Skip to main content

Reduction in vertical transmission rate of bean common mosaic virus in bee-pollinated common bean plants


Vertical transmission, the transfer of pathogens across generations, is a critical mechanism for the persistence of plant viruses. The transmission mechanisms are diverse, involving direct invasion through the suspensor and virus entry into developing gametes before achieving symplastic isolation. Despite the progress in understanding vertical virus transmission, the environmental factors influencing this process remain largely unexplored. We investigated the complex interplay between vertical transmission of plant viruses and pollination dynamics, focusing on common bean (Phaseolus vulgaris). The intricate relationship between plants and pollinators, especially bees, is essential for global ecosystems and crop productivity. We explored the impact of virus infection on seed transmission rates, with a particular emphasis on bean common mosaic virus (BCMV), bean common mosaic necrosis virus (BCMNV), and cucumber mosaic virus (CMV). Under controlled growth conditions, BCMNV exhibited the highest seed transmission rate, followed by BCMV and CMV. Notably, in the field, bee-pollinated BCMV-infected plants showed a reduced transmission rate compared to self-pollinated plants. This highlights the influence of pollinators on virus transmission dynamics. The findings demonstrate the virus-specific nature of seed transmission and underscore the importance of considering environmental factors, such as pollination, in understanding and managing plant virus spread.

Main text

We have previously shown that virus-infected plants exhibit the ability to influence their animal pollinators. For instance, infected tomato (Solanum tuberosum L.) and bean (Phaseolus vulgaris L.) plants emit volatile organic compounds that attract bumblebees (Bombus terrestris L.) [12, 21]. Furthermore, the negative impact of virus infection on tomato seed yield was ameliorated by bee pollination, and tomato pollen transfer by bumblebees was biased in favor of virus-infected plants in cross-pollination [12, 23], underscoring the complexity of these ecological interactions. In this study, we investigated the vertical transmission of the most important viruses limiting Phaseolus vulgaris (common bean) bean yield: the potyviruses bean common mosaic virus (BCMV) and bean common mosaic necrosis virus (BCMNV) and the cucumovirus, cucumber mosaic virus (CMV) [22, 31, 32, 35]. These viruses are primarily transmitted by aphids, with seed-borne transmission accounting for about 2% of the infections [5, 35]. Yet, despite the progress in understanding vertical virus transmission, the environmental factors exerting influence on this process remain largely unexplored [27]. We investigated vertical transmission of BCMNV, BCMV, and CMV in P. vulgaris plants that had been allowed to self-pollinate under controlled conditions, and also compared the seed transmission rate of BCMV in self-pollinated, hand-pollinated and bee-pollinated plants grown in a glasshouse and in an experimental field plot. By exploring both controlled and outdoor growth conditions, along with the influence of bee pollination, we aimed to unravel the environmental factors shaping the vertical transmission of these viruses. Our investigation not only contributes to the growing body of knowledge on plant virus ecology but also sheds light on the broader implications of these interactions for crop productivity and ecosystem dynamics.

Vertical transmission, the passage of pathogens from one generation to the next through seed or pollen, plays a pivotal role in the persistence of plant viruses. Vertical transmission ensures the sustained presence of viruses in plant populations across successive generations, even in the absence of suitable alternative hosts or vectors [26, 28]. In crops, infected seeds are a significant source of primary inoculum that can lead to damaging epidemics upon germination [13, 26]. Mechanisms governing vertical transmission are diverse, encompassing direct invasion through the suspensor and virus entry into developing gametes before symplastic isolation [28]. Seedborne viruses, associated with the maternally-derived seed coat, can also occasionally give rise to infected offspring, tobamoviruses being a notable example [6]. While vertical transmission garners increasing research attention, questions persist regarding the molecular mechanisms and environmental factors influencing this process [16, 27].

Notably, more than a quarter of known plant viruses exhibit vertical transmission [28, 30]. The intricate relationship between plants and their pollinators further complicates this dynamic. Animal-mediated pollination, particularly by bees, is indispensable for the reproduction of a substantial portion of major crops and an astounding 90% of wild flowering plants [1, 25]. Recent literature highlights the dual role of pollen not only in fertilisation but also as a potential vector for viruses infiltrating plant seeds [3, 10]. An increasing number of plant viruses have been identified within pollen [9, 10]. While the detection of a virus in pollen does not necessarily mean that a virus is pollen-transmitted, insect-assisted pollination nevertheless introduces a novel layer of complexity to the understanding of virus transmission dynamics.

Differential rates of seed transmission for three bean viruses

Under controlled growth conditions (described in [33]), plants of P. vulgaris cv. ‘Wairimu’/Red Haricot-GLP 585 (Simlaw Seeds, Nairobi, Kenya) were mechanically inoculated with BCMNV (PV-0413), BCMV (PV-0915), or CMV (bean isolate PV-0473) (obtained from the German Collection of Microorganisms and Cell Cultures) 10 days post-germination on the first two true leaves. Seed progeny from virus-infected, self-pollinated bean plants from each treatment group were germinated and tested for the presence of virus using double-antibody sandwich enzyme-linked immunosorbent assay (ELISA) for BCMV, BCMNV, or CMV coat protein (Bioreba AG, Reinach, Switzerland). Vertical transmission of viruses from self-pollinated plants was highest for BCMNV (29.4%), followed by BCMV (22%) and CMV (8%) (Fig. 1B). The proportion of plants where seed transmission of the virus was detected was similarly highest for BCMNV-infected plants and lowest for CMV (Fig. 1A).

Fig. 1
figure 1

Rate of seed transmission for three viruses. Both at (A) parental and (B) progeny seedling levels, BCMNV recorded the highest seed transmission rate, followed by BCMV and CMV. Seeds from 18–24 plants in each treatment group were germinated for virus seed transmission testing. n = number of seedlings tested

Bee pollination under field conditions reduces the rate of BCMV seed transmission

Systemically-infected plants that had been inoculated 10 days post germination with BCMV, were transferred from a glasshouse to a field site (Botanic Garden Experimental Plot, University of Cambridge) at the onset of flowering (twenty days later). Plants were either kept under netting to exclude large insect pollinators, or left uncovered. Plants under netting had a BCMV seed-transmission rate of 30% (Fig. 2 C), comparable to the seed transmission rate of BCMV in plants grown in a controlled growth room (Fig. 1B). Most (8 out of 10) of the plants transferred outdoors produced a portion of offspring that were positive for BCMV (Fig. 2A). Remarkably, pollination by bees of the uncovered plants elicited a significant reduction in BCMV seed transmission rate to 12%. Daily observations of the uncovered plants revealed that one species of wild bumblebee visited flowers on these plants, Bombus pascuorum (common carder bee: Fig. 3A and B). The reduction in the rate of BCMV vertical transmission was also reflected in the lower proportion of plants that gave rise to infected progeny (Fig. 2A, C).

Fig. 2
figure 2

Bee pollination elicited a reduction in BCMV seed transmission both at parent plant and progeny seeding levels. Seed collected from BCMV-infected bean plants were germinated and tested for BCMV. The proportion of plants that permitted BCMV seed transmission (A) is shown. n = number of plants from which seed was collected. Plants grown in the greenhouse were either moved outdoors at the commencement of flowering and placed in the field plot so that wild bee pollinators could access the flowers or placed under bee-proof netting. In other experiments, flowering plants remained in the greenhouse and were either hand-pollinated by mechanically "tripping" the hull and wings of the bean flower to expose the stamens and pistil, or exposed to bumblebees that could pollinate freely. Seed harvested from bee- or hand-pollinated plants was germinated and tested for BCMV (B). There was a significant reduction in seed transmission of BCMV in outdoor bee-pollinated plants compared to plants under netting with no access to bees (Chi-square: X2 (1, N = 299) = 15.1, p = 0.000104). There was no significant difference in the seed transmission rate of hand- and bee-pollinated plants that remained in the greenhouse (Chi-square: X.2 (1, N = 324) = 0.127, p = 0.721)

Fig. 3
figure 3

Bee visitation to uncovered flowering bean plants. An initial 14-h dawn to dusk observation indicated that only one species of bumblebee, B. pascuorum (common carder bee), visited an array of 10 uninfected and 10 BCMV-infected bean plants placed outside and that there was no peak foraging period (A). Over the subsequent seven days between 10:00 am and 2:00 pm, the frequency of bee visits to flowers of both mock-inoculated and BCMV-infected plants was recorded (B). The cumulative frequency is shown (equating to not more than 8 visits per day to any individual plant). Floral visitation frequency was similar to flowers of both mock-inoculated plants and BCMV-infected plants

Bee and hand-pollination under glasshouse conditions reduces the rate of BCMV seed transmission

Experimental plants were raised in batches. Plants were mechanically inoculated with BCMV 10 days post-inoculation on the first two true leaves. During the second week of flowering, half of each batch of plants were exposed to bumblebees, while the other half underwent hand-pollination at the same time, all under glasshouse conditions. Hand-pollination involved manually depressing the hull petal of the bean flower, or “tripping”, to force the stamens and stigma into physical contact to thereby enhance self-pollination.

Pollination of infected plants by B. terrestris from commercially produced colonies (Koppert Biological Systems, Berkel en Rodenrijs, The Netherlands) resulted in a comparably low rate of vertical transmission of BCMV as plants pollinated outdoors by wild bumblebees (Fig. 2B). Similarly, hand-pollination of common bean flowers resulted in a 16% BCMV transmission rate, not significantly different from the vertical transmission rate in bee-pollinated plants (Fig. 2).


Virus seed transmission can be achieved directly (internally) through invasion of the developing ovule (before fertilisation) or the embryo (after ferilisation) and indirectly by infected male gametes [28]. In direct embryo invasion after fertilisation, Wang and Maule [34] showed that viruses invade the embryo via the suspensor, which functions as a conduit for nutrient flow to support the growth of the embryo. Both direct and indirect embryo invasion processes can operate simultaneously for certain viruses in specific hosts, as observed in barley stripe mosaic virus in barley [19] and BCMV in common bean [20, 29]. Importantly, we found that BCMV-infected plants, when pollinated by bees under glasshouse and field conditions, or hand-pollinated, produced progeny seedlings with significantly lower BCMV transmission rates compared to plants where pollination was not assisted.

Although common bean is self-fertile, pollination services from almost exclusively hymenopteran insects can significantly increase seed yield [8, 11]. This is likely due to the improved efficiency of pollen deposition onto the stigma that occurs when large pollinators (i.e. bees and certain wasps) with sufficient weight and strength mechanically "trip" the hull and wings of the bean flower as they forage on the pollen and nectar [2]. Delivery of pollen loads to the stigma that exceed the threshold necessary to fertilise all ovules will lead to competition among pollen grains, which may improve offspring quality and maternal fitness [14]. Given that infected pollen is known to contribute to BCMV vertical transmission [20, 29], it is possible that the reduction in BCMV vertical transmission by bee or hand-assisted pollination could be explained by pollen competition with BCMV-free pollen outcompeting pollen carrying the virus, reducing the likelihood of embryo invasion. Although there is no direct evidence that BCMV-infected pollen is less fit than virus-free pollen, pollen from BCMV-infected plants has been shown to result in shorter germ tubes than pollen from healthy bean plants [20].

Our investigation into the efficiency of seed transmission rates revealed considerable variation among different virus species, with CMV exhibiting the lowest transmission rate, followed by BCMV, and BCMNV displaying the highest. Other studies in Arabidopsis have shown that the efficiency of poty- and cucomovirus vertical transmission was dependent on both the virus species and accession/ecotype of Arabidopsis [4]. The virus/host interaction factors influencing the likelihood of seed transmission include virus virulence, speed of movement within the host, multiplication in reproductive tissues, survival of virus-infected gametes and embryos, and host defence responses [4, 7, 15, 26, 28, 34]. Our results align with these ideas as we found that BCMNV, which is more virulent than BCMV in common bean, also had the highest rate of vertical transmission. However, Kyrychenko et al. (2020) [18] reported that P. vulgaris cv. Chervona Shapochka transmitted the Ukrainian BCMV strain in 77% of the seeds produced by infected plants, indicating an unusually high vertical transmission rate for this BCMV isolate that may be due either to the low resistance of the cultivar to BCMV, or the high virulence of BCMV strains circulating in common bean in Ukraine.

Hamelin et al. [13] and Pagán [26] emphasise the risks associated with seed transmission, particularly in introducing diseases to new areas, for example through the seed trade or when growers produce their own seed. Even an initial low incidence of seed transmitted virus has been known to initiate epidemics [17]. This is especially important for self-fertile leguminous crops in sub-Saharan Africa and South Asia where farmer produced seed is popular, as an alternative to the formal seed sector because of affordability [24]. 

This study expands our understanding of virus seed transmission dynamics and highlights the importance of pollinator behaviour in mediating and mitigating disease spread. Here, we suggest bee-pollination as an environmentally friendly method capable of both enhancing seed production and lowering the rate of virus-seed transmission.

Availability of data and materials

No datasets were generated or analysed during the current study.


  1. Klein AM, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T. Importance of pollinators in changing landscapes for world crops. Proc R Soc B. 2007;274:303–13.

    Article  PubMed  Google Scholar 

  2. Aouar-Sadli M, Louadi K, Doumandji SE. Pollination of the broad bean (Vicia faba L. var. Major) (Fabaceae) by wild bees and honey bees (Hymenoptera: Apoidea) and its impact on the seed production in the Tizi-Ouzou area (Algeria). Afr J Agric Res. 2008;3(4):266–72.

    Google Scholar 

  3. Card SD, Pearson MN, Clover GRG. Plant pathogens transmitted by pollen. Australas Plant Pathol. 2007;36:455–61.

    Article  Google Scholar 

  4. Cobos A, Montes N, López-Herranz M, Gil-Valle M, Pagán I. Within-host multiplication and speed of colonization as infection traits associated with plant virus vertical transmission. J Virol. 2019;93:e01078-e1119.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Davis RF, Hampton RO. Cucumber mosaic virus isolates seedborne in Phaseolus vulgaris: serology, host-pathogen relationships, and seed transmission. Phytopathol. 1986;76:999–1004.

    Article  Google Scholar 

  6. Dombrovsky A, Smith E. Seed transmission of Tobamoviruses: Aspects of global disease distribution. Adv Seed Biol. 2017;12:233–60.

    Google Scholar 

  7. Domier LL, Hobbs HA, McCoppin NK, Bowen CR, Steinlage TA, Chang S, et al. Multiple loci condition seed transmission of Soyabean mosaic virus (SMV) and SMV-induced seed coat mottling in soyabean. Phytopathol. 2011;101:750–6.

  8. Elisante F, Ndakidemi P, Arnold SEJ, Belmain SR, Gurr GM, Darbyshire I, Xie G, Stevenson PC. Insect pollination is important in a smallholder bean farming system. PeerJ. 2020;8:e10102.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Fetters AM, Cantalupo PG, Wei N, et al. The pollen virome of wild plants and its association with variation in floral traits and land use. Nat Commun. 2022;13:523.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Fetters AM, Ashman TL. The pollen virome: a review of pollen-associated viruses and consequences for plants and their interactions with pollinators. Am J Bot. 2023;110:e16144.

    Article  PubMed  Google Scholar 

  11. Franceschinelli EV, Ribeiro PLM, Mesquita-Neto JN, Bergamini LL, Madureira de Assis I, Elias MAS, Fernandes PM, Carvalheiro LG. Importance of biotic pollination varies across common bean cultivars. J Appl Entomol. 2022;146:32–43.

    Article  CAS  Google Scholar 

  12. Groen SC, Jiang S, Murphy AM, Cunniffe NJ, Westwood JH, Davey MP, et al. Virus infection of plants alters pollinator preference: a payback for susceptible hosts? PLoS Pathog. 2016;12(8):e1005790.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Hamelin FM, Allen LJS, Prendeville HR, Hajimorad MR, Jeger MJ. The evolution of plant virus transmission pathways. J Theor Biol. 2016;396:75–89.

    Article  PubMed  Google Scholar 

  14. Hildesheim LS, Opedal ØH, Armbruster WS, Pélabon C. Quantitative and qualitative consequences of reduced pollen loads in a mixed-mating plant. Ecol Evol. 2019;9(24):14253–60.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Hull R. Plant virology. 5th ed. London: Academic Press; 2014.

    Google Scholar 

  16. Hoffmann G, Incarbone M. A resilient bunch: stem cell antiviral immunity in plants. New Phytol. 2024;241:1415–20.

    Article  CAS  PubMed  Google Scholar 

  17. Jones RAC. Plant virus emergence and evolution: Origins, new encounter scenarios, factors driving emergence, effects of changing world conditions, and prospects for control. Virus Res. 2009;141:113–30.

    Article  CAS  PubMed  Google Scholar 

  18. Kyrychenko A, Hrynchuk K, Antipov I, Likhanov A. Bean Common Mosaic Virus Transmission by Bean Seed cv. Chervona Shapochka. In: Tiwari AJ, editor. Advances in Seed Production and Management. 2020.

    Chapter  Google Scholar 

  19. Mandahar CL. Virus transmission through seed and pollen. In: Maramorosch K, Harris KF, editors. Plant Diseases and Vectors: Ecology and Epidemiology Chapter 8, Academic Press. 1981. ISBN 9780124702400.

    Google Scholar 

  20. Medina AC, Grogan RG. Seed transmission of bean common mosaic viruses. Phytopathol. 1961;51:452–6.

    Google Scholar 

  21. Mhlanga NM, Murphy AM, Wamonje FO, Cunniffe NJ, Caulfield JC, Glover BJ, Carr JP. An innate preference of bumblebees for volatile organic compounds emitted by Phaseolus vulgaris plants infected with three different viruses. Front Ecol Evol. 2021;9:626851.

    Article  Google Scholar 

  22. Morales FJ. Common beans. In: Loebenstein G, Carr JP, editors. Natural resistance mechanisms of plants to viruses. The Netherlands: Springer; 2006. p. 367–82.

    Chapter  Google Scholar 

  23. Murphy AM, Jiang S, Elderfield JAD, Pate AE, Halliwell C, Glover BJ, Cunniffe NJ, Carr JP. Biased pollen transfer by bumblebees favors the paternity of virus-infected plants in cross-pollination. iScience. 2023;26(3):106116.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Ojiewo C, Monyo E, Desmae H, Boukar O, Mukankusi-Mugisha C, Thudi M, et al. Genomics, genetics and breeding of tropical legumes for better livelihoods of smallholder farmers. Plant Breed. 2019;138:487–99.

  25. Ollerton J, Winfree R, Tarrant S. How many flowering plants are pollinated by animals? Oikos. 2011;120:321–6.

    Article  Google Scholar 

  26. Pagán I. Movement between plants: Vertical transmission. In: Palukaitis P, García-Arenal F, editors. Cucumber Mosaic Virus. Washington: APS Press; 2019. p. 185–98.

    Chapter  Google Scholar 

  27. Pagán I. Transmission through seeds: The unknown life of plant viruses. PLoS Pathog. 2022;18:e1010707.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Sastry KS. Seed-borne plant virus diseases. India New Delhi: Springer; 2013.

    Book  Google Scholar 

  29. Schippers B. Transmission of bean common mosaic virus by seed of Phaseolus vulgaris L. cultivar Beka. Acta Bot Neerlandica. 1963;12:433–97.

    Article  Google Scholar 

  30. Simmons HE, Munkvold GP. Seed transmission in the Potyviridae. In: Gullino ML, Munkvold GP, editors. Global perspectives on the health of seeds and plant propagation material. Dordrecht: Springer; 2014. p. 3–15.

    Chapter  Google Scholar 

  31. Thompson JR, Langenhan JL, Fuchs M, Perry KL. Genotyping of Cucumber mosaic virus isolates in western New York State during epidemic years: Characterization of an emergent plant virus population. Virus Res. 2015;210:169–77.

    Article  CAS  PubMed  Google Scholar 

  32. Wainaina JM, Kubatko L, Harvey J, Ateka E, Makori T, Karanja D, Boykin LM, Kehoe MA. Evolutionary insights of Bean common mosaic necrosis virus and Cowpea aphid-borne mosaic virus. PeerJ. 2019;7:e6297.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Wamonje FO, Donnelly R, Tungadi TD, Murphy AM, Pate AE, Woodcock C, et al. Different plant viruses induce changes in feeding behaviour of specialist and generalist aphids on common bean that are likely to enhance virus transmission. Front Plant Sci. 2020;10:1811.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Wang D, Maule AJ. A model for seed transmission of a plant virus: genetic and structural analysis of pea embryo invasion by Pea seed-borne mosaic virus. Plant Cell. 1994;6:777–87.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Worrall EA, Wamonje FO, Mukeshimana G, Harvey JJW, Carr JP, Mitter N. Bean common mosaic virus and bean common mosaic necrosis virus: relationships, biology, and prospects for control. Adv Virus Res. 2015;93:1–46.

    Article  CAS  PubMed  Google Scholar 

Download references


Not applicable.


This work was supported by the Biotechnology and Biological Sciences Research Council (BBSRC-SCPRID Grant BB/J011762/1 and BBSRC-GCRF Grant BB/P023223/1). AMM was supported by grants from the BBSRC (21ROMITIGATIONFUND CAMBRIDGE BB/W510609/1), the Royal Society (ICA\R1\201221) and from The Leverhulme Trust (RPG-2022–134). NM was supported by studentships from the Schlumberger Foundation, Cambridge Trust, and Magdalene College Cambridge. WA had a Cambridge Africa studentship with additional support from a Cambridge Department of Plant Sciences Frank Smart Studentship, and the Cambridge Philosophical Society.

Author information

Authors and Affiliations



NM, AMM, and JPC conceived the work. NM, AMM, AEP collected the data and conducted the data analysis.NM, AMM, and JPC drafted the manuscript. NM, AMM, WA and JPC contributed to manuscript editing. All authors gave final approval for submission.

Corresponding author

Correspondence to Alex M. Murphy.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit The Creative Commons Public Domain Dedication waiver ( applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mhlanga, N.M., Pate, A.E., Arinaitwe, W. et al. Reduction in vertical transmission rate of bean common mosaic virus in bee-pollinated common bean plants. Virol J 21, 147 (2024).

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: