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Susceptibility of annual medics (Medicago spp.) to powdery mildew (Erysiphe trifolii)

RA Ballard1, DM Peck1, DL Lloyd2, JH Howie1, SJ Hughes1, RE Hutton1 and BA Morgan1

1South Australian Research and Development Institute, GPO Box 397, Adelaide, SA, 5001
2
DEEDI, PO Box 102 Toowoomba, Qld, 4350 (retired)

Abstract

Data from greenhouse and field studies have been used to rate the susceptibility of commonly grown annual medics to powdery mildew (PM). Strand medic (Medicago littoralis) cultivars Angel, Herald and Harbinger are susceptible, as are the barrel medic (M. truncatula) cultivars Jester and Jemalong. Paraggio barrel medic has shown delayed development of disease symptoms and useful levels of field resistance as a mature plant. Gama medic (M. rugosa) cv. Paraponto also showed a useful level of resistance. While these cultivars provide growers with opportunity to manage PM in some areas, resistance is needed in other medic species and cultivars so that the disease can be better managed across the extensive areas where medics are grown and the disease is prevalent.

PM resistant plants (PM2) were selected from one strand medic accession and were crossed with the cultivar Angel. A cohort of lines with PM resistance was developed and field evaluation of these lines has confirmed they have good levels of PM resistance and agronomic performance. There are good prospects that a PM resistant cultivar of strand medic will be released in the medium term. The development of resistant cultivars is considered the best option for reducing the impact of the disease in medic pastures.

Key Words

Pasture, legume, medic, clover, Erysiphales, Erysiphe trifolii, Oidium, resistance

Introduction

Powdery mildew (PM) infects and causes damage to a broad range of annual Medicago species. The disease is common, with medic pastures observed by the authors to be affected from South Australia (SA) to southern Queensland (Qld), where PM was first recorded on naturalised M. lupulina in the early 1990s. In 1999, a workshop was held in Roma, Qld to determine farmer priorities for a second phase of the National Annual Pasture Legume Improvement Program. The report of that workshop to the Grains Research and Development Corporation (GRDC) stated ‘Powdery mildew in medics was the only severe disease issue that was recognised by the groups (of farmers) who utilise temperate legumes in their systems’.

The appearance of white powder (conidia) on the leaves typically occurs in spring and can cause premature leaf senescence and reduced dry matter production. In 2011, the disease caused sufficient damage to medic pastures on Eyre Peninsula in autumn that livestock carrying capacity was severely reduced (R. Latta and A. Bates pers. comm.). This coincided with increased PM infections in wheat and barley (caused by Erysiphe graminis). This general increase in mildew activity was probably associated with an increase in PM inoculum on host plants that had germinated early in the season, following late summer rains.

There are few reports describing the susceptibility of annual medics to PM. Nair et al. (2006) found accessions of M. arabica to be resistant, while barrel medic (cv. Jester), hybrid disc medic (cv. Toreador) and button medic (cv. Bindaroo) were susceptible. The barrel medic cultivar Jemalong has been reported as being resistant to Erysiphe pisi (Carine Ameline-Torregrosa et al. 2008) while Morgan et al. (2007) reported a level of resistance to Erysiphe trifolii in the cultivar Paraggio. A better understanding of the susceptibility of available cultivars is needed so that farmers and advisors in areas where the disease occurs can make informed decisions regarding their choice of pasture cultivar, and for researchers to direct efforts in the development of resistant cultivars.

In this paper we report on the susceptibility of a range of current annual medic cultivars to PM and the progress that has been made toward the development of cultivars with improved resistance.

Methods

Powdery mildew resistance of cultivars

Eight species of annual medic represented by 32 cultivars (Figure 1) were assessed for their susceptibility to PM in the field and greenhouse. They were: barrel medic (M. truncatula cv. Parabinga et al.); strand medic (Medicago littoralis cvv. Harbinger and Herald); burr medic (M. polymorpha cv. Serena et al.); disc medic (M. tornata cv. Swani et al.); snail medic M. scutellata (cv. Kelson et al.); murex medic (M. murex cv. Zodiac); sphere medic (M. sphaerocarpus cv. Orion) and gama medic (M. rugosa cv. Paragosa et al.). Common names are used hereafter.

Field plots were sown at locations where medics were known to develop PM, and were reliant upon natural infection by PM at each location. In the field at Oakey (Qld, 2000), medic cultivars were grown on an alkaline black earth as swards in small (23 m) plots, with three replicates. Plots were sown on 26 June 2000 and the proportion of medic leaves covered by PM conidia assessed on 19 October (1 = no leaves with visible PM conidia, 5 = all leaves covered with PM conidia). In the field at Urrbrae (SA, 2000), each cultivar was grown on a red-brown earth as single spaced plants forming a 1 m row, without replication. Plants were sown on 24 April 2000 and assessed on 1 November. In the greenhouse (SA, 2003), medics were grown in pots containing a soil mix providing all nutrient requirements. There were seven pots of each cultivar, with three plants in each pot. Plants were inoculated at the 2-3 leaf stage by gently brushing the plants in each pot with medic leaves covered with PM conidia. PM severity was assessed 28 days after inoculation.

Rate of disease development

At Toowoomba (Qld, 2006), cultivars of strand medic (Angel and Herald) and barrel medic (Jester, Caliph and Paraggio) were grown as swards on a neutral, gradational red earth in small (23 m) plots, with four replications. Plots were reliant upon natural infection by PM. The appearance of PM conidia was first noted on 2 October 2006. Spread of conidia on the leaves (score 1-5) was assessed 16 times over the next 53 days.

Selection and evaluation of powdery mildew resistant strand medics

One hundred and ten accessions of strand medic were screened in the greenhouse for their susceptibility to PM. One accession with a low PM score was identified and was further screened for PM susceptibility in the greenhouse and field. Within this accession, about 20% of individual plants were found not to develop PM symptoms. Progeny testing of four individual plants without PM symptoms showed that of these, two plants produced only PM resistant progeny (i.e. homozygous), hereafter referred to as ‘PM2’. The strand medic cultivar Angel was crossed with pollen from PM2. F2 plants were selected on the basis of agronomic performance and then progeny tested to identify the F2 plants homozygous for PM resistance (denoted PM-strand 1 etc.).

In 2011, 14 annual medics (six cultivars representing four medic species, seven PM-strand lines and PM2) were grown at two field sites in South Australia (Howie et al. 2012). Medics were grown as swards in 41.2 m plots, arranged in a spatially designed randomised block, with 3 replicates. At one site (Netherton, SA) a natural infection of powdery mildew was noted on 7 October and developed rapidly. As PM symptoms spread, differences in the susceptibility of the medic genotypes became more pronounced and two weeks later swards were assessed for leaf senescence (%) that was associated with the PM symptoms. Seed yields were estimated by harvesting two subsamples per plot (2 0.2 m2). Data were analysed using Linear Mixed Models (REML), GenStat (VSN International Ltd., 14th edition).

Results

Powdery mildew resistance of cultivars

PM score for most cultivars of barrel, strand, burr and disc medic was ≥ 3.5 (Figure 1). For these four species of medic, PM scores were generally consistent in the different field and greenhouse experiments, with mean scores of 3.9 (Oakey), 3.6 (Urrbrae) and 4.0 (greenhouse). Within this group of medics, the barrel medic cultivar Paraggio had the lowest PM score (mean of experiments = 2.6). Greatest variation within a species occurred between cultivars of barrel medic, where mean PM score ranged between 4.1 (Parabinga and Cyprus) and 2.6 (Paraggio). For snail, murex, sphere and gama medic, their PM score was higher in the greenhouse (mean 3.8) than in the field at Urrbrae (mean 1.6). Nonetheless, within each experiment PM score of the gama medics and in particular the cultivar Paraponto was lowest.

Rate of disease development varied substantially between medic cultivars, with the appearance of conidia significantly delayed on the cultivar Paraggio (Figure 2). PM score for Paraggio did not increase after the 43 day assessment (score 3.8) and remained significantly less (compared with Angel) at the final assessment.

Figure 1. Powdery mildew rating of 32 cultivars (eight species) of annual medic in the greenhouse and field at Urrbrae (SA) and in the field at Oakey (Qld). Not all cultivars included in all experiments. Grey bars show mean value of all experimental values for a cultivar. L.s.d. (0.05) for Oakey = 0.9, SA greenhouse = 0.4. Assigned susceptibility rating to each PM Score: 1 = resistant, 2 = moderately resistant, 3 = moderately susceptible, 4 = susceptible, 5 = very susceptible.

Figure 2. PM scores (1-5) for strand medic cultivars Angel and Herald and barrel medic cultivars Jester, Caliph and Paraggio at Toowoomba, Qld.

Figure 3. Leaf senescence (%) associated with the development of powdery mildew symptoms (bar), and kg/ha seed yield (line) of annual medic cultivars and PM-strand medic lines at Netherton, SA.

Field evaluation of PM resistant strand medics

PM2 and all of the PM-strand lines displayed less leaf senescence than the susceptible cultivars, Caliph, Angel, Herald, Toreador, Tornafield and to a lesser extent, Scimitar (Figure 3). They also out-yielded the susceptible cultivars Herald and Angel with respect to seed yield by at least 24%.

Discussion

Management of PM in medic pastures is presently limited by the level of resistance in the suite of cultivars that is available. This study indicates that most cultivars are susceptible or very susceptible to PM. An exception is the barrel medic cultivar Paraggio which has shown useful levels of resistance in both the greenhouse and field. The delayed development of symptoms on this cultivar may be of value in areas prone to autumn infections, provided it is suitably adapted to those areas. The pod holding variant of Herald strand medic (cv. Jaguar, not tested in this study) has been observed to be less susceptible than other strand medics (R. Latta pers. comm.) although this needs to be confirmed. While cultivars of snail and gama medic (this study) and accessions of spotted medic (M. arabica ) (Nair et al. 2006) are reported to have useful levels of resistance, their adaptive range and use by growers is limited. There are no commercial cultivars of spotted medic. Our finding that the barrel medic cultivar Jemalong is susceptible does not conflict with a previous report of resistance by Carine Ameline-Torregrosa et al. (2008) because that study used Erysiphe pisi. Isolates from infected medics from SA and Qld indicate that the species E. trifolii was responsible for the PM symptoms reported in this paper (I. Pascoe pers. comm.). Greater disease pressure most likely resulted in higher PM scores in the greenhouse than field for some cultivars. Cultivars with low greenhouse PM scores should have useful levels of field resistance.

Options are very limited for controlling PM where susceptible medic cultivars are grown. While fungicides are used as seed dressings on cereals to provide several weeks post sowing protection, or as preventative crop sprays in areas prone to PM, no fungicides are presently registered for use on annual medics and would rarely, if ever, be economic in the extensive farming systems where medics are grown. Where fungicides have been used to control mildews in crops such as barley, reduced mildew sensitivity to the fungicides has also been reported (Thomas et al. 2011). Resistant cultivars provide the best strategy for management of the disease. Durable resistance to PM in field pea shows that a long-term solution can be delivered by plant breeding (Tiwari et al. 1997). For the annual medics in this study, the segregation ratio of 16 F3 families suggests that the inheritance of resistance from PM2 is likely to be controlled by a single dominant gene. Better understanding of the mechanisms of resistance in medics and of pathogen variability, including possible susceptibility to Erysiphe pisi which affects field pea crops in Australia (Davidson et al. 2004), is needed to help maximise and prolong the benefits of the PM resistant medics that are being developed.

The PM-strand lines are tolerant of SU herbicide residues and bluegreen aphids. Some are also tolerant of spotted alfalfa aphids. The best of these lines have demonstrated excellent agronomic performance with up to 30% greater dry matter and seed yield than Herald and Angel across several sites (Howie et al. 2012). There are good prospects that one of the lines will be developed into a cultivar.

Acknowledgement

Funding for this work has been provided by GRDC and SAGIT. Excellent technical support provided by Jeff Hill, Sue O’Brien, Brian Johnson and Kemp Teasdale is gratefully acknowledged.

References

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Davidson JA, Krysinska-Kaczmarek M, Kimber RBE and Ramsey MD (2004). Screening field pea germplasm for resistance to downy mildew (Perononspora viciae) and powdery mildew (Erysiphe pisi). Australasian Plant Pathology 33, 413-417.

Howie J, Ballard R and Peck D (2012). Better medics update. Eyre Peninsula Farming Systems Summary 2011, 68-70.

Morgan BA, Ballard RA, Nair RM, Peck DM and Haskard K (2007). Progress in the development of barrel medic cultivars with resistance to powdery mildew (Erysiphe trifolii). Proceedings of the 16th biennial Australasian Plant Pathology Society Conference. Adelaide, South Australia, September 2007. p. 157.

Nair RM, Hughes SJ, Peck DM, Crocker G, Ellwood S, Hill JR, Hunt CH and Auricht GC (2006). Progress in the development of spotted medics (Medicago arabica L. huds.) for Mediterranean farming systems. Australian Journal of Agricultural Research 57, 447-455.

Thomas G, Jayasena K, Beard C and Blakey P (2011). Farm note 466-Management of barley powdery mildew in the face of fungicide resistance. Department of Agriculture and Food. Western Australia.

Tiwari KR, Penner GA and Warkentin TD (1997). Inheritence of powdery mildew resistance in pea. Canadian Journal of Plant Science 77, 307-310.

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