New and Emerging Diseases of Temperate Grain Legumes in the Nile Valley and Red Sea Region: Faba Bean Gall and Virus Diseases: A Review

Abstract

Temperate grain legumes, including faba bean, field pea, chickpea, lentil, and grass pea, are important food and forage crops in the cereal-based cropping system in the Nile Valley and Red Sea region countries. Despite their importance, local production remains insufficient, and the countries are forced to import to narrow the demand gaps. Emerging diseases, such as faba bean gall disease and several viruses (Chickpea chlorotic dwarf virus, Chickpea chlorotic stunt virus, Faba bean necrotic yellows virus, and Pea seed-borne mosaic virus), are on the rise due to climate variability, changes in farming systems such as monocropping, reduced crop rotations, limited knowledge about the pathogens, and absence of varieties with good levels of resistance. This review synthesizes research achievements in the region and identifies focus areas, primarily resistance breeding, characterization of pathogen populations, developing efficient screening techniques, investigations of mixed virus infections, advancement of pathogen diagnostic techniques, and developing agroecologically based disease management strategies to reduce economic impacts of new and re-emerging diseases. Moreover, research collaboration and information exchange among countries in the region are essential to mitigate the growing threat of emerging legume diseases.

1. Introduction

Temperate grain legumes [faba bean (Vicia faba L.), field pea (Pisum sativum L.), chickpea (Cicer arietinum L.), lentil (Lens culinaris Medik.), and grass pea (Lathyrus sativus L.) are important components of the mixed farming systems in the Nile Valley and Red Sea (NVRS) region countries (Egypt, Eritrea, Ethiopia, Sudan, and Yemen [1]. Most of the population in Egypt (114 million), Ethiopia (129 million), Sudan (50 million), Yemen (39 million), and Eritrea (3.5 million) obtains their protein supply (Figure 1) from legumes as compared with meat [1]. Legumes provide environmental services through nitrogen fixation and reducing the use of herbicides to control weeds for the success of cereal crop production [2,3]. Straw of temperate food legumes is a valuable animal feed in the crop-livestock farming system of the region [4,5]. Legume crops are produced under rainfed conditions in the cool highlands of Ethiopia, Eritrea, and Yemen, and under irrigation in the lowlands of Sudan and Egypt during the winter cropping season. In 2023, the local temperate legume production of the countries in the region was about 2.6 million tons of dry pulses (Figure 2) and 229,028 tons of green pea and green faba bean [1]. Green seeds of faba beans, field peas, and chickpeas are consumed locally and marketed to provide income for smallholder farmers. Since local production is insufficient to meet the local demand, these countries have imported more than 700,000 tons of dry pulses (Figure 3) and over 10,000 tons of green seeds of various temperate grain legumes [1].

The NVRS region represents rainfed and irrigation production systems of temperate food legume production. The countries in the region and ICARDA have implemented various systems/networks to address problems such as viruses and their vectors, wilt/root rot, and wheat rust [6]. Currently, the food legume breeding program of ICARDA and partners considers the region as one of the target product profiles and market segments to develop breeding pipelines to develop disease-resistant cultivars appropriate for the region.

The productivity of temperate grain legumes in the region has declined due to biotic and abiotic constraints and limited adoption of improved crop and pest management innovations [7,8,9]. The decline in grain legume productivity impacts nutrition and food security, food sovereignty, and income, and has resulted in increased cereal monocropping and animal feed shortages. The reduced inclusion of temperate grain legumes in rainfed and irrigated cereal crop rotations has increased production costs due to reduced soil fertility and increased herbicide application to control weeds.

Invasive alien species are threatening food security by impacting staple food crops [10]. Emerging and new diseases are increasingly threatening the cultivation of temperate protein food legumes in the NVRS region countries. New and emerging pathogens are known for their virulence/aggressiveness and severity in key economic crops, and their increasing expansion within a specific country/region or beyond [11,12]. The epidemics of these pathogens are aggravated by climatic and cropping system changes, and the movement of infected seeds for research, trade, and humanitarian food aid across the region [13,14]. For example, in Ethiopia, food aid is believed to have played a role in the introduction of the pea weevil (Bruchus pisorum) infestation back in 1940 [15,16], broomrape (Orobanche crenata) in the early 1980s [17], and Parthenium hysterophorus invasion in 1980 [18].

This review focuses on the distribution, importance, epidemiology, and management practices of emerging diseases (faba bean gall and viruses) affecting temperate grain legumes. It highlights their impact on food security and crop biodiversity among smallholder farmers in the NVRS region countries. Furthermore, it identifies key research gaps, proposes future research priorities, and collaboration opportunities to support sustainable disease management within crop-livestock farming systems.

2. Faba Bean Gall Disease

2.1. Geographic Distribution and Economic Importance

Faba bean gall disease (FBG) caused by an obligate parasite Physoderma viciae (synonymous: Olpidium viciae), was reported as O. viciae in Japan in 1912, infecting Vicia unijugae [19] and in 1936 infecting faba bean and pea. Following the reports from Japan, the disease was described as “blister disease” in spring-planted faba bean crops in the high altitude of Sichuan Province of China [20,21]. The first FBG outbreak was reported in 2010, causing complete crop losses in some farmers’ fields in the central highlands of Ethiopia [22]. Later, farmers reported a high incidence and disease severity in faba bean crops across various locations, indicating that the disease was likely present at low prevalence and intensity before 2010. Since the 2013/14 cropping season, several FBG surveys have been conducted in major faba bean-growing areas across the Central, Northeastern, and Northwestern highlands, Western Oromia, and Arsi highlands, which revealed high disease prevalence with varying levels of severity [23,24,25,26,27,28,29,30,31,32]. Not only did FBG quickly spread and become established across all main faba bean-growing regions in Ethiopia, but its severity also exceeded that of all other faba bean diseases [23]. Except for Ethiopia, currently, there is no evidence of the existence of FBG on faba bean or other known hosts in the NVRS region countries.

2.2. Yield and Quality Losses

Disease appears at different stages of crop growth, depending on favorable environmental conditions and the crop varieties most susceptible to the disease. The disease causes defoliation and deformation of infected plant parts that can lead to significant yield losses, particularly at the seedling stage. Field studies using fungicide sprays in different locations showed that FBG can cause yield losses of more than 40%, with losses being higher in local landraces than improved faba bean varieties [33,34,35]. However, [26] reported losses from FBG up to 100%, particularly at the higher altitudes of 2000 to 4000 m.a.s.l. range where rainfall was greatest. In addition to quantity losses, FBG reduces seed size, which affects the market price of the grain [34,36].

2.3. Epidemiology of Faba Bean Gall Disease

Many factors play roles in disease initiation and subsequent epidemics, and their knowledge helps researchers and farmers for better decisions in managing FBG disease in different agro-ecologies.

2.3.1. Causative Agent, Symptomatology, and Host Range

After the first report of FBG in Ethiopia, a significant effort was made to identify its causal agent. For example, in 2014, dried infected faba bean leaf and stem samples were sent to Prof. Huazhi Ye, Sichuan Agricultural University, Sichuan, China, and he identified the pathogen as O. viciae based on symptoms and pathogen morphology [22,37]. Ethiopian identification of the diseases was based on symptom similarities [38] and observation of resting spores within the galls of affected leaves, as reported in China for morphological studies by [20,21,39]. However, a concerted research effort on pathogen identity, epidemiology, and disease management commenced in 2018 with a project supported by the Australian Center for International Agricultural Research (ACIAR) led by the University of Western Australia and co-led by the Ethiopian Institute of Agricultural Research. It was evident that the FBG pathogen field behavior and epidemiology did not match what could be expected if the pathogen was truly O. viciae. For example, if it were truly O. viciae, then this would be the first ever Olpidium species to operate via foliar disease cycles rather than root infection. Hence, the identity of the pathogen was revisited and identified as Physoderma viciae, not O. viciae, based on morphological [38] and molecular [40] approaches.

Two molecular diagnostic primers, Physo 1, that specifically detect P. viciae, and Physo D have been developed to separate mixed infections of P. viciae with Didymella/Phoma spp. [40]. The two diagnostic primers can be used to quickly identify and confirm the presence of P. viciae, particularly on new alternative hosts.

In-field symptoms of FBG detected in Ethiopia in 2017 are shown in Figure 4A–C [22,41]. First FBG symptoms are green galls that develop mainly on the undersides of young leaves (Figure 4A), which gradually increase in size and number (Figure 4B), later become brownish in color and severely debilitating the whole plant (Figure 4C) (see also [36,38,41]). Initially, the brownish color of FBG disease symptoms led to their confusion with Botrytis chocolate spot symptoms by farmers, leading to spray application of largely ineffective fungicides like mancozeb to protect their faba bean crops.

Farmers in Ethiopia recognize FBG disease under different local names, viz., Qordim/Kordim in north Shoa and south Wollo; Kolsim and Kortim in North Gondar, Chimid and Kurnchit in South Gondar, and Aqorfid in East Gojjam [23,26]. The local names were given based on different symptoms of the disease on the faba bean plant, including deformation (gall formation, twisting) and stunting. Symptoms are observed on faba bean leaves, stems, pods, and petioles. Despite severe symptoms on the pods, there is no evidence of FBG spread via seed harvested from such pods in Ethiopia.

Knowledge of the host range of FBG helps growers to select crops to include in their rotation to minimize primary sources of inoculum and reduce epidemics in faba bean crops. A range of cultivated and non-cultivated dicot plant species are reported as primary and alternative hosts of P. viciae in Ethiopia, China, and Japan. In China, many dicot plants are reported as alternative hosts of P. viciae [42]. Under natural infection in Ethiopia, while faba bean and field pea are the most common primary hosts, lentil (Lens culinaris), Trifolium spp., Medicago scutellata, and Polygonium spp. have also been identified as alternative hosts [32,41,43]. Under controlled environmental conditions, P. viciae infected lupin, grass pea, vetch, and clover [31,44].

2.3.2. Weather Conditions for FBG Disease Development

FBG disease develops across a wide range of temperatures (10–25 °C) and rainfall [21] conditions. However, weather is a key driver of FBG disease, with it being most prevalent and severe in areas with high rainfall and cool temperatures during the growing season. In the Ethiopian highlands, many disease surveys showed that the incidence and severity of FBG were high in faba bean and field pea producing areas, greater between 2000 and 4000 m.a.s.l., and especially at the highest altitudes, areas naturally characterized by the coolest temperature and highest rainfall [23,30,31,32,43,44,45].

2.3.3. Pathogen Survival and Variability

Studies in China and Ethiopia showed that the FBG pathogen can survive at least for two years on infested faba bean straw and in the soil [21,42,46]. Straw of infested faba bean, field pea, clovers, and animal manure play key roles as primary sources of inoculum to initiate and expand disease epidemics in Ethiopia.

The presence of virulent pathogen populations drives disease epidemics and causes high-yield losses. Preliminary studies on some faba bean genotypes showed there was variability of virulence among P. viciae isolates [47]. This variability between isolates was due to differences in incubation period (5–16 days) and infection efficiency (number of galls per leaf) across different faba bean genotypes. Pathogen isolates with a short incubation period and high infection efficiency would favor more severe FBG epidemics, leading to high yield losses.

2.3.4. Pathogen Dispersal and Associations of Biophysical Factors with Faba Bean Gall Disease Severity

The dispersal of the pathogen within and between fields is facilitated by water movement, rain splashes, farm implements, and grazing animals. In Ethiopia, animals are free to graze crop residues after harvest and can easily disperse the disease from farm to farm via manure and from mouth and foot contamination with FBG. During the rainy season, farmers drain excess water from their fields and foster zoospore movement into neighboring fields. Wind dispersal can be important during the traditional threshing and winnowing process, as the wind can carry straw and hay to nearby farms. Faba bean straw is not only a major animal feed, but animal manure is widely used as organic fertilizer in faba bean production. Manure can easily spread FBG pathogen and initiate early disease development. Currently, there is no evidence that P. viciae infects faba bean seed. However, the pathogen can move to new locations via faba bean residue contaminants mixed with faba bean grain.

Faba bean crop surveys assessing the role of biophysical parameters in FBG epidemics showed that FBG disease severity is positively associated with high altitude, poor soil drainage, poor weeding practices, high faba bean plant densities, and animal manure applications [23,25,26,27,30,31,32]. As indicated earlier, the cool temperatures and high rainfall during the main cropping season in high-altitude regions favor the development of FBG disease [29]. A similar finding was reported, with FBG severity high when faba bean was grown in areas at elevations over 2400 m.a.s.l. in China [21]. In field pea crops, plant growth stage, sowing date, poor weeding, and high altitude were positively associated with high FBG incidence and severity in northwest Ethiopia [43]. Although severity was not as high as in the main rainy season, FBG was observed during the ‘small rainy season’ earlier in the year in the central highlands of Ethiopia [30], which can help build FBG inoculum that then enhances disease epidemiology during the subsequent main cropping season.

Faba bean is often grown in waterlogged soil with poor drainage, enabling motile zoospores to move easily and cause more infections. To address this, in some areas, farmers grow faba bean on raised beds, which reduces disease severity compared with flatbed planting.

High faba bean plant population and weed abundance were associated with high FBG incidence and severity by creating a conducive environment for early infection. In the highlands of Ethiopia, many farmers do not weed their faba bean crops until the podding stage, as they use the weeds as green feed for their livestock [45,48].

Cattle manure is widely used as organic fertilizer, especially for faba bean crops, and is reported to foster high FBG development in China [21]. There is clear evidence that a similar situation occurs in Ethiopia. It is possible that improved management of primary FBG inoculum from infected straw and manure could be obtained from composting, which is known to help kill other pathogens and minimize their primary inoculum [49].

Intercropping of faba bean with wheat and mustard reduced FBG disease [50,51]. Faba bean is usually intercropped with field pea, and field observations showed no effect on overall FBG incidence and severity from these two intercropped species.

2.4. Faba Bean Gall Disease Management Practices

2.4.1. Cultural Practices

Various cultural practices are used by farmers to manage diseases in faba bean and other grain legume diseases. These include crop rotation, mixed cropping and intercropping, removal of infested debris, better fertilization, improved soil drainage, and more rigorous weeding practices. Disease surveys in Ethiopia highlighted that the above practices all offer reduced FBG disease incidence and severity across different locations and regions.

2.4.2. Fungicide Application

In Ethiopia, pesticides are applied to manage diseases and insect pests on approximately 16% of the total crop area [52]. Many fungicide screening trials have been conducted since the first report of FBG. While most fungicides have shown only limited success (

Table 1. List of recommended fungicides for the management of faba bean gall disease in Ethiopia.

Trade Name and Formulation	Active Ingredient	Method of Application	References
Bayleton 25% WP	Triadimefon	- Seed treatment: (150–300 g/100 kg of seeds) - Foliar sprays: 700 g/ha	[51,55,56,58,59,60,61,62,63,64,65]
Noble 25%WP	Triadimefon	- Seed treatment: (150–300 g/100 kg of seeds) - Foliar sprays: 700 g/ha	[54,58,66]
Nativo 300 SC	Trifloxystrobin 100 gm/L  +  Tebuconazol 200 gm/L	- Foliar sprays: 0.5 L/ha	[64,66]
Ridomil Gold MZ 68 WG	40 g/Kg Metalaxyl-M + 640 g/Kg Mancozeb	- Foliar sprays: 2.5 kg/ha	[58,59,61,62,66]
Eminent Star 312.5 SE	Chlorothalonil (250 g/L + Tetraconazole (62.5 g/L)	- Foliar sprays: 2 L/ha	[66]

), some have shown good efficacy. For example, based on their effectiveness and cost-benefit analyses, Fungicides containing the active ingredient Triadimefon are widely used as seed treatments and foliar sprays on both improved and landraces faba bean cultivars, due to their demonstrated effectiveness and favorable cost-benefit advantages [53,54,55,56,57,58]. Due to the extensive use of Triadimefon, farmers are advised to rotate fungicide types to avoid the risk of pathogens acquiring resistance to fungicides.

2.4.3. Host Plant Resistance

Developing and growing disease-resistant faba bean varieties is the most economical and effective approach in FBG disease management. The Ethiopian research system has released over 36 faba bean varieties for different agro-ecologies, but most of these were released before the epidemics of FBG disease. Through fast-track screening of released varieties and elite germplasm in FBG hotspot areas, faba bean varieties like Degaga (R-878-3), NC-58, Dosha (COLL 155/00-3), Tumsa (EH99051-3), Hachalu (EH00102-4-1), Walki (EH96049-2), Gachena (ETH91001-13-2), Gora (EK 01024-1-2), Gebelcho (EH 96009-1), Obse (EH95073-1) and Numan (EH 06007-2) and elite breeding lines (EH0110008-5, EH010058-1, and EH06070-1) showed partial resistance to FBG [33,41,51,67,68,69,70,71]. Some faba bean landraces from the Ethiopian Biodiversity Institute (26872, 26873, 28107, 26867, 26869, 26883, 26884; COLL-0038, 25280, and 26885) and breeding lines from ICARDA showed low FBG severity [41,72,73]. These partially resistant varieties and landraces are key inputs towards developing more resistant faba bean varieties with good agronomic traits in the future.

2.4.4. Integrated Faba Bean Gall Management

Integrating cultural and fungicidal management treatments along with available partially resistant faba bean varieties is a key approach towards improved management of FBG disease and associated boost in faba bean productivity [35,51,56,60,73]. Currently, the main components of FBG disease management used by farmers and seed growers include growing partially resistant varieties in combination with seed treatment and foliar spraying with fungicides [34,35,55,74]. In heavy waterlogged soil areas, the use of better-drained raised beds is also incorporated into the overall IDM approach. Even in areas where more resistant faba bean varieties are not available, seed treatment of landraces with fungicide remains an effective management option against FBG.

3. Virus Diseases of Temperate Food Legumes

Worldwide, more than 20 viruses affect chickpea and more than 40 viruses affect faba bean, field pea, and lentil as single and/or multiple infections [75,76,77,78,79], and several of them have been reported in NVRS region countries with varying levels of importance in terms of adversely impacting the productivity of grain legume crops (

Table 2. Virus reported from naturally infected temperate grain legume crops in the NVRS region countries.

Virus Species	Mode of Transmission			Distribution	Major Legume Crops **	References
	Vectors *	Mechanical	Seeds
Alfalfa mosaic virus (AMV)	Aphids-NP	Yes	Yes	Egypt Ethiopia Sudan Yemen	FB FB, Fp FB FB	[76]
Bean leafroll virus (BLRV)	Aphids-P	No	No	Egypt Ethiopia Sudan Yemen	FB FB, L FB FB	[76,77,80]
Bean yellow mosaic virus (BYMV)	Aphids-NP	Yes	Yes	Egypt Ethiopia Sudan Yemen	FB, L FB, L FB FB	[76,77,80,81,82]
Beet western yellows virus (BWYV)	Aphids-P	No	No	Eritrea Ethiopia Yemen	Cp FB, L, Cp FB	[76,77,80,83]
Broad bean mottle virus (BBMV)	Beetles	Yes	Yes	Egypt Ethiopia Sudan	FB FB, Cp, L FB	[76]
Broad bean stain virus (BBSV)	Beetles	Yes	Yes	Egypt Ethiopia Sudan	FB FB, L FB	[76,77]
Broad bean true mosaic virus (BBTMV)	Beetles	Yes	Yes	Egypt Ethiopia Sudan	FB FB FB	[76]
Broad bean wilt virus (BBWV)	Aphids-NP	Yes	Yes	Egypt Ethiopia Sudan	FB FB, Cp FB	[76,77]
Chickpea chlorotic dwarf virus (CpCDV)	Leafhoppers	No	No	Egypt Eritrea Ethiopia Sudan Yemen	FB Cp FB FB, Cp FB	[76,83,84,85]
Chickpea chlorotic stunt virus (CpCSV)	Aphids-P	No	No	Egypt Eritrea Ethiopia Sudan Yemen	FB, L, Cp Cp FB, L, Cp FB, Cp FB, L, Cp, Fp	[83,86,87]
Cotton leafroll dwarf virus (CLRDV)	Aphids-P	No	No	Sudan	Cp	[88]
Cucumber mosaic virus (CMV)	Aphids-NP	Yes	Yes	Egypt Ethiopia Sudan	FB FB, L, Fp FB	[76,77]
Cucurbit aphid-borne yellows virus (CABYV)	Aphids-P	No	No	Sudan	Cp	[88]
Faba bean necrotic yellows virus (FBNYV)	Aphids-P	No	No	Egypt Eritrea Ethiopia Sudan Yemen	FB, Cp, L, Fp Cp FB, L, Cp FB, Cp FB	[76,77,83,88]
Pea enation mosaic virus (PEMV)	Aphids-P	Yes	Yes	Egypt Ethiopia Sudan	FB FB, L FB	[76,77]
Pea seed-borne mosaic virus (PSbMV)	Aphids-NP	Yes	Yes	Egypt Ethiopia Sudan Yemen	FB, L FB, L FB FB	[76,77,79,80,87,89]
Pepo aphid-borne yellows virus (PABYV)	Aphids-P	No	No	Sudan	Cp	[88]
Pepper vein yellows virus (PeVYV)	Aphids-P	No	No	Sudan	Cp	[88]
Soybean dwarf virus (SbDV)	Aphids P	No	No	Ethiopia	FB, L	[76,77]

* Aphids NP = Aphids in non-persistent manner, Aphids P = Aphids in persistent manner. ** FB = Faba bean, Cp = Chickpea, L = Lentil, Fp = Field pea.

).

3.1. Geographic Distribution and Economic Importance

Chickpea chlorotic dwarf virus (CpCDV, genus Mastrevirus, family Geminiviridae) is one of the most important viral pathogens affecting grain legumes in the region and other countries. It was first observed as a chickpea stunt disease at low incidence in the early 1980s in Sudan [90,91], but the causal virus was not identified until 1994, when it was confirmed that CpCDV was one of the causative agents [85]. CpCDV is widespread in the Gezira Scheme and River Nile State of Sudan and has been reported to naturally infect grain legumes in Yemen, Egypt, Ethiopia, and other countries [76,84,92,93,94]. In northern and central Sudan, the virus causes up to 50% yield losses on chickpea [95]. In India, it caused yield losses exceeding 75–90% when plants are infected during flowering [96,97].

Chickpea chlorotic stunt virus (CpCSV, genus Polerovirus, family Solemoviridae) was first reported in Ethiopia and Syria [86] and was later detected in Egypt, Eritrea, Yemen, and other countries [83,86,87,98,99]. In Ethiopia and Eritrea, CpCSV is considered the most economically damaging virus to chickpea and lentil [83,87,100]. Since 2019, a widespread CpCSV outbreak has led to a significant decline in lentil-growing areas in the highlands of Ethiopia [87].

Faba bean necrotic yellows virus (FBNYV, genus Nanovirus, family Nanoviridae) was first detected in faba bean near Lattakia, Syria [101], and later identified in Egypt, Ethiopia, Eritrea, Sudan, and Yemen [76,77,83,86]. It is endemic in many countries in West Asia and North Africa and can cause complete crop failure in Egypt, the Jordan Valley, the coastal region of Syria, and the Cup-Bon region of Tunisia [76,77,102,103]. Since 1990, FBNYV has caused a serious epidemic on the faba bean crop in Middle Egypt, leading to almost complete crop failure during the 1991/92 growing season [77,104].

Pea seed-borne mosaic virus (PSbMV, genus Potyvirus, family Potyviridae) is a globally distributed pathogen that affects lentil, chickpea, faba bean, field pea, grass pea, fenugreek, and forage legumes. PSbMV can cause yield losses ranging from 3% to 61% [105], with seed weight reductions of up to 36% on lentil crops [106]. Despite crop losses, PSbMV affects trade due to restrictions on virus-infected seeds [89,107]. In the NVRS region countries, the virus was first reported in Ethiopia and Sudan on faba bean [89], and later in other legumes, including lentil [76,77,93,108]. High PSbMV incidence was observed in central and northern Ethiopia. Field surveys conducted between 2018 and 2022 confirmed widespread PSbMV infection, reaching epidemic levels where farmers lost their entire lentil crops in the Amhara region of Ethiopia [87]. Although no research has been conducted to quantify the reduction in nodule formation due to virus infection, negative effects of virus infection on nodule formation have been reported in other legume crops [109,110,111].

3.2. Host Ranges

The four major viruses (CpCDV, CpCSV, FBNYV, and PSbMV) affect many primary and alternative hosts in many countries. The alternative hosts contribute to the virus survival during off-seasons and the disease epidemiology of these viruses on major grain legumes (

Table 3. Alternative hosts for four economically important viruses affecting food legumes (chickpea, faba bean, field pea, and lentil).

Virus	Cultivated and Wild Plant Species	References
Chickpea chlorotic dwarf virus (CpCDV)	French bean (Phaseolus vulgaris), sugar beet (Beta vulgaris), cotton (Gossypium spp.), okra (Abelmoschus esculentus), spinach (Spinacia oleracea), tomato (Solanum lycopersicum), papaya (Carica papaya), watermelon (Citrullus lanatus), squash (Cucurbita pepo), cucumber (Cucumis sativus), pepper (Capsicum annuum), Acacia spp., Cajanus cajan, Dolichos lablab, Rhynchosia minima, Sesbania bispinosa, Xanthium strumarium	[76,85,94,97]
Chickpea chlorotic stunt virus (CpCSV)	Fenugreek (Trigonella foenum-graecum), grass pea (Lathyrus sativus), forage legumes (Vicia sativa, V. ervilia, V. narbonensis, Medicago spp.), Apium sp., Euphorbia sp., Physalis longifolia, Sinapis arvensis, Aeschynomene indica.	[83,86,98,99,112,113]
Faba bean necrotic yellows virus (FBNYV)	Cowpea (Vigna unguiculata), Egyptian clover (Trifolium alexandrinum), Soybean (Glycine max), French bean (Phaseolus vulgaris) and cowpea (Vigna unguiculata), (athyrus sativus, L. gorgonet, L. annuus, Medicago polymorpha, M. praecox. M. ridigula, Trifolium arvense, T. hirtum, T. lappaceum, T. subterraneum, Vicia ervilia, V. hybrida, V. palestina, V. sativa), Onobrychis spp. and Medicago sativa and other forage legumes	[77,101,102,103,114,115]
Pea seed-borne mosaic virus (PSbMV)	Grass pea (Lathyrus sativus), fenugreek (Trigonella foenum-graecum), Lathyrus spp., Trifolium spp., Vicia spp. and over 35 species	[79,89]

).

3.3. Symptomatology of Major Virus Diseases

The chickpea plants infected with CpCDV exhibit symptoms of stunting, internode shortening, phloem browning, and reddening (desi type chickpea) or yellowing (kabuli type chickpea) of leaves (Figure 5) [92,97]. The main symptoms of CpCSV are interveinal chlorosis, yellowing, stunting, curling, reddening, and phloem browning (Figure 6) [86]. FBNYV on faba bean causes stunted growth, followed by thick, brittle leaves, and ultimately necrosis, leading to plant death within 5–7 weeks (Figure 7) [101]. Legume plants infected with PSbMV show mosaic patterns, chlorosis, leaf distortion, necrotic seed lesions, and a significant reduction in plant height and yield. In addition, it causes pod deformation, seed coat cracking, and reduced seed sizes (Figure 8) [89,105].

3.4. Mode of Transmission

The primary modes of transmission of economically important viruses are through insect vectors and contaminated seeds. Besides transmitting viruses, some insect vectors can also cause direct yield losses in some food legumes in the NVRS region.

CpCDV is transmitted by two species of leafhoppers (Orosius orientalis and O. albicinctus) [76,92]. CpCSV is a phloem-limited virus spread by aphids (Aphis craccivora and Acyrthosiphon pisum) in a persistent manner and can also be transmitted by grafting [116]. FBNYV is spread by aphids (A. pisum, A. craccivora, and A. fabae) in a persistent manner, with the first two being more efficient vectors [102]. PSbMV is transmitted mechanically and by several aphid species (e.g., A. pisum, A. fabae, A. craccivora, Myzus persicae, and Rhopalosiphum padi) in a non-persistent manner [79,89], and by infected seeds of faba bean, lentil, chickpea, and field pea [89,105,108].

3.5. Detection and Characterization

CpCDV is detected using specific antisera by serological techniques such as ELISA and tissue blot immunoassay (TBIA) [92,117] and PCR assay [118]. CpCSV is identified serologically by ELISA and TBIA using specific monoclonal and polyclonal antibodies [98,99,119], and by RT-PCR using specific uniplex and multiplex primers [83,99,100]. FBNYV diagnosis relies on ELISA and TBIA using monoclonal and polyclonal antibodies [120], dot-blot hybridization, and PCR using specific primers [101]. PSbMV can be detected from infected seeds or tissue using ELISA, TBIA, dot-blot, immunospecific electron microscopy (ISEM), and dot immuno binding (DIB) [77,79,89], and molecular RT-PCR for pathotype-specific identification [121] using single primers [122,123] or multiplex primers [124].

3.6. Phenotypic and Genetic Diversity of Major Legume Viruses

Pathotyping of PSbMV strains is essential for breeding, for resistance, and for crop management. Four pathotypes (P-1, P-2/L-1, P-3, and P-4) of PSbMV [125] have been identified so far using field pea differential lines [126]. The two pathotypes (P-1 and P-4) have been identified from field pea, whereas the L-1 pathotype was isolated from lentil. The L-1 pathotype is more virulent on chickpea and lentil than P-1 and P-4 pathotypes [121,125,127]. Two additional pathotypes (U-1 and U-2) have been reported from the PSbMV population in Pakistan [128]. The different pathotypes vary in their transmission efficiency through infected seeds and vectors [121]. A phylogenetic analysis of nine Ethiopian PSbMV isolates collected from lentil and chickpea grouped them into four major and sub-groups [123]. One Ethiopian lentil isolate (OQ867259) showed 97.4% nucleotide identity to the well-studied American pathotype P-2 isolate (AJ252242). Two Ethiopian isolates (OQ867257, OQ867258) showed 99.5% nucleotide identity to the Australian pathotype P-2 isolates (HQ185579). All Ethiopian isolates shared 92.5–94.2% nucleotide identity with the Chinese pathotype P-2 isolate (HQ185580). Phenotyping of these isolates using differential field pea lines is important to know their virulence on chickpea and lentil varieties in Ethiopia and other countries in the region.

The differences between the three PSbMV pathotypes could be explained by the properties of two viral cistrons, and predicted the existence of a fourth pathotype, P3 [127]. Two recessive resistance genes (sbm1 and sbm2) are operating in the pea/PSbMV pathosystem [129]. The sbm1 gene (found in germplasm of Indian and Ethiopian origin) confers resistance to all four PSbMV pathotypes, whereas a different allele (sbm1¹), present in PI 269774 and PI 269818 accessions, confers resistance to P1 and P2 pathotypes. The sbm2 gene, present in ‘Dark Skin Perfection’ and many commercial pea lines, provides resistance only to pathotypes P2 and P3.

Using two differentials, one with the sbm1¹ gene and one with the sbm2 gene, allows classification of PSbMV into one of the four pathotypes from Australian pea seed [130]. Pathotyping of major temperate food legume viruses is not studied in the NVRS region.

Advances in genomic studies have enabled the determination of the extent of genetic variation among and within grain legume viruses. In CpCDV, genetic recombination studies highlight the emergence of new variants capable of invading new hosts [94]. Chickpea mastrevirus legacy isolates collected from Australia, Eritrea, India, Iran, Pakistan, Syria, Turkey, and Yemen have shown that the genetic diversity in Australian isolates is greater than those from other countries [94]. In Sudan, seven of the 12 known CpCDV strains were identified, with the CpCDV-H strain being dominant (73%), and four new strains (CpCDV-M, -N, -O, and -P) were identified, demonstrating genetic recombination could play a significant role in CpCDV diversity [131].

Through genome sequencing over the past three decades, at least 13 distinct viruses have been identified that cause stunting and yellowing symptoms in grain legumes [132]. In a recent study by [133], comparative sequence analysis of 10 Ethiopian CpCSV isolates (five chickpea and five lentil isolates) showed nucleotide sequence identity of 94.9–100% and 91.9–98.7% with each other and with the reference isolates, respectively. One chickpea CpCSV isolate (MZ043728) showed a close relationship to serotype II isolates, while the remaining nine isolates were closely related to serotype I isolates.

Diversity among CpCSV isolates was previously analyzed using MAbs raised against CpCSV isolates, which placed them into two distinct serogroups based on geographical origin [99]. Group I comprised isolates from Ethiopia and Sudan, while Group II included those from Egypt, Morocco, and Syria. The CpCSV isolate of Syrian origin causes more severe symptoms compared to Ethiopian isolates [98]. Studies on coat protein variation [120] among FBNYV isolates and their serological relatedness to taxonomically similar legume nanoviruses [milk vetch dwarf virus (MDV) and subterranean clover stunt virus (SCSV)] by determining the cross-reactivity of 19 FBNYV monoclonal antibodies (MAbs). Their results indicated that FBNYV and SCSV share a common epitope (only one MAb reacted with SCSV), whereas FBNYV and MDV are closely related serologically and are two strains of the same virus (16 MAbs reacted with MDV). Additionally, when the same 19 MAbs were tested on 107 FBNYV samples collected from Egypt, Ethiopia, Jordan, Morocco, and Syria, five MAbs showed differential reactions. About 20% of the tested FBNYV samples did not react with any of these five MAbs, allowing FBNYV serotypes to be distinguished and indicating significant coat protein variability among FBNYV isolates from the surveyed countries. The MDV isolate from Japan and five FBNYV samples from Ethiopia appeared to be the least closely related to typical FBNYV isolates, as they did not react with three and four, respectively, of the five differentiating MAbs.

3.7. Mixed Infections

Mixed infections occur naturally and are common in cultivated crops, and occur when two or more viruses are present in a single plant, resulting in complex symptoms. Mixed infections involving two or more viruses are characterized by complex interactions that can lead to high disease severity [134]. For mixed virus infections, there could be interaction between viruses through a complementary event, interaction between viruses through an interference event, or a situation where there is no interaction event between viruses despite sharing the same host [135]. These interactions could be synergistic, antagonistic, or neutral, with a direct impact on the host plant and the relationship with the insect vector. If the interaction is synergistic, it can have consequences on epidemiology, biology, and economic implications by altering host ranges and increasing vector transmission [136]. Several synergistic interactions involving a member of the genus Potyvirus [137] have been reported to affect the accumulation and pathogenicity of other viruses [138]. Mixed infections may also affect virus evolution; for example, they may increase the fitness of interacting viruses and can lead to a significant loss of yield [139]. Vector-mediated transmission contributes to multiple infections in the same plant [139]. There are instances where potyviruses interact antagonistically in co-infection [137]. Co-infection of soybean with Soybean mosaic virus (SMV, genus Potyvirus) and Alfalfa mosaic virus (AMV) resulted in severe symptoms in dually infected plants, regardless of strain. The high levels of AMV indicate that AMV and SMV interact synergistically. This synergism suggests an increased likelihood of AMV becoming a serious viral disease of soybeans.

Mixed infections of PSbMV (genus Potyvirus) and CpCSV (genus Polerovirus) were found to be the most common viruses on lentil in Ethiopia, which might have arisen because both viruses are transmitted by aphid vectors such as A. craccivora and A. pisum [123].

3.8. Management of Temperate Grain Legume Viruses and Vectors

3.8.1. Agronomic Practices Play an Essential Role in Managing Legume-Infecting Viruses

In northern Sudan, field studies have shown that delaying chickpea planting by 3 to 4 weeks, combined with short irrigation intervals, can significantly reduce the incidence of CpCDV [95]. An increase in faba bean production in Yemen could be achieved by avoiding viral diseases through resistant cultivars and sowing before the first of December [140]. Crop rotation helps avoid sources of infection, including volunteer crop legume crops that may have been infected through seeds or survived from previous crops. These measures are important components of IDM approaches to controlling virus spread in cool-season grain legume crops [141]. For FBNYV, selecting an appropriate sowing date that avoids the peak periods of aphid activity—especially those migrating from susceptible summer legumes or nearby wild hosts—is a critical cultural measure [142]. Additional cultural tactics include the use of reflective mulches, which have been shown to reduce PSbMV incidence by up to 78% in faba bean fields in Japan [143]. Rouging or the early removal of infected plants has also been recommended for FBNYV to reduce secondary spread within the field. Moreover, adopting an appropriate seeding rate improves plant vigor and can help suppress the build-up of virus inoculum and vector populations [102,142]. In Egypt, application of Rhizobium inoculation was found to reduce infection of BYMV and AMV on faba bean [144,145].

3.8.2. Vector Management Is Another Essential Component of Virus Control

Aphid control is particularly relevant for viruses such as FBNYV and PSbMV. For FBNYV, the application of aphicides once or twice during key vector activity periods has been shown to be effective in reducing virus incidence [142]. Additionally, seed treatment with systemic insecticides like imidacloprid prior to planting offers early protection against aphid vectors [142]. Although insecticides are generally less effective for controlling viruses like PSbMV that are transmitted in a non-persistent manner, their use may still reduce the spread of virus inoculum within the field, especially when the initial infection arises from infected seed [75,146].

3.8.3. The Use of Healthy Seeds Is a Cornerstone of Managing Seed-Borne Viruses Such as PSbMV

In Ethiopia, high PSbMV incidence has been linked to the use of infected seed lots by farmers [123]. Ensuring the use of virus-free seed not only prevents initial infection but also reduces the inoculum pressure for subsequent vector transmission. Establishing seed certification programs and encouraging seed multiplication organizations to produce and distribute certified, virus-free seeds are crucial steps to reduce the burden of PSbMV and other seed-borne viruses in farmers’ fields [13].

3.8.4. Host Plant Resistance Provides a Long-Term and Cost-Effective Approach to Virus Management

Although no fully resistant chickpea varieties to CpCDV are currently available, cv. Shendi showed a low infection rate and can be considered an option in virus-prone areas of Sudan [95]. Other chickpea sources of resistance to CMV, BYMV, and PEMV viruses are reviewed by [147].

Six lentil genotypes with combined resistance to different viruses were identified [142]: ILL 75 (Chile) showed resistance to BLRV, FBNYV, and SbDV, whereas ILL 74 (Chile), ILL 85 (Tajikistan), ILL 213 (Afghanistan), ILL 214 (Afghanistan), and ILL 6816 (ICARDA) were resistant to FBNYV and BLRV. Through 10 cycles of recurrent selection of faba bean under field conditions and inside an insect-proof screen house, 27 FBNYV-resistant single-plant selections originating from China, Spain, Sudan, and Tunisia were identified, and their populations are deposited at the International Center for Agricultural Research in the Dry Areas (ICARDA) GenBank under accessions numbers IG 159162 through IG 159188 [148]. In Australia, resistant faba bean cultivars (PBA Nasma and PBA Nanu) resistant to BLRV are released for commercial production [149]. Other sources of resistance in faba bean genotypes to CMV, BYMV, and PEMV are reviewed elsewhere [150]. For PSbMV, some lentil cultivars (Red Chief, Crimson, Palouse) and genotypes LL6198, 99/209XILWL118, and ILL10750XILL1982 showed low seed transmission and low infection rates, which can be used for resistance breeding [105,123].

3.8.5. Integrated Virus and Vector Management

This approach offers the most effective and sustainable means of controlling viral diseases. This strategy involves combining timely planting, the use of certified virus-free seeds (virus-free seed), the deployment of resistant or partially resistant cultivars, judicious application of insecticides for vector control, seed treatments, removal of both major and alternative crop hosts, and the removal of infected plants [142,151,152]. When multiple control measures with different effects are combined, their effects complement each other, resulting in significantly greater overall control effectiveness. Selecting the optimal combination of measures for each disease system and production situation requires a comprehensive understanding of the epidemiology of the causal virus and the mechanism of action of each individual control measure. In addition, developed strategies must be robust and require minimal additional expenditure, labor requirements, and disruption to standard practices [141,151]. Such an integrated approach is particularly recommended in regions where FBNYV and PSbMV are endemic, as it provides a multifaceted defense against both virus and vector. Coordination among research institutions, seed certification authorities, and extension services is essential to ensure that farmers have the skills, knowledge, and input needed to implement effectively.

3.9. Viruses of Other Legume Crops in the Region

Farmers grow other food and forage legumes that can diversify major temperate food legume crops during the summer and rainy seasons. In addition to the viruses mentioned on major traditional temperate grain legumes in the region, some viruses are reported to cause damage to other emerging legume crops (common bean, cowpea, lupine, peanuts, soybean, mung bean) being promoted for diversification and intensification of the cropping system.

(a)

Soybean mosaic virus (SMV, genus Potyvirus, family Potyviridae) is one of the most devastating soybean diseases, causing severe yield losses and reduced seed quality. It is transmitted by aphids in a non-persistent manner and via seeds. SMV has a narrow range, primarily affecting plants in the legume family (Fabaceae), but also some other families such as Amaranthaceae and Solanaceae [153]. SMV is present in all soybean-growing regions of the world, including Egypt [154].

(b)

Soybean vein necrosis virus (SVNV, genus Orthotospovirus, family Tospoviridae) is transmitted by soybean thrips (Neohydatothrips variabilis). SVNV has spread rapidly in soybeans since it was first recorded in 2008 and was reported in the Giza region of Egypt in 2017 [155].

(c)

Cowpea mosaic virus (CPMV, genus Comovirus, family Secoviridae) is one of the most common viral diseases of cowpea reported in Egypt [156]. CPMV is transmitted mechanically, by beetles, and via seeds. Symptoms caused by CPMV range from light green mottle to distinct yellow mosaic, leaf distortion, and premature plant death. The virus has a wide host range, including several food and forage temperate legumes.

(d)

Peanut stunt virus (PSV, genus Cucumovirus, family Bromoviridae) is transmitted by mechanical inoculation, by several aphid species in a non-persistent manner, and via peanut seeds. PSV is an economically important virus of the family Leguminosae. In addition to peanuts, PSV has been reported to naturally infect beans, cowpea, clover, peas, soybeans, alfalfa, and lupine. PSV has been detected in Sudan and can cause significant damage to legume crops like peanuts and cowpeas. PSV infection reduced several growth and yield parameters (shoot and root dry weight, number, and weight of nodules, flowers and pods, seed production, and yield per unit area), including nodule number and weight, and even plant death. Several aphid species are known to transmit the virus [157].

(e)

Bean common mosaic virus (BCMV, genus Potyvirus, family Potyviridae) poses a serious threat to bean cultivation worldwide because it is seed-transmitted at a very high frequency. It is also transmitted by mechanical inoculation and by aphids in a non-persistent manner. BCMV exhibits a range of symptoms, including mosaic patterns on leaves, vein clearing, blistering, mottling, and pod distortions, which can lead to significant yield losses. BCMV has been reported in common bean plants in Egypt [158].

(f)

Cucumber mosaic virus (CMV, genus Cucumovirus, Family Bromoviridae) is a widely distributed viral agent with a broad host range, including several legumes. The virus is transmitted through seeds and by several aphid species in a non-persistent manner. The virus causes mosaic symptoms in both temperate and tropical legumes and affects yield. It synergistically interacts with co-infecting potyviruses and causes severe symptoms and plant death [152].

(g)

Cowpea mild mottle virus (CPMMV, genus Carlavirus, family Betaflexiviridae) is a whitefly-transmitted virus widespread in legume production zones in low and mild-altitude zones. Like other legume viruses, it is also seed-borne and induces mild to severe mosaic symptoms depending on cultivar susceptibility.

4. Phytoplasma of Temperate Grain Legumes

Faba bean phytoplasma (phyllody) was first reported in Sudan by [159], who demonstrated its transmission by grafting, not by sap inoculation or leafhopper (Empoasca lybica Berg.). Later, the disease was reported in northern Sudan, with the highest incidence in early-sown chickpea crops [160]. In 1982/83, disease incidence reached 20% on some faba bean fields in the Gezira [161]. The faba bean phytoplasma in Sudan (Genebank Acc. No. X83432) was later identified as 16SrII-C subgroup [162,163]. In 2011, chickpea and faba bean plants showed phytoplasma symptoms in Gezira state, Sudan, and molecular tests indicated that the phytoplasmas were more closely related to the 16SrII-D subgroup [164].

In Egypt, phytoplasma disease was reported on faba beans [165,166], which is transmitted by dodder (Cucusta camestris) and produces disease symptoms within 25–35 days [165]. The phytoplasma was sub-group 16SrII-D and affected sesame, faba bean, and cowpea exhibiting phyllody symptoms in Egypt [167].

Naturally infected faba bean plants showed shoot proliferation, witches’ broom, stunting, phyllody, and yellowing and little leaves [165,166,167]. In Yemen, phytoplasma disease of faba bean, caused by Mycoplasma-like organisms (MLO), was recorded in Wadi Hadhramaut in the spring of 1990 [168]. The most prominent symptom was the transformation of most flowers into green, leaf-like structures, with few or no seeds. Basal buds may proliferate and ramify excessively, resulting in a distinctive growth pattern resembling a witch’s broom.

The symptoms of infected chickpea include pale green leaves with smaller leaflets and bushy appearance due to axillary shoot proliferation, abnormal green structures develop in place of normal flowers, and the pod set is affected [169].

Phytoplasma can be managed by controlling leafhopper vectors and removing infected plants, but neither prevention method has been fully effective in field conditions. Therefore, the only real way to control phytoplasma is to prevent outbreaks or use resistant varieties [170].

5. Conclusions and Perspectives

New and emerging diseases of temperate grain legume crops affect smallholder farmers by reducing grain and straw yields and nitrogen fixation for succeeding cereal crops in the region. Besides economic losses, emerging and new diseases can cause genetic erosion, leading to loss of biodiversity, as local landraces are usually susceptible. Furthermore, climate change poses significant challenges to viral disease management, as a warmer climate increases the activity of insect vectors and the replication and transmission of viruses, potentially leading to increased viral disease morbidity and production losses. Viruses that cause serious diseases are a concern for farmers and researchers, highlighting the need to develop disease management strategies.

Rapid pathogen detection is essential to limit the spread of viral diseases and facilitate effective management practices. Next-generation sequencing methods have shown great potential for detecting multiple viruses simultaneously, which could help reduce crop losses from emerging diseases [171]. However, much remains to be discovered to advance the current state of viral disease diagnostics. Despite significant successes in pathogen diagnostic tools, there remains a need for easy-to-use, inexpensive, and simple approaches, especially in countries in NVRS regions. Furthermore, mixed infections remain a barrier to disease diagnosis. Mixed infections with unrelated viruses can also cause synergistic diseases, exacerbating the disease impact compared to single viral infections and making them more difficult to control.

Fragmented research efforts have been made over the past decade, which have made significant progress toward recommending short-term solutions for farmers. Disease surveillance of FBG covers the highlands of Ethiopia, Eritrea, and Yemen, where the disease was observed above 2000 m.a.s.l., where major faba bean and field pea are mainly grown.

Besides, serological diagnostic tools, multiplex PCR is critical for viruses with mixed infections. Developing resistant breeding by the national program and ICARDA for emerging viruses and FBG is very limited. To develop resistant genotypes against FBG and viruses, Focused Identification of Germplasm Strategy (FIGS) can be used to assemble accessions collected from different countries. Moreover, effective screening methods at the seedling and adult plant stages are very important for supporting breeding efforts.

The difficulty of controlling or limiting the spread of new diseases is that farmers, researchers, and national plant protection officers lack sufficient knowledge of pathogen identity, spread mechanisms, and effective control measures. Capacity building in diagnostics and management practices enhances preparedness against emerging disease threats. Collaboration among NPPOs, farmers, researchers, and development agents to improve knowledge of new and emerging diseases is very important for managing and limiting pathogen movements. Countries of the NVRS regions obtain food legume seeds through imports for research, consumption, and food aid, which represent key pathways for the transboundary movement of seed-borne pathogens, mainly viruses. Mostly, these countries get germplasm for variety development from many CGIAR centers, where the Germplasm Health Unit plays a key role in the safe movement of germplasm. Food aid is critical in some of the countries in the region affected by conflict and climate shocks. Enhanced coordination among national and regional plant protection organizations, CGIAR, FAO, and humanitarian agencies is vital to harmonize disease surveillance and germplasm exchange and to foster knowledge sharing among stakeholders.