Belonging to the Class Mollicutes (which includes another plant parasitic group-- the spiroplasmas), they are among the smallest of all free-living organisms. Their small size does not permit them to be viewed using light microscopy, instead the techniques of fluorescence and electron microscopy are required, to determine the presence of a phytoplasma. Pleomorphic in nature, when viewed in cross section using electron microscopy, phytoplasmas often appear as oval shaped bodies within the sieve elements of the phloem tissue. Unlike many bacterial and fungal plant pathogens phytoplasmas cannot be cultured, making diagnosis of phytoplasma associated diseases difficult. When it was learned that phytoplasmas respond to the use of antibiotics, this provided a means of determining an association between

the presence of a phytoplasma and development of disease. With the advent of recombinant DNA technology, PCR based tests made identification of specific phytoplasmas and their relatedness to each other possible. PCR amplication of the 16S r RNA genes and Restriction Fragment Length Polymorphisms (RFLP) form the basis of phytoplasma diagnostics. This does pose challenges to laboratories that are not equipped or have staff who are not familiar with molecular techniques. Aster Yellows Phytoplasma Capable of inciting disease in over 300 plant species, the aster yellows (AY) phytoplasma is present across Canada, and around the world (see Appendix 1 for a partial list). In Manitoba, a wide range of crops and weed species can become infected by aster yellows. Vegetable crops (carrot, parsnip, cabbage, lettuce, cucurbits, tomato, potato, broccoli, onions, garlic, cauliflower, rutabaga, celery), typically suffer the greatest damage relative to other crops, due in part to the reduction in quality, the unmarketable appearance, but also due to the unpalatable taste that can be imparted to the plant by infection with the AY phytoplasma.

Field Crops including oilseeds such as canola, flax, sunflower; grains including corn, wheat, barley, and oats; can all serve as host to the aster yellows phytoplasma. Leguminous crops, such as alfalfa and soybean can also serve as hosts. Among fruit crops strawberry, can be severely impacted, as well as special crops such as buckwheat, echinacea, caraway, and coriander. Grasses such as brome and ryegrasses, can also serve as hosts to the phytoplasmas. Many weed species such as plantain, dandelion, and sow thistlecan serve as reservoirs for the phytoplasma.

The aster yellows or six spotted leafhopper (Macrosteles quadrilineatus Forbes =Macrosteles fascifrons) is considered the chief vector of the aster yellows phytoplamsa in Manitoba. The leafhoppers are phloem feeders, which acquire the phytoplasma, through feeding on infected plants. The phytoplasma is capable of reproducing within the tissues of the leafhopper, and is able to transmit the

phytoplasma to healthy plants, inciting disease. The association is beneficial to the leafhopper and phytoplasma. The phytoplasma gains the benefit of a dispersal mechanism and an additional location to reproduce, while the leafhopper has been shown to have a longer life span and lay more eggs (Beanland et al. 2000), relative to leafhoppers that do not carry the phytoplasma.

Figure 1. Aster leafhopper (Macrosteles quadrilineatus) (B.Elliott)

As there is no practical way of controlling the phytoplasma directly, the leafhopper vector, must be managed in high value crops, such as carrots, lettuce, and many other vegetables.

Figure 2. Size comparison of the aster leaf hopper to a penny.

Symptom Expression Residing in the phloem, the phytoplasmas inhabit the region where nutrients, sugars, and hormones are transported. Disruption of the hormone balance in a plant can have significant effects on plant development, essentially the “blue print” of the plant is rewritten. The cause of

the symptoms caused by aster yellows is not well understood, but a number of explanations offer some insights, alteration of phloem sap content, changes in the expression of the flower development gene, clogging of sieve elements, and the action of long distance toxins.

One symptom that strongly suggests a phytoplasma is associated with a plant disorder is phyllody, the replacement of floral parts with leaves (or more accurately the prevention of the development of development of floral parts). The flowers are replaced with green parts that may appear as flattened leaf like or thickened “bladder-like structures (Figure 3) depending on the time of infection and the host plant involved.

Pigment expression is also altered by infection with the aster yellows phytoplasma. Purple, yellow, red, and bronze discolouration have been observed in a number of hosts. In carrots, leaves can appear in a

range of colours, brassica crops such as canola (Figure 4) and cabbage, and rutabaga may show reddish purple pigments in leaf tissue.

Figure 3. Bladder-like pods (phyllody) on canola. (C.Olivier)

Discolouration by itself is not necessarily a good diagnostic feature, as the degree of altered pigment expression varies with the crop. Symptoms on canola can be confused with sulfur deficiency, anthocyanin production, and Group 2 herbicide damage. In cereals, symptoms of BYDV virus can be very difficult to distinguish from infections by Aster Yellows. Taking into account a greater number of plants in many field crops often appear along field edges, due to movement into fields by the leafhopper, misdiagnosis of herbicide injury may be common.

Another symptom associated with aster yellow infection is proliferation, also referred to as “witches’-brooms”. This is the extensive (over) production of shoot and in some cases root tissue. Multiple branching may occur and the result is a “bunchy” appearing plant (Figure 5). This may be the first symptom that is likely to be observed, especially under dry conditions, when other plants may be reduced in size, these plants will be much more distinctive and easier to notice. In potatoes, the symptoms are quite unusual with tubers (which is are modified stem tissue) produced above ground (Figure 6).

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Figure 4. Discolouration of canolaster yellow infection.(M

a leaves due to .Desjardins)

Generally, not all floral parts are replaced, on a plant, and depending on the host, any remaining “normal looking” seeds may or may not be viable. Work with canola, determined that between 0.3% and 0.7% of the seeds were misshapen and 50-90% of the “normal looking” appearing seeds could germinate (Olivier et al 2007).

Figure 5. Proliferation-“bunchy growth” on carrot.

While work has been conducted with the objective of determining if aster yellows could be spread through seed, the prevailing view is that seed transmission of phytoplasma diseases does not occur, With no vascular connection between the phloem and the developing embryo, it appears improbable that seed transmission is possible. The presence of aster yellows phytoplasma has been reported on canola seed however (Olivier et al 2006).

Agronomic Considerations for Management The percentage of canola fields in Manitoba and Saskatchewan, surveyed for the presence of aster yellows, from 2001 through to 2007 is shown in Figure 7. The number of fields surveyed for each of the provinces in each of the years are shown in Table 1.

In Manitoba, the number of fields that have plants with symptoms of aster yellows, varies considerably, ranging from 2% of the fields (2003) to as high as 94% (2004). Levels in 2007 were 80% in MB, 83% in SK. The changes in the number of fields with symptoms of the disease in Manitoba from year to year do not suggest any predictive ability. It must be considered that fields with trace levels (symptoms observed at levels too low to be detected by the sampling procedures employed) to levels in excess of 20% were reported. This information suggests there is no guarantee that a region that had aster yellows in one year, will have the same or an increased level of symptomatic plants the following year. Figure 6. Stem proliferation on

potatoes (WCPD Potato Image collection).

Figure 7. Plot of the number of the percentage of canola fields with symptoms of aster yellows in Manitoba and Saskatchewan for 2001 to 2007. Due to drought conditions, there was no Saskatchewan survey in 2002.

Table 1. Number of fields examined in each of the years for canola disease surveys, conducted in each of the three prairie provinces from 2001-2007.

Year Manitoba Saskatchewan Alberta 2001 277 95 N/A 2002 297 N/A (no survey-drought) N/A 2003 259 85 N/A 2004 68 87 182* 2005 81 107 N/A 2006 33 101 N/A 2007 40 99 N/A

*Alberta data is not shown in graphs, trace amounts (<0.1% to 0.7% were detected in 2004, no other annual surveys in Alberta have been reported).

The unpredictability of the appearance of aster yellows in canola crops is contrasted to the situation with carrots, grown in Manitoba (Figure 8). In carrot production, aster yellows is an annual problem and of considerable concern. It is expected that aster yellows will be observed

in any given year to some degree, in any of the major production fields. Considering the high value of the carrot crop relative to that of most field crops, and developing a management strategy becomes more feasible. Conversely the sporadic nature of the disease in canola and other field crops make chemical uses impractical.

Figure 8. Plot of the percentage of canola (Brassica napus) fields with symptoms of aster yellows, compared to carrot (Daucus carota) fields in Manitoba over the past seven years.

The average incidence levels (the % of plants in a canola field with symptoms of aster yellows) within production fields, both 2004 and 2007 in Manitoba were higher than the rest of the values in MB and SK. In 2007, incidence levels in SK were higher than reported for the previous six years in SK. Aster yellows levels on average in canola are generally low on average, rarely exceeding 1-2% in both provinces (See Figure 9).

Figure 9. Plot of the incidence of canola (Brassica napus) with symptoms of aster yellows in Manitoba and Saskatchewan over the past seven years.

The results of the weekly monitoring of carrots conducted as part of the Manitoba Weekly Vegetable Report in 2007 are shown in Figure 10. Five carrot fields in Manitoba are represented on the graph. Seeding of some carrot fields occurred in Mid-May, and harvest took place in September. Sampling of leaf hoppers was conducted each week unless rainfall events or spray operations were in progress. On June 7th, sampling began and the first leaf hoppers were collected on July 5th, which exceeded the economic threshold level for carrots. Multiple local maxima (peaks) and local minima (valleys) were observed on the graph and indication of rising and falling population levels. The declines in the population could be attributed to application of insecticides, corresponding increases could be due to both the increase in local populations and the entrance into the field of migratory populations.

The 2007 “average” canola growing season is overlaid on the graph, seeding generally occurred around mid to late May. Flowering took place at approximately June 21st to June 28th.

If an application of dimethoate (CygonTM or Lagon®), the only active ingredient registered for aster leafhopper control in canola, was applied prior to June 28th,to canola, based on the levels caught in carrot fields, there would be no leafhoppers to spray (in addition, flowering of the crop needs to be considered to avoid negative effects on the bee population). It appears that in the carrot field, a migratory population appeared quite rapidly. An early season spray would be of

little use, as the rapid influx of leafhoppers could not have been predicted. An insecticide application would be based on a high level of uncertainty

Figure 10. Weekly changes in the aster leafhopper (Macrosteles quadrilineatus) populations in five carrot fields in Manitoba in 2007, with key events in the canola growing season superimposed over the graph. The horizontal black line represents the economic threshold for application of insecticides to for leafhopper management in carrots. The preharvest interval of dimethoate for use in canola is 21 days prior to harvest.

A single application of a dimethoate product, would also be of limited use due to the multiple generation of leaf hoppers in Manitoba (2-4 per year) and multiple migrations into fields. Generations may overlap and migrations at various times may occur which would be unaffected by a single application of dimethoate. In 2003 to 2006 aster leaf hoppers generally appeared in late June to early July, applying an insecticide prior to this would be of little use (Figure 11).

It has not been demonstrated that the aster leafhopper can overwinter in Manitoba, as the winter conditions are too harsh. Previous sweeping work in multiple years appears to confirm this, as no leafhoppers have been caught (See Figure 11). It is possible that if they were present and infective, they could be at such low levels that they cannot be detected by sweeping. Any contribution of any “overwintering leafhoppers” to disease levels could be of limited impact, as the high number of migratory leafhoppers would account for the vast majority of the leaf hopper population.

Figure 11. Weekly changes in the populations of aster leafhoppers (Macrosteles quadrilineatus) in Manitoba carrot fields from 2003 to 2006, showing the multiple generation and migration events. The orange line represents the economic threshold for application of insecticides to manages the aster leaf hopper.

Economic Considerations for Aster Yellows Management Figure 12, depicts the relationship between bushel price, gross revenue, net revenue before and after one, two or three applications of dimethoate for control of aster leaf hoppers at a yield of 30 bushels/acre. At yields below 25 bushels/acre, net revenue was below $0 for all of the price levels depicted. Only the cost of the insecticide is considered. Costs associated with the application of insecticide such as labour, fuel, machinery maintenance, etc is not considered.

At $7.75 per bushel, the net revenue is already in a loss position prior to any application of insecticide. Any additional costs would only put a producer further in a loss position. At a price of $9.21 a bushel, net revenue would be negative after a third application. At $10.00 an acre, all applications still leave the producer with a positive revenue position.

Figure 12. The relationship between gross revenue at three bushel prices, and effect on the net revenue of 0, 1, 2, or 3 applications of dimethoate (CDN$9.50) for a yield of 30 bushels/acre of canola. Cost of dimethoate application is only the cost of the chemical per acre, other costs associated with application have not been considered.

Considering the sporadic nature of aster yellows, the use of an insecticide is largely uneconomical. The typically low levels of crop loss observed in most fields, do not warrant management through chemical applications. Seeding of canola as early as possible would be worth considering, though this does not guarantee that some degree of loss will not occur. In short aster yellows will be more of an annoyance for most producers of canola, and remains a significant concern for vegetables, notably carrot grower. Summary Aster yellows is a disease caused by a phytoplasma, which is vectored by the aster or six spotted leaf hopper. Crop rotation is ineffective for aster yellows management due to the wide host range of the phytoplasma, and the annual migratory populations that come into Manitoba from the south. Diagnosis is difficult and requires specialized equipment and techniques that are not available in more basic laboratories. Visual assessment of symptoms may be sufficient in limited cases, but in some hosts symptoms can be easily confused with stress responses, nutrient deficiencies, or herbicide damage.

The sporadic nature of this disease in canola and other field crops make chemical use impractical. Planting crops as early as possible may have some benefit as the arrival of

leafhoppers in recent years often occurs in late June or early July. An insecticide application early in the year, will be of little benefit as the population of leafhoppers may be very low to non-existent, one application will do very little. The multiple generations within a season combined with migratory populations would necessitate multiple applications. When economic considerations are considered as well. management of the aster leafhopper and aster yellows with chemical means is not worthwhile in canola.

Appendix 1 Partial List of known Aster Yellow Phytoplasma hosts (modified from O’Mara et al 1993.) Family: Genus/species Common name Amaranthaceae Amaranthus retroflexus Rough pigweed Apiaceae Anethium graveolens Dill Apium graveolens Celery Apium graveolens rapaceum Celeriac Carum carvi Caraway Coriandrum sativum Coriander Daucus carota Carrot Pastinaca sativa Parsnip Petroselinum crispum Parsley Apocynaceae Catharanthus roseus Periwinkle Asclepiadaceae Asclepias nivea Common milkweed Asteraceae Ambrosia artemisiifolia Ragweed Anthemis cotula Mayweed Aphanostephus humilis Lazy daisy Bidens frondosa Beggar-ticks Bidens pilosa Hairy bur marigold Brachycome iberidifolia Swan River daisy Callistephus chinensis Aster Calendula officinalis Pot marigold Centaurea americana Basket flower Centaurea cyanus Cornflower,Bachelor’s button Chrysanthemum carinatum Tricolor chrysanthemum Chrysanthemumcinerariifolium Pyrethrum Chrysanthemum coronarium Crown daisy Chrysanthemum frutescens Marguerite daisy Chrysanthemum segetum Corn chrysanthemum Conyza canadensis Horseweed Cichorium endivia Endive Cichorium intybus Common chicory Cirsium spp Thistles Coreopsis grandiflora Tickseed Coreopsis lanceolata Tickseed Cosmos bipinnatus Cosmos Dyssodia wrightii Fetid marigold Erigeron canadensis Horseweed Erigeron linifolius Flax-leaved fleabane

Family: Genus/species Common name Asteraceae Erigeron philadelphicus Philadelphia fleabane Gaillardia pulchella Annual blanket flower Galinsoga parviflora Small flower galinsoga Gnaphalium decurrens California everlasting Gnaphalium ramosissimum Pink everlasting Helenium autumnale Common sneezeweed,

Helen’s flower Helenium latifolium Sneezeweed Helenium nudiflorum Purple sneezeweed Helenium puberulum Rosilla Helianthus annus Common sunflower Helichrysum bracteatum Strawflower Hemizonia corumbosa Coast tarweed Lactuca spp. (altaica, canadensis,

floridana, graminifolia, indica, perenis, muralis, raddeana, saligna, spicata, squarrosa, virosa)

Lettuce

Lactuca sativa Garden lettuce Lactuca scariola var. integrate Prickly lettuce Leontodon autumnalis Fall dandelion Matricaria suareolens Pineapple weed Parthenium hysterophorus Santa Maria Picris echioides Bristly oxtongue Pyrrhopappus multicaulis False dandelion Rudbeckia hirta Hairy coneflower,

Black-eyed Susan Scorzonera hispanica Black salsify Senecio vulgaris Common groundsel Sonchus oleraceus Common sowthistle Tagetes erecta African or American marigold Tagetes patula French marigold Taraxacum offinicale Dandelion Tragopogon dubius Western salsify Tragopogon porrifolius Oyster plant Verbesina enceliodes Crownbeard Zinnia elegans Zinnia Begoniaceae Begonia semperflorens Wax begonia Boraginaceae Myosotis scorpiodes Forget-me-not Brassicaceae Armoracia rusticana Horseradish (Cruciferae) Brassica campestris Common yellow mustard Brassica oleracea var. botrytis Cauliflower Brassica oleracea var. capitata Cabbage Brassica oleracea var. italica Broccoli Brassica napus Canola Brassica rapa Turnip Capsella bursa-pastoris Shepherd’s purse Cheiranthus cheiri Wallflower Raphanus sativus Radish

Family: Genus/species Common name Brassicaceae Raphanus raphanistrum Wild Radish (Cruciferae) Rorippa curvisiliqua Western yellow cress Sisymbrium irio Mustard Campanulaceae Lobelia erinus var. compacta Edging lobelia Caricaceae Carica papaya Papaya Caryophyllaceae Dianthus barbatus Sweet William Dianthus caryophyllus Carnation Gysophila paniculata Baby’s breath Spergula arvensis Corn spurry Stellaria media Common chickweed Chenopodiaceae Chenopodium album Lamb’s quarters Spinacia oleracea Spinach Cistaceae Helianthemum chamaecistus Rockrose Cucurbitaceae Cucurbita muschata Musky gourd Cucurbita pepo Pumpkin Datiscaceae Datisca cannabina Akalbir Dipsacaceae Dipsacus fullonum Fuller’s teasal Scabiosa atropurpea Pincushion flower, sweet

scabious Fabaceae Glycine max Soybean (Leguminosae) Medicago hispida Bur-clover Medicago sativa Alfalfa Trifolium fragiferum Strawberry clover Trifolium hybridum Alsike clover Trifolium pratense Red clover Trifolium repens White clover Vicia faba Faba bean Geraniaceae Erodium cicutarium Redstem filaree Erodium moschatum Whitestem filaree Gesneriaceae Didymocarpus horsfeldii Hydrangeaceae Hydrangea macrophyllum French Hydrangea Iridaceae Gladiolus x hortulanus Gladiolus Labiatae Lamium amplexicaule Dead henbit nettle (Lamiaceae) Monarda fistulosa Monarda, Bergamot Salvia azurea Azure sage Liliaceae Allium ascalonicum Shallot Allium cepa Onion Linaceae Linum usitatissium Flax Loasaceae Blumenbachia hieronymii Cajophora lateritia Malvaceae Malva parviflora Little mallow Malva rotundifolia Common mallow Onagraceae Clarkia concinna Red ribbons Clarkia unguiculata Clarkia, farewell-to-spring,

godetis Epilobium californicum California willow herb Epilobium paniculatum Panicled willow herb Gaura lindheimeri White guara

Family: Genus/species Common name Papaveraceae Eschscholzia californica California poppy Plantaginaceae Plantago major Great plantain Plumbaginaceae Limonium sinuatum Annual statice Poaceae Agropyron repens L Quackgrass (Gramineae) Andropogon scoparius Little bluestem Aristida adscensionis Needle grass Avena sativa Oats Bromus arvensis Field brome Bromus secalinus Chess brome Hordeum vulgare Barley Lolium multiflorum Common rye grass Lolium perenne Perennial ryegrass Phalaris canadensis Annual canary grass Poa pratensis Kentucky blue grass Sorghastrum nutans Indian grass Triticum aestuvum Wheat Zea mays Corn Polemoniaceae Gilia capitata Globe gilia Phlox drummondii Annual phlox Polygonaceae Polygonum convolvulus Black bindweed Rumex acetosella Sheep sorrel Portulacaceae Calandrinia grandiflora Rock purslane Portulaca oleracea Purslane Primulaceae Anagallis arvensis Scarlet pimpernel Primula polyantha Primula Ranunculaceae Anemone coronaria Poppy anemone Consolida (Delphinium) ajacis Rocket larkspur Delphinium x cultorum Hybrid larkspur Nigella damascene Love-in-a-mist Ranunculus asiaticus Persian buttercup Rosaceae Fragaria x ananassa Garden strawberry Geum chiloense Geum Scrophulariaceae Linaria bipartita Clover-lip toad flax Linaria canadensis Oldfield toad flax Mimulus cardinalis Scarlet monkey-flower Mimulus guttatus Common monkey-flower Veronica americana American speedwell Veronica buxbaumii Byzantine speedwell Solanaceae Lycopersicon esculentum

(L. lycopersicum) Tomato

Nicotiana rustica Wild tobacco Petunia x hybrida Garden petunia Solanaceae Salpiglossis sinuata Painted-tongue Solanum nigrum Black nightshade Solanum tuberosum Potato Tropaeolaceae Tropaeolum majus Garden nasturtium Urticaceae Urtica californica Nettle Vitaceae Vitis spp. Grape

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