Revisiting a discussion on banana streak viruses and the distribution of genebank material

Anne Vézina Thursday, 14 August 2014

One of the workshops to be held during the IHC2014 ProMusa symposium will discuss the problem banana streak viruses (BSV) pose to the distribution of genebank material. It will pick up on a discussion started by Australian virologist Andrew Geering at the 2007 ISHS-ProMusa symposium. Geering argued that the distribution of germplasm should be guided by the International Plant Protection Convention (IPPC), which states that it is the responsibility of the importing country, not of the exporter (in this case the ITC[1]), to impose phytosanitary measures. In 2008, he reprised his arguments on the old ProMusa website. He was joined by Pierre-Yves Teycheney, a virologist at the French Agricultural Research Centre for International Development CIRAD who argued against relaxing the ITC guidelines. Their arguments are reproduced below, but first some background information.

Andrew Geering
Andrew Geering

BSV form a complex of species that cause streak disease in bananas - the main species being Banana streak Obino l’Ewai virus (BSOLV) and Banana streak Goldfinger virus (BSGfV).  The viruses are transmitted by mealybugs and infected planting material, but unlike other banana viruses, and the vast majority of plant viruses for that matter, they are also integrated in the genome of Musa balbisiana, the wild banana species that donated the so-called B genome to many cultivars. Under certain circumstances, such as tissue culture and hybridization, integrated sequences can excise themselves and produce infectious particles. Therapies exist to clean plantlets of the autonomous viral particles, called episomal, but not of the integrated sequences. So when an ITC accession that has the B genome tests positive for the episomal form of BSV, it is not cleaned to make it available for distribution, as would happen for accessions that don’t have the B genome, since the plantlets may produce BSV viral particles when they are tissue cultured. Under the current guidelines, infected accessions that belong to the AAB, ABB or AAAB genome groups, with Plantains (AAB) being the most affected group, are not available for distribution. In 2008, these represented about 20% of the accessions at the ITC.

At the time, Geering argued that the ITC should make an exception for material infected with BSV, as long as approval is granted by the relevant plant protection authority in the importing country, whereas Teycheney  argued that there is not enough information to make an informed decision. Here are their arguments.

The argument for relaxing the ITC guidelines by Andrew Geering

Principles guiding the international movement of plants and plant products

The IPPC is the principal treaty by which countries abide to help prevent the spread of pests (including pathogens) in plants and plant products. As of 2 August 2007, there were 163 contracting governments to the IPPC. The IPPC is governed by the Commission on Phytosanitary Measures, which prepares International Standards for Phytosanitary Measures (ISPM) in order to achieve international harmonization of quarantine policies and to facilitate trade by preventing countries from using unjustifiable measures as trade barriers.

Under the IPPC, an importing country has the right to impose phytosanitary measures for regulated pests only, whether they are quarantine or non-quarantine pests. A quarantine pest is defined as “a pest of potential economic importance to the area endangered thereby and not yet present there, or present but not widely distributed and being officially controlled”. A regulated non-quarantine pest is defined as “a non-quarantine pest whose presence in plants for planting affects the intended use of those plants with an economically unacceptable impact and which is therefore regulated within the territory of the importing contracting party”. The IPPC further stipulates that the phytosanitary measures must also not be any more stringent than those presently in place if the pest is already in the country. It is the duty of the importing country to publish and transmit their phytosanitary requirements, which may require consignments to enter through specified points of entry if the imports need to be inspected, treated or accompanied by a phytosanitary certificate. The importing country can also “make special provision, subject to adequate safeguards, for the importation, for the purpose of scientific research, education, or other specific use, of plants and plant products and other regulated articles, and of plant pests”.

Pest risk analyses

One of the fundamental principles of the IPPC is managed risk, recognising that there is always a risk of spread and introduction of pests when importing plants and plant products and that importing countries should only institute phytosanitary measures consistent with the pest risk involved. The technical tool used to identify appropriate phytosanitary measures is a pest risk analysis (PRA). A PRA may be initiated when “there is an intention to import for selection and/or scientific research a plant species or cultivar not yet introduced that could potentially be a host of pests” (ISPM No. 2 – 2007). It is the responsibility of the importer to prepare the PRA and to communicate any recommendations from this PRA to the exporter.

In preparing a PRA, a number of factors should be considered including the category of the pest, the economic impact of the pest, the potential for establishment and spread of the pest, and the proposed uses of the plants or plant products. “The conclusion of the pest risk management stage will be whether or not appropriate phytosanitary measures adequate to reduce the pest risk to an acceptable level are available, cost-effective and feasible” (ISPM No. 2 – 2007). If the pest risk is considered unacceptable and there are no measures vailable to mitigate the risk, then the import can be prohibited. At the other end of the spectrum, if the pest risk is considered negligible, the import may be permitted with few if any phytosanitary measures. Pest categorisation The first stage of a pest risk analysis is to identify pests that may require phytosanitary measures.

Pest categorisation

The first stage of a pest risk analysis is to identify pests that may require phytosanitary measures. As previously mentioned, an importing country can only impose phytosanitary measures for regulated pests (quarantine or regulated non-quarantine pest) but not for non-regulated pests (i.e. pests that are indigenous or introduced and widespread). It is beyond the scope of this paper to provide advice on which category BSOLV and BSGFV may fall into in the different banana-producing countries but some general comments can be made.

BSOLV and BSGfV, being endogenous badnaviruses linked to the B genome of Musa, can be expected to be found in any country where Musa A×B hybrids are grown, and therefore are unlikely to be categorised as quarantine pests anywhere in the world. In some countries, these viruses may already be abundant and widespread in distribution and therefore classified as non-regulated pests. Both BSOLV and BSGfV have been recorded in Australia, but are restricted in distribution and are under active control, and therefore would be categorized as regulated non-quarantine pests.

Recommendations There are probably many instances where the benefits of distributing BSOLV- or BSGfV-infected accessions from the ITC to partner organizations or growers may far outweigh the risks. Examples include:
(i) Export of accessions to regions where the viruses are already well-established and widespread.
(ii) Export of accessions for experimental purposes where the viruses could be contained by geographic isolation or by growing them in a glasshouse.
(iii) Export of accessions to countries where economic gains from use of the accessions may far outweigh losses caused by the virus (e.g. if the accessions have resistance to black leaf streak disease or Fusarium wilt).
(iv) Export of accessions to countries where the risk of spread and establishment of the viruses is low (e.g. where the rate of mealybug spread is very slow).

It is the responsibility of each respective national plant protection organization to determine whether an importation of BSOLV- and BSGfV-infected plants into a country should be allowed and what phytosanitary measures should be imposed. If permission has been granted, there is no basis under the IPPC for Bioversity International to restrict movement of the plants from the ITC. The only obligation on Bioversity International is to ensure the accuracy of the information and additional declarations contained in phytosanitary certificates and to follow any requested phytosanitary measures (ISPM No. 1 - 2006).

The argument against relaxing the guidelines by Pierre-Yves Teycheney

Several endogenous banana streak virus sequences (eBSVs) are present in the nuclear genome of Musa balbisiana, hereafter referred to as the B genome. So far, no germplasm containing the B genome has been found to be free of eBSVs. The discovery that some eBSVs can be activated to cause infection in AAB and AAAB genotypes following in vitro culture or genetic crosses has lead CIRAD to introduce a moratorium (i) on the use of M. balbisiana for breeding new interspecific hybrids and (ii) on the distribution of plant material harbouring the B genome. This moratorium is based on the precaution principle to avoid spreading infectious BSV species resulting from the activation of eBSVs.

Only two potentially infectious eBSVs have been identified so far in the B-genome. Nevertheless, considering the diversity of BSV species and that of the eBSVs characterized so far, it is expected that more eBSVs, including activable ones, are present in the B genome.

The main risk associated with eBSVs is the introduction in farmers’ fields of infectious viral particles following the wide distribution of B-containing germplasm whose integrated sequences have been activated by in vitro culture or abiotic stresses, such as changes in temperature or water stress. Such outbreaks could be amplified by the natural transmission of viral particles by mealybugs, whose population dynamics remain largely unknown. Therefore, several countries do not allow the importation of plants and plant products infected with BSV species. Under French quarantine regulations, for example, the only exemptions are in vitro banana plantlets derived from Musa acuminata, which may be brought into French overseas departments subject to quarantine and virus indexing for a number of viruses, including banana streak viruses.

Why not recommend the export of B-containing germplasm to regions where BSV species are already well established and widespread?

It is likely that the B genome contains more activable eBSVs than those characterized so far. Exporting B-containing germplasm, even to regions where known BSV species are present, might promote the diffusion of new BSV species and should be prohibited until the sequencing of the M. balbisiana nuclear genome has been completed, leading to the characterization of all eBSVs.

Why not recommend the export of B-containing germplasm for experimental purposes where BSV species could be contained by geographic isolation or by growing them in a glasshouse?

Importation of quarantine pathogens for experimental purposes is possible under tightly regulated conditions established by plant protection and quarantine services of importing countries. B-containing germplasm should be considered as potentially infected and handled accordingly, unless BSV species as a whole are not considered a quarantine pathogen by relevant authorities. Containment by geographical isolation is not an option unless the surveillance of experimental plots can be guaranteed to avoid the dissemination of the plant material.

Why not recommend the export of B-containing germplasm to countries where economic gains would outweigh losses caused by BSV species?

Several disease-resistant AAB and AAAB interspecific hybrids have been successfully bred by FHIA’s breeding programme in Honduras. They have been widely distributed in Africa, Central and South America and the Caribbean even after activation of eBSVs under stress conditions had been experimentally demonstrated for at least one of these hybrids, FHIA-21. It is now established that all AAB or AAAB interspecific hybrids can become infected following stress-induced activation of eBSVs. Although BSV infections have been reported in areas where in vitro plantlets of AAB or AAAB hybrids have been distributed, no statistically supported data are available on the impact the distribution of these hybrids has had on the spread of BSV. It is therefore currently impossible to evaluate this risk and decide on a scientific basis whether the benefit of using AAB or AAAB hybrids outweighs the risk of spreading BSV. This type risk/benefit analysis needs to be undertaken to inform decisions on the matter.

Why not recommend the export of B-containing germplasm to countries where the risk of spread and establishment of BSV species is low?

Data on the epidemiology of BSV is very scarce and inexistent with regards to the population dynamics of its insect vectors. Therefore, it is currently impossible to decide whether and where “the risk of spread and establishment of BSV species is low” and to design forecasting models to assess this risk. This shortage of information currently prevents the identification of low-risk countries and areas.


There is a growing need to provide developing countries with higher-yielding as well as disease- and stress-resistant Musa genotypes. Unfortunately, the presence of eBSVs in the B genome is a major constraint to the mass multiplication and distribution of germplasm containing the B genome. The CIRAD moratorium on this type of germplasm was decided in order to prevent the spread of BSV. It was initially planned to revisit it when sufficient scientific data on the activation of eBSVs have been gathered and fighting strategies have been developed and implemented. Despite major scientific breakthroughs in the past five years, the genetic and molecular mechanisms underpinning the activation of eBSVs still need to be unraveled. Moreover, little efforts have been made to assess the risks of spreading BSV through the distribution of B-containing germplasm. There are currently not enough data to justify relaxing the ITC guidelines regarding the distribution of BSV-infected germplasm. In order to resolve this critical issue without taking inconsiderate risks, there is an urgent need to assess the risk of spreading BSV species through such a distribution. This will lead to guidelines for the safe movement and distribution of B-containing germplasm, and might possibly also lead to the restoration of the use of M. balbisiana in breeding programmes.

2014 workshop on BSV and their impact on the distribution of germplasm

Both virologists will be participating in the workshop that will be held during the IHC2014 ProMusa symposium in Brisbane, Australia. Geering will be talking about the risks associated with the distribution of germplasm affected by BSV activation issues and Teycheney about possible alternatives to using this germplasm. They will be joined by Edson Amorin, a breeder at Embrapa, who will be presenting current needs and Bart Panis, a Bioversity International scientist based at KU Leuven, where the ITC is hosted, who will talk about the responsibilities of importers and exporters. With the other participants they hope to come up with possible solutions to these issues.

1. Each accession that is introduced to the ITC is inspected for virus symptoms and undergoes extensive testing for Banana bunchy top virus (BBTV), Cucumber mosaic virus (CMV), Banana bract mosaic virus (BBrMV), Banana mild mosaic virus (BanMMV) and banana streak viruses (BSV). It is not available for distribution until it has received a clean bill of health.