Australasian Plant Pathol. (2013) 42:321–327 DOI 10.1007/s13313-012-0180-0

Aphanomyces root rot of beans and control options A. Watson & S. L. Browne & M. G. Snudden & E. M. Mudford

Received: 7 September 2012 / Accepted: 15 November 2012 / Published online: 11 December 2012 # Australasian Plant Pathology Society Inc. 2012

Abstract Aphanomyces root rot caused by Aphanomyces euteiches is a serious disease in certain green bean (Phaseolus vulgaris) growing regions of Australia. The disease causes browning of the roots and hypocotyl and is commonly seen after periods of heavy rain. Plants often survive till harvest but yield is severely reduced, but mechanically harvested crops are often abandoned. Hymexazol proved to be a useful seed dressing to reduce disease levels. Hymexazol, azoxystrobin, and propamocarb reduced disease as soil drenches but azoxystrobin was shown to be phytotoxic in some situations. The Aphanomyces euteiches isolate used in the trials was found to infect green beans but peas were not affected. Keywords Beans . Aphanomyces euteiches . Root rot

Introduction In the 1980s a root disease of green beans (Phaseolus vulgaris) was identified in the Macksville/Valla area of the North Coast of New South Wales (NSW), Australia. The disease caused browning of the roots and hypocotyl and is commonly seen after periods of heavy rain. Plants often survive till harvest but yield is severely reduced. Investigations identified the disease as Aphanomyces root rot caused by Aphanomyces euteiches (Allen et al. 1987). Le-san® (fenuminosulph) had some efficacy against the disease however not long after this work was conducted Le-san® was withdrawn from use. Since that time large yield losses have resulted when conditions have been conducive to disease. A. Watson (*) : S. L. Browne : M. G. Snudden : E. M. Mudford NSW Department of Primary Industries, Yanco Agricultural Institute, Yanco, NSW 2703, Australia e-mail: [email protected]

Aphanomyces has been recorded on other crops in Australia including lucerne (Abbo and Irwin 1990), clover (Barbetti 1991), subterranean clover (Greenhalgh et al. 1985) faba beans (Leur et al. 2003), peas and beetroot (Hutton and O’Brien 1964; Martin 2003). A thorough review of Aphanomyces species that affected both peas and sugar beet was undertaken by Papavizas and Ayers (1974). But since then the fungus has been identified on beans and recognised as one that is specific to beans alone (Pfender and Hagedorn 1982). Since that time others have found it associated with bean root rot (Allen et al. 1987; Oyarzun and Loon 1989). Aphanomyces euteiches can be difficult to isolate from plant material and when attempted, fungi such as Pythium spp. and Fusarium spp. often outgrow it on fungal media. A selective media (Pfender et al. 1984) for Aphanomyces species is available. Identifying the fungus on the plant may be achieved by placing roots with water in small dishes such as petri dishes and observing under a microscope for the next 48 h for the characteristic sporangia and method of zoospore production. Oospores on roots typical of A. euteiches also assist in its identification. In Australia there is no routine testing of soils through a bioassay as is carried out in other countries. Control of this fungus is difficult; fungicides that are commonly used for Pythium spp. do not control Aphanomyces spp. Hymexazol has some efficacy against Aphanomyces spp. (Tomlin 2003) and is used as a seed dressing for sugar beets affected by A. cochlioides in the United States (Harveson et al. 2007). In Australia, control of this fungus relies on avoidance of infected fields, however this becomes difficult where land is either under development or buying new land is not possible. There is a lack of resistant varieties and the loss in other agronomic traits renders the resistant varieties unacceptable for production. There are no alternative management options for this disease. This paper describes investigations and trials

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conducted in Australia on control options for Aphanomyces root rot (ARR) of beans. Materials and methods In the following trials summarised in Table 1, disease was assessed by examining the hypocotyl region on bean plants and in some cases the finer roots for browning. The disease ratings were from 0 to 5 with zero indicating no disease and five the highest with severe necrosis. Plants in trials were “wet up” to induce symptoms. This was achieved by watering three times a day for 3 days in excess of field capacity at the two true leaf stage of the bean plants. This was achieved by adding 150 ml of sterile water to each pot three times a day. Assessment was carried out by carefully removing plants from the growing medium, washing them under running water and examining each plant. Analysis was undertaken using linear mixed models and fitted using the statistical software ASReml (Gilmour et al. 2006).

Experiment 1—pathogenicity test A pathogenicity test was undertaken to confirm earlier reports that the disease was caused by A. euteiches (Allen et al. 1987). A culture of A. euteiches that was isolated from infected beans was used for the test. Pieces of bean stems 1 cm above a brown lesion in healthy material were placed onto either ¼ strength Potato Dextrose Agar (PDA-Oxoid®) or selective media (Pfender et al. 1984) in 90 mm petri dishes in an incubator at 25 °C. After 2 days actively growing hyphal tips were transferred to ¼ PDA plates and placed in an incubator at 25 °C. After 5 days the plates were examined for typical A. euteiches characteristics, pieces were placed in water to observe zoospore production. Typical oospore and zoospore production was observed from the isolates on both types of media. Hyphal tips were taken from 1 week old actively growing cultures and placed onto ¼ PDA in 58 mm petri-dishes. Table 1 Experiments undertaken when investigating Aphanomyces root rot of bean in the northern NSW bean growing region Experiment

Description

1 2 3

Pathogenicity test to confirm disease causal organism Greenhouse seed dressing trial to control ARR A. euteiches levels in various soils collected from a bean growing region. Greenhouse seed dressing trial to control ARR Greenhouse soil drench trial to control ARR Field fungicide trials to control ARR Seed dressing trials to control ARR

4 5 6 7

After 1 week in an incubator at 25 °C, nine petri dishes were blended with 450 ml of sterile distilled water. Sterile vermiculite was placed into ten 100 mm pots. Five seeds (without seed dressing) of the variety Strike were sown into each pot 20 mm below the surface. Pots were placed in a greenhouse at 20/27 °C. After 1 week half the pots were treated with 25 ml of the A. euteiches solution by removing beans from the vermiculite carefully and placing the mixture at the level the roots would be and then replacing the plants. The pots were subsequently watered three times a day with 150 ml of sterile water for 3 days to induce infection. One month after sowing, all plants were assessed for disease symptoms. Experiment 2—the effect of the A. euteiches isolated on peas Ten seeds from a number of commercially available bean (11) and pea (5) varieties were planted into 200 mm pots containing infected soil. The soil was mixed with sterile vermiculite in a ratio of 50:50 (v/v). Seeds of each variety were planted 20 mm below the surface and the three replicate pots of each variety were placed randomly in a greenhouse at 20/27 °C. The pots were watered at the two leaf stage as described previously then examined 4 weeks after sowing for disease symptoms. Experiment 3—the level of disease in soils collected from a bean growing region To examine the level of disease in soils with various histories of bean cropping, soils from 12 blocks collected from five farms were used in the trial. Sampling was conducted using a soil corer (50 mm diameter) to a depth of 100 mm with 30 cores collected per block. Each soil was sieved to remove stones and then placed into tubs (square plastic containers 385 long×290wide×130 mm deep; soil depth 75 mm). There were six replicates. Thirty Simba seeds were sown 20 mm below the soil surface into each tub. Plants were maintained in a greenhouse at temperatures between 19 °C and 31 °C. At the two leaf stage plants were wet up and at 22 days after sowing, plants were assessed by counting the number with hypocotyl lesions as a percentage of the total number of plants that had germinated. Experiment 4—greenhouse seed dressing trial to control ARR The 12 soils (with varying history of bean cropping) were used immediately after the previous trial for a seed dressing trial. The tubs were planted with seed variety Simba treated with various seed dressings that included captan, thiram, A (azoxystrobin), F (fludioxonil), MF (metalaxyl + fludioxonil), FM (fludioxonil + metalaxyl-M), DM (difenoconazole + metalaxyl-M), AFM (azoxystrobin + fludioxonil + metalaxyl-

Aphanomyces root rot of beans and control options

M), hymexazol, and fosetyl Al. Six rows with ten seeds of each seed dressing were sown 20 mm below the soil surface into each tub. There were three replicates per treatment. After 9 days plants were exposed to a wetting up period. After 15 days all the plants were assessed for disease symptoms. Plants were dried at 60 °C for 3 days and weighed.

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drench of water only. The drenches were applied after planting Simba variety seed with an Earthway Precision Garden seeder at a rate of 18 seeds per metre 30 mm below the soil surface. Plots were assessed 6 weeks after sowing by removing 20 plants from each treatment when hypocotyls were rated for disease.

Experiment 5—greenhouse soil drench trial to control ARR Results Six litres of known Aphanomyces infected soil was placed into plastic tubs as described previously in Experiment 4. Drench treatments included two rates each of thiram, captan, azoxystrobin, propamocarb, and hymexazol or water only. One litre of each treatment was applied as a soil drench per tub and each treatment was replicated three times. Twenty seeds of the variety Simba were planted into each tub. The greenhouse was maintained at 18–25 °C. At the two leaf stage the tubs were wet up and after 25 days each plant was assessed for disease symptoms where only the hypocotyl was examined. Height of plants was measured (from soil level to the base of the uppermost leaves) and plants dried at 60 °C for 3 days and dry weights measured. Experiment 6—Field fungicide seed dressing trials to control ARR Two field trials were established to examine the efficacy of fungicides to control bean root disease in the field. The trials were based at two sites. Site 1 had not had beans for 6 years previously whereas Site 2 had beans grown immediately before the trials were established. The seed dressings were the same as those used in the greenhouse trial (Table 2). They were applied to untreated Simba seed and allowed to air dry. Simba seed that had already bean commercially treated with ApronXL®/Maxim® was also included in the trial. Seed was sown 30 mm below the soil surface at a rate of 18 seeds per metre using an Earthway Precision Garden seeder. Untreated seed was also sown. Plots were assessed 6 weeks after sowing by removing 20 plants from each treatment when hypocotyls were rated for disease.

Experiment 7—field fungicide soil drench trials to control ARR There were two fungicide drench trials in that same sites as the seed dressing trials i.e. Site 1 and Site 2. The fungicides used for the drench treatments were commonly available fungicides (Table 3). Each treatment was replicated four times. The plots were 5 m long and consisted of one row of beans. The fungicides were applied at a rate of 0.5 L per metre in a band width of 20 cm, untreated plots were also included. The control plots without fungicide received a

Experiment 1—pathogenicity test The beans in the pots treated with added A. euteiches showed browning of the lower stem and roots, the beans in pots without the added A. euteiches showed no disease symptoms. Roots were placed in water and zoospore production confirmed A. euteiches. To confirm Koch’s postulates A. euteiches was reisolated from the infected bean stems. Experiment 2—disease expression on beans and peas All bean varieties expressed symptoms of ARR whereas peas were not showing signs of disease with clean white stems and roots. Experiment 3—aphanomyces levels in various soils collected from a bean growing region Disease incidence was related to cropping history (Table 4). Presence of A. euteiches was confirmed by placing roots in water and examining under a microscope for characteristic zoospore production. Experiment 4—greenhouse seed dressing trial to control ARR Hymexazol reduced disease symptoms on both the hypocotyl (1.3) and roots (1.7) and had higher dry weight (3.31 g) significantly (P<0.001) compared to the other treatments (Table 5). Captan showed a significant reduction in disease compared to the untreated control. The treatments with azoxystrobin had significantly lower dry weight compared to the other treatments. There was no significance with the interaction between dressings and soils as all soils exhibited similar disease scores. The soils that had lower disease ratings previously in the cropping history trial had higher disease ratings. Experiment 5—greenhouse soil drench trial to control ARR Hymexazol (disease rating00), propamocarb (0.1), and azoxystrobin (0.2) as soil drenches were successful at controlling ARR significantly better than the untreated controls (2.7) (P<0.001) (Table 6). Hymexazol also had significantly higher dry plant dry

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Table 2 Fungicides used in trials to investigate the effect of seed dressings on ARR of beans

Seed treatment Code

Active ingredient(ai)

Rate

Captan®

captan

High

800

0.5 kg

Captan® Captan® Thiram® Thiram® Thiram® A Hymexazol F MF FM DM AFM

captan captan thiram thiram thiram azoxystrobin hymexazol fludioxonil metalaxyl + fludioxonil fludioxonil + metalaxyl-M difenoconazole + metalaxyl-M azoxystrobin + fludioxonil + metalaxyl-M

Medium Low High Medium Low

800 800 800 800 800 5 700 5 5.625+3.75 3.75+1.5 11.96+2.99 7.5+1.25+3.75

1 kg 2 kg 0.5 kg 1 kg 2 kg 50 ml 0.5 kg 50 ml 150 ml 150 ml 130 ml 100 ml

weight (9.4 g) compared to the untreated control (6 g). The hymexazol treatments had the tallest plants but not significantly taller than many other treatments. The high rate of azoxystrobin was had significantly lower plant height (10.5 cm) compared to all the other treatments (P<0.001).

Experiment 6—field fungicide seed dressing trials to control ARR Site 2 had more disease than Site 1, which had not grown beans for 6 years, as indicated by the higher disease ratings recorded in both the seed dressing and the soil drench trials (Experiment 7). At Site 1, seed treated with A and FM had significantly less disease (P < 0.001) with disease ratings of 1.3 and 1.4

Concentration of ai g/kg

respectively compared to the untreated control (3.7) in the seed dressing trial (Table 7). There were seed treatments that reduced disease at Site 2 but disease was high across all treatments, hymexazol (2.9), AFM (2.9), thiram H (3.2), DM (3.5), and captan H (3.6) had significantly (P<0.001) less disease than Simba seed on its own (3.8). At Site 2, azoxystrobin L (2.6), propamocarb H (3.2) and propamocarb L (3.7) had significantly less disease (P<0.001) compared to the plots without a treatment (4.0). Site 2 had beans a short time before the trial was established and therefore higher disease pressure.

Table 4 Soils collected from blocks in a bean growing region in northern NSW: samples collected, history of bean production and disease incidence Soil number

Farm

History

Percentage of stems showing infectiona

1 2 3 4 5

1 2 3 4 4

Beans 30 years previous. Never had beans before. No beans for 6 years. Last beans 8 years ago. Last beans 10 years ago.

2.3 a 6.1 ab 10.7 ab 17.7 b 27.9 c

6 7 8 9 10 11 12 P LSD 5 %

5 3 5 3 3 4 3

Beans 3 years ago. Beans 3 years ago. Beans previous year. Beans within the last year. Beans within the last year. Beans within the last year. Beans within the last year.

68.1 d 69 de 78.6 ef 80 fg 86.4 fg 91.1 g 96.4 g <0.001 9.6

Table 3 Fungicides used in trials to investigate the effect of soil drenches on ARR of beans Fungicide active ingredient(ai)

Concentration of ai

Rate

Product Rate/100 l

Azoxystrobin Azoxystrobin

500 g/kg

High Medium

100 g 50 g

Low High Medium Low High Medium Low High Medium Low

25 g 125 g 62.5 g 31.5 g 250 ml 125 ml 62.5 ml 150 g 100 g 50 g

Azoxystrobin Captan Captan Captan Propamocarb Propamocarb Propamocarb Thiram Thiram Thiram

800 g/kg

600 g/L

800 g/kg

Product rate/ 100 kg seed

a

Values with the same letter not significantly different

Aphanomyces root rot of beans and control options Table 5 Disease levels and plant dry weights in a seed dressing trial for ARR

a

Values with the same letter are not significantly different

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Fungicide

Active ingredient

Hymexazol Captan® Alliette® Thiram® AFM

hymexazol captan fosetyl Al thiram azoxystrobin + fludioxonil + metalaxyl-M fludioxonil difenoconazole + metalaxyl-M fludioxonil + metalaxyl-M azoxystrobin metalaxyl+fludioxonil

F DM FM A MF Untreated P LSD 5 %

Experiment 7—field fungicide soil drench trials to control ARR At Site 1, thiram M (0.5), and thiram H (1), azoxystrobin H (0.7), M (1.4), and L (0.8), had significantly less disease (P<0.001) than the untreated plots in the soil drench trial (2.5) (Table 8).

Discussion In field and greenhouse observations on ARR, the disease does not kill the plant, although a severe check is made on plant growth and other fungi may invade weak plants contributing to plant death. Beans can recover by developing new roots above Table 6 The effect of fungicide drenches on controlling disease in Aphanomyces infected soil

a

Values with the same letter are not significantly different

Active ingredient concentration g/100 kg seed

Hypocotyl ratinga

700 800 480 800 7.5+1.25+3.75 5 11.96+2.99 3.75+1.5 5 5.625+3.75

Root ratinga

Mean plant dry weighta (g)

1.3 a 2.9 b 3.0 bc 3.1 bcd 3.1 bcd

1.7 a 2.3 b 2.4 bc 2.4 bc 2.3 b

3.31 e 2.50 bc 2.82 d 2.62 bcd 1.99a

3.2 cde 3.2 cde 3.2 cde 3.2 cde 3.3 de 3.4 e <0.001 0.24

2.4 bc 2.6 d 2.6 d 2.5 cd 2.4 cd 2.6 d <0.001 0.16

2.63 cd 2.49 bc 2.59 bcd 1.92a 2.31 b 2.54 bcd <0.001 0.31

severe lesions; production can be achieved if beans are hand picked but the lack of uniformity in flower production renders the crop useless for mechanical harvesting. The pathogenicity of Aphanomyces euteiches f.sp. phaseoli on beans was confirmed after first being determined by Allen et al. (1987), but it was not found to infect peas. The level of disease from different soils was demonstrated to be related to the time since beans were last grown. Blocks that had grown beans in more recent years had higher levels of disease. This confirms growers’ experience that they need to leave blocks without beans for many years before replanting beans. This situation makes it very difficult to continue bean production as new ground must always be found. Growers do not have land available to achieve this therefore it is critical for management options to be found for ARR to ensure the survival of the bean industry in affected regions.

Fungicide

ai/m2

Mean hypocotyl ratinga

Percentage of disease free plantsa

Average Plant Heighta (cm)

Mean plant dry weight (g/plant)a

Hymexazol H Propamocarb H Azoxystrobin H Propamocarb L Azoxystrobin L Thiram H Hymexazol L Captan H Captan L Thiram L Untreated P LSD 5 %

3.8 13.4 4.5 3.4 1.1 10.7 1.3 9.0 2.9 3.6

0.0 a 0.1 a 0.2 ab 0.4 ab 0.5 ab 0.9 bc 1.3 cd 1.5 cde 1.9 de 2.2 ef 2.7 f <0.001 0.71

100.0 96.2 82.9 73.4 56.2 46.8 16.4 20.8 21.3 10.4 7.3 <0.001 25.0

14.2 a 12.3 bc 10.5 d 13.6 ab 12.9 ab 12.8 ab 14.2 ab 13.5 ab 13.8 ab 13.9 ab 13.2 ab <0.001 1.7

9.4 a 7.6 de 7.2 de 9.0 a 9.0 a 7.8 cde 8.8 ab 7.8 cde 8.3 abc 9.1 a 6.0 f <0.001 1.1

g g g g g g g g g g

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Table 7 Disease ratings for the field trials at Site 1 and Site 2 with various seed dressings Site 1

Site 2

Fungicide

Disease ratinga

A FM Hymexazol AFM Captan M Captan H F Thiram H Simba ApronXL®/Maxim® Captan L DM Thiram L MF Thiram M Simba untreated P LSD 5 % a

1.3 1.4 1.7 1.7 1.7 2.0 2.0 2.1 2.2 2.3 2.4 2.4 3.3 3.7 3.7

a a ab ab ab bc bc bc bc c c c d d d

Fungicide

Disease ratinga

hymexazol AFM thiram H DM captan H A Simba thiram L captan M Simba untreated MF F captan L FM thiram M

<0.001 0.5

2.9 a 2.9 a 3.2 ab 3.5 b 3.6 bc 3.7 bcd 3.7 bcd 3.7 bcd 3.8 cd 3.8 cd 3.8 cd 3.9 d 3.9 d 3.9 d 4.0 d <0.001 0.3

Values with the same letter are not significantly different

The greenhouse seed dressing trials showed some improvement with disease control using thiram and captan but

Table 8 ARR disease ratings for field trials at Site 1 and Site 2 with various soil drenches applied to beans Site 1 Fungicide

Site 2 Disease ratinga

Fungicide

Thiram M Azoxystrobin H Azoxystrobin L Thiram H Propamocarb L Captan M

0.5 a 0.7 ab 0.8 ab 1.0 bc 1.1 bc 1.2 bc

azoxystrobin L propamocarb H propamocarb L captan H azoxystrobin H thiram M

Azoxystrobin M Propamocarb H Propamocarb M Simba Captan L Thiram L Captan H P LSD 5 %

1.4 c 1.7 c 2.4 d 2.5 d 2.5 d 2.5 d 2.6 d <0.001 0.5

propamocarb M thiram L azoxystrobin M thiram H captan L captan M Simba

a

Disease ratinga

Values with the same letter are not significantly different

2.6 3.2 3.7 3.8 3.8 3.8

a b c cde cde cde

3.9 cde 3.9 de 3.9 de 4.0 de 4.0 de 4.0 e 4.0 e <0.001 0.2

the best control was achieved with hymexazol. Hymexazol has registration in other countries to control A. cochlioides on sugar beet (Harveson et al. 2007). The product is not available in Australia. Hymexazol also performed the best in the greenhouse soil drench trial although azoxystrobin and propamocarb also showed disease control potential. The success of propamocarb and azoxystrobin is important as these fungicides are available in Australia and are potential control options. Previcur® (active ingredient propamocarb) is used for Aphanomyces spp. control in European countries. Apart from the potential of having some of these fungicides for ARR, the economics of the application of these fungicides as soil drenches needs to be considered. Further development of the rates used also needs to be examined. The field trial results were not as clear as the greenhouse trials. Site 2 had more severe disease levels than Site 1. Site 1 was adjacent to the current season’s crop whereas Site 2 had beans in the current year. Site 2 was also watered heavily to induce disease whereas Site 1 was watered only as the crop needed it. A. euteiches thrives on heavily watered situations. Azoxystrobin and propamocarb as soil drenches and hymexazol as a seed dressing reduced disease levels. The field trials were left for much longer than the glasshouse trials so disease progressed more than in the greenhouse. Follow up applications of drenches may improve disease control. As there was some reduction in disease levels the use of targeted soil drenches may be useful in managing ARR. One observation was that azoxystrobin had some phytotoxic effect on young seedlings. This was observed in the greenhouse drench trial but was not observed in the field trials. If the product is not close to germinating seedlings then the effect on the plant may be minimised. Aphanomyces euteiches was found to cause ARR most severely in heavy rainfall situations. However it was observed that the fungus infected bean roots under normal irrigation applications but symptoms under these conditions are less severe. Zoospores of the fungus only move short distances with free water (Papavizas and Ayers 1974), therefore the fungus requires old infected bean tissue in the soil close to current bean roots/hypocotyls. Observations during this project confirmed that old bean residue is the source of the fungus. It was observed that if beans were planted away from any old bean residue the beans did not have symptoms of ARR whereas those near residue had symptoms. Beans cannot be grown on old bean ground for many years after the previous crop. This has been observed by others (Sherwood and Hagedorn 1962). It appears that oospores left in the crop residue are the primary source of new infection and not from the fungus surviving in plant material as a saprophyte. After harvest bean residues (stems and roots) are either worked in or more likely eaten by stock. However the lower stem and roots remain in the soil as an inoculum supply for

Aphanomyces root rot of beans and control options

future crops. Breakdown of this material is critical for reducing carryover of the disease. Using a pre planting soil assessment to evaluate disease levels should be considered by growers who have issues with ARR as it provides important information on disease levels before planting. Acknowledgments This work has been partly funded by HAL using the vegetable levy and matched funds from the Australian Government.

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