Journal of the Department of Agriculture, Western Australia, Series 4

Volume 35 Number 1 1994 Article 12

1-1-1994

Virus diseases of subterranean pastures and their management

David Ferris

Roger Jones

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Recommended Citation Ferris, David and Jones, Roger (1994) " diseases of subterranean clover pastures and their management," Journal of the Department of Agriculture, Western Australia, Series 4: Vol. 35 : No. 1 , Article 12. Available at: https://researchlibrary.agric.wa.gov.au/journal_agriculture4/vol35/iss1/12

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By David Ferris and Roger Jones Although infected plants cannot be cured of Plant Virologists, Plant Protection Branch virus infection, pastures can be managed to South Perth reduce both virus spread and persistence from year to year. Management options depend on In Western Australia and southern Australia which virus is present and include reseeding generally, subterranean clover mottle (SCMV) with resistant varieties; changing the pasture and bean yellow mosaic (BYMV) are the most composition so that non-host species damaging virus diseases of subterranean predominate; altering grazing practices to clover pastures. limit spread; and application of pesticide Recent surveys have shown that both are far sprays to kill . more widespread in Western Australia than was previously recognised, the most seriously affected pastures being in high rainfall areas (more than 600 mm) around Albany, Bunbury, The Busse/ton and Manjimup. Pastures grazed by SCMVand BYMV only survive in living sheep and cattle are affected equally. tissue; they cannot survive in soil or in plant The extent of virus infection within individual debris. The minuscule virus particles are pastures varies. In winter infection is normally spherical (SCMV) or filamentous (BYMV). low, but it spreads rapidly in spring and can SCMVinfects , medics and , but exceed 95 per cent of plants. Unless infection spreads fully through the plant subterranean clover plants are inspected only in some clover species. closely, infection is often overlooked. BYMV has a wider host range, infecting This has led to considerable underestimation many legumes - for example, lupins, of the losses caused by virus diseases in subterranean clovers, several species of pastures in the past. naturalised clovers and some perennial SCMV is spread in pastures by the grazing and native legumes. BYMV can also infect a few trampling of animals, while BYMV is species in other families of flowering plants. transmitted by aphids. When pastures die at SCMVis a stable virus found at very high the end of the growing season, both viruses concentrations in infected plants. It is are carried over in seed, but with BYMV there spread by the chewing and trampling of is also some secondary carry-over in native grazing animals. Sap from damaged leaves of perennial legumes. infected plants is transferred by the grazing Both viruses reduce herbage and seed animal to healthy plants and enters cells production, and pasture persistence, through wounds in their leaves. cause subterranean clover plants to develop BYMV occurs at lower concentrations in less efficient root nodules, and are a cause of plants and is transmitted from infected to pasture deterioration. These effects on healthy plants by aphids. When the pastures diminish production in all animal• feeds, its mouthparts become contaminated based industries.

40 W.A. JOL'RJ 'AL OF AGRICULTI;RE Vol. 35 1994 with virus particles that adhere to the internal surfaces. These particles infect healthy plants when the aphid probes to feed on them. However, the aphid loses the virus after only one or two probes on healthy plants. The blue-green aphid trampling. When stock move away, they spread the virus away from the original () is the most •ABOVE LEFT: Patch of widespread and important carrier (vector) infection sites to form new ones. dwarfed and mottled of BYMV in subterranean clover pastures, Infection with both viruses spreads slowly in BYMV-infected plants in a but cowpea (Aphis craccivora), green peach pastures until late winter and then increases Karri.dale sward. (Myzus persicae) and spotted very rapidly in spring, sometimes affecting .... (Therioaphis trifolii) aphids are also almost all plants (see Figures la and b). involved. ABOVE RIGHT: Patch of However, when there is an early start to the dwarfed and mottled SCMV• season and above average autumn aphid infected plants in a Virus persistence over summer activity, there is sometimes a burst of early Woogenellup sward. SCMV is seed-borne at a relatively low level spread of BYMV. The spread continues until in subterranean clover, normally less than temperatures are lower in winter, when 0.5 per cent. It is also seed-borne at low aphids become less active. levels in several naturalised clovers found in pastures. These include hop (Trifolium campestre) and woolly (T. tomentosum) clovers. Seed transmission in these clovers en 100 is its only known means of survival in pas• E G) Dinninup 0 tures over the dry summer. Q. 80 -E In contrast, BYMV does not seem to be >, seed-borne in subterranean clover. en 60 > However, several naturalised clovers ~ including hare's foot (T. arvense), cluster o 40 (T. glomeratum) and hop clovers can carry Cl) Q) 20 BYMV in their seed, but the level of seed Cl transmission is low, less than 1 per cent. cca oz Q) 0 In a large scale survey of perennial native ,._o 15/9 30/9 20/10 Q) legumes, BYMV was detected in only 1 per n, cent of samples. Species of Hovea and Assesssment date Kennedia were both found to harbour BYMV and are potential minor sources from which BYMV could spread to pastures. en 100 E Ju nee Narrow-leafed lupin crops infected with 0 G) Q. 80 BYMV are not a source of infection for -E >, subterranean clover pastures because the en virus kills the plants. The virus spreads to > 60 lupins crops mostly from infected subterra• ~ o 40 nean clover pastures. Cl) Q) Virus spread within pastures Cl ca 20 Wingless aphids are mainly responsible for c -Q) localised spread of BYMV outwards from ,._o Q) infection sites. They walk from plant to n, O 29/9 6/10 20/10 3/11 17/11 plant, resulting in expanding often circular patches of infection in the pasture. Flights of Assesssment date winged aphids spread BYMVto new sites of infection. .... Figure 1. Spread of SCMV in spring in grazed rows of varieties of subterranean The spread of SCMV is similarly patchy clover differing in resistance/susceptibility. Susceptible (Junee and Dinninup), owing to increased spread around sources moderately susceptible (Karri.dale) and partially resistant (Gou/bum) (a) 1992 of the virus during localised grazing or (Busse/ton) (b) 1993 (Manjimup).

W.A. JOUR.."lAL OF AGRICULTURE vot. 35 1994 41 ... In general, spread of infection is favoured Heavy grazing directly favours spread of ABOVE LEFT: BYMV SCMV, and it also indirectly favours spread infection in Woogenellup by: leaves showing vein • greater numbers of seed-infected plants of both viruses by preventing shading out of clearing (centre) and vein becoming established, infected plants by more vigorous healthy clearing and mottle (left). ones. When infected plants are shaded out, Healthy leaf on the right. • the presence of susceptible subterranean the source of infection for spread is clover varieties, removed . • heavy grazing, The abundance and activity of aphids in the ABOVE RIGHT: SCMV• pasture are important in determining the infection in Woogenellup • warm winter conditions, extent of BYMV spread. Early aphid arrival, leaves showing mottle, leaf followed by rapid colonisation and build-up deformation and reduced • high aphid populations and low plant leaf size. Healthy leaf on density (BYMVonly), and to large numbers, results in infection of the the right. greatest numbers of plants. Bare areas in • an extended growing season in spring. newly-sown pastures and in older pastures with low densities of plants often attract BELOW- lnterveinal pallor At the start of the season, good rains favour (chlorosis), mottle and establishment of seed-infected plants. This incoming winged aphids, resulting in in• leaf deformation in BYMV• increases the primary virus source for creased BYMV infection, starting with the infected plants of variety secondary spread to susceptible healthy plants around the edges of bare patches. Karridale. ... plants . Warm conditions increase virus concentra• When most plants in the pasture belong to tion in plants and the virus is then spread B07TOM: Close up of sheep more readily to healthy plants. Warmer track showing dwarfed plants a variety (or varieties) of subterranean with SCMVsymptoms clover that is susceptible to SCMV, the conditions also favour early aphid build-up. surrounded virus spreads more readily. The same An extended growing season allows the by healthy plants. ... applies for BYMV susceptible varieties and rapid phase of spread to continue for longer ____....., __BYMV spread. in spring, resulting in more extensive infection. Finding infection in pastures The first signs of SCMV and BYMV infection in subterranean clover are a paleness of minor veins (vein clearing) followed by a distinct mottle in newly expanded leaves. The vein clearing later disappears. Symptoms of both viruses are generally similar as infected plants age, but BYMV usually causes an obvious interveinal pallor (chlorosis) in young leaves, which can help to distinguish the two viruses. Plants in• fected with either virus become dwarfed with misshapen, small and mottled leaves. It is often difficult to find infection with either virus before September, because in winter there are few infected plants and they are often dwarfed and hidden among taller healthy clover plants. In spring, the number of SCMV-infected plants increases rapidly and newly infected plants develop more distinct disease symp• toms. The easiest places to find SCMVare around gateways, along sheep tracks and in heavily trampled areas. Expanding pale yellow patches of affected plants in heavily grazed pastures are also typical.

42 \\ .A. JOURNAL OF AGRICULTLRE Vol. 35 1994 BYMV also spreads quickly in spring. Surveys of subterranean clover pastures in BYMV-affected patches are often more the south-west corner of the State during ... abundant towards the edges of paddocks, spring in 1989 and 1990 (SCMV) and 1990 ABOVE RIGHT:A trial at Mt Barker to determine the on raised areas within them and centred (BYMV)detected SCMV in 94 of 155 pastures effect of SCMV on around small areas of bare ground. Newly tested and BYMV in 23 of 87 pastures. In productivity of grazed sown pastures with low plant densities are some pastures the incidence was greater swards. particularly liable to BYMV infection. than 95 per cent of plants infected. These BYMV is not associated with sheep tracks, surveys were based on sampling 100 shoots ABOVE• LEFF: Heavily but is sometimes common in heavily per pasture, so failure to detect virus does SCMV-infected pasture at trampled areas, for example around gates. not mean that it was not present at a lower the end of the growing SCMV or BYMV infection alone rarely cause level in the pasture. season showing general plant dwarfing, early plant death or patches of dead pasture. The BYMV survey was in a non-epidemic senescence and yellowing. However, in late spring they can cause early year (1990). Much higher incidences were senescence, which is sometimes confused found in 1992, an epidemic year for BYMV. with the effects of clover scorch disease (Kabatiella caulivora). Losses in productivity Subterranean clover pastures severely Distributionin WesternAustralia infected with virus disease produce less Areas most affected by SCMV and BYMV infection is found in sub• herbage and seed. Deleterious effects of SCMVand BYMV infection terranean clover pastures in high rainfall virus infection include losses in green feed, in subterranean clover regions from Esperance to Pinjarra, with the hay, silage and dry summer feed, reduced pastures in the south• western comer of Western distribution of BYMV also extending to nutritive value, reduced legume persistence Australia. Geraldton and to medium rainfall zones. and increased susceptibility to root rots. However, individual pastures seriously .... affected ( over 50 per cent of plants infected) are usually only found in high rainfall areas (more than 600 mm) in the south-west corner of the State (see map). The Albany, Bunbury, Busselton and Manjimup districts Perth are the most affected. •

0 25e 50 75 100 I I I I I Table I. Virus infection lowers productivity of km subterranean clover

Variety % decrease % decrease in herbage in seed yield dry weight Harve• y Subterranean clover mottle virus Spaced plants Karri dale 49 91 Bunbury Woogenellup 91 93 Grazed swards Dalkeith 20 19 Dinninup 15 31 Woogenellup 28 Bean yellow mosaic virus Spaced plants Esperance 88 76 Green Range 63 58 Grazed swards Denmark 18 47 Karridale 49 12 Leura 25 35

W.A. JOURNAL OF AGRICULTUREVol . 35 1994 43 FAR RIGHT: An SCMV resistance screening trial, showing grazed test rows.

RIGHT: Screening for resistance to SCMV - left row, Denmark (partially resistant); right row, Woogenellup (susceptible). Only Woogenellup shows widespread SCMV symptoms of yellowing and dwarfing. Infected plants also produce less efficient We have established the extent of herbage root nodules. Reduction in clover seed yield, and seed productivity losses caused by compounding year by year, hastens pasture SCMV and BYMV infection in field trials. deterioration. We did this using spaced plants and The impact of virus infection on productiv• subsequently in grazed subterranean clover ity is most severe when virus spread starts swards (see Table 1). Losses within virus• early and the subsequent spread results in a infected patches in grazed swards were up high level of infection in the pasture. to 49 per cent for herbage and 47 per cent The impact is less severe when spread for seed. develops later, because plant stunting is less Results showed that herbage production in marked in recently virus-infected plants and swards increased as the percentage of the season may cut out before many plants infected plants decreased (see Figure 2). become infected. Reduced seed yields were partly due to The impact of virus infection on fewer seeds forming and partly to seed being productivity is also less severe when smaller. Poorer seed yields result in dimin• Figure 2. The relationship healthy subterranean clover plants ished pasture regeneration because fewer between loss in herbage dry weight and percentage overgrow stunted, infected plants within seedlings grow and smaller seeds deplete virus infection in grazed swards. seedling vigour. subterranean clover For example, this occurs when grazing swards. pressure is low or pastures are closed up for Susceptibility and resistance hay production. We have developed procedures to screen subterranean clover for resistance to BYMV and SCMV in the field. Resistance/suscepti• c? 5 .c bility results were obtained for BYMV (1991, Woogenellup 1992, 1993) and SCMV (1992, 1993) mainly --.x:Ol 0 4 infected with with varieties grown in the medium to high 0 SCMV rainfall areas (SCMV) and for the full range ~0 3 of named varieties (BYMV). .c -Ol Subterranean clover mottle virus ·a5 2 3: Our method of screening subterranean Karri da..le C' clover varieties and breeding lines for SCMV -0 1 infected with resistance under field conditions is to Q) Ol BYMV establish plots consisting of paired rows, cu transplant small plants infected with SCMV .0 0 L. between the paired rows to act as an infec• Q) 0 10 20 30 40 50 60 70 80 90 100 I tion source, graze plots continuously with Percentage plants with virus symptoms sheep, and make visual assessments for virus symptoms. Based on glasshouse screening work, we Table 2. Subterranean clover mottle virus previously used three categories of susceptibiJity/resistance ratings in subterranean resistance to SCMV infection: 'susceptible', clover varieties 'partially resistant' and 'highly resistant'. Susceptibility in varieties Dalkeith, Dinninup, Susceptible Moderately Partially Highly Junee and Woogenellup was confirmed in susceptible resistant resistant the field (see Table 2 and Figures la and b). In the field, partial resistance largely breaks Daliak Green Range Denmark Clare down in varieties Green Range, Karridale and Mt Barker but was confirmed in Dalkeith Karri dale Goulburn Gosse Denmark, Goulburn, Leura, Nuba and Seaton Dinninup Mt Barker Leura Larisa Park. Green Range, Karridale and Mt Barker are therefore now placed in the new Ju nee Nuba Meteora category 'moderately susceptible'. High resistance is found in varieties of the Woogenellup Seaton Park Rosedale yanninicum subspecies - Gosse, Larisa, Trikkala Meteora, Trikkala and Yarloop. Two Yarloop varieties of the brachycalycinum subspecies, Clare and Rosedale, are also highly resistant. This high resistance is effective in the field.

44 W .A. JOlcRNAL F AGRICULTl,Rf. Vol. 35 1994 A BYMV resistance screening trial, showing test rows with BYMV- . infected transplants at the end of each row.

White (T repens), red (T pratense), and Bean yellow mosaic virus balansa (T balansae) clovers are resistant Our method of screening subterranean to SCMV in the field. Naturalised suckling clover varieties and breeding lines for BYMV clover (T dubium) is resistant also but resistance in the field is to establish single cluster clover is often found infected in row plots, each thinned to 100 plants, and pastures. It is likely that other naturalised transplant small infected plants at both ends clovers which include drooping flower of each row to allow natural aphid activity to (T cemuum), hare's foot, hop and woolly transmit BYMV from the transplants. Visual clovers become infected in pastures because assessments are made for virus symptoms they are readily infected in the glasshouse within the rows. and SCMV has been shown to be seed-borne Field experiments show that there is a wide in some of them. range of resistance to BYMV. Among cur• Highly resistant clovers can become infected rently recommended mid and late season locally when infective sap is inoculated to varieties of subterranean clover Denmark, leaves but the virus fails to move systemi• Karridale, Leura and Meteora are 'highly cally in the plant. With partially resistant susceptible', Goulburn, Larisa, Seaton Park clovers, systemic movement occurs only in and Trikkala are 'susceptible', Junee is a proportion, usually small, of the infected 'moderately susceptible' and Dalkeith and plants. Northam are 'moderately resistant' Based on experiments in growth cabinets (see Table 3). with SCMV and subterranean clover varie• No variety of subterranean clover is highly ties, we believe that the systemic infection resistant to BYMV. Within the 'resistant' that develops in some plants in partially category, a small proportion of plants resistant varieties is mainly in response to always become infected when there are higher temperatures in spring. many virus-carrying aphids. 'Resistance' appears associated with early maturity of varieties.

Table 3. Bean yellow mosaic virus susceptibility/resistance ratings in subterranean clover varieties

Highly Susceptible Moderately Moderately Resistant Highly susceptible susceptible resistant resistant

Bacchus Marsh Clare Daliak Dalkeith Dwalganup one Denmark Esperance Dinninup Northam Nungarin Karri dale Gou I burn Enfield Uniwager Rosedale Leura Gosse Gerald ton Meteora Green Range Howard Nangeela Larisa Junee Tallarook Mt Barker Seaton Park Trikkala Woogenellup Yarloop

¥..A. JOUR. AL OF ;XGRICl'LTl RE Vol. 35 1994 45 Further reading Arrowleaf (T. vesiculosum), red and balansa • Strip grazing is not recommended where Jones, R.A.C. (1992). clovers are susceptible to BYMVbut white there has been a history of SCMV in the Further studies on losses and strawberry er. fragiferum) clovers are pasture, since this practice will maximise in productivity caused resistant. Infection in arrowleaf and balansa virus spread. by infection of annual pasture legumes with clovers is a worry in annual pastures, given three viruses. Australian the current interest in these two species. Management strategies for BYMV only Journal of Agricultural Susceptible naturalised clovers in pastures In pastures affected by BYMV there is a Research 43: 1229-1241. include suckling, hop, woolly, hare's foot balance between aphid numbers, relative Jones, R.A.C. (1994). and drooping flower clovers. content of susceptible subterranean clover Infection of subterranean varieties, pasture height and virus disease. clover swards with bean Management to minimise losses yellow mosaic : Colonisation of clover swards by aphids is losses in herbage and Although infected plants cannot be cured of the main cause of increased spread of BYMV seed yields and patterns virus infection, subterranean clover pas• infection and is most likely to occur after of spread. Australian tures can be managed to reduce virus aphid flights in autumn and late winter I Journal of Agricultural spread, production losses and persistence spring. Research 45: of the viruses in seed over summer. • When reseeding pastures, sow at the McKirdy, S.J., Coutts, Pastures should be monitored throughout B.A. and Jones, R.A.C. highest possible seeding rate. Sparse swards (1994). Occurrence of the growing season for the presence of virus with bare earth between plants tend to bean yellow mosaic virus symptoms. This is particularly important in attract migrant aphids; complete ground in subterranean clover September and October when spread is cover, as in dense swards, has the opposite pastures and perennial rapid. If infection is found, the following effect. native legumes. general management practices help to Australian Journal of • When resowing, varieties like Dalkeith, Agricultural Research 45: reduce losses: 183-194. Junee and Northam that are moderately • In spring, reduce stock numbers to allow susceptible, moderately resistant or resist• Wroth, J.M. and Jones, pastures to grow to more than 20 cm. R.A.C. (1991). Virus ant, may be worth using where there is a Healthy plants will then shade out some of history of heavy BYMV infection in a pas• diseases of subterranean the infected plants that are the source for clover. Department of ture. Use the highest possible seeding rate Agriculture, Western further virus spread. to dilute the proportion of susceptible Australia Farmnote No. varieties in the seed bank. 68/91. • Use the most virus-infected pastures for hay production in late September rather • If small BYMV-infected patches or iso• Wroth, J.M. and Jones, than continue grazing. This will limit both R.A.C. (1992). lated infected plants are seen scattered Subterranean clover further virus spread and losses in herbage about in the pasture in autumn, consider mottle virus infection of and seed production. Also, less seed will be applying a pesticide spray in winter to kill subterranean clover: infected. widespread occurrence aphids and delay further BYMVspread. In in pastures and effects • Increase the proportion of non-suscepti• spring, sprays may be more effective after on productivity. ble species in the pasture. For example, heavy grazing, since the spray may not Australian Journal of penetrate a dense sward well. Pesticides are Agricultural Research 43: abundant ryegrass can help reduce virus 1597-1608. spread in subterranean clover by both most likely to be economical with seed grazing animals (SCMV) and aphids (BYMV). crops or when a spray is used to kill another insect pest at the same time as the aphids. Management strategies for SCMV only • Do not graze pastures heavily in spring In pastures infected with SCMVthere is a to reduce aphid numbers because this balance between stocking rate, pasture favours both the survival of BYMV-infected height, relative content of susceptible source plants and the spread of SCMV. subterranean clover varieties and virus infection. Heavy grazing, the principle factor Acknowledgements responsible for increasing spread of SCMV, has its greatest effect during spring. The Australian Wool Corporation provided financial support and technical support • Do not sow subterranean clover seed came from members of the Department of harvested from SCMV-infected pastures. Agriculture's plant virus research group. • Resowing with Trikkala or with mixtures Some of the data used were provided by S.J. of Trikkala and Larisa or Trikkala and McKirdy (BYMV)and J.M. Wroth (SCMV). ._J Meteora (varieties with high resistance) is recommended for paddocks with a history of pasture production problems caused by SCMV. Use the highest possible seeding rate to dilute the proportion of susceptible varieties in the seed bank.

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