Lupins (Lupinus spp.) are grown as annual cool-season grain legume (pulse) crops in all continents apart from Antarctica. The main production areas include countries surrounding the Mediterranean Sea (European, North African, and Middle Eastern), northeast Europe, the Andean region of South America, southern Australia, southern Africa, and southeast USA. The most important, widespread, and damaging viral pathogen of grain lupins is bean yellow mosaic virus (BYMV).
1. Introduction
Lupin grain is used to feed humans not only directly but also indirectly by providing feed for domestic animals and fishmeal in aquaculture. Depending upon the world region, they are grown as summer crops where the climate is temperate, as winter crops where it is Mediterranean or subtropical, and as wet season, high altitude crops where it is tropical at lower altitudes
[1][2][3][4][5][6][7][8][1,2,3,4,5,6,7,8]. From 2014 to 2021, the 10 countries that produced the most lupin seed, which are located in Australasia, Europe, South America, and Africa, produced a combined 1.1–1.6 million tonnes of seed annually
[9]. The main species cultivated for their grain are narrow-leafed lupin (
L. angustifolius), white lupin (
L. albus), yellow lupin (
L. luteus), and pearl lupin (
L. mutabilis). Both pearl and white lupins were first domesticated to produce land races in their centres of origin in the Andean region of South America and the Mediterranean region, respectively. The centre of origin of both yellow and narrow-leafed lupin was also in the Mediterranean region. Of these four species, pearl and white lupin were first domesticated >2,500 years ago, whereas narrow-leafed and yellow lupin were domesticated recently in northern Europe (Baltic countries and Germany)
[3][5][6][7][10][11][3,5,6,7,10,11]. Lupin land races show evidence of early farmer selection of beneficial traits, such as drought avoidance, reduced vegetative growth, permeable seeds, and greater seed size. However, full domestication of crop lupins requires crossing programs designed to increase other key domestication traits, such as vernalisation insensitivity, low alkaloid levels, early flowering, non-shattering pods, yield stability, and pest and disease resistance, so this did not commence until the early 20th century. This was in Germany in 1928, when the first alkaloid-free lupin plants were isolated
[1][2][5][6][7][12][1,2,5,6,7,12]. Although the rough-seeded lupin species sandplain lupin (
L. cosentinii) was domesticated in the 1970s in Australia, it currently only persists in pastures as feed for domestic animals
[1][2][3][5][6][12][13][1,2,3,5,6,12,13]. Additional lupin species that are recently domesticated, under domestication, or potentially suitable for domestication include three other rough-seeded lupin species,
L. atlanticus,
L. pilosus, and
L. digitatus [5][6][7][14][15][5,6,7,14,15], and
L. hispanicus, which resembles yellow lupin
[7]. Lupin species grown as ornamental plants include yellow and pearl lupins,
L. pilosus,
L. hartwegii,
L. polyphyllus, and the interspecies cross
L. polyphyllus × L. arboreus [5][7][5,7].
Lupins not only tolerate growing in poor, nitrogen-deficient soils but also contribute nitrogen to the soil, making them ideal for sowing in rotation with crops unable to fix nitrogen. However, they also suffer from diverse abiotic and biotic constraints that limit their productivity
[2][3][5][6][12][16][17][2,3,5,6,12,16,17]. Amongst these constraints, disease is a major contributor, as lupins become infected by a wide range of fungal and viral pathogens that diminish both the yield and the quality of their seeds
[18][19][20][21][22][18,19,20,21,22]. The magnitude of the disease-induced losses in seed yield and quality that develops varies between different cultivated lupin species, pathogen species and types, climatic differences, and world region
[18][19][20][21][22][18,19,20,21,22].
2. Bean Yellow Mosaic Virus
The most important, widespread, and damaging viral pathogen of grain lupins is bean yellow mosaic virus (BYMV)
[18]. Although BYMV causes a mild disease in pearl lupin, a damaging disease develops in the other four cultivated lupin species (
Table 1). Its principal foliage symptoms vary between lupin species: pearl lupin—mild mosaic and slight plant stunting; yellow lupin—narrowing of leaflets, vein mosaic, bunchy growth, and plant dwarfing; and both white and sandplain lupin—severe mosaic, necrotic spotting and deformation of leaves, and plant stunting (
Figure 1A–C)
[18]. In narrow-leafed lupin, BYMV symptom development depends upon the virus strain present (necrotic or non-necrotic) and the growth stage when infection occurs. Early infection with the necrotic strain causes bending over of the shoot tip, necrotic stem streaking, and plant death (
Figure 1D,E), whereas late infection of mature plants remains restricted to one or some branches, which develop black pod syndrome (BPS) and/or systemic necrosis (
Figure 1F)
[18][23][18,52]. In contrast, the necrotic phenotype is lacking when plants become infected by the non-necrotic strain, which causes mosaic and stunting symptoms (
Figure 1G)
[24][25][53,54]. The earliest reports of virus symptoms resembling those caused by BYMV were in yellow lupin in Germany in 1929, in Argentina in white lupin in 1932, and in narrow-leafed lupin in New Zealand in 1934. During the period from 1938 to 1960, typical BYMV symptoms were reported under different names in plants of these three lupin species in Europe, Australasia, North America, and Southern Africa. They were also reported in pearl lupin in Australia, New Zealand, and South Africa, and in sandplain lupin in Australia
[18]. Because it occurs worldwide
[26][27][28][55,56,57], BYMV infection poses a serious threat to the lupin crop wherever it is grown in the world. It infects many species of flowering plants (both monocots and dicots) and causes damaging diseases in legume species
[26][28][29][30][23,24,55,57]. It is vectored non-persistently by >50 aphid species, including
Myzus persicae,
Aphis craccivora,
A. fabae,
Acyrthosiphon kondoi,
Acyrthosiphon pisum, and
Macrosiphum euphorbiae [18][29][30][31][18,23,24,58]. It is readily seed-borne in yellow and white lupin, and sowing their infected seed stocks creates primary infection foci from which aphid vectors spread the virus within the crop. In contrast, seed transmission has never been found in narrow-leafed, pearl, or sandplain lupin. Therefore, with them, lupin crop infection depends solely on aphid vectors bringing in BYMV from infected alternative hosts growing nearby, such as legume weeds, pasture plants, and crops
[18][32][18,59]. Weather conditions that promote aphid build-up both before and during the growing season (especially rainfall and warm temperatures) favor its spread within lupin crops
[32][33][59,60].
Figure 1. Plants of different lupin (Lupinus) species with foliage symptoms caused by infection with bean yellow mosaic virus (BYMV) (A–G), or being screened for BYMV resistance in the field (H). (A), Plants of yellow lupin (L. luteus) with typical narrow-leaflet symptoms and reduction in leaf size (South Perth 1995). (B), Plants of white lupin (L. albus) with typical leaf symptoms of mosaic and deformation (front) and unaffected plants with larger dark green leaves (behind) (South Perth 1997). (C), Plant of sandplain lupin (L. costentinii) with typical leaf symptoms of severe mosaic and deformation, and reduction in size (front) with unaffected plant (behind) (South Perth 1989). (D), Plant of narrow-leafed lupin (L. angustifolius) with typical initial early necrotic strain symptom consisting of shoot tip bending over (‘shepherds crook’) (South Perth 1989). (E), Three plants of narrow-leafed lupin killed by early necrotic strain infection (right), and healthy plant (left) (South Perth 1992). (F), Plant of narrow-leafed lupin with black pod syndrome caused by late necrotic strain infection (centre), and healthy plant with normal-looking pods (top left) (South Perth 1995). (G), Plant of narrow-leafed lupin with typical chlorosis and downcurling of leaflets in apical leaves caused by recent infection with the non-necrotic strain (Avondale 1995). (H), Single row plots of cultivars, breeding lines, and germplasm accessions of different lupin species undergoing BYMV resistance screening (South Perth 1993). Note the BYMV-infected clover transplants positioned at both ends of each row to provide a uniform infection source for naturally occurring aphid vectors to spread the virus.
Table 1.
Viral pathogens causing diseases in grain lupin species.
Pathogen |
Virus Genus |
Mode of Vector Transmission |
Main Disease Symptoms |
World Regions Where Lupin Infection Reported |
Narrow-Leafed Lupin |
White Lupin |
Yellow Lupin |
Pearl Lupin |
Sandplain Lupin |
Main pathogens |
|
|
|
|
|
|
|
|
|
Bean yellow mosaic virus * |
Potyvirus |
Aphid |
Leaf mosaic, chlorosis, narrowing, deformation, plant stunting, or strain-specific systemic necrosis or black pod syndrome |
Australasia, Europe, North and South America, Southern Africa |
+++++ |
+++++ |
+++++ |
++++ |
+++++ |
Cucumber mosaic virus * |
Cucumovirus |
Aphid |
Leaf mosaic, chlorosis, downcurling, plant stunting |
Australasia, Europe, South America, Southern Africa |
+++++ |
- |
+++++ |
++++ |
- |
Minor pathogens |
|
|
|
|
|
|
|
|
|
Alfalfa mosaic virus * |
Alfamovirus |
Aphid |
Mild leaf mosaic, downcurling, plant stunting |
Australasia, Europe |
+++ |
(+) |
++ |
+ |
- |
Bean common mosaic virus |
Potyvirus |
Aphid |
Mild leaf mosaic, deformation, stunting |
Europe |
(+) |
- |
+ |
- |
- |
Bidens mottle virus |
Potyvirus |
Aphid |
Leaf narrowing, rugosity |
North America |
+ |
- |
- |
- |
- |
Broad bean wilt virus |
Fabavirus |
Aphid |
Mosaic, leaf deformation, shoot apical necrosis, necrotic stem streaking, plant stunting, death |
Europe |
- |
- |
+ |
- |
- |
Clover yellow vein virus |
Potyvirus |
Aphid |
Leaf chlorosis, necrotic spotting, shoot apical necrosis, stem necrosis, plant stunting |
Australasia, Europe |
++ |
+ |
+ |
- |
- |
Pea early browning virus |
Tobravirus |
Nematode |
Necrotic stem streaking, shoot apical necrosis |
Europe |
- |
(+) |
+ |
- |
- |
Pea enation mosaic virus |
Enamovirus |
Aphid |
Leaf deformation, axillary shoot proliferation |
Europe |
- |
- |
+ |
- |
- |
Peanut stunt virus |
Cucumovirus |
Aphid |
Severe leaf and flower deformation, plant stunting |
Europe |
+ |
+ |
+ |
- |
- |
Lettuce necrotic yellows virus |
Cytorhabdovirus |
Aphid |
Leaf chlorosis, plant stunting |
Australasia |
+ |
+ |
- |
- |
- |
Tobacco streak virus |
Ilarvirus |
Thrips |
Not reported |
North America |
(+) |
(+) |
- |
- |
- |
Tomato black ring virus |
Nepovirus |
Nematode |
Leaf mosaic, deformation, necrotic spotting, plant stunting |
Europe |
(+) |
(+) |
+ |
(+) |
- |
Tomato spotted wilt virus |
Orthotospovirus |
Thrips |
Leaf ringspots (chlorotic or necrotic), deformation, and necrosis (stem streaking or dieback) |
Australasia, Europe, North America |
+ |
+ |
- |
+ |
+ |
Soybean dwarf virus |
Luteovirus |
Aphid |
Leaf chlorosis, reddening, and cupping/rolling |
Australasia, East Asia |
+ |
+ |
+ |
- |
+ |