Open Access

Interactions of viruses in Cowpea: effects on growth and yield parameters

Virology Journal20074:15

DOI: 10.1186/1743-422X-4-15

Received: 28 November 2006

Accepted: 08 February 2007

Published: 08 February 2007

Abstract

The study was carried out to investigate the effects of inoculating three cowpea cultivars: "OLO II", "OLOYIN" and IT86D-719 with three unrelated viruses: Cowpea aphid-borne mosaic virus (CABMV), genus Potyvirus, Cowpea mottle virus (CMeV), genus Carmovirus and Southern bean mosaic virus (SBMV), genus Sobemovirus singly and in mixture on growth and yield of cultivars at 10 and 30 days after planting (DAP). Generally, the growth and yield of the buffer inoculated control plants were significantly higher than those of the virus inoculated plants. Inoculation of plants at an early age of 10 DAP resulted in more severe effect than inoculations at a later stage of 30 DAP. The average values of plant height and number of leaves produced by plants inoculated 30 DAP were higher than those produced by plants inoculated 10 DAP. Most of the plants inoculated 10 DAP died and did not produce seeds. However, " OLOYIN" cultivar was most tolerant and produced reasonable yields when infected 30 DAP. The effect of single viruses on growth and yield of cultivars showed that CABMV caused more severe effects in IT86D-719, SBMV had the greatest effect on "OLO II" while CMeV induced the greatest effect on "OLOYIN". Yield was greatly reduced in double infections involving CABMV in combination with either CMeV or SBMV in "OLOYIN" and "OLO II", however, there was complete loss in yield of IT86D-719. Triple infection led to complete yield loss in all the three cultivars.

Background

Cowpea is an annual tropical grain legume, which plays an important role in the nutrition of people in developing countries of the tropics and subtropics, especially in sub-Saharan Africa, Asia Central and South America. Due to its high protein content (20 – 25%), cowpea has been referred to as "poor man's meat". It is very palatable, highly nutritious and relatively free of metabolites or other toxins [1, 2].

Cowpeas are susceptible to a wide range of pests and pathogens that attack the crop at all stages of growth [3]. These include insects, bacteria, fungi and viruses. Estimated losses due to virus infection have been variously put at between 10 and 100% [4, 5], depending on the virus-host-vector relationships as well as the prevailing epidemiological factors. Host- plant resistance is currently the most effective method for the control of cowpea virus diseases in Africa. Thus, an adequate knowledge of the viruses and the strains occurring in the main cowpea-growing areas of Africa is a pre-requisite for effective control [6].

Out of more than 20 viruses reported on cowpea from different parts of the world [79] nine are known to infect the crop naturally in Nigeria [1012]. They include the following viruses: Cowpea aphid-borne mosaic virus (CABMV), genus Potyvirus, Cowpea yellow mosaic virus (CPMV), genus Comovirus, Southern bean mosaic virus (SBMV), genus Sobemovirus, Cowpea mottle virus (CMeV), genus Carmovirus, Cowpea golden mosaic virus (CPGMV), genus Bigeminivirus, Cucumber mosaic virus (CMV), genus Cucumovirus, Cowpea mild mottle virus (CPMMV), genus Carlavirus, Sunn-hemp mosaic virus (SHMV), genus Tobamovirus and Blackeye mosaic virus (BICMV), genus Potyvirus. On the basis of geographical distribution, pathogenic variability and yield losses, CABMV, CPMV and occasionally SBMV are the most important viruses in Nigeria. CMeV, CPGMV and CMV are of localized importance while CPMMV and SHMV are not important. BICMV has a low rate of occurrence. Separation and identification of these viruses is by vector transmission, mechanical inoculation to diagnostic host species, symptomatology and serology [12].

Mixed viral infections in plant have been known for a long time and the mechanisms by which co-infecting viruses interact to alter host response have been a matter of speculation for a long time [13]. Mixed viral infections are common in plants and interactions may occur between viruses within the same host cell. Such viral interactions may be antagonistic or synergistic [14]. Antagonism usually occurs when the co-infecting viruses are related, resulting in interference [15] or cross-protection [16, 17]. Synergism normally occurs in mixed infections when the pair of viruses involved are unrelated, resulting in more severe disease symptoms than those produced by single infections [1820].

Surveys conducted by Shoyinka et al. [21] in Nigeria indicated that viruses occur in mixtures naturally and they cause mixed infections in cowpea crops. This research was designed to address the following objectives:

(a) to examine the effects of single and mixed infections by CABMV, CMeV and SBMV on growth and yield parameters of three Nigeria commercial cowpea cultivars and

(b) to determine the effect of age of plant at time of inoculation on the above parameters

Materials and methods

One isolate each of Cowpea Aphid-borne mosaic virus (CABMV), genus Potyvirus, Cowpea mottle virus (CMeV), genus Carmovirus and Southern bean mosaic virus (SBMV) genus Sobemovirus were obtained from the International Institute of Tropical Agriculture (IITA), Ibadan, Nigeria. In order to increase the viruses and to ensure their availability, the three viruses were maintained by periodic transfer to healthy cowpea cultivar; Ife brown, in the greenhouse.

Three cowpea cultivars; IT86D-719, "OLO-II" and "OLOYIN" were used for the study. IT86D-719 obtained from IITA, Ibadan, "OLO-II" and "OLOYIN", which are two of Nigeria's commercial cowpea cultivars obtained from Mushin market, Mushin, Lagos State.

In the greenhouse, perforated plastic pots were filled with loamy soil obtained from Shodex Beautification Land Mark, Anthony, Lagos. The soil was sterilized with cypermethrin 10% E.C. to eliminate soil inhibiting microorganisms and enriched with farm yard manure. Two seeds of each cowpea cultivar were sown in each pot in October 2003. The plots were arranged in a split plot in a randomized complete block design with three replications. There were two factors, the virus treatment as main plot and cultivars as subplots. Each block consisted of 72 plastic pots and a total of 144 pots were utilized for the study. The seedlings were constantly watered and weeds removed manually as at when necessary. Inoculations were performed at 10 and 30 days after planting with single and mixed viruses consisting of CABMV, CMeV, SBMV, CABMV+CMeV, CABMV+SBMV, CMeV+SBMV and CABMV+CMeV+SBMV.

Virus extracts from infected plants maintained in greenhouse were prepared by grinding infected leaves with sterilized pestles and mortars in buffer. The buffer used throughout the study was 0.05 M dipotassium hydrogen orthophosphate (K2HPO4) pH 7.5 at a ratio of 1:2 (tissue weight: buffer volume). Leaf surfaces of plants to be inoculated were dusted with carborundum (180 grit) and pestles were used to apply the inoculum. Mixed virus inocula were prepared by weighing the leaves containing the different viruses separately and grinding equal weights of the infected leaves with sterilized pestles and mortars in K2HPO4 at a ratio of 1:2 wt/vol. The plants that served as control were inoculated with buffer solution only. Hands were thoroughly washed with detergent between treatments to prevent contamination. All the inoculated plants were rinsed with water after inoculation and kept in a greenhouse with temperatures at 25–28°C.

The effect of the different inocula on the growth parameters such as number of leaves and plant heights were determined by counting the number of leaves and measuring the heights of plants (in centimeters) that received the different treatments including controls and the averages of each parameter per replicate were determined. The effect of the different inocula on yield parameters was also determined by counting the number of flowers per plant, number of pods per plant length of each pod, and number of seeds per plant that received the different treatments including the controls replicate wise. A sensitive weighing balance (Mettler Toledo) was used to determine the weight of seeds after drying the seeds in the sun for seven days.

The statistical package for social scientist (SPSS) was used for the analysis of the data obatained. Duncan's multiple range test was used to determine the level of significance between the virus treatments at 5% probability level.

Results

Effect of virus inocula and age of plant at time of inoculation on growth and yield of "OLO II" cultivar

From the results in Table 1, all the treatments at 10 days after planting (DAP) had significantly different reduction in the heights of inoculated plants compared with buffer inoculated control plants. However, the heights of plants inoculated 30 DAP with CABMV alone and CMeV alone were not different from those of the controls. Inoculation of the "OLO II" with a mixture of the three viruses resulted in the greatest reduction in plant height with the average values at 12.7 cm and 22.1 cm for plants inoculated at 10 and 30 DAP compared with the 69.3 cm for the buffer inoculated plants. Infections with SBMV either singly or in combination with CMeV resulted in the greatest reduction in plant heights.
Table 1

The Effects of Virus Inoculum and Stage of Plant Growth at the Time of Inoculation on Growth and Yield of Cowpea Cultivar "OLO II"

Inoculum

API

Plant Height(cm)

No. of Leaves

No. of Flowers

No. of Pods

Pod length(cm)

Seed no./pod

Seed Weight(g)

CABMV

10

20.8bc

12.0b

0.0*

0.0

0.0

0.0

0.0

 

30

66.6a

23.0ab

4.7a

1.3b

4.1b

2.0b

0.05b

CMeV

10

26.7bc

7.0c

0.0

0.0

0.0

0.0

0.0

 

30

66.5a

18.1b

0.7b

0.0

0.0

0.0

0.0

SBMV

10

19.1c

3.5c

0.0

0.0

0.0

0.0

0.0

 

30

50.6ab

15.8b

1.0b

0.0

0.0

0.0

0.0

CABMV+

10

22.4bc

2.9c

0.0

0.0

0.0

0.0

0.0

CMeV

30

32.8b

11.0b

0.7b

0.7b

2.1b

1.3b

0.04c

CABMV+

10

25.7bc

3.1c

0.0

0.0

0.0

0.0

0.0

SBMV

30

36.3b

14.9b

0.7b

0.0

0.0

0.0

0.0

CMeV+

10

13.5c

3.6c

0.0

0.0

0.0

0.0

0.0

SBMV

30

56.9ab

25.1ab

5.0a

2.0a

8.1a

3.7a

0.1b

CABMV+

10

12.7c

2.4c

0.0

0.0

0.0

0.0

0.0

CMeV+

30

22.1bc

10.2b

0.0

0.0

0.0

0.0

0.0

SBMV

10

65.5a

18.7b

3.7a

2.7a

9.4a

3.3a

0.14b

BUFFER

30

69.3a

40.4a

4.7a

3.0a

10.4a

4.3a

0.16a

API-Age of plant at inoculation; CABMV-Cowpea aphid-borne mosaic virus, CMeV-Cowpea mottle virus, SBMV-Southern bean mosaic virus.

Each value is the mean of 3 replicates. In each column means followed by the same letter are not significantly different (P < 0.05) according to Duncan's multiple range test.

*All zero (0) values carry the letter c according to Duncan's multiple range test.

Similarly, all plants inoculated at 10 and 30 DAP produced significantly fewer leaves compared with the buffer inoculated control except for inoculation with CABMV alone (Table 1). The number of leaves was greatly reduced when the plants were inoculated with a mixture of the three viruses with average values of 2.4 and 10.2 for plants inoculated at 10 and 30 DAP respectively. These values were significantly different from the 18.7 and 40.4 observed for the buffer inoculated control plant of the same age.

Still from Table 1, virus treated plants produced lower yields compared with the control. The effect of the viruses on the yield of "OLO II" revealed that plants inoculated with single and mixed viruses at 10 DAP produced no flowers or flowers aborted prematurely and therefore no seeds were produced. However, plants inoculated with CABMV, CABMV+CMeV and CMeV+SBMV at 30 DAP produced a few seeds.

Effect of virus inocula and age of palnt at time of inoculation on growth and yield of IT86D-719 cultivar

In table 2, severe stunting was induced in plants inoculated with a mixture of the three viruses. Inoculations with CABMV alone and in mixture with SBMV at 10 (DAP) resulted in the greatest reduction in plant height. Single inoculations with CMeV, SBMV or double inoculation with CABMV+ CMeV and CABMV+SBMV resulted in fairly similar effects on plant height. Inoculation of cowpea cultivars IT86D-719 with the three viruses caused the greatest reduction in number of leaves at 10 DAP with an average value of 0.6 while CABMV alone and its combination with SBMV also resulted in significantly reduced number of leaves with 1.0 and 3.3 respectively compared to 9.0 for the control plant at the same age of inoculation. The effect of inoculating with CMeV alone and in combination with SBMV were not significantly different from those of the controls in the number of leaves at 10 and 30 DAP.
Table 2

The Effect of Virus Inoculum And Stage of Plant Growth at the Time of Inoculation on Growth and Yield of Cowpea Cultivar IT86D-719

INOCULUM

API

Plant height(cm)

No. of leaves

No. of Flowers

No. of Pods

Pod length(cm)

Seed no./pod

Seed Weight(g)

CABMV

10

21.8b

1.0c

0.0*

0.0

0.0

0.0

0.0

 

30

40.4a

10.0b

1.0b

0.0

0.0

0.0

0.0

CMeV

10

25.9b

5.2b

0.0

0.0

0.0

0.0

0.0

 

30

37.9ab

16.0a

3.0ab

0.0

0.0

0.0

0.0

SBMV

10

28.5b

14.0a

0.0

0.0

0.0

0.0

0.0

 

30

38.7ab

14.1a

6.3a

3.3ab

9.1a

6.7a

0.1b

CABMV+

10

33.5ab

14.2a

0.3bc

0.0

0.0

0.0

0.0

CMeV

30

37.8ab

6.0b

0.7bc

0.0

0.0

0.0

0.0

CABMV+

10

24.9b

3.3c

0.0

0.0

0.0

0.0

0.0

SBMV

30

36.1ab

6.9b

0.0

0.0

0.0

0.0

0.0

CMeV+

10

25.2b

8.8b

1.7b

0.0

0.0

0.0

0.0

SBMV

30

41.7a

24.6a

1.7b

0.0

0.0

0.0

0.0

CABMV+

10

19.8c

0.6c

0.0

0.0

0.0

0.0

0.0

CMeV+

30

25.7b

12.6a

0.0

0.0

0.0

0.0

0.0

SBMV

10

37.6ab

9.0b

4.3a

2.7b

7.9b

5.0b

0.2a

BUFFER

30

42.3a

13.0a

6.7a

4.0a

8.6a

5.0b

0.2a

API-Age of plant at inoculation; CABMV-Cowpea aphid-borne mosaic virus, CMeV-Cowpea mottle virus, SBMV-Southern bean mosaic virus.

Each value is the mean of 3 replicates. In each column means followed by the same letter are not significantly different (P < 0.05) according to Duncan's multiple range test.

*All zero (0) values carry the letter c according to Duncan's multiple range test.

In the same Table 2, the various virus treatments resulted in a complete loss in yield of cultivar IT86D-719 except for plants inoculated with SBMV at 30 DAP. A few flowers were produced by some of the plants but seeds were generally not produced.

Effect of virus inocula and age of plant at time of inoculation on growth and yield of "OLOYIN" cultivar

From the result in table 3, the effect of CMeV+SBMV and a combination of the three viruses produced the most severe effect on plant height with average values of 7.8 cm to 8.1 cm respectively. In single viral infections, the severity of infection on plant height was milder than those of the mixed infections with CMeV having the least effect at early and late inoculations with mean values of 23.1 cm and 27.7 cm respectively. The effect of SBMV on plant height was not significantly different from the controls at early inoculation. The greatest reduction in number of leaves was observed in plants inoculated with a mixture of CABMV and CMeV at 10 and 30 DAP with means of 5.7 and 13.6 compared with 18.9 and 25.0 for buffer inoculatd control respectively. In single infections, CMeV produced the greatest effect on number of leaves followed by CABMV while SBMV induced the least effect. However, in double infections, it was the mixture of CABMV and CMeV that produced the greatest effect (Table 3).
Table 3

The Effects of Virus Inoculum and Stage of Plant Growth at the Time of Inoculation on Growth and Yield of Cowpea Cultivar "OLOYIN" Cultivar

INOCULUM

API

Plant height(cm)

No. of Leaves

No. of Flowers

No. of Pods

Pod length(cm)

Seed no./pod

Seed Weight(g)

CABMV

10

24.9b

11.1b

0.0*

0.0

0.0

0.0

0.0

 

30

33.8ab

20.9b

3.7b

3.0b

9.6a

6.7a

0.09b

CMeV

10

23.1b

6.9c

0.0

0.0

0.0

0.0

0.0

 

30

27.7b

17.1b

3.3b

2.0b

7.1b

2.0b

0.01c

SBMV

10

28.2b

17.2b

0.0

0.0

0.0

0.0

0.0

 

30

40.4a

18.0b

2.3b

1.3b

10.2a

6.7a

0.1b

CABMV+

10

11.9c

5.7c

0.0

0.0

0.0

0.0

0.0

CMeV

30

26.7b

13.6b

1.3b

1.0b

5.2b

3.3ab

0.06b

CABMV+

10

12.4c

17.9b

0.0

0.0

0.0

0.0

0.0

SBMV

30

30.4b

22.1a

2.0b

1.7b

4.1b

2.7b

0.05b

CMeV+

10

7.8c

12.8b

0.0

0.0

0.0

0.0

0.0

SBMV

30

23.8b

23.4a

3.0b

2.0b

4.0b

1.7b

0.09b

CABMV+

10

8.1c

9.3c

0.0

0.0

0.0

0.0

0.0

C MeV+

30

12.2c

14.4b

1.0b

0.0

0.0

0.0

0.0

SBMV

10

29.7b

18.9b

6.0a

5.3a

9.3a

4.3a

0.145a

BUFFER

30

42.7a

25.0a

7.0a

6.3a

10.0a

5.3a

0.145a

API-Age of plant at inoculation; CABMV-Cowpea aphid-borne mosaic virus, CMeV-Cowpea mottle virus, SBMV-Southern bean mosaic virus.

Each value is the mean of 3 replicates. In each column means followed by the same letter are not significantly different (P < 0.05) according to Duncan's multiple range test.

*All zero (0) values carry the letter c according to Duncan's multiple range test.

Still in Table 3, no flowers or seeds/pods were produced by all the plants inoculated 10 DAP. This was significantly different from the controls which had an average value of 6.0 flowers and 4.3 seeds/pods. However, the plants inoculated at 30 DAP produced flowers and seeds except in plants inoculated with combination of the three viruses, which produced no seeds (Table 3).

Discussion

The results of this study indicate that the three cowpea cultivars used in this investigation were susceptible to the three viruses and the viruses replicate in them in both single and mixed infections. There have been reports of Cowpea aphid-borne mosaic virus [22, 23], Cowpea mottle virus [24] and Southern bean mosaic virus [21] existing in Nigeria.

Early infection of cowpea cultivars with single or mixed viruses resulted in shortening of internode, apical necrosis, which led to cessation of growth, stunting and eventual plant death. This fact is substantiated by the research of Pio-Ribeiro et al. [25] which indicated that CABMV and Cucumber mosaic cucumovirus interact synergistically to produce cowpea stunt, a disease characterized by severe stunting and yields loss. Also, Niblett and Claflin [26] and Uyemoto et al. [27] demonstrated that maize dwarf mosaic virus (MCMV) in maize (Zea mays) to induce the necrosis disease which resulted in up to 91% yield loss and death of many plants especially when infection occurred early. This is also confirmed by this study where early infection of cultivars by viruses resulted in more drastic response than infection at a later stage of growth.

The results of the effect of single and mixed virus infection on the growth parameters of cowpea cultivars showed significant reduction in the growth parameters in plants inoculated at an early age. Inoculation of cultivars with CABMV, CMeV and SBMV alone and in mixed infection at 10 days after planting resulted in fewer leaves and reduced plant height than inoculation at 30 days after planting. This finding is in agreement with the previous report that the younger the plants at the time of viral infection the greater the severity of disease symptoms [28].

The result of this study showed that single or multiple inoculation of the three cultivars with CABMV, CMeV and SBMV at an early age (10 days after planting) resulted in complete loss in yield. The earlier a virus infects a plant, the more severe the reduction in yield [29, 30]. Gilmer et al. [31] showed that inoculation of cowpea cultivars with Cowpea yellow mosaic virus (CpMV) 7 days after emergence reduced yield by 40%-60% compared to the 10%-15% loss in yield when plants were inoculated at flowering. In "OLOYIN" cultivar yields were not affected when plants were infected 30 days after planting but in "OLO II" and IT86D-719, there was complete loss in yield in almost all the treatments irrespective of time of inoculation. This is in agreement with the report of Wells and Deba [32] which reported up to 100% yield loss in cowpea in Western Nigeria due to CpMV. Raheji and Leleji [5] also reported that CABMV resulted in a complete loss of an irrigated cowpea crop in Northern Nigeria. Owolabi et al. [33] reported that infection of some Nigeria commercial cowpea lines by BICMV could result in a complete loss in yield.

The losses recorded in the commercial variety vary from one cultivar to another. "OLO II" is more susceptible to viral infection than "OLOYIN". This in accordance with the report of Owolabi et al. [33] that when both Ife brown and the Nigerian B7 cultivars were each single inoculated with BICMV and CPMV, the effect was more pronounced on the Nigerian B7 than the Ife brown. A report says that many of the severe disease caused by viral synergistic interactions occur when one of the infecting viruses is a member of the genus Potyvirus [34]. This statement is substantiated by the result obtained for the yield of the three cultivars where the mixture of CABMV with either CMeV and or SBMV produced severe loss in yield. This may be due to virus infection depending among other factors on virus isolate, the presence of another virus, the tolerance of the infected cowpea cultivars and the stage of the host plant at the time of the infection [3537].

The two commercial varieties used in this study are susceptible to the three viruses. Taiwo [12] reported that in Nigeria, the most economical, practicable and effective method of control of legume viruses is through the use of resistant varieties. Cowpea lines with individual or combined resistance to severe cowpea viruses has been identified at IITA [11]. Source of resistance have also been identified in soybean [38]. Such legume lines are being tested in different localities for selection of the best locally adapted varieties with multiple virus resistance [11]. However, the rate of acceptance and utilization of such resistant varieties is rather poor.

There is need to prevent early infection and complete loss of crop by producing virus free seeds and controlling virus vectors. There is also a need to ensure availability of acceptable horticulturally desirable cowpea cultivars with a high level of resistance to cowpea viruses for the nation to sustain its high level of productivity.

Authors’ Affiliations

(1)
Department of Microbiology University of Agriculture
(2)
Department of Botany, Microbiology University of Lagos

References

  1. Kay DE: Food legumes. Tropical Development and Research Institute London 1979.Google Scholar
  2. Quass CF: Guidelines for the Production of Cowpeas, National Department of Agriculture, Pretoria. 1995.Google Scholar
  3. Allen DJ: The Pathology of Tropical Food Legumes. John Wiley and Sons, Chichester; 1983.Google Scholar
  4. Shoyinka SA: Status of virus diseases of cowpea in Nigeria. In Proceedings of the First IITA grain Legumes Improvement Workshop. IITA, Ibadan, Nigeria.; 1974:270-273.Google Scholar
  5. Raheja AK, Leleji OI: An aphid – borne virus disease of irrigated cowpea in Northern Nigeria. Plant Disease Reporter 1974, 58: 1080-1084.Google Scholar
  6. Rossel HW, Thottappilly G: Control of virus diseases in Africa's major food crops through breeding for resistance. In Virus Diseases of Plants in Africa. Edited by: Williams AO, Mbiele AL and Nkouka N. Organisation of African Unity/Scientific, Technical and Research Commission, Lagos; 1988:169-187.Google Scholar
  7. Thottappilly G, Rossel HW: World-wide occurrence and distribution of virus diseases. In Cowpea research, production and utilization. Edited by: Singh SR and Rachie KO. John Wiley and sons, Chichester, UK; 1985:155-171.Google Scholar
  8. Mali VR, Thottappilly G: Virus diseases of cowpea in the tropics. In Reviews of Tropical Plant Diseases. Volume 3. Edited by: Raychandhuri SP and Varma JP. ; 1986:361-403.Google Scholar
  9. Brunt A, Crabtree K, Gibbs A: Viruses of Tropical Plants. CAB International, Wallingford, UK; 1990.Google Scholar
  10. Taiwo MA, Shoyinka SA: Viruses infecting cowpeas in Africa with special emphasis on the potyviruses. In Virus Diseases of Plants in Africa. Edited by: Williams AO, Mbiele AL and Nkouka N. OAU/STRC Scientific Publication, Lagos, Nigeria; 1988:93-115.Google Scholar
  11. Thottappilly G, Rossel HW: Virus diseases of cowpea in tropical Africa. Tropical Pest Management 1992,38(4):337-348.View ArticleGoogle Scholar
  12. Taiwo MA: Viruses infecting legumes in Nigeria: case history. In Plant Virology in Subsaharan Africa. Proceedings of Plant Virology. Edited by: AHughes J'd' and Odu B. IITA, Ibadan, Nigeria; 2003:364-378.Google Scholar
  13. Ross REF: Interaction of viruses in the host. Acta Hortic 1974, 36: 247-260.View ArticleGoogle Scholar
  14. Hull R: Matthew's plant Virology. 4th edition. san Diego: Academic press; 2002.Google Scholar
  15. Sakai E, Dawson JRO, Watts JW: Interference in infections of tobacco protoplasts with bromoviruses. J Gen virol 1983, 64: 1347-1354.View ArticleGoogle Scholar
  16. Watts JW, Dawson JRO: Double infection of tobacco protoplasts with brome mosaic virus and cowpea chlorotic mottle virus. Virology 1980, 105: 501-507. 10.1016/0042-6822(80)90050-1PubMedView ArticleGoogle Scholar
  17. Khan JA, Lohuis H, Goldbach RW, Dijkstra J: Distribution and localization of bean common virus and bean black root virus in stems of doubly infected bean plants. Arch Virol 1994, 138: 95-104. 10.1007/BF01310041PubMedView ArticleGoogle Scholar
  18. Walkey DGA, Payne CJ: The reaction of two lettuce cultivars to mixed infection by beet western yellows virus. Plant Pathol 1990, 39: 156-160.View ArticleGoogle Scholar
  19. Jensen SG, Lane LC, Seifers DL: A new disease of maize and wheat in the high plains. Plant Disease 1996, 80: 1387-1390.View ArticleGoogle Scholar
  20. Cho JD, Kim JS, Choi HS, La YJ, Kim KS: Ultrastructural aspects of the mixed infections of watermelon mosaic potyvirus isolated from pumpkin and cucumber green mottle mosaic tobamovirus from watermelon. Plant Pathol J 2000, 16: 216-221.Google Scholar
  21. Shoyinka SA, Thottappilly G, Adebayo GG, Anno-Nyako FO: Survey on cowpea virus incidence and distribution in Nigeria. International Journal of Pest Management 1997,43(2):127-132. 10.1080/096708797228816View ArticleGoogle Scholar
  22. Huguenot C, Furneaux MT, Thottappilly G, Rossel HW, Hamilton Rl: Evidence that cowpea aphid-borne mosaic virus and blackeye cowpea mosaic viruses are two different potyviruses. Journal of General Virology 1993, 74: 335-340.PubMedView ArticleGoogle Scholar
  23. Huguenot C, Furneaux MT, Hamilton RI: Capsid protein properties of cowpea aphid- borne mosaic virus and blackeye cowpea mosaic virus confirm the existence of two major subgroups of aphid-transmitted, legume infecting potyviruses. Journal of General Virology 1994, 75: 3555-3560.PubMedView ArticleGoogle Scholar
  24. Rossel HW, Thottappilly G: Virus diseases of important food crops in tropical Africa. IITA Publication Series, Ibadan, Nigeria; 1985.Google Scholar
  25. Pio-Riberio G, Wyatt SD, kuhn CW: Cowpea stunt: a disease caused by a synergistic interaction of two viruses. Phytopathology 1978, 68: 1260-1265.View ArticleGoogle Scholar
  26. Niblett CL, Clafin LE: Corn lethal necrosis, a new virus disease of corn in Kansas. Plant Dis Reptr 1978, 62: 15-19.Google Scholar
  27. Uyemoto JK, Claflin LE, Wilson DL, Rayney RJ: Maize Chlorotic mottle and maize dwarf mosaic viruses: Effect of single and double inoculations on symptomatology and yield. Plant Disease 1981, 65: 39-41.View ArticleGoogle Scholar
  28. Agrios GN, Walker ME, Ferro DN: Effect of cucumber mosaic virus inoculation at successive weekly intervals on growth and yield of pepper ( Capsicum annum ) plants. Plant Disease 1985, 69: 52-59.View ArticleGoogle Scholar
  29. Matthews REF: Plant Virology. Academic Press London, New York; 1970:778.Google Scholar
  30. Chant SR: The effect of infection with tobacco mosaic and cowpea yellow mosaic viruses on growth rate and yield of cowpea in Nigeria. Emp J exp Agric 1960, 28: 114-120.Google Scholar
  31. Gilmer RN, Whitney WK, Williams RJ: proccedings of the first IITA grain legume improvement programme workshop. International Institute of Tropical Agriculture, Ibadan; 1974:325.Google Scholar
  32. Wells DG, Deba R: Sources of resistances to cowpea yellow mosaic virus. Plant Dis Reptr 1961, 45: 878-881.Google Scholar
  33. Owolabi AT, Taiwo MA, Mabadeje SA: Effects of single and mixed inoculations with blackeye cowpea mosaic virus on two Nigerian cowpea cultivars. Nigerian Journal of Basic and Applied Sciences 1988, 2: 25-33.Google Scholar
  34. Anjos JR, Jarlfors U, Ghabrial SA: Soybean mosaic virus potyvirus enhances the titer of two comoviruses in dually infected soybean plants. Phytopath 1992, 82: 1022-1027.View ArticleGoogle Scholar
  35. Ross JP: Effect of single and double infections of soyabean mosaic and bean pod mottle viruses on soyabean yield and seed characters. Plant Dis Reptr 1968, 52: 344-348.Google Scholar
  36. Ross JP: Effect of time and sequence of inoculation of soybean with soybean mosaic and bean pod mosaic viruses on yield and seed characters. Phytopathology 1969, 59: 1404-1408.Google Scholar
  37. Lana AO, Adegbola MOK: Important virus diseases in West African crops. CMI Review of Plant Pathology 1977, 56: 854-855.Google Scholar
  38. Rossel HW: Rice yellow mottle and African soybean dwarf, newly discovered virus diseases of economic importance in West African. Paper presented at the International Symposium on Virus Diseases and Rice Leguminous Crops , Tsukuba, Japan. 1985.Google Scholar

Copyright

© Kareem and Taiwo; licensee BioMed Central Ltd. 2007

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Advertisement