Seedborne Viral Pathogens of Principal Leguminous Crops: History
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Eliana Dell’Olmo
,
Antonio Tiberini
,
Loredana Sigillo

Viruses are obligate, acellular agents that reproduce inside living cells, spread between tissues, and frequently cause diseases in plants. Among all plant viruses, about one-quarter are transmitted through seeds. Pulses have gained popularity due to their use as a source of protein in food and their favorable impact on soil fertility. Plant species belonging to Leguminosae are vulnerable to a range of seedborne disease, and since they are planted by direct sowing, they are among the plants in which the occurrence of these diseases is a real risk.

  • legumes
  • viruses
  • virus strain
  • pathogens

1. Introduction

Viruses are obligate, acellular agents that reproduce inside living cells, spread between tissues, and frequently cause diseases in plants. Among all plant viruses, about one-quarter are transmitted through seeds [1]. Since viruses can survive for a long time in seeds, it is possible for a seedborne virus to spread commercially over great distances [1]. Two main pathways of seed transmission can be distinguished:
  • Seed contamination: The virus remains on the coat of the seed, and infection occurs mainly through wounds of plantlets during emergence. Viruses harbored externally can be readily inactivated by a number of treatments to totally or partially eliminate seedborne infections. This type of seed transmission is specifically associated with tobamoviruses (tobacco mosaic virus—TMV; tomato mosaic virus—ToMV; tomato brown rugose fruit virus—ToBRFV) and also with some potexviruses, such as Pepino mosaic virus (PepMV) [2][3], usually with a low transmission rate.
  • True seed transmission: The virus resides within the tissues of the embryo. The developing embryo can be infected either prior to fertilization (by gametic transmission) or after fertilization (by direct invasion). The latter type of transmission is more common.
The percentage of contaminated seed and seed transmission rates can be impacted by a variety of parameters: (i) virus epidemiology and genomic features; (ii) host–pathogen interaction; (iii) the location of the seed in the plant; (iv) the age of the seed; (v) environmental conditions; (vi) host resistance [4][5]. Viral diseases are major biotic constraints to legume production, especially in tropical and subtropical areas [6][7]. Cultivated food legumes are susceptible to natural viral infections due to 168 species belonging to 39 genera and 16 families [8][9]. The genomes of viruses infecting legumes can be single-stranded RNA or single-stranded DNA. An estimated 50% of legume viruses are seedborne; most of them are localized in the cotyledon/embryo, resulting in a true seed transmission pathway [10] that can result in a rate of transmission of up to 100%. Seed transmission is considered an effective method of virus introduction into a crop, as well as an excellent means of survival and dispersal, which is further boosted by insect vectors. Subsequently, the onset of vector activity and population growth in the field affect the secondary virus spread and crop losses [11][12][13].

2. Alfalfa Mosaic Virus

Alfalfa mosaic virus (AMV) (taxonomic position: family: Bromoviridae; genus: Alfamovirus; species: Alfalfa mosaic virus) was described in alfalfa (Medicago sativa L.) in 1931 and later in pea (Pisum sativum L.) in 1933 [14][15]. The virus has natural and experimental hosts that belong to nearly 700 plant species in 70 families [16][17]. AMV is currently found worldwide and has a wide distribution (EPPO). Alfalfa is probably the main source of inocula, but the virus is reported to also infect natural hosts including bean, faba bean, soybean, red and white clovers, chickpea, and lentil [18]. Generally, AMV is considered a major pathogen only in alfalfa [19][20], but, in Australia and in the USA, it was sporadically detected on chickpea, lentil, lupin, and soybean [14]. AMV consists of a tripartite genome containing three single-stranded RNA species and a fourth sub-genomic RNA from which the coat protein is translated. The size and shape of virions can range from spherical to bacilliform, with a diameter of 18 nm and a maximum length of 56 nm. Transmission requires the presence of RNA-1, consisting of 3644 nucleotides (nt), RNA-2 (2593 nt), and RNA-3 (2037 nt), together with the coat protein or RNA-4 (881 nt). Serologically, AMV is unrelated to any other known virus species. The virus is transmitted in a non-persistent manner by at least 14 different aphid species but can be introduced in fields from infected weeds. The effectiveness of the transmission of AMV through seeds is up to 50% in alfalfa, 5% in lentil, 10% in chickpea, and, 5% in bean [21]. The symptoms induced by AMV are generally in the form of systemic mosaic and mottle, with plant size reduction and stunting; in lentil and chickpea, it can induce necrosis along the leaflet margins and apex. Flowering and pod formation are reduced, and seeds are small and shriveled.

3. Bean Yellow Mosaic Virus

Bean yellow mosaic virus (BYMV) (taxonomic position: family: Potyviridae; genus: Potyvirus; species: Bean yellow mosaic virus) was discovered in common bean (Phaseolus vulgaris L.) in 1925, and it was the first pathogenic virus reported in chickpea (1956) [22][23]. BYMV is distributed worldwide, including in several Mediterranean countries. Many different isolates of the virus occur in economically important leguminous crops (lentil, common bean, pea, and faba bean), but minor species can also be affected [24]. BYMV is a flexuous rod-shaped virion 750 nm in length containing single-stranded RNA, with a coat protein of 282 amino acids. The genome is monopartite with 10,000 nucleotides that code for a polyprotein [25]. BYMV is serologically related to clover yellow vein virus (ClYVV), which also infects many legume species (the BYMV coat protein shares 68–76% amino acidic identity with ClYVV). On the other hand, BYMV shares less similarity with legume-infecting potyviruses such as bean common mosaic virus, bean common mosaic necrosis virus, pea seedborne mosaic virus, and soybean mosaic virus. BYMV has a broad host range of over 200 plant species, predominantly legumes. More than 20 different aphid species spread the virus in a non-persistent way from infected perennial and weed plants. Clover (Trifolium spp. and Melilotus albus), vetch (Lathyrus spp.), and alfalfa (Medicago sativa) are common field sources of the virus, while, among cultivated legumes, faba bean and pea represent the favored hosts of aphids that act as foci for the virus. BYMV is also seed-transmitted in most temperate pulses, including bean (7%), faba bean (up to 9%), field pea (10–30%), lentil, and lupin [26]. Consistent with other potyviruses, BYMV is also mechanically transmissible. Symptoms produced in response to BYMV infection may vary depending on the time of infection, the plant variety, and the virus strain. Generally, symptomatology includes mosaic, mottling green vein banding, and chlorosis; twisting and curling of the leaves can occur. Flowering and pod formation are reduced, and consequently, few seeds are produced, especially in cases where the incidence of BYMV is high.
In severe infections in faba bean, stem and tip necrosis and early death may occur. Crinkling, downward cupping, yellow mottling, and dead areas along the veins of infected leaves can be observed in bean. Measures to control BYMV include the management of the sowing date, spraying with mineral oils, soil mulching with reflective polyethylene sheets, and crop isolation from known overwintering disease sources [18].

4. Cucumber Mosaic Virus

Cucumber mosaic virus (CMV) (taxonomic position: family: Bromoviridae; genus: Cucumovirus; species: Cucumber mosaic virus) was first described in 1916 (Doolittle and Jagger), and it is distributed worldwide in both temperate and tropical climates, affecting agricultural and horticultural crops of 1000 plant species in 85 families [14]. Despite it representing one of the major viruses in cucurbits, in recent years, it has increasingly been reported as the causal agent of epidemics in major leguminous crops in the tropics [27] and southern Europe [28]. CMV has a tripartite genome encapsidated in isometric particles 29 nm in diameter that contain RNA-1 (3389 nt), RNA-2 (3035 nt), or RNA-3 (2197 nt). The sub-genomic RNA-4 is also encapsidated in the particles that contain RNA-3. The coat protein consists of 218 amino acids with a molecular weight of 24.2 kDa. The species has been divided into distinct serogroups called subgroups I and II, with the latter comprising 70% of the isolates. Phylogenetic analyses have shown that subgroup I can be divided into subgroups IA and IB, both of which are distantly related to isolates belonging to subgroup II [29]. CMV is distantly related to the Cucumovirus species Peanut stunt virus and Tomato aspermy virus. In many weed species, as well as in green vegetation and crops in temperate zones, the virus can survive from year to year. Even if they show no symptoms, perennial legumes such as clover and alfalfa can serve as easy sources of inocula. Over 80 distinct aphid species can spread the virus non-persistently [27][28]; M. persicae and A. gossypii are two of the most prevalent aphid vectors among them. Mechanical inoculation and transmission through seeds are further known routes of virus spread. The rate of seed transmission is reported to be from 10% to 100% in bean, from 50 to 90% in soybean [26], and from 7 to 64% in lentil, whereas in other hosts, such as chickpea, it is erratic and can vary from 0.1% to 1%, occasionally reaching 2% [15]. The CMV symptomatology pattern varies with the host [27]. In lentil, symptoms include plant chlorosis, leaf malformation, and stunting; in chickpea, internode reduction, shoot proliferation, and bushy stunting occur. Finally, mild mosaic and severe plant malformation were observed in bean. Pods can be reduced in number or only partially filled with seeds, resulting in yield losses, whose incidence ranges from 5% to 75% depending on the cultivar, age of infection, virus strain, and environmental conditions [30].

5. Pea Seedborne Mosaic Virus

Pea seedborne mosaic virus (PSbMV) (taxonomic position: family: Potyviridae; genus: Potyvirus; species: Pea seedborne mosaic virus) was first identified in Europe in 1966 and then in Japan in 1967. It was subsequently discovered in the US in 1969 and in New Zealand in 1980 [14]. PSbMV is now found throughout the world. The virus naturally infects lentil, pea, faba bean, and other legumes, and it is a minor issue in chickpea [14]. Because of the potential for high rates of seed transmission and the international trade of breeding lines, PSbMV continues to be a very serious disease in many pulse crops, particularly under predisposing environmental conditions. This virus consists of flexuous rod-shaped particles with a modal length of ca. 770 nm. The genome consists of monopartite single-stranded positive-sense RNA of about 9.9 kb, coding for a polyprotein of approximately 334 kDa in size that is cleaved into various functional proteins by viral proteases. PSbMV has a distant serological relationship with bean yellow mosaic virus. Pathotypes designated P-1, P-2 (also called lentil strains), P-3, and P-4 have been distinguished by the susceptibilities of different lines of pea and based on sequence variability in two coding regions of the RNA [31]. More than 20 aphid species can transmit PSbMV in a non-persistent manner; however, the spreading of the pathogen in new areas can also be associated with the global trade of breeding lines and with its seedborne nature. The establishment in these areas is further favored by vectors, if present. Moreover, the ongoing usage of contaminated seeds, which are collected at the end of a season and then utilized in successive plantings, is a significant contributor to PSbMV’s persistence. Pea (up to 90%) and lentil (up to 44%) have been shown to have high seed transmission rates; however, other hosts such as chickpea (1%) and faba bean (3%) may show lower transmission efficacy. A wide range of symptoms are associated with PSbMV infection. They consist of mosaic, vein clearing, leaf rolling, chlorosis, necrosis of shoot tips, and plant stunting. Pods may be deformed and fail to set, and seed production can drastically decrease (by up to 77% in lentil). Virus-infected seeds may be abnormal with low germination. Symptoms may vary due to cultivar differences, different virus strains, the occurrence of mixed infections (with PEMV), and environmental effects. Symptoms are typically more severe in the case of seedborne infections [18].

6. Other Impacting Viruses Limited to Specific Hosts

The following part discusses two cases of viruses that, based on their epidemiological characteristics and effects on yield losses, are regarded as severe threats despite only having a few hosts (bean and soybean).

6.1. Bean Common Mosaic Virus and Bean Common Mosaic Necrosis Virus

Bean common mosaic virus (taxonomic position: family: Potyviridae; genus: Potyvirus; species: Bean common mosaic virus) and bean common mosaic necrosis virus (taxonomic position: family: Potyviridae; genus: Potyvirus; species: bean common mosaic necrosis virus) are two potyviruses considered to be the most important viruses causing diseases in common bean [32]. While BCMNV is restricted to Africa, Europe, North America, and South America, BCMV is widespread and is documented in all locations where legumes are grown (EPPO). BCMNV and BCMV are formally classified as separate potyvirus species (ICTV), despite the fact that BCMNV was once believed to be a serotype of BCMV. It is thought that in Central or Eastern Africa, BCMNV evolved from BCMV [33]. BCMV and BCMNV have a negative impact on both the commercial-scale cultivation of this high-value crop and production by smallholder farmers in developing nations where beans represent a significant source of dietary protein and minerals. Yield losses due to BCMV and BCMNV may vary between 6 and 98%, depending on the cultivar, the time of infection [33], and the virus strain [34][35]. Both viruses have flexuous, filamentous particles ca. 750 nm long and 12–15 nm wide and a genome monopartite structure with 10,000 nucleotides that code for a polyprotein [25]. Both BCMV and BCMNV are mechanically transmitted, and several aphid species (e.g., A. pisum, A. fabae, and M. persicae) act as vectors in a non-persistent manner. The rate of seed transmission for both viruses has been shown to be 35% [25], and it significantly contributes to the first crop infection. In susceptible bean genotypes, BCMV and BCMNV induce similar symptoms, including mosaic, dwarfing, chlorosis, and leaf curling [36]. The intensity and severity of the symptoms depend on various parameters, including the strain, the bean cultivar, and the plant age. The difference between the two viruses relies on the phenotypes generated in resistant cultivars [32].

6.2. Soybean Mosaic Virus

Soybean mosaic virus (SMV) (taxonomic position: family: Potyviridae; genus: Potyvirus; species: Soybean mosaic virus) [37] was first observed in the US and documented in the Western scientific literature by Clinton. In soybean, more than 100 viruses are reported, and among them, SMV is considered a major threat [38] since it is able to cause serious yield losses and the deterioration of seed quality. SMV is present in all soybean-growing areas of the world [39]. In contrast to its wide distribution, this virus has a very narrow host range; indeed, it is reported to infect cultivated soybean (Glycine max), its wild relative (G. soja), and a limited number of natural hosts [40]. The virus particle is a long and flexuous rod. The genome consists of single-stranded, positive-sense, polyadenylated RNA of approximately 9.6 kb with a virus-encoded protein (VPg) linked at the 5′ terminus. Yield losses due to SMV range between 8 and 25%, depending on the infection time, and only when the plant is co-infected with bean pod mottle virus can the percentage increase up to 66–86% [37][41]. SMV shows significant variability between strains based on symptomatology and on the cultivars that they can infect [37]. SMV is transmitted by over 30 species of aphids in a non-persistent manner, including Aphis glycines, whose flight is correlated with the incidence of the disease [42]. The infection rate of SMV in soybean seeds is higher if the plant is infected before flowering [43][44]. Plants originating from infected seeds can serve as the initial points of inocula in a field with secondary infections resulting from aphid feeding. Seed infection can be as high as 75% depending on the soybean cultivar and the strain of the virus, but it is usually less than 5% (Table 1) [37]. Infection with SMV may result in smaller, less vigorous seeds with lower oil but increased protein and amino acid contents [45][46]. Foliar symptoms vary from moderate to severe leaf mottling, the distortion of leaves, necrosis, overall stunting, and, occasionally, the death of the plant. As for most plant viruses, the extent of crop damage is dependent on the host genotype, the predominant virus strain, infection incidence, environmental conditions, and the developmental stage at which soybean plants become infected [39].
Table 1. List of seed-transmitted viruses impacting leguminous hosts.
Virus Family or Other Group/Genus Virus Species Acronym Transmission Hosts Rate of Seed Transmission (%) *
Family Bromoviridae          
Alfamovirus Alfalfa mosaic virus AMV Aphids, seeds Medicago sativa L.
Trifolium spp.
Phaseolus vulgaris L.
Vigna unguiculata L.
Cicer arietinum L.
Vicia faba L.
Arachis ipogea L.
Glycine max L.
Lens culinaris Medik.		 0.2–74
60–70
0.7–4.9
7–82
0.1–1
0.4
-
5–9
0.1–5
Cucumovirus Cucumber mosaic virus CMV Aphids, seeds Medicago sativa L.
Trifolium spp.
Phaseolus vulgaris L.
Vigna unguiculata L.
Cicer arietinum L.
Vicia faba L.
Arachis ipogea L.
Glycine max L.
Lens culinaris Medik.		 0.1–0.3
8–10
Up to 100
4–37
0.1–1
0–10
1.3
50–95
7–9
Family Potyviridae        
Potyvirus Bean yellow mosaic virus BYMV Aphids, seeds Trifolium spp.
Phaseolus vulgaris L.
Cicer arietinum L.
Vicia faba L.
Pisum sativum L.
Lens culinaris Medik.		 12–15
7
3
0.1–9.8
10–30
18
  Pea seedborne mosaic virus PSbMV Aphids, seeds Pisum sativum L.
Cicer arietinum L.
Vicia faba L.
Lens culinaris Medik.		 8–90
1
3
44
  Soybean mosaic virus SMV Aphids, seeds Glycine max L. Up to 75
  Bean common mosaic virus BCMV Aphids, seeds Phaseolus vulgaris L.
Vigna unguiculata L.		 2–80
0.8–12.4
* Seed transmission rates according to Sastry, 2013 [26]; Latham and Jones, 2001 [14].

This entry is adapted from the peer-reviewed paper 10.3390/plants12102040

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