Viruses Infecting Yam in Africa: Existing Knowledge and Future Perspectives

Received 25 Oct, 2024

Accepted 01 Dec, 2024

Published 02 Dec, 2024

Yam is one of the nutritional crops feeding a large population in West Africa in particular and currently expanding to the other parts of the continent. However, its productivity is being hampered by biotic stresses particularly viruses which are mainly propagated through infected tubers as planting materials. Viruses infecting yam have been reported worldwide in yam production areas affecting both the quality and quantity of tubers, subsequently interfering with the international germplasm exchange. There are few, not well-described yam viruses in Sub-Saharan Africa (SSA) that induce such symptoms as mosaic, chlorotic spotting, curling and mottling. Despite the strides made in describing and diagnosing yam viruses in SSA, a lot remained and is still unknown due to scarcity and limited access to knowledge, particularly the epidemiology of yam viruses. This review presented the current status of yam viruses occurring in Africa. Future directions on yam viruses and diagnostics using molecular methods are discussed.

INTRODUCTION

The yam (Dioscorea spp., family Dioscoreaceae) is an herbaceous vine with underground edible tubers and major staple foods in the world, especially in some regions of the tropics and subtropics. The edible varieties of yam serve as important sources of carbohydrates for millions of people in these regions^1,2. The yam is currently, the third most important tuber crop worldwide, while in Africa, it’s a second after cassava by value and production^3,4. Over 95% of world yam production occurs in West and Central Africa^3,4. Due to its strength in adverse weather and wide agroecological tailoring, yam is an important crop for food security. Also, as compared to other tuber and root crops, it’s offer good options for both value-addition and consumption⁵.

Besides its food and economic value, yam is also a culturally important food crop in some tropical and subtropical regions⁶. Several factors such as pests and diseases, limited access to quality planting materials and low soil fertility, are responsible for its low production⁷. Pests and diseases, such as insects, nematodes, fungi, bacteria and viruses are the major causes of global yam production decrease leading to severe economic losses^8,9.

Viruses infecting yam have been reported in yam-producing regions to affect tubers’ quantity and quality subsequently interfering with the international germplasm exchange^10,11. To date, virus species including Yam mosaic virus (YMV: Potyvirus), Yam mild mosaic virus (YMMV: Potyvirus), Cucumber mosaic virus (CMV: Cucumovirus), Dioscorea bacilliform AL virus (DBALV: Badnavirus), Dioscorea bacilliform SN virus (DBSNV: Badnavirus), Dioscorea bacilliform RT virus 1 (DBRTV1: Badnavirus), Dioscorea bacilliform RT virus 2 (DBRTV2: Badnavirus), Dioscorea latent virus (DLV: Potexvirus), Dioscorea mottle virus (DMoV: Comovirus), Dioscorea mosaic associated virus (DMaV: Sadwavirus), Yam spherical virus (YSV: Aureusvirus), Yam ampelovirus 1 (YaV1: Ampelovirus), Ethiopian yam virus (EYV: Potyvirus), Yam virus 1 (YV-1: Crinivirus), Yam virus Y (YVY: Unknown genera) and unknown species of yam badnavirus have been reported in yam producing areas in Africa^1,10,12-22. They often induce leaf symptoms like mosaic, chlorotic spotting, curling and mottling²³. Except for some species of Badnavirus and Ampelovirus, which can be transmitted by mealybugs in a semi-persistent manner, the rest of the viruses infecting yam are transmitted by a wide range of aphid species^11,21. Mechanical transmission of the viruses to yam and Nicotiana plants has also been reported⁸. Farmers’ practices like the exchange of seed materials contribute to widespread distribution and increased incidence of viral diseases in yam eld¹.

In Africa, efforts are being made to control yam viruses and increase yam production through their identification, diagnosis and control strategies^24,25. Despite the progress on yam research in West Africa, data on the occurrence and distribution of yam viruses are scanty in other countries in SSA, particularly in Central and East Africa.

This paper presented the existing knowledge of yam viruses reported in Africa to date and the diagnostic tools developed. Finally, future perspectives on the virus infecting yam in Africa are discussed.

Diversity of viruses infecting yam in Africa: Among 16 virus species reported to infect yam in Africa (Table 1), only four viruses are most important and well characterized in some SSA countries^9,10,12,23. These are YMV, YMMV, CMV and Badnaviruses. The YMV is known to be the most severe virus in reducing tubers yield, followed by YMMV²³.

Genus Ampelovirus (family Closteroviridae): Based on their genome organization and biological properties such as insect vectors, host plants and transmission mechanisms, the family Closteroviridae harbors viruses of the genus Closterovirus, Ampelovirus, Crinivirus and Velarivirus²⁶. In the genus Ampelovirus, viruses have a monopartite positive-sense RNA genome and show wide variation in size and organization²⁶. According to Martelli et al.²⁷ viruses of this genus are grouped into two subgroups. The YaV1 belongs to first subgroup²¹.

Yam ampelovirus 1 (YaV1): The YaV1, renamed Yam asymptomatic virus 1, has been reported in yam germplasm collection from South America, Africa (Nigeria and Cote d’Ivoire), the Caribbean and South Pacific²¹. The genome sequence of YaV1 comprises 14,855 nucleotides (nt) in length and has 10 ORFs²¹. Like other Ampelovirus, YaV1 is transmitted by mealybugs in a semi-persistent manner^26,28. Attempt for mechanical and seed-based transmission have not been successful²¹. Despite the presence of YaV1 in Nigeria and Cote d’Ivoire, YaV1 occurrence in others yam-producing regions in SSA is less reported and documented.

Yam virus 1 (YV-1) : Using HTS, a novel specie of the family Closteroviridae, named YV-1 was first reported on D. rotundata in Ethiopia²⁸. The genome of YVY isolates has a monopartite positive-sense single-stranded RNA genome of 7911 nt long with three putative ORFs and 8435 nt long with eight putative ORFs, respectively for YV-1 RNA2 and YV-1 RNA1 isolates²⁸. To date, no information on the epidemiology of YV-1 in other yams producing zones in Africa is available.

Genus Aureusvirus (family Tombusviridae): Members of the family Tombusviridae have small single-stranded, positive-sense, RNA genome. It contains the genus Tombusvirus, Auresvirus, Carmovirus, Necrovirus, Avenavirus, Machlomovirus, Panicovirus and Diathovirus. Based on genome organization, these genera are divided into three distinct groups tombusvirus-like, carmovirus-like and Diathoviruses³¹. Plant viruses in Aureusvirus genus have a positive stranded RNA genome with four ORFs, encoding RNA-dependent RNA polymerase (ORF1), a coat protein (ORF2), the protein involved in movement (ORF3) and a silencing suppressor proteins (ORF4)¹⁷. These viruses are soil-borne viruses and the mechanical transmission by sap inoculation from infected plants to health ones has been reported by Martelli et al.²⁷.

Yam spherical virus (YSV): The YSV is the first plant virus infecting yam and the fifth plant virus species of the genus Aureusvirus¹⁷. First reported from D. rotundata in Nigeria, the genome sequence of YSV comprises 4,464 nt and has 4 putative ORFs, anked by non-translated regions (NTR) at the 5’ and 3’ ends¹⁷. Mechanical transmission of YSV to other test plants is possible¹⁷. To date, no information on the presence of YSV in others yam producing zones in Africa is available.

Genus Badnavirus (family Caulimoviridae): The plant viruses of the family Caulimoviridae have a non-covalently closed circular dsDNA genomes of 7.1-9.8 kbp with a bacilliform or isometric particles non-enveloped³². This family contains genera Caulimovirus, Soymovirus, Cavemovirus, Petuvirus, Solendovirus, Rosadnavirus, Badnavirus and Tungrovirus. However, the last two have a bacilliform virion whilst others have an isometric virion³². The Badnaviruses are a circular double stranded DNA genome of around 7.3-9.2 kbp with at least 3 ORFs^19,33. In some regions of Africa, yams are infected by several species of Badnavirus^19,34 and induce severe chlorosis and distortion on leaves. The virus can be transmitted in a semi-persistent manner by mealybugs between yams species, but mechanical transmission can also be possible^13,15,19,33.

The presence of endogenous pararetrovirus in the genome of Africa yam D. cayenensis-rotundata complex, called endogenous D. bacilliform viruses (eDBVs) and the high level of sequence variation among Badnavirus complicates the development of specific reliable molecular detection tests for yam-infecting badnaviruses^18,35.

Dioscorea bacilliform AL virus (DBALV) Syn.
Dioscorea alata bacilliform virus (DaBV): The DaBV occurs on Dioscorea spp., in Africa¹³ and was first reported on D. alata in Nigeria³⁶. The complete genome of the DaBV isolates from Nigeria was reported by Bhat et al.³⁶ and comprises 7413 and 7415 bp for two isolates. Its sequence has three ORFs. However, the comparison of DaBV sequence with others Badnavirus shows the highest levels of similarity to the Cacao Swollen Shoot Virus which occurs in the same regions where the DaBV isolates from Nigeria were described by Briddon et al.³⁷. Data on geographical distribution and epidemiology of DaBV in others yam producing countries in Africa, particularly in Central and Eastern Africa, where badnaviruses were reported in other tropical crops^36,38,39, remains scarce.

Dioscorea bacilliform SN virus (DsBV) Syn.
Dioscorea sansibarensis bacilliform virus (DsBV): The DsBV was first reported by Seal and Muller¹⁵ on a wild plant named D. sansibarensis from Benin. However, in other yam-producing areas in Africa, no information on the occurrence of DsBV is available. The genome size of DsBV is ~7.3 kbp, encoding for three open reading frames⁴⁰. However, the molecular analysis of a full-length sequence shows that DsBV shared the most identity of around 61.9% to DaBV¹⁵.

Dioscorea bacilliform RT virus 1 (DBRTV1) and Dioscorea bacilliform RT virus 2 (DBRTV2): The two Badnavirus species (DBRTV1 and DBRTV2) were first detected on D. rotundata from Nigeria¹⁹. They have a single molecule of circular double-stranded DNA genome of 7438-7708 bp in length^19,41. The genome sequence of DBRTV1 and DBRTV2 has three to four ORFs^19,41. However, the ORF 4 partially overlapped the 3’ end of ORF3 and encodes a 138 amino acid putative protein⁴¹. Despite the existence of DBRTV1 and DBRTV2 in West Africa, no available information on their presence in other African countries is up to date.

Genus Cucumovirus (family Bromoviridae): Plant viruses of the family Bromoviridae are among the most important viruses which attack a wide host’s range including herbaceous plants, shrubs and trees. The members of the Bromoviridae family have a tri-segmented, positive-sense, single-stranded RNA genomes of 8 kb with a spherical or bacilliform virion non-enveloped^42,43. However, Bujarski et al.⁴³ report that viruses of this family Bromoviridae have three genomic RNAs from the end 5’. The RNA1 and RNA2 code for viral replicase proteins, respectively while the RNAs 3 encode the movement (MP) and coat proteins (CP).

Plant viruses of the family Bromoviridae include genera; Alfamovirus, Ilarvirus, Bromovirus, Cucumovirus, Oleavirus and Idaeovirus^44-46. Members of the genus Cucumovirus have a wide host range where more than 1200 plant species are infected and some of them are responsible of major disease epidemics in crop plants⁴⁷. Also, viruses in the Cucumovirus genus have tri-segmented, positive-sense, single-stranded RNA genomes of 8 kb with a spherical virion particle of a diameter 26-35 nm⁴⁷. Transmission occurs mechanically or in insect vectors in a non-persistent manner⁴⁷. Among virus species of Cucumovirus genera, CMV is the most economic and has already been reported on yam in Africa²⁹.

Cucumber mosaic virus (CMV): The CMV was first described as the causal agent of plant diseases reported on cucumber by Roossinck⁴⁸ and has a wide range of host plants^48-50. On yam, it has been reported on D. alata and D. rotundata in West Africa^16,29,51,52 and well characterized by Eni et al.⁵³. To date, no information on the presence, distribution and incidence of CMV in others yam producing zones in central and Eastern Africa are available.

The CMV has a tripartite plus-sense RNAs virus non-enveloped⁵⁴. A part of genomic RNAs, a subgenomic RNA and named RNA 4 is enveloped in virion of all strains of CMV with the genomic RNA3. In strains of subgroup II, an additional subgenomic RNA called RNA 4A is also enveloped⁵⁵. Rizos et al.⁵⁰ showed that more than one hundred isolates of CMV have been well characterized and are available in GenBank. In this fact, the existence of these isolates confirms the greatest degree of variation of CMV⁵⁰. Based on serological relationships and nucleic acid hybridization, CMV isolates are split into two subgroups (I and II)⁵⁶. However, CMV strains infecting yam belong to subgroup one⁵³.

More than 80 species of Aphids are responsible for CMV transmission from infected plants to healthy ones in a non-persistent manner; among them, Aphis gossypii and Myzus persicae are the most efficient⁵⁷. Apart from the transmission by vectors, CMV can also be spread mechanically or through infected seeds^58,59.

Unresolved genera of the family Secoviridae: Members of the Secoviridae family have positive-sense single-stranded RNA genomes (mono or bi-partite) of 9-13.7 kb in size with an icosahedral virion particle non-enveloped of 25-30 nm of diameter⁶⁰.

In Africa, DMaV and DMoV have been reported in yam production areas^14,22,61. The DMaV was first detected in Nigeria by HTS. Currently, it is likely to be distributed across West Africa on Dioscorea sp.^22,61, but remains less documented. The plant-to-plant transmission has been described by Bakayoko et al.²². Apart from DMaV, Nyaboga et al.¹⁴ reported the existence of another member of the family Secoviridae infecting D. alata in West Africa named DMoV and susceptible to being spread throughout West Africa.

Genus Potexvirus (family Alphaflexiviridae): Viruses of the Alphaflexiviridae family have a single-stranded, positive-sense RNA genome of 5.4 -9 kb with flexuous filamentous virions ranging in size from 470-800 nm in length and 12-13 nm in diameter⁶². The family Alphaflexiviridae contains plant viruses of genera Potexvirus, Mandarivirus, Lolavirus, Allexivirus, Botrexvirus, Platypuvirus and Sclerodarnavirus^63,64.

Among genera belonging to Alphaflexiviridae family, species of the genus Potexvirus have been detected in yam growing regions in Africa⁹ but remain less documented. Although, the geographical distribution of their host plants makes the members of potexvirus genus, the broadest host range plant virus, despite some members can infect a limited number of host plants⁶⁵.

Dioscorea latent virus (DLV): The DLV was first reported on an asymptomatic plant of Dioscorea spp., in West Africa⁹. To date, no information on the occurrence, distribution and incidence of DLV in other yam-producing zones in Africa is available. The DLV has a single-stranded RNA genome of 7.5 kb with a flexuous filamentous virion of 445 nm in length^66,67 and it is mechanically transmitted to Dioscorea spp. and some herbaceous hosts.

Unknown genus of family Betaflexiviridae: The family of Betaflexiviridae contains two subfamilies (Trivirinae and Quinvirinae) including 15 genera^68,69. It has a monopartite positive-sense single-stranded RNA genome of 6.5-9 kb with non-enveloped flexuous filamentous virions ranging in size from 600-1000 nm in length and 12-13 nm in diameter^63,68.

Viruses belonging to this family infect mostly woody plants while only some herbaceous plants can be infected⁷⁰. The transmission plant to plant by insect vectors like aphids, mealybugs, mites and scale insects and mechanical transmission is also possible^68,69. The representative species belonging to the Betaflexiviridae family that occurs in yam-production area in Africa is Yam virus Y.

Yam virus Y (YVY): The YVY was first described on D. rotundata from Nigeria and Ghana by HTS²⁰. The complete genome of YVY isolates (YVY-Dan and YVY-Mak isolates) has been sequenced and has a monopartite positive-sense single-stranded RNA genome of 7557 and 7584 nt in length, respectively for YVY-Dan and YVY-Mak isolates, with five ORFs encoding large replication protein (ORF1), the three proteins involved in viral movement (ORF2 orF3 and ORF4) and a putative coat protein (ORF5)^20,71.

Genus Potyvirus (family Potyviridae): Viruses in the Potyviridae family constitute the most important group of plant viruses which cause yield losses and affect the quality of many crops worldwide⁷². The family of Potyviridae has a positive-sense, single-stranded RNA genome of 8-11 kb in size with a exuous laments particles ranging in size from 11-20 nm in diameter and 680-900 nm in length for some viruses in Potyviridae family and others have a virion with two modal lengths of 200-300 and 500-600 nm^73,74.

Based on host range, genomic features and phylogeny, Yang et al.⁷⁵ showed that plant viruses in Potyviridae include Bevemovirus, Brambyvirus, Bymovirus, Celavirus, Ipomovirus, Macluravirus, Poacevirus, Potyvirus, Roymovirus, Rymovirus and Tritimovirus. The Potyvirus genus is the most economically important and contains 167 to 183 out of 228 species belonging to the Potyviridae family⁷⁵.

Viruses in Potyviridae are usually transmitted by insect vectors (Aphids, whiteflies and mites) in a non-persistent manner. An exception of Bymoviruses which have a bipartite genome are transmitted by the fungus Polymyxa graminis and mechanically by inoculation of sap^73,75.

Species of Potyvirus genus are widely distributed in the world, especially in tropical and sub-tropical regions and have a greater diversity of vectors than other members of Potyviridae^73,76.

Yam mosaic virus (YMV): The YMV was first reported on D. cayenensis in Côte d’Ivoire¹² and it occurs in many yam production areas worldwide on several species of Dioscorea^77,78. To date, the complete genome of two isolates (Côte d’Ivoire and YMV-NG) have been sequenced and are respectively a single-stranded RNA genome of 9608 and 9594 nt in length^79,80. According to Bousalem et al.⁷⁷ and Mendoza et al.⁸¹, YMV has a monopartite positive-sense single-stranded RNA genome of 9-12 kbp exhibiting high genetic diversity and consisting of more than one serotype. Njukeng et al.²³ have shown that the prevalence of YMV depends on host plants, varieties and regions. However, the information on YMV prevalence in other yam producing zones, particularly in Eastern and Central Africa remains scanty. This information is relevant to understand epidemiology of YMV and develop control strategies for effective management.

The use of YMV infected tuber seeds, mechanical and insect vector transmissions are the most important mechanisms of transmission through which YMV is known to be spread^8,77. The efficiency of transmission of YMV by insect vectors has little been explored¹² and has never been compared between yam species and other YMV strains. Although, the transmission test made by Thouvenel and Fauquet¹² using YMV isolates from Cote d’Ivoire, suggested that YMV was being transmitted by a wide range of aphid species (A. gossypii, A. craccivora, M. persicae, Rhopalosiphum maidis and Toxoptera citricida) in a non-persistent manner.

Yam mild mosaic virus (YMMV): The YMMV was first reported on D. alata in West Africa¹⁰ and described to be the most important virus on yam which reduces tuber yield and quality after YMV²³. Based on serological and molecular characterization of isolates from Martinique, Colombia and Brazil, Mumford and Seal²⁴ confirmed YMMV as a distinct Potyvirus.

To date, the virus occurs in other yam growing areas worldwide, particularly on the most widely cultivated D. alata than other yam species^{1,16,23,24,40,82-85}.

The YMMV has flexuous filamentous virions with around 750 nm in length¹⁰. The complete genome sequences of YMMV isolates available in the NCBI nucleotide database range from 9521 to 9538 nt in length, without the poly (A) tail. The coat protein (CP) gene of YMMV is 798 nt in length and encodes for a protein of 266 aa and 30 kDa^2,86. The YMMV is transmitted by aphid vectors from the natural host to herbaceous hosts, particularly cowpea. However, as with other Potyviruses, the DAG motif belonging to this protein plays an important role in aphid transmission⁸⁷. Also, it is mechanically transmitted by inoculation sap within some Dioscorea and Vigna sp.¹⁰. No information on the epidemiology of YMMV in other yam-producing countries in Central Africa is available, except in Cameroon where YMMV was first detected in single or mixed infection with YMV¹.

Ethiopian yam virus (EYV): The EYV was first reported on D. rotundata from Ethiopia by high-throughput sequencing (HTS)²⁸. Using HTS, the genome of EYV has been sequenced and has a monopartite positive-sense single-stranded RNA genome of 9557 nt in length with the ORF encoding a protein of 3087 aa with around 347.5 kDa of molecular mass²⁸. To date, no information on the occurrence and epidemiology of EYV in other yams-producing zones in Africa is available.

Distribution of yam viruses reported in Africa: Studies on the geographical distribution of yam viruses reported the presence of sixteen yam virus species in Africa (Table 1). The occurrence of YMV in several countries revealed that it’s the most important virus in the yam field across Africa²³. However, some yam virus-like symptoms have been reported in yam field in Eastern and Central Africa^84,88,89, although the current status of yam viruses in these areas remains unknown.

Disease symptoms and yield losses in yam field: The yam viruses reported in Africa can induce yam leaves common symptoms like mosaic, chlorosis, mottling and leaf deformation^20,23,24,61. However, typical symptoms of yam viruses on leaves have been reported and are variable depending on the yam species or cultivars, nature of virus species/strains and agroecological zones^17,90.

Table 1:

List of viruses infecting yam in Africa

Family	Genus	Species	Transmission	Diagnostic tools	First report	References
Alphaflexiviridae	Potexvirus	Dioscorea latent virus (DLV)	Aphids and mechanical	ELISA and RT-PCR	Cote d’Ivoire	Bakayoko et al.22
Betaflexiviridae	Unknown	Yam virus Y (YVY)	Unknown	RT-PCR	Nigeria, Ghana	Silva et al.20
Bromoviridae	Cucumovirus	Cucumber mosaic virus (CMV)	Aphids	ELISA and IC-RT-PCR	West Africa	Diouf et al.29
Caulimoviridae	Badnavirus	Dioscorea bacilliform AL virus (DBALV)	Mealybugs	DAS-ELISA and IC-PCR	Nigeria	Phillips et al.13
		Dioscorea bacilliform SN virus (DBSNV)	Mealybugs	PAS-ELISA and IC-PCR	Benin	Seal and Muller15
		Dioscorea bacilliform RT virus 1	Mealybugs	IC-PCR	Nigeria	Bömer et al.19
		Dioscorea bacilliform RT virus 2	Mealybugs	IC-PCR	Nigeria	Bömer et al.19
		Uncharacterized species of yam badnavirus	Unknown	IC-PCR	Benin, Nigeria	Eni et al.30, Umber et al.18 and Bömer et al.19
Closteroviridae	Ampelovirus	Yam ampelovirus 1 (YaV1)	Mealybugs	RT-PCR	Nigeria	Marais et al.21
	Crinivirus	Yam virus 1 (YV-1)	Whiteflies	RT-PCR and HTS	Ethiopia	Gogile et al.28
Potyviridae	Potyvirus	Yam mosaic virus (YMV)	Aphids	ELISA and RT-PCR	Cote d’Ivoire	Thouvenel and Fauquet12
		Yam mild mosaic virus (YMMV)	Aphids	ELISA and RT-PCR	Nigeria	Odu et al.10
		Ethiopian yam virus (EYV)	Unknown	ACP-ELISA and RT-PCR	Ethiopia	Gogile et al.28
Tombusviridae	Aureusvirus	Yam spherical virus (YSV)	Mechanical	ELISA and RT-PCR	Nigeria	Menzel et al.17
Secoviridae	Unknown genera	Dioscorea mosaic associative virus (DMaV)	Beetle	HTS	Nigeria	Silva et al.20
		Dioscorea mottle virus (DMoV)	Beetle	ELISA	West Africa	Nyaboga et al.14
ELISA: Enzyme Linked Immunosorbent Assay, RT-PCR: Reverse Transcriptase Polymerase Chain Reaction, DAS: Double antibody sandwich, IC: Immuno capture, PAS: Protein a-sandwich, HTS: High throughout sequencing and ACP: Antigen-coating plate

Some yam viruses such as DaBV, DsBV, DLV and YSV-infected plants can reveal symptoms like mild chlorosis and leaf distortion which can differ from yam species, while others plants remain symptomless despite YSV and yam badnaviruses infection^17,36. In addition, other studies^9,24,28 reported that some species of Dioscoreaceae (D. alata, D. cayenensis-D. rotundata complex and D. trifida) infected by YMMV, EYV and YV-1 shown symptoms like mild mosaic and mild mottle, while others yam species (D. rotundata for example) remain symptomless despite viral infection. Otherwise, YVY induces symptoms like mosaic and chlorotic on leaves of infected plants especially in mixed infection with YMV whilst singly-infected plants remain asymptomatic²⁰. On D. alata, YMMV induces similar symptoms to those induced by YMV, in addition to mild chlorosis and severe stunting^{1,16,23,24,40,82,83,85}. Moreover, YMV induces leaves symptoms like mosaic, chlorotic spotting and curling²³. The similar symptoms induced by YMV can be observed in yam infected with DsBV, DMoV and DMaV^14,15,61. Eni et al.⁵³ showed that the strain of CMV-infecting yam induces systemic chlorosis, necrotic lesions and leaf distortion on Nicotiana glutinosa and systemic mosaic on Cucumis sativus. To date, no apparent symptoms are visible on African yam infected by YaV1²¹.

These characteristics of yam infected by viruses with no apparent symptoms show that some species or cultivars are resistant to viral infection but can make it difficult to develop the control strategies. As a consequence, yam tubers’ quantity and quality are affected and so the international movement of germplasm is restricted¹⁰. Thus, the evaluation of species/cultivars of yam for tolerance to yam viruses is relevant to develop control strategies based on preventing or reducing spread of yam viruses.

Yield losses estimated due to plant virus diseases are not easy due to different parameters that must be considered to produce effective results⁹¹. The impact of yam virus diseases on yield in Africa remains less documented, except for some yam viruses such as YMV, YMMV and CMV^52,92-95. Amusa et al.⁹⁵ reported that yield loss due to yam mosaic virus in the field of around 50% and more could be unregistered. However, studies in Cote d’Ivoire and Nigeria have shown that the significant yield losses of 30-50% could be caused by YMV and CMV⁵².

Mainly focused on viruses in single infection, the results of these experiments are not only sufficient but for a good assessment, other parameters such as yield losses due to yam viruses in mixed infection, decreased tuber size and different agroecological zones, should have been considered. In addition, some biotic factors such as viral loads and symptom severity may influence yield losses in the field. So, for a good assessment, it will be important to consider these factors⁹⁶.

Diagnostic tools: Currently, available methods for diagnosis of yam viruses are biological assays, immunoassays and nucleic acid-based techniques. Various epidemiological factors such as the nature of isolates or strains of pathogens, appearance of symptoms origin of inoculum, mixed infections, environmental conditions and choice of the indicator plant, can affect the results of diagnosis using biological assays and therefore their reliability⁹⁷. For example, many yam viruses like YSV, CMV, DLV, YVY, YMMV and some Badnavirus species, which remain symptomless on herbaceous hosts or clearly appear in mixed-infection and non-transmissible mechanically by inoculation of sap, diagnostic using biological assays shall be less sensitive and not reliable^{9,17,19,20,24}.

Recent progress in immunology, biochemistry and molecular biology makes serological and molecular analysis the most common methods known to detect and identify pathogens and thus, could provide a reliable alternative to biological assays. Due to their high sensitivity and reliability, ELISA and PCR are largely useful in yam viruses’ diagnosis and hence used for certification of planting materials²⁴. Many serological and PCR-based techniques have been developed for diagnosis of yam viruses^{2,16,19,24,25,35,98-106}.

The triple antibody sandwich enzyme-linked immunosorbent assay (TAS-ELISA), protein A-sandwich enzyme-linked immunosorbent assay (PAS-ELISA) and immunocapture reverse transcription polymerase chain reaction (IC-RT-PCR) are largely used for yam potyviruses detection^24,25,77,100. These methods offer

some advantages such as reliability, sensitivity, specificity and results available in a short time¹⁰⁵. However, some of them such as PCR require high-quality DNA/RNA which takes time and can hardly be done in the field.

Silva et al.¹⁰⁵ reported a rapid test for yam potyviruses (YMV and YMMV) called Direct Reverse Transcription-Recombinase Polymerase Ampli cation (Direct RT-RPA). Through this method, the virus is directly detected from plant leaf extract prepared with inexpensive reagents which provide high-quality of nucleic acids and take a short time (~30 min) to get results. In addition, Nkere et al.¹⁰⁴ developed a method for the detection of YMV called Closed-Tube Reverse Transcription Loop-Mediated Isothermal Amplification (CT-RT-LAMP). They asserted that this method had the same specificity and was 100 times more sensitive compared to the RT-PCR standard.

Since the discovery of CMV serotypes, the ELISA test using polyclonal or monoclonal antibodies has become very useful for routine detection of CMV¹⁰⁷. To date, the polyclonal antibodies against CMV isolates infecting yam are available and already used by Eni et al.¹⁰⁸. In case of low concentration of virus in the CMV infecting plants and mixed infections, this method tends to provide false results¹⁰⁷. However, to resolve this problem, PCR-based methods variants (RT-PCR, IC-RT-PCR) have been developed to detect and identify CMV in the plants^{98,99,109,110}. A multiplex RT-PCR which can detect, identify and subgroup CMV isolates including their satellite RNA has already been developed by Chen et al.¹¹⁰ and provides good results.

Among the diagnosis methods used for virus species, including Badnavirus, ELISA is very useful for routine detection and identification¹¹¹. However, the high level of natural variation of Badnavirus infecting yams, the existence of endogenous pararetrovirus in the genome of yam plants and the unavailability of antibodies in adequate numbers, constitute the main limiting factors for the development of serological and molecular diagnostic tools for Badnavirus infecting yam plants^35,106,112. To solve these problems, several diagnostic methods were evaluated. For example, Eni et al.³⁵ developed a multiplex PCR-DGGE for screening of badnavirus sequences from African yam germplasm. In addition, Bömer et al.¹⁹ evaluated a sequence-independent multiply-primed rolling circle ampli cation (RCA) method to determine which episomal viruses have integrated Badnavirus sequences in some yam genomes. This approach shows the existence of eleven full-length yam badnavirus sequences, giving a total of four species groups that can occur in single or mixed infections in Western Africa.

For the detection of unknown viruses or strains of known viral species or novel pathogens, Next-Generation Sequencing (NGS) based detection has been described in diagnosing yam viruses^28,113. For example, Silva et al.²⁰ reported the presence of a new yam viral species named YVY in leaf samples of D. rotundata from Nigeria and Ghana using NGS technique. In addition, Gogile et al.²⁸ reports two new species named EYV and YV-1 in symptomatic and asymptomatic yam plants from Ethiopia. These discoveries show that, in the areas where data on yam viruses are scanty like in SSA regions, NGS technique will be very helpful for the discovery of new viral species on yam.

Using PCR-dependent denaturing gradient gel electrophoresis (PCR-DGGE) methods, Turaki et al.¹⁰³ showed that this method was capable of detecting the virus in the complex mixtures of potentially episomal and endogenous Badnavirus sequences. Moreover, numerous RCA protocols including random-primed RCA (RP-RCA), primer-spiked random-primed RCA (primer-spiked RP-RCA), directed RCA (D-RCA) and specific-primed RCA (SP-RCA) have been evaluated and optimized for use on yam, taro, banana and sugar cane infected with DBALV¹⁰⁶. They, therefore, suggest that using optimized RCA protocols together with NGS was reliable enough to characterize and detect other species of yam Badnavirus.

Future perspectives: Increasing yam productivity in SSA through improved knowledge of the occurrence and detection of types of yam viruses’ diseases for effective management is one of the factors important for poverty elimination. Several scientific publications have shown very strong findings in yam viruses’ research in West Africa and demonstrate that yam viruses are one of the major causes of global yam production decrease leading to severe economic losses and limiting the exchange of planting materials between yam-producing zones^{1,10-13,16-24,29,30,34,35,40,51,61,77,90,96,104,114}.

Despite this progress on yam viruses’ research in West Africa, data are scanty in other countries of SSA, particularly in Central and Eastern parts of Africa continent, probably due to the inattentiveness of research centers in some countries where yam is considered an orphan crop^1,7,89. Although, based on yam virus-like symptoms, the data on the presence of yam virus diseases have been reported in these areas^84,88,89. Thus, suggesting their possible existence. So, additional studies in other yam-producing zones in Africa are needed for the development of diagnostic methods and disease control strategies to prevent or control yam virus diseases and increase yam productivity.

Serological and molecular methods are most common for the diagnosis of yam viruses. The reliability of each diagnostic method depends on the nature of the virus, plant species, plant tissue samples and the objective of assay^115,116. However, the secondary metabolites like glutinous polysaccharides and polyphenols, presents in high concentration in yam plants can limit getting of good quality DNA for PCR analysis²⁵. In parallel with secondary metabolites, virus infecting plant induce a high concentration of these compounds¹¹⁷. So, the identification of the plant part with high viral titer would contribute to the quick detection of pathogens using molecular methods.

In addition, the efficiency of these methods for the detection of yam viruses has little been explored^52,100,115 and never compared yam plant tissues from different species and at specific growing periods for YMV detection. This will represent an ideal step for future perspectives and will not only add to the efficiency, reliability and quick detection but also a cost-effective option.

CONCLUSION

This review paper presented the existing knowledge on yam viruses across Africa, their biological characteristics and geographical distribution. The reported symptoms of diseases and yield losses associated with viral infections and the existing diagnostic tools have been elucidated. Based on the available data, the most important viruses infecting yam in SSA have been documented. This includes YMV, YMMV, CMV and some species of Dioscorea infecting Badnavirus. Other new yam viruses such as YaV1, YSV, EYV, YV-1, DMaV, DMoV, DLV and YVY have likewise been reported on yam in West Africa. Further studies are needed in order to prevent or control yam virus diseases in all yam-producing zones in Africa. Also, several methods and techniques have been developed to diagnose and detect yam viruses with high sensitivity, specificity and reliability. However, enhancing the reliability of molecular detection will pass through the use of plant parts which high viral titer. We, therefore, suggest that the selection of the most suitable plant part will contribute to the reproducibility of yam viruses’ detection by PCR. This review will serve as a reference for advances in research on yam viruses worldwide particularly in yam-producing countries in Africa.

SIGNIFICANCE STATEMENT

The yam viruses are one of the constraints of yam production decrease leading to severe economic losses. Increasing yam productivity through improved knowledge of occurrence and detection of yam viruses’ diseases for effective management is an important factor for poverty elimination in Africa. This paper provides the existing information on yam viruses in Africa and diagnostic tools developed up to date. In conclusion, further studies on knowledge of occurrence of yam viruses in yam fields are needed to prevent or control yam virus diseases in Africa. Also, enhancing the reliability of molecular detection through the use of plant parts with high viral titer will facilitate quick detection and action against viral diseases for effective management.

ACKNOWLEDGMENTS

We acknowledge the Partnership for Skills in Applied Sciences, Engineering and Technology (PASET) through the Regional Scholarship and Innovation Fund (RSIF) awarded to Emmanuel Kulimushi to carry out doctoral studies at SACIDS Africa Centre of Excellence for Infectious Diseases, SACIDS Foundation for One Health, Sokoine University of Agriculture, Morogoro, Tanzania. The authors thank the direction of the Smart services sarl and Dr Isaac BALUME for spelling and grammar check.

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