Australian Cool-Season Pulse Seed-Borne Virus Research: 1. Alfalfa and Cucumber Mosaic Viruses and Less Important Viruses

Abstract

Here, we review the research undertaken since the 1950s in Australia's grain cropping regions on seed-borne virus diseases of cool-season pulses caused by alfalfa mosaic virus (AMV) and cucumber mosaic virus (CMV). We present brief background information about the continent's pulse industry, virus epidemiology, management principles and future threats to virus disease management. We then take a historical approach towards all past investigations with these two seed-borne pulse viruses in the principal cool-season pulse crops grown: chickpea, faba bean, field pea, lentil, narrow-leafed lupin and white lupin. With each pathosystem, the main focus is on its biology, epidemiology and management, placing particular emphasis on describing field and glasshouse experimentation that enabled the development of effective phytosanitary, cultural and host resistance control strategies. Past Australian cool-season pulse investigations with AMV and CMV in the less commonly grown species (vetches, narbon bean, fenugreek, yellow and pearl lupin, grass pea and other Lathyrus species) and those with the five less important seed-borne pulse viruses also present (broad bean stain virus, broad bean true mosaic virus, broad bean wilt virus, cowpea mild mottle virus and peanut mottle virus) are also summarized. The need for future research is emphasized, and recommendations are made regarding what is required.

Keywords: Australia; epidemiology; future challenges; history; losses; management; research priorities; seed-borne viruses; virus diseases.

Figure 1

The acronyms of Australian states and territories used here are WA (Western Australia), SA (South Australia), VIC (Victoria), TAS (Tasmania), NSW (New South Wales), QLD (Queensland) and NT (Northern Territory). Australian Bureau of Meteorology (BOM) climate groupings are used to distinguish the main regions where grain crops grow, but letters distinguish the smaller irrigated grain production regions in WA, BR—Broome and OR—Ord River Irrigation Area; the NT, DD—Douglas/Daly and K—Katherine; QLD, BU—Burdekin, BN—Bundaberg, G—Gilbert, F—Flinders and M—Mareeba (including Atherton and Ravenshoe); NSW, NR—Northern Rivers. Black lines delineate boundaries of distinct agro-ecological zones (a modified version of those employed by the Australian Grains Research and Development Corporation (GRDC) [79]. Image reproduced from Jones et al. [24]. Image credit @Department of Primary Industries and Regional Development/P. Goulding.

Figure 2

The critically important aphid vector Myzus persicae and examples representing the diversity of current-season symptoms that cucumber mosaic virus (CMV) infection elicits in the foliage of different cool-season pulse plant species. (A), Winged and unwinged individuals of M. persicae. (B), Typical appearance of a narrow-leafed lupin crop with 100% CMV infection, its uneven crop canopy resulting from plants with different extents of dwarfing due to infection at different plant growth stages (Corrigin, 1993). (C), Narrow-leafed lupin plant with typical foliage symptoms of leaflet size reduction, downcurling and chlorosis in new growth and plant dwarfing but with normal-looking lower leaves (front), healthy plants (back) (Wongan Hills, 1995). (D), Yellow lupin plant with typical foliage symptoms of leaflet size reduction, faint mottle, chlorosis and downcurling in new growth and overall plant dwarfing (front), healthy plants (back) (South Perth, 1993). (E), Upper portion of the pearl lupin plant showing leaf with mosaic indicated by a white arrow (South Perth, 1993). (F), Lentil plants showing leaflet symptoms of pallor and size reduction, and overall plant dwarfing indicated by a white arrow (front), healthy plants (behind) (Cunderdin, 1997). (G), Plant of Kabuli chickpea with typical foliage symptoms of leaflet chlorosis (centre), healthy plants (above and below) (South Perth, 1997). (H), Plants of desi chickpea with typical foliage symptoms of leaflet reddening (South Perth, 1997). (I), Plant of desi chickpea showing leaflet reddening and chlorosis (front), healthy plants (back) (South Perth, 1996).

Figure 3

Cucumber mosaic virus infection of single-row narrow-leafed lupin breeding plots growing at South Perth in 1986. (A), Block of short single-row F1-generation plots. (B), Single-row plots showing uneven growth due to CMV spread from seed-infected to current-season-infected plants, most evident in the first 4 rows (bottom left). (C), Part of F1-generation progeny single-row lupin plot showing young seed-infected plant (centre) with healthy plants on either side; seed-borne infection caused leaflet size reduction, chlorosis and downcurling and plant dwarfing. (D), close up of F1 lupin seedling plant with seed-borne infection. (E), Size comparison between seed-infected F1 seedling (left) and much taller healthy F1 seedling of the same age (right), seed-infected seedling plant severely dwarfed. (F), F1-generation single-row lupin plot showing early CMV spread from small seed-infected seedling (furthest left) to the two nearest seedlings but not to normal-looking seedlings further to the right. (G), Single-row plot of wild lupin germplasm accession showing early CMV spread from tiny seed-infected seedling (next to white pot label) to chlorotic dwarfed seedlings on its left but not to normal-looking healthy seedlings on its right. (H), Single-row plot of wild lupin germplasm accession showing early CMV spread from tiny seed-infected seedling (centre) to dwarfed seedlings on its right but not to normal-looking healthy seedlings on its left. (I), End plant of single-row F1-generation lupin plot with interplot CMV spread showing typical late current-season foliage symptoms consisting of leaflet chlorosis, reduced size and downcurling of young leaves combined with normal-looking lower leaves. (J), Volunteer plants: seed-infected plant at centre with all leaves showing chlorotic symptoms, current-season-infected plant behind has foliage symptoms in its apical leaves but normal-looking lower leaves, unaffected volunteer plant on the right side. (K), Volunteer lupin plants with typical current-season CMV symptoms (leaflet chlorosis, size reduction and downcurling, and plant dwarfing) in apical growth.

Figure 4

Field experiments examining the effectiveness of different control measures at controlling cucumber mosaic virus (CMV) spread in narrow-leafed lupin stands (A–K) and aphid transmission by different aphid vector species in the field (L). (A), Arrangement of single-row plots of narrow-leafed lupin with or without reflective mulch in a field experiment (South Perth 1987). (B), Typical arrangement of multi-row plots of narrow-leafed lupin separated from one another by wide (30 m width) non-host (cereal) buffers in field experiments examining the use of different cultural, phytosanitary or chemical control measures to suppress CMV spread (Badgingarra 1995). (C) and (D), Lupin plots at the end of the growing season, which were originally sown with 5% CMV-infected (C) or healthy (D) seed showing chlorotic foliage symptoms resulting from comprehensive current-season CMV infection (C) or remaining healthy due to lack of CMV spread (D) (Badgingarra 1989). (E) and (F), Late growing season images of portions of plots originally sown with 5% infected (E) or healthy (F) lupin seed showing current-season CMV foliage symptoms in all plants (E) or remaining healthy (F) (Badgingarra 1989). (G). Commercial lupin crop sown at high seeding rate showing shading out of the dwarfed seed-infected plant by a dense canopy of healthy lupin plants (Three Springs, 1988) (G image credit: Department of Primary Industries and Regional Development @ Peter Nelson). (H) and (I), Plots recently sown at a low seeding rate with lupin seed at narrow (H) or wide row (I) row spacing (Badgingarra 1992). Images (J) and (K) both show single seed-infected plants (indicated by white arrows) growing within narrow- (J) or wide-spaced (K) rows; the greater crowding of plants within wide-spaced than narrow-spaced rows is evident (both images also show plants with current-season CMV symptoms, which differ from seed-infected plants by the normal appearance of their lower leaves) (Badgingarra 1992). (L), Fine net used to trap and remove airborne winged vector aphids downwind of CMV-infected lupin plants (South Perth 1996). Figure (L) is modified from Berlandier et al. [130].

Figure 5

Direct aphid feeding damage, host resistance to cucumber mosaic (CMV) virus and spatial spread patterns of CMV-infected lupin plants. (A), Direct aphid feeding damage caused by colonisation of a narrow-leafed lupin plant by Myzus persicae. (B), CMV screening procedure involving single-row plots employed every year to evaluate wild germplasm accessions, early-stage breeding lines and/or cultivars of narrow-leafed lupin for CMV resistance: A uniform CMV inoculum source exposure was achieved by separating adjacent plots using ‘spreader rows’ planted with cv. Wandoo seed with a high CMV seed transmission rate and naturally occurring aphid vectors spread CMV from seed-infected plants to healthy plants. Irregular plant heights visible within spreader and test rows reflect plant infection at different plant growth stages (South Perth 1997). (C), Same single-row plot CMV screening procedure with alternate spreader and test rows being used to evaluate wild germplasm accessions, breeding lines and/or cultivars of diverse lupin species for CMV resistance (South Perth 1993). (D), Sap-inoculated leaf of yellow lupin cv. Motiv showing a localized hypersensitve resisistance (LHR) response consisting of necrotic local lesions. (E), Plants of yellow lupin cvs Motiv (right) and Reda (left) sap inoculated with CMV isolate SN showing a systemic susceptible phenotype involving severe plant dwarfing in Reda but complete lack of systemic invasion in Motiv resulting from its LHR inoculated leaf phenotype. (F), Yellow lupin cv. Popiel plant showing an LHR phenotype (necrosis localized to the stem immediately beneath the graft union) following graft inoculation with a CMV-infected scion. (G), L. hispanicus P26858 leaf showing an LHR phenotype (necrotic local lesions) after sap inoculation with CMV. (H), L. hispanicus P26858 (right) and P26853 (left) plants showing an LHR phenotype preventing any systemic invasion or a susceptible phenotype (leaflet downcurling, mosaic and size reduction, and severe plant dwarfing), respectively. (I), Pearl lupin plants sap inoculated with CMV showing a severe susceptible phenotype (leaflet mosaic, chlorosis, deformation and size reduction, and plant dwarfing) (right) compared with healthy plants (left). (J), Gradients of plants with current-season symptoms of CMV or bean yellow mosaic virus necrotic strain (BYMV-N) infection across a 10.4 × 15 rectangular plot of lupins in 1994 at South Perth; incidences of plants with CMV (red line and ■) and BYMV-N (black line and ■) infection. CMV and BYMV sources were on the plot’s right and left sides, respectively, causing a steeply declining curved infection gradient typical of a polycyclic spread pattern (CMV) and a shallow linear gradient typical of a monocyclic spread pattern (BYMV-N). (K), Clustering index (v) map of plant numbers with current-season CMV symptoms within a rectangular 2.8 m × 10 m lupin plot sown with 7% CMV-infected seed in 1996 at Badgingarra. The map shows the predominantly localized CMV spread around seed-infected infection foci. Distances shown are in cm. Spots denote quadrat units consisting of infection patches with v > 0 (red) or gaps with v < 0 (blue). The v values represented by spots of different sizes are large spots > 1.5 or <−1.5, intermediate-sized spots of +/−1 to +/−1.49 and small spots of 0 to +/−0.99. Black lines are zero-value contours, red lines around patch clusters are v = 1.5 contours and blue lines around gap clusters are of v = −1.5 and represent patch and gap regions cluster boundaries with counts close to the sample mean. (C,D,H) are modified from Jones [51]. (J,K) are modified from Jones [135].

Figure 6

Australian forecasting model and decision support system for cucumber mosaic virus (CMV) epidemics in narrow-leafed lupin. (A), Relationship between the amount of annual rainfall in March and April and the first record date for aphid arrival in lupins at six different southwestern Australian grainbelt sites over the period 1988–2001. (B), Relationship between model predictions for the annual first record date for aphid arrival over a 2–4-year period and their actual arrival date at three locations. (C), CMV-lupin pathosystem risk maps for southwest Australian grainbelt in 2007 and 2008 assuming Julian day 120 crop emergence and sowing 2% CMV-infected seed. Individual forecast areas shown as square cells and shire boundaries as lines. Upper and lower rows are for 2007 and 2008, respectively: (1,4) best case (tenth percentile); (2,5) most likely (50th percentile); (3,6) worst case (90th percentile). Black to white colours represent 100% to 0–10% incidence, with 10% intervals representing colour changes between them. (A,B) are from Thackray et al. [153], and (C) is from Jones et al. [80].

Scheme 1

Diagrammatic overview of the cucumber mosaic virus (CMV) narrow-leafed lupin pathosystem forecasting model’s five principal components and the relationships between them. From Thackray et al. [153].

Figure 7

Australian field studies with cucumber mosaic virus (CMV) infecting lentil and chickpea. (A), Rows consisting of many plants showing foliage symptoms of leaflet chlorosis, deformation and size reduction and plant dwarfing caused by CMV infection within an experimental plot of lentil cv. Digger (South Perth 1996). (B), Group of plants showing foliage symptoms of leaflet chlorosis, deformation and size reduction and plant dwarfing caused by CMV infection (bottom left) growing within an otherwise healthy experimental lentil plot (Cunderdin 1997). (C), Plants showing foliage symptoms of leaflet chlorosis, deformation and size reduction caused by CMV (right) or lacking symptoms (left) within an experimental plot of lentil (South Perth 1997). (D), Rows of Kabuli (left) and Desi (right) chickpea plants showing foliage symptoms of chlorosis (Kabuli) and reddening (Desi) caused by CMV infection (South Perth 1996). (E), Individual seed-infected (centre) and current-season-infected (left) lentil plants that developed CMV foliage symptoms or remained healthy (right); symptoms were leaflet chlorosis, deformation and size reduction affecting all leaves (white arrow, seed infection) or without affecting lowermost leaves (blue arrow, current-season infection) (South Perth 1997). (E) Image credit: Department of Primary Industries and Regional Development @ Simon McKirdy]. (F), Infector transplant of chickpea cv. Sona in situ (pink ribbon tag) in exp 1 with leaflet symptoms of chlorosis, reddening, downcurling and bunching caused by CMV infection (Avondale 1999). (G), Example of an experimental plot of chickpea cv. Sona from exp 1 showing its rectangular shape (2.8 m × 10 m = 28 m²) and the 20 m wide non-host canola buffer that surrounded it (Avondale 1999). (H), Part of chickpea cv. Sona plot from exp 1 with widespread CMV infection causing foliage symptoms of leaflet chlorosis and plant dwarfing (Avondale 1999). (I), Part of square (20 m × 20 m = 400 m²) plot of chickpea cv. Tyson from exp 2 with CMV infection focus consisting of lupin plants with white flowers (white arrow) and diseased chickpea plants tagged at two different times using red tape (red arrows) or blue tape (blue arrows) (Avondale 1997). (J), Clustering index (v) map of plants with current-season CMV symptoms within a portion of a square 20 m × 20 m chickpea cv. Tyson plot from exp 2 with five CMV infector foci sown with infected lupin seed, one central and one near each corner (Avondale 1997). The portion of this plot shown shows the extent of CMV spread around the central and left lower corner infector foci. Distances shown are in cm. Spots denote quadrat units consisting of infection patches with v > 0 (red) or gaps with v < 0 (blue). The v values represented by spots of different sizes are large spots > 1.5 or <−1.5, intermediate-sized spots of +/−1 to +/−1.49 and small spots of 0 to +/−0.99. Black lines are zero-value contours, red lines around patch clusters are v = 1.5 contours and blue lines around gap clusters are of v = −1.5 and represent patch and gap regions cluster boundaries with counts close to the sample mean. Images (F) and (H–J) are from modified Jones et al. [97].

Figure 8

Australian field studies with alfalfa mosaic virus (AMV) infecting the cool-season pulses lentil, faba bean and chickpea. (A), Plant of lentil cv. Matilda showing foliage symptoms of leaflet chlorosis, mild mosaic, downcurling and size reduction caused by infection with AMV (Avondale 1998). (B), Plant of lentil cv. Matilda showing foliage symptoms of leaflet chlorosis, downcurling and size reduction, along with plant dwarfing caused by infection with AMV (front right), other plants all healthy (Avondale 1998). (C), Plant of Kabuli chickpea showing foliage symptoms of leaflet chlorosis and shoot necrosis caused by infection with AMV (bottom right), other plants healthy (South Perth 1996). (D), Plant of Desi chickpea showing foliage symptoms of leaflet necrosis and reddening caused by infection with AMV (Avondale 1999). (E), Experimental plots of lentil showing foliage symptoms of chlorosis and plant dwarfing caused by infection with AMV (Cunderdin 1997). (F), Experimental plot of desi chickpea showing foliage necrosis and reddening (central region) caused by infection with AMV (South Perth 1996). (G), Example of field experimental layout used in 1998–1999 for field experiments designed to quantify seed yield losses caused by AMV in lentil, chickpea and faba bean; square (20 × 20 m) plots were surrounded by 5 m wide non-host canola buffers (Faba bean cv. Fiord experiment, Medina 1998). (H), Portion of experimental field plot with surrounding canola buffer behind it from yield loss experiment with lentil cv. Matilda; stake indicated by white arrow marks position of introduced AMV infection focus and dwarfed plants with chlorotic foliage are AMV-infected (Avondale 1998). (I), Central portion of experimental plot of lentil cv. Matilda showing AMV infector plant focus consisting of infected burr medic transplants surrounding central white stake; AMV-infected lentil plants are those with chlorotic foliage and plant dwarfing and different coloured ribbon tags indicate when symptoms first appeared (Avondale 1998). (J), Central portion of experimental plot of desi chickpea cv. Tyson showing central infector plant focus consisting of AMV-infected medic transplants surrounded by AMV-infected chickpea plants having shoots with leaflet necrosis and reddening (orange-coloured ribbon tags), plants surrounding them had not yet developed symptoms (Avondale 1999). (K), Plants of lentil cv. Matilda with foliage symptoms of leaflet chlorosis, downcurling and reduced size, and plant dwarfing caused by AMV infection; infected plants dwarfed to different extents based on whether symptoms first appeared earlier (white ribbons) or later (green ribbons) (Avondale 1998). (L), Plants of chickpea cv. Tyson with foliage symptoms of leaflet necrosis and reddening and apical shoot necrosis caused by AMV infection; orange tags record when symptoms first appeared (Avondale 1999).

Figure 9

Screening for susceptibility and sensitivity to alfalfa mosaic virus (AMV) in major and minor cool-season pulse species at Medina, southwest Australia in 1998 (A–H), and studies on host resistance to AMV in lupin species at South Perth in 1996 or 2006 (I–L). (A), Single shoots of Desi chickpea showing foliage symptoms of leaflet reddening and necrosis caused by AMV infection (right) or without symptoms (left). (B), Row of Kabuli chickpea plants showing chlorotic foliage symptoms caused by AMV infection (front and rear) or without symptoms (central). (C), Portion of lentil row consisting of plants with foliage symptoms of leaflet chlorosis, reddening, downcurling and necrosis caused by AMV infection. (D), Portion of field pea row with foliage symptoms of yellow leaflet chlorosis and necrosis caused by AMV infection (left) or lacking symptoms (right). (E), Row of dwarf chickling plants showing foliage symptoms of leaflet chlorosis, curling and size reduction in upper leaves, necrosis in lower leaves and plant dwarfing caused by AMV infection; annual pasture legume row behind lacked symptoms. (F), Portion of grass pea row showing foliage symptoms of leaf chlorosis, deformation and size reduction and plant dwarfing caused by AMV infection (front), or without symptoms (back). (G), Two narbon bean plants showing foliage symptoms of yellow leaflet chlorosis, deformation and size reduction, and plant dwarfing caused by AMV infection (left and bottom right corner) and two tall plants without symptoms (central and right). (H), Shoot of common vetch with apical shoot necrosis caused by AMV infection. (I), Plants of narrow-leafed lupin cv. Gungurru (2/pot) sap inoculated with AMV and/or cucumber mosaic virus (CMV); plants inoculated with both viruses show severe dwarfing (left), plants inoculated with CMV alone show moderate dwarfing (centre left), plants inoculated with AMV alone show mild dwarfing (centre right), uninoculated healthy control plants without symptoms (right) (1996). (J), Shoot of narrow-leafed lupin cv. Tanjil sap inoculated with AMV showing foliage symptoms of leaflet chlorosis, faint mosaic, downcurling and size reduction (2006). (K), Leaf of pearl lupin plant sap inoculated with AMV showing localized hypersensitive phenotype consisting of necrotic local lesions (brown spots) (2006). (L), Lupinus digitatus plant graft inoculated (side graft) with an AMV-infected scion (now dead, blue arrow); localized hypersensitive phenotype consisting localized stem necrosis just below the graft union (yellow arrow) (2006). Images (D,G,H) modified from Latham and Jones [180], (J–L) modified from Jones [51].