# Mechanisms and recent advances in biological control mediated through the potato rhizosphere

Stéphanie Diallo, Alexandre Crépin, Corinne Barbey, Nicole Orange,

Jean-François Burini, Xavier Latour

► To cite this version:

Stéphanie Diallo, Alexandre Crépin, Corinne Barbey, Nicole Orange, Jean-François Burini, et al.  
Mechanisms and recent advances in biological control mediated through the potato rhizosphere. FEMS  
Microbiology Ecology, 2011, 75 (3), pp.351-364. 10.1111/j.1574-6941.2010.01023.x.  
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MINIREVIEW

# Mechanisms and recent advances in biological control mediated through the potato rhizosphere

Stéphanie Diallo¹,², Alexandre Crépin¹,², Corinne Barbey¹, Nicole Orange¹, Jean-François Burini¹ & Xavier Latour¹

¹Laboratoire de Microbiologie du Froid Signaux et Micro-Environnement, EA 4312 Université de Rouen, Evreux, France; and ²Comité Nord, Station de Recherche et de Création Variétale, Bretteville du Grand Caux, France

**Correspondence:** Xavier Latour, Laboratoire de Microbiologie du Froid Signaux et Micro-Environnement, EA 4312 Université de Rouen, IUT Evreux 55 rue Saint-Germain, F-27000 Evreux, France. Tel.: +33 232 291 549; fax: +33 232 291 550; e-mail: xavier.latour@univ-rouen.fr

Received 11 July 2010; revised 6 November 2010; accepted 16 November 2010.
Final version published online 11 January 2011.

DOI:10.1111/j.1574-6941.2010.01023.x

Editor: Ian Head

**Keywords**

biological control; *Solanum tuberosum*; potato; rhizosphere; mechanisms and strategies.

## Introduction

The rhizosphere concept was first introduced in 1904 by Dr Lorenz Hiltner as the soil compartment influenced by the root (Smalla *et al.*, 2006; Hartmann, 2008). The implication of root exudates as a nutrient source for bacteria was then initiated, explaining why bacterial density was more important than in bulk soil. This phenomenon was called the ‘rhizosphere effect’ by Rovira (1956), another major contributor in rhizosphere research (Burns, 2010).

Plant rhizobiota can develop at different levels of proximity to the plant roots (for a recent review, see Buée *et al.*, 2009). Soil microorganisms found in the soil loosely adhering to the roots are named rhizospheric microorganisms. Directly outside root tissue, the rhizoplane, the interface between root and soil, always shows a profusion of microorganisms (Föster, 1986). In contrast, the extent of internal colonization observed is reduced in the endosphere (leaf and stem tissues) or the endorhiza (root tissue), a name semantically better than the endorhizosphere (Kloepper, 1992). The observed high microbial diversity is dependent on plant species, growth stage and culture substrates (Marschner *et al.*, 2004). Another level of

diversity has been noticed in the types of plant–microorganism interactions. Plant-associated microorganisms can have a beneficial, deleterious or neutral effect on the plant (Raaijmakers *et al.*, 2009). Hiltner highlighted the important role of rhizobacteria on roots and consequently on plant health. He proposed that nonpathogenic microorganisms colonized healthy roots. As the rhizosphere concept was refined, new ideas were presented on the concept of microbiological control. Today, biocontrol methods represent a significant complement to other control methods, which are based on prophylactic measures, chemical treatments or genetic approaches. This is even more important considering that many diseases affect underground organs, which are usually out of reach of germicidal treatments. However, the reliability of biocontrol practices generated scepticism because published accounts of control showed a lack of consistency. This is principally due to the biotic and abiotic diversity of soils, which conditions the colonization and development of sufficient numbers of the protecting agent and sustainable activity to enable disease control (Compant *et al.*, 2005; Latour *et al.*, 2009).

All these concepts perfectly apply to the potato *Solanum tuberosum* L. This plant hosts an important microbial

## Abstract

Potato cultivation has a strategic role as a food source for the human population. Its promising future development relies on improving the control of the numerous microbial diseases that affect its growth. Numerous and recent studies on the potato rhizosphere, mycorrhizosphere and endorhiza reveal the presence of a diverse and dense microbial community. This microbial community constitutes a rich source for plant growth-promoting rhizobacteria and biocontrol agents. So far, the beneficial effects achieved are related to microbial siderophores, antibiotics, biosynthesis of surfactants and phytohormones, nutrient and spatial competition, mycoparasitism, induced systemic resistance, phage therapy, quorum quenching and construction of transgenic lines. Considering the crucial role for food and the diversity of mechanisms involved in growth promotion and microbial protection, potato constitutes a historical and accurate model in developing new biocontrol strategies.
community on its roots as well as on its stolons and tubers (geocaulosphere). Recent reviews have summarized techniques and strategies used to extract and to select potential biocontrol agents from diverse plants including the potato (Latour *et al.*, 2009; Neumann *et al.*, 2009). In 2008, the Food and Agriculture Organization (FAO) proposed highlighting the potato for (1) its key role in the world global food system as it is the world's fourth most produced food commodity, (2) its ability to grow worldwide, (3) its convenience for farming systems in developing countries – potato crops harbour a high ratio of yield productivity to soil occupation (85% of the plant is comestible compared with only 50% in cereals), and (4) its nutritive qualities, with a higher amount of vitamins than grass plants (FAO, 2008). Cultivation of potato is promoted by the United Nations for its high development potentialities in Asia and Africa and as a possibly decisive weapon in the fight against starvation. Unfortunately, potato is susceptible to numerous pathogens for which control methods are lacking. In addition to the different pests (i.e. insects, nematodes), microbial pathogens are annually responsible for the loss of 25% of worldwide production (Priou & Jouan, 1996; FAO, 2008). Therefore, knowledge of the potato microbial community is of special interest in order to develop control methods, which can limit recurrent losses and promote its widespread implantation. This paper reviews the potato rhizobiota and the microbial mechanisms involved in creating beneficial effects on potato growth.

## Potato rhizosphere, endorhiza and microbial community

The structural analysis of potato rhizosphere microbial communities has been detailed by describing spatial and temporal colonization of underground organs by rhizobacteria (Loper *et al.*, 1985; Bahme & Schroth, 1987; Bahme *et al.*, 1988; Frommel *et al.*, 1993). During plant growth, bacteria multiply exponentially and quickly colonize the underground part of the shoots, stolons, roots, progeny tubers as well as rhizospheric soil. Denser populations are found near the seed piece, which constitutes the main nutrient reservoir and often carries the microbial inoculum or contaminations promoting the plant and daughter tubers' infestation (De Boer *et al.*, 1978; Hélias *et al.*, 2000). Bacterial densities in the potato rhizosphere vary from $10^7$ to $10^8$ CFU g$^{-1}$ fresh weight (Lottmann *et al.*, 1999; Berg *et al.*, 2002, 2005; Krechel *et al.*, 2002). Endorhizal populations, mainly located in intercellular spaces, are 100–1000 times less dense than rhizospheric ones (Krechel *et al.*, 2002; Berg *et al.*, 2005; Rasche *et al.*, 2006b). When the potato plants grow in hydroponic systems, as used for cultivar multiplication, bacterial colonization of the roots is greater than when they grow in soil (Latour *et al.*, 2008). We have

measured bacterial density levels up to $10^8$ CFU g$^{-1}$ fresh weight in the rhizoplane of young potato plants, and $10^{10}$ CFU g$^{-1}$ fresh weight at the surface of *S. tuberosum* roots and tubers during tuber production stage (unpublished data).

The fungal genera *Alternaria*, *Clonostachys*, *Fusarium*, *Penicillium* and *Rhizoctonia* are cited to be commonly encountered in both the rhizosphere and the geocaulosphere of potato (Pieta & Patkowska, 2003; Fiers *et al.*, 2010), and > 60 bacterial genera have been identified by culture-dependent methods in different potato cultivars (Table 1). Three genera, known to mainly contain rhizobacteria species, were consistently identified in each microenvironment: *Agrobacterium*, *Bacillus* and *Pseudomonas*. To a lesser extent, genera such as *Arthrobacter*, *Comamonas*, *Curtobacterium*, *Enterobacter*, *Paenibacillus*, *Pantoea*, *Serratia*, *Sphingobacterium*, *Stenotrophomonas*, *Variovorax* and *Xanthomonas* are frequently found in the vicinity of the potato. Cultivation-independent population analysis was also assessed to evaluate bacterial diversity associated with this plant. 16S rRNA gene-based techniques such as terminal-restriction fragment length polymorphism (T-RFLP), denaturing gradient gel electrophoresis as well as 16S rRNA gene cloning and sequencing analysis confirmed the presence of genera *Agrobacterium*, *Arthrobacter*, *Bacillus*, *Curtobacterium*, *Micrococcus*, *Pseudomonas*, *Sphingobacterium* and *Streptomyces* in the rhizosphere and endorhiza of the potato (Garbeva *et al.*, 2001; Smalla *et al.*, 2001; Sessitsch *et al.*, 2002; Reiter *et al.*, 2003; Berg *et al.*, 2005).

The species in the genus *Pseudomonas* and particularly the group of fluorescent pseudomonads are of high interest as they include well-known species, which play a role in plant protection (Weller, 2007). Among them, *Pseudomonas fluorescens* and *Pseudomonas putida* species extensively colonize potato rhizosphere in soil ($10^6–10^8$ CFU g$^{-1}$ root) and hydroponic systems where they represent 10% of the total cultivable rhizobacterial population (Xu & Gross, 1986; Van Peer & Schippers, 1989; Bergsma-Valmi *et al.*, 2005; Cirou *et al.*, 2007). Interestingly, strains belonging to these two species have been regularly chosen as models to describe the impact of growth stage or environmental factors on the establishment and persistence of a bacterial inoculum on underground organs (Loper *et al.*, 1985; Bahme & Schroth, 1987; Bahme *et al.*, 1988; Andreote *et al.*, 2009). *Pseudomonas* spp. are also highly represented in endorhiza, where they can reach 36–48% of the isolates (Sturz, 1995; Sturz *et al.*, 1998; Garbeva *et al.*, 2001). They are frequently mentioned in studies focusing on isolating biocontrol agents from the roots (Sturz & Matheson, 1996; Kastelein *et al.*, 1999; Berg *et al.*, 2002; Reiter *et al.*, 2002). Globally, potato rhizosphere hosts an important bacterial diversity since 50 other bacterial genera were less frequently found, suggesting that numerous other genera associated with potato plants are yet to be discovered (Table 1). Bacterial species responsible for potato diseases (*Dickeya* spp., *Pectobacterium* spp.,
<table><caption>**Table 1.** Diversity of culturable bacteria reported in the rhizosphere and underground organs of potato</caption><thead><tr><th rowspan="2">Genus</th><th colspan="3">Microenvironment</th></tr><tr><th>Rhizosphere and rhizoplane</th><th>Endorhiza</th><th>Geocaulosphere and tuber</th></tr></thead><tbody><tr><td colspan="4">Major components of the bacterial population</td></tr><tr><td>Agrobacterium</td><td>+ (1,4,7,8)*</td><td>+ (7,8)</td><td>+ (1,3,4)</td></tr><tr><td>Arthrobacter</td><td>+ (6,7,8)</td><td>+ (6,8)</td><td>+ (3)</td></tr><tr><td>Bacillus</td><td>+ (1,6,7,8)</td><td>+ (6,7,8)</td><td>+ (1,2,3,4,9)</td></tr><tr><td>Comamonas</td><td>+ (1,5,6)</td><td>+ (6)</td><td>+ (4)</td></tr><tr><td>Curtobacterium</td><td>+ (1,6,8)</td><td>+ (8)</td><td>+ (2,3)</td></tr><tr><td>Enterobacter</td><td>+ (8)</td><td>+ (6,7,8)</td><td>+ (4)</td></tr><tr><td>Flavobacterium</td><td>+ (6,8)</td><td>+ (6,8)</td><td>+ (9)</td></tr><tr><td>Paenibacillus</td><td>+ (4,6,8)</td><td>+ (8)</td><td>+ (4)</td></tr><tr><td>Pantoea</td><td>+ (4,8)</td><td>+ (6,8)</td><td>+ (3)</td></tr><tr><td>Pseudomonas</td><td>+ (1,4,5,6,7,8)</td><td>+ (6,7,8)</td><td>+ (1,2,3,4,9)</td></tr><tr><td>Rhodococcus</td><td>+ (6,8)</td><td>+ (8)</td><td></td></tr><tr><td>Serratia</td><td>+ (1,4,8)</td><td>+ (7,8)</td><td>+ (2)</td></tr><tr><td>Sphingobacterium</td><td>+ (6,7,8)</td><td>+ (6,8)</td><td></td></tr><tr><td>Stenotrophomonas</td><td>+ (4,5,8)</td><td>+ (6,8)</td><td>+ (4)</td></tr><tr><td>Streptomyces</td><td>+ (6,7)</td><td>+ (6)</td><td>+ (9)</td></tr><tr><td>Variovorax</td><td>+ (6,7,8)</td><td>+ (7,8)</td><td></td></tr><tr><td>Xanthomonas</td><td>+ (1,6,8)</td><td></td><td>+ (1,2,3)</td></tr><tr><td colspan="4">Minor components of the bacterial population</td></tr><tr><td>Acinetobacter</td><td>+ (1,8)</td><td></td><td>+ (1)</td></tr><tr><td>Actinobacillus</td><td>+ (1,4)</td><td></td><td>+ (1)</td></tr><tr><td>Actinomyces</td><td>+ (1)</td><td></td><td>+ (1)</td></tr><tr><td>Alcaligenes</td><td>+ (8)</td><td>+ (8)</td><td></td></tr><tr><td>Aureobacterium</td><td>+ (6)</td><td>+ (6)</td><td></td></tr><tr><td>Brevibacillus</td><td>+ (8)</td><td>+ (8)</td><td></td></tr><tr><td>Brevibacterium</td><td>+ (8)</td><td>+ (6,8)</td><td></td></tr><tr><td>Brevundimonas</td><td></td><td>+ (8)</td><td></td></tr><tr><td>Brochothrix</td><td></td><td>+ (8)</td><td></td></tr><tr><td>Burkholderia</td><td>+ (4,8)</td><td>+ (8)</td><td>+ (4)</td></tr><tr><td>Cellulomonas</td><td>+ (8)</td><td>+ (8)</td><td>+ (3)</td></tr><tr><td>Chryseobacterium</td><td>+ (6,8)</td><td>+ (6,8)</td><td></td></tr><tr><td>Citrobacter</td><td>+ (8)</td><td>+ (8)</td><td></td></tr><tr><td>Clavibacter</td><td>+ (6,8)</td><td>+ (6,8)</td><td></td></tr><tr><td>Corynebacterium</td><td>+ (1,8)</td><td>+ (8)</td><td></td></tr><tr><td>Cytophaga</td><td>+ (5,6)</td><td>+ (6)</td><td></td></tr><tr><td>Dactylosporangium</td><td>+ (6)</td><td></td><td></td></tr><tr><td>Dickeya</td><td></td><td></td><td>+ (9)</td></tr><tr><td>Ensifer</td><td></td><td></td><td>+ (9)</td></tr><tr><td>Erwinia</td><td>+ (1,6)</td><td>+ (7)</td><td></td></tr><tr><td>Francisella</td><td>+ (4)</td><td></td><td></td></tr><tr><td>Gluconobacter</td><td>+ (8)</td><td></td><td></td></tr><tr><td>Janthinobacterium</td><td>+ (5)</td><td></td><td>+ (2)</td></tr><tr><td>Kingella</td><td></td><td></td><td>+ (2)</td></tr><tr><td>Klebsiella</td><td></td><td>+ (8)</td><td></td></tr><tr><td>Kluyvera</td><td>+ (5)</td><td></td><td>+ (2)</td></tr><tr><td>Kocuria</td><td>+ (6,8)</td><td>+ (6,8)</td><td></td></tr><tr><td>Kurthia</td><td>+ (8)</td><td></td><td></td></tr><tr><td>Leclercia</td><td></td><td>+ (8)</td><td></td></tr><tr><td>Leuconostoc</td><td>+ (1)</td><td></td><td></td></tr><tr><td>Lysobacter</td><td>+ (7)</td><td></td><td>+ (9)</td></tr><tr><td>Microbacterium</td><td>+ (8)</td><td>+ (8)</td><td></td></tr><tr><td>Micrococcus</td><td>+ (6,7)</td><td>+ (6)</td><td></td></tr><tr><td>Micromonospora</td><td>+ (6)</td><td></td><td></td></tr><tr><td>Nesterenkonia</td><td>+ (8)</td><td>+ (8)</td><td></td></tr></tbody></table>

<table><caption>**Table 1.** Continued.</caption><thead><tr><th rowspan="2">Genus</th><th colspan="3">Microenvironment</th></tr><tr><th>Rhizosphere and rhizoplane</th><th>Endorhiza</th><th>Geocaulosphere and tuber</th></tr></thead><tbody><tr><td>Ochrobactrum</td><td></td><td>+ (8)</td><td></td></tr><tr><td>Pedobacter</td><td>+ (8)</td><td></td><td></td></tr><tr><td>Photobacterium</td><td></td><td>+ (8)</td><td></td></tr><tr><td>Phyllobacterium</td><td>+ (8)</td><td></td><td></td></tr><tr><td>Proteus</td><td>+ (4)</td><td></td><td></td></tr><tr><td>Psychrobacter</td><td></td><td></td><td>+ (3)</td></tr><tr><td>Rahnella</td><td>+ (8)</td><td></td><td></td></tr><tr><td>Ralstonia</td><td></td><td>+ (8)</td><td></td></tr><tr><td>Salmonella</td><td></td><td>+ (8)</td><td></td></tr><tr><td>Sphingomonas</td><td>+ (8)</td><td>+ (8)</td><td>+ (4,8)</td></tr><tr><td>Staphylococcus</td><td>+ (7,8)</td><td>+ (8)</td><td></td></tr><tr><td>Streptoverticillum</td><td>+ (6)</td><td></td><td></td></tr><tr><td>Tsukamurella</td><td>+ (8)</td><td>+ (8)</td><td></td></tr><tr><td>Xanthobacter</td><td>+ (8)</td><td></td><td></td></tr></tbody></table>

*The symbol '+' indicates a successful isolation of at least one member of the genus from the corresponding microenvironment. It is followed by references: numbers correspond to the works from (1) Sturz (1995), (2) Sturz & Matheson (1996), (3) Sturz et al. (1998), (4) Lottmann et al. (1999), (5) Berg et al. (2002), (6) Krechel et al. (2002), (7) Berg et al. (2005), (8) Sturz et al. (2005), and (9) Weinert et al. (2010).

Ralstonia solanacearum and pathogenic forms of Streptomyces scabiei have rarely been isolated from healthy potato plants except for Clavibacter michiganensis, which is known to contain nonpathogenic forms (Krechel et al., 2002). In these studies, bacterial pathogens are rarely detected probably because their concentrations on healthy plants are below detection levels.

The diversity and abundance of microbial communities colonizing potato plants have been considered by comparing diversity assessment methods, searching for new protectors or rating the impact of protection methods on indigenous bacterial flora (Garbeva et al., 2001; Smalla et al., 2001; Krechel et al., 2002; Sessitsch et al., 2004; Berg et al., 2005; Bergsma-Valmi et al., 2005; Sturz et al., 2005). These studies revealed that the roots harbour a larger and more diverse reservoir of microorganisms than the aerial parts of the potato. A higher density and a higher number of microbial species are always measured in the rhizosphere compared with the phyllosphere or in the endorhiza compared with the endosphere (Krechel et al., 2002; Berg et al., 2005).

The source of the internal colonization has been a recurrent issue. Kloepper (1992) hypothesized that root cortical colonization originated from rhizospheric microbial community, assuming that rhizosphere and endorhiza bacteria formed a continuum. Ten years later, this continuum theory was partially confirmed, showing strong similarities between the two compartments, although this does not exclude phyllosphere as a source of endophytic bacteria
(Krechel *et al.*, 2002). Additionally, similarities were found between rhizosphere- and endorhiza-protecting agents, suggesting a selective colonization of beneficial bacteria through the root tissue during plant development (Sturz *et al.*, 2005). Noncultivable bacterial communities were also studied (Berg *et al.*, 2005; Becker *et al.*, 2008). For example, Berg *et al.* (2005) compared T-RFLP 16S rRNA gene patterns from rhizosphere, endorhiza, endosphere and phyllosphere. This study revealed 19 different bacterial T-RFs. The comparison showed that half of the T-RFs were common to all the plant microenvironments. The highest number of T-RFs was found in the rhizosphere suggesting more diversity. However, the weak similarities displayed between rhizosphere and endorhiza T-RFLP patterns did not support the idea of the rhizosphere as a major source for endophytic bacteria.

## The potato mycorrhizosphere partly unveiled

Most studies on potato microbial communities have focused on bacterial communities as noted above. Nevertheless, mycorrhizal fungi are among the most frequent rhizosphere microorganisms, and they can also influence the growth and health of plants (Buée *et al.*, 2009). Their interactions with their rhizosphere neighbours have long been underestimated.

Arbuscular mycorrhizal fungi form symbiotic associations with the roots of a great majority of terrestrial plant species. During the formation of symbiosis, the fungus penetrates the root cortical cell walls, and then forms arbuscules or coils providing an increased surface area for metabolic exchanges between the partners. The mycorrhizosphere is the zone influenced by both the root and the mycorrhizal fungus (for a review, see Johansson *et al.*, 2004). The strategic role of mycorrhizal fungi is related to their spreading ability, both within the plant and the surrounding soil. Sen (2005) considers that these fungi, in symbiosis with roots, act as bridges connecting the rhizosphere to bulk soil. Arbuscular mycorrhizae are also suspected to influence the diversity of rhizobacteria growing on fungal exudates rather than directly on root exudates (Buée *et al.*, 2009). Finally, mycorrhizal colonization could stimulate plant defences promoting border cell production from the root cap into the rhizosphere (Niemira *et al.*, 1996b). Indeed, border cells are detached living cells, which are suspected to interact with both beneficial and pathogenic organisms and to alert the parent plant to the presence of a potential soilborne pathogen. Arbuscular mycorrhizae and border cells are both found in the potato rhizosphere (Niemira *et al.*, 1996b).

Recently, the potato mycorrhizosphere was investigated in two different soils (Cesaro *et al.*, 2008). The potato rhizoplane was found to be poorly colonized by arbuscular mycorrhiza, perhaps because the phosphorus concentration was high in the two soils. However, although small fractions

of the root systems were colonized, the arbuscule levels in the colonized areas were high and could be interpreted as the presence of active fungi. Arbuscular mycorrhiza communities differed between potato roots and bulk soil. The roots were preferentially colonized by mycorrhizal fungi belonging to the *Glomus intraradices* species and to a lesser degree to the *Glomus mosseae* species whereas in bulk soil a markedly greater diversity was shown (Cesaro *et al.*, 2008). This mycorrhizosphere compartment is even extended to saprophytic fungi that have close associations with roots (Buée *et al.*, 2009). Among them, *Trichoderma* and *Penicillium* communities have been described and detected at concentration levels ranging from $10^4$ to $10^5$ CFU g$^{-1}$ of potato cultivated soil (Larkin & Honeycutt, 2006; Meincke *et al.*, 2010).

The potential biocontrol effect of mycorrhizal fungi on *Solanaceae* diseases needs to be further developed. Potato minitubers grown in a peat-based medium containing *G. intraradices* are better protected against the tuber dry rot caused by *Fusarium sambucinum* than minitubers grown in the same medium without the mycorrhiza (Niemira *et al.*, 1996a). Moreover, two studies on a related *Solanaceae* (tomato) demonstrated mycorrhiza's ability to limit the density of the soft-rot pathogen *Pectobacterium carotovorum* in the rhizosphere and to induce a systemic response to *Phytophthora* infection (Garcia-Garrido & Ocampo, 1988; Pozo *et al.*, 2002). The ability of arbuscular mycorrhiza in the control of soilborne diseases would be strongly related to their capacity to specifically stimulate the establishment of rhizobacteria unfavourable to pathogen development within the mycorrhizosphere before root infection (Lioussanne, 2010). Bharadwaj *et al.* (2008) have isolated from spores of *G. intraradices* and *G. Mosseae*, bacteria selected upon their ability to inhibit the growth of plant pathogens. Among them, some *Arthrobacter*, *Pseudomonas* and *Stenotrophomonas* strains are able to stimulate potato growth and are antagonistic to potato pathogens *P. carotovorum*, *Verticillium dahliae*, *Phytophthora infestans* and *Rhizoctonia solani*.

Biocontrol applications on potato plants require a better knowledge of its beneficial fungal partners. This kind of microbial community has been poorly studied, particularly because *in vitro* cultivation of mycorrhizae remains difficult (Louche-Tessandier *et al.*, 1999). Recently, these technological constraints have been lifted by researchers at the Center of Study on Arbuscular Mycorrhizal Fungi Monoaxenics (CESAMM), who have developed autotrophic culture systems. Voets *et al.* (2005) specifically described this system for potato-associated arbuscular mycorrhizal fungi. It consists in an *in vitro* agar growth medium containing potato roots and fungi, while photosynthetic shoots grow under open-air condition. This microcosm allows the study of spore production, root colonization, spore germination capacity and fungal life cycle (Gallou *et al.*, 2009). It might also open new doors to study the implication of mycorrhizal fungi on disease suppression.
## Potato growth-promoting rhizobacteria

Some rhizospheric bacteria have a beneficial agronomic effect on plant growth. These bacteria are commonly referred to as plant growth-promoting rhizobacteria (PGPR) (Compant *et al.*, 2005). PGPR can directly stimulate plant growth by synthesizing hormones (phytostimulators) or by supplying the plants with nutrients (biofertilizing). Growth stimulation can also be indirectly achieved by suppressing or preventing the deleterious effects of pathogens. Thus, potato seeds bacterized with fluorescent pseudomonad strains were shown to improve the yields by about 10% compared with noninoculated seeds. This result was obtained through trials conducted on different field sites over several years (Burr *et al.*, 1978; Kloepper *et al.*, 1980). Geels & Schippers (1983) also obtained a reduced loss of yield by combining a short rotation process and tuber seed bacterization with some strains of fluorescent pseudomonads. The beneficial effect resulted from the inhibition of deleterious microbial communities, among which hydrogen cyanide-producing *Pseudomonas* spp. were replaced by protective agents. The antagonistic effect exerted by these potato rhizosphere strains is usually imputed to result from (1) siderophore production by the biocontrol strain *P. fluorescens* WCS358, (2) the root competence of *P. fluorescens* WCS365 and (3) the capacity of *P. fluorescens* WCS374 to induce plant systemic resistance demonstrated by split root experiments (De Weger *et al.*, 1986, 1995; Schippers *et al.*, 1987; Van Loon *et al.*, 1998). Overall, beneficial effects have been noticed on root, stolon and tuber growth rate and on the size of the commercialized tubers (Kloepper & Schroth, 1981; Van Peer & Schippers, 1989; Frommel *et al.*, 1993).

PGPR showing biological control activities are referred to as biocontrol agents or biopesticides. Because of their proximity to telluric pathogens and the host to be protected, rhizosphere and endorhiza are privileged microenvironments in biocontrol agent research. Compared with phyllosphere, endosphere and geocaulosphere, the potato rhizosphere and endorhiza are the most important reservoirs in the search for antagonists against the telluric fungus *V. dahliae* even though the geocaulosphere contains the organs targeted by this fungus (Lottmann *et al.*, 1999; Berg *et al.*, 2005). Sturz (1995) and Sturz *et al.* (2005) have estimated that endophytic growth-promoting bacteria ranged from 10% to 20% of the total bacterial population, and a similar proportion of the total bacterial population were shown to be growth inhibiting. These ratios were also found within each bacterial genus, which confirms that stimulating or inhibiting properties are strain dependant. The effectiveness of these endophytic PGPR has been evaluated in a multidisciplinary study combining *in planta, in vitro* and molecular analysis (Sessitsch *et al.*, 2004). It revealed that positive effects on plant growth and health were correlated with either siderophore production, production of the

phytohormone indole-3 acetic acid or both. Only a few isolates demonstrated antifungal activity *in vitro* against the ascomycetes *V. dahliae* and *Sclerotinia sclerotium* or the basidiomycete *R. solani*, and none of the isolates were antagonistic to the oomycete *Phytophthora cactorum*. On the other hand, 43% and 29% of the isolates had antibacterial activity against *Streptomyces* sp. and *Xanthomonas* sp., respectively. Comparing rhizosphere and endorhiza as sources of protecting strains has proven difficult. If the antagonists of *V. dahliae* are more numerous in the rhizosphere, a similar percentage of isolates was shown to be antagonistic to *R. solani* (Krechel *et al.*, 2002; Berg *et al.*, 2005; Sturz *et al.*, 2005). On the other hand, antagonists against *Phytophthora erythroseptica* and *Fusarium oxysporum* are more abundant in the endorhiza than in the rhizosphere (Sturz *et al.*, 2005). The preferential or random localization of biocontrol strains, depending on the pathogen, remains to be explained. Nevertheless, the higher level of intimacy level between the endorhiza and the plant could facilitate induction of systemic resistance (ISR). ISR and systemic acquired resistance (SAR) are resistance mechanisms used by many plants to respond to local attack by pathogens both in the plant organ originally attacked and in distant, yet unaffected, parts. Contrary to SAR, ISR is induced by the determinants of nonpathogenic bacteria or fungi (e.g. lipopolysaccharides, siderophores, salicylic acid) that trigger changes in cell wall composition and in the production of pathogenesis-related proteins and phytoalexins by the plant (Van Loon *et al.*, 1998; Bakker *et al.*, 2007). For example, treatment of potato leaves by the polyunsaturated fatty arachidonic acid induces local synthesis of salicylic acid and confers systemic resistance to *P. infestans* and *Alternaria solani* (Coquoz *et al.*, 1995). This powerful mechanism controls aerial diseases as well as telluric ones. It is involved in the potato plant defence against late blight, *Rhizoctonia* black scurf and bacterial wilt (Table 2).

## Biological control of potato pathogens

Today, biocontrol formulations are an expanding market as they represent 1% of the overall pesticides sales. Montesinos (2003) and Fravel (2005) have drawn up lists of biocontrol products and strains registered by the United States Environmental Protection Agency (USEPA) and the European Protection Agency (EPA). These strains mainly belong to *Bacillus* and *Pseudomonas* bacterial genera and *Aspergillus* and *Trichoderma* fungal genera. Because most formulations are targeted at ornamental and food crop plants grown in greenhouses or nurseries, only a few of them are recommended for potato protection. More generally, the cost and complexity of studies for the registration of microbial pesticides is a barrier to the transfer of laboratory knowledge to the commercialization of these substances.
<table><caption>**Table 2.** Diversity of microbial antagonists and mechanisms providing biological control of potato pathogens</caption><thead><tr><th>Diseases (Pathogen)</th><th>Biocontrol agents</th><th>Mechanisms involved (hypothesized or demonstrated)</th><th>Biocontrol assays</th><th>References</th></tr></thead><tbody><tr><td>Bacterial diseases</td><td></td><td></td><td></td><td></td></tr><tr><td>Bacterial wilt/brown rot (Ralstonia solanacearum)</td><td>Bacillus polymyxa<br>Bacillus subtilis and Paenibacillus macerans<br>Fluorescent pseudomonads</td><td>Preemptive colonization<br>Induced systemic resistance<br>Induced systemic resistance, preemptive colonization</td><td>Soil microcosm<br>In vitro screening and soil microcosm<br>Tuber assay, soil microcosm and field trial</td><td>Aspiras & de la Cruz (1986)<br>Naser et al. (2008)</td></tr><tr><td>Blackleg and soft-rot (Dickeya spp./ Pectobacterium spp.)</td><td>Nonpathogenic Ralstonia solanacearum<br>Bacillus subtilis</td><td>Induced systemic resistance<br>Antibiosis</td><td>Tuber assay and field trial<br>In vitro screening and tuber assay<br>In vitro screening, tuber assay, soil microcosm and field trial</td><td>Kempe & Sequiera (1983), Aspiras & de la Cruz (1986), Naser et al. (2008)<br>Kempe & Sequiera (1983)<br>Sharga & Lyon (1998)</td></tr><tr><td>Ring rot (Clavibacter michiganensis ssp. sepedonicus.)</td><td>Pectobacterium spp.</td><td>Competition</td><td>Tuber assay</td><td>Kloepper (1983), Xu & Gross (1986), Rhodes & Logan (1987), Axelrood et al. (1988), Cronin et al. (1997), Kastelein et al. (1999)</td></tr><tr><td>Scab (Streptomyces spp., mainly Streptomyces scabiei)</td><td>Streptomyces bacteriophage<br>Fluorescent pseudomonads<br>Nonpathogenic Streptomyces</td><td>Antibiosis, preemptive colonization<br>Cell lysis<br>Not determined<br>Antibiosis, competition</td><td>In vitro screening and soil microcosm<br>Tuber assay<br>Field trial<br>In vitro screening, tuber assay, soil microcosm and field trial</td><td>Costa & Loper (1994)<br>De la Cruz et al. (1992)<br>McKenna et al. (2001)<br>Nanri et al. (1992)<br>Liu et al. (1996), Neeno-Eckwall et al. (2001)<br>Hiltunen et al. (2009)</td></tr><tr><td>Fungal diseases</td><td></td><td></td><td></td><td></td></tr><tr><td>Fusarium dry rot (Fusarium spp., mainly Fusarium roseum var. sambucinum and some Fusarium oxysporum)</td><td>Bacillus spp.</td><td>Antagonism</td><td>In vitro screening and tuber assay</td><td>Sadfi et al. (2002), Kotan et al. (2009)</td></tr><tr><td>Late blight/Mildew (Phytophthora infestans)</td><td>Enterobacter cloacae<br>Fluorescent pseudomonads</td><td>Antagonism<br>Antagonism</td><td>Tuber assay and storage<br>Tuber assay and storage</td><td>Schisler et al. (2000)<br>Schisler et al. (2000)</td></tr><tr><td>Rhizoctonia black scurf and stem canker (Rhizoctonia solani)</td><td>Binucleate Rhizoctonia<br>Rhizoctonia zeae<br>Verticillium bigutattum</td><td>Induced systemic resistance<br>Antagonism<br>Antibiosis, competition<br>Induced systemic resistance</td><td>Soil microcosm<br>Greenhouse trial (leaf assay)<br>Soil microcosm<br>Soil microcosm</td><td>Doke et al. (2008)<br>Hultberg et al. (2010)<br>Andreote et al. (2009)<br>Strömberg & Brishammar (1991)<br>Soil microcosm and field trial<br>Soil microcosm<br>Soil microcosm and field trial</td></tr><tr><td>Verticillium wilt (Verticillium dahliae)</td><td>Trichoderma harzianum<br>Clonostachys rosea<br>Pseudomonas fluorescens<br>Talaromyces flavum</td><td>Competition, induced systemic resistance<br>Mycoparasitism<br>Antagonism<br>Mycoparasitism</td><td>Tuber assay, sand and plantlet microcosms<br>Soil microcosm<br>Soil microcosm<br>Soil microcosm</td><td>Escande & Echandi (1991)<br>Brewer & Larkin (2005)<br>Van den Boogert & Velvis (1992)<br>Wilson et al. (2008), Gallou et al. (2009)<br>Keinath et al. (1991)<br>Leben et al. (1987)<br>Nagtzaam & Bollen (1997)</td></tr></tbody></table>

Most of the studies aimed at finding agents that protect potato are focused on *Proteobacteria* and *Firmicutes* (Table 2). The first studies on potato plant biocontrol focused on

fighting against different *Pectobacterium* species (formerly *Erwinia carotovora*), which are important bacterial pathogens leading to severe losses during the potato growth and the
tuber conservation steps (Pérombelon, 2002; Toth et al., 2006). Fluorescent pseudomonads, previously selected for their antagonistic activity in Petri dishes, have been used in these experiments (Kloepper & Schroth, 1981; Kloepper, 1983). The ability to colonize and the persistence of *Pseudomonas* strains on treated plants were assessed. Additionally, the influence of soil fine texture and neutral pH promoting the expression of protecting activities was observed. Subsequently, the nature of the antagonistic properties of these strains was investigated: 2,4 diacetylphloroglucinol antibiotic synthesis, iron competition via pyoverdine and pseudobactin production and their related receptors were found to be the means of protection (De Weger et al., 1986, 1995; Xu & Gross, 1986; Rhodes & Logan, 1987; Cronin et al., 1997). However, large-scale application of these candidate biocontrol *Pseudomonas* showed limited protection effect. Gross (1988) demonstrated that selected strains were able to colonize plants, but were ineffective in *Pectobacterium atrosepticum* disease suppression. Quickly, members of *Bacillus* spp. also drew the attention of researchers because of their effective protecting activities. This interest is also due to a certain facility for commercial product development linked to endospore production and consequent resistance of these bacteria to environmental stresses (Jacobsen et al., 2004). Therefore, *Bacillus subtilis* strains were tested for the control of potato diseases caused by *Pectobacterium* spp. and revealed reduced maceration symptoms in planta (Sharga & Lyon, 1998). Since then, many other experiments have been conducted with *Bacillus* and *Pseudomonas* agents on potato pathogens including quarantine organisms (Table 2). The selected strains have antibiotic activity against potato pathogens (in vitro screening), a strong ability to colonize potato roots (soil microcosm) or to induce systemic resistance of potato plant (split-root system), but to our knowledge, not much data are available regarding their successful field application.

More recently, investigations for biocontrol agents have been broadened to other bacterial species mainly selected from within the rhizosphere as a guarantee for their ability to colonize this microenvironment. Berg et al. (2001) isolated 20 rhizobacteria from the potato showing antagonism to *V. dahliae*. Among them, 15 belonged to *Pseudomonas* and five were classified in the following genera: *Janthinobacterium*, *Kluyvera*, *Cytophyga*, *Comamonas* and *Stenotrophomonas*. Krechel et al. (2002) screened other candidates in different potato microenvironments in order to find antagonists of various fungi or nematodes. Among the 32 selected strains, 13 were *Pseudomonas* strains and eight were *Streptomyces* strains. The remaining 11 strains were divided into the following genera: *Bacillus*, *Streptococcus*, *Ralstonia*, *Stenotrophomonas*, *Sphingomonas*, *Kitasatosporia* and *Amycolatopsis*. Moreover, isolates from the potato rhizosphere belonging to *Lysobacter* sp. appeared as a dominating group, which was able to antagonize *R. solani* and *R. solanacearum* (van Over-

beek & van Elsas, 2008). Finally, using a similar approach without taxonomic *a priori*, a series of bacterial and fungal combinations, including commercial products used to protect other crops, were tested for effectiveness against *R. solani* on potato. Some of these formulations and a combination of *B. subtilis* and *Trichoderma virens* reduced black scurf and stem canker (Brewer & Larkin, 2005). It therefore appears that some nonpathogenic fungi and filamentous bacteria (*Streptomyces*) strains are also of interest for biocontrol applications. They are generally selected for their ability to reside within the same ecological niche as their pathogenic counterparts. This competition over settlement is one of the main protection mechanisms, which aims at fighting against potato scab caused by pathogenic *Streptomyces* (Neeno-Eckwall et al., 2001; Krechel et al., 2002; Sessitsch et al., 2002; Hiltunen et al., 2009). Hyperparasitism and the induction of potato defences are other ways by which antagonistic fungi limit *Rhizoctonia* black scurf and *Verticillium* wilt (Table 2).

A less known alternative to bacterial biocontrol is the use of bacteriophages. These are viruses that can very specifically destroy certain bacteria while being harmless to the eucaryote host. The use of phages for plant disease control is a rapidly expanding area of plant protection with considerable potential to replace chemical or antibiotic treatments (Jones et al., 2007). Phage therapy has allowed disinfection of *S. scabiei*-infected seed potatoes and reduced tobacco bacterium wilt due to *R. solanacearum* by coapplication with an avirulent strain of this bacterium (Tanaka et al., 1990; Mc Kenna et al., 2001). This method seems to be of a potential interest to control soft rot too. The existence of phages targeting *Pectobacterium* pathogens was revealed long ago. Coons & Kotila (1925) isolated bacteriophages from soil samples, rotting carrots or river water, that they were active against *Pectobacterium* species. They demonstrated that coinoculation of *P. atrosepticum* with phage successfully inhibited the pathogen and prevented rotting of potato tubers during growth chamber experiments. A major limiting factor in using phages for control of soft rot was the probability of developing *Pectobacterium* strains resistant to the phage. To prevent this problem, the formulation of a phage cocktail with different receptor specificity for the pathogenic bacteria is generally recommended (Petty et al., 2006; Jones et al., 2007). The identification of a flagellatropic phage of *P. atrosepticum* and that of bacterial mutants attenuated in virulence are important elements for the realization of this cocktail in addition to phages requiring membrane proteins and lipopolysaccharide receptors (Evans et al., 2010).

## Management of the potato rhizosphere to improve biological control

The metabolites produced in the rhizosphere have an impact on the composition of microbial communities associated
with the plant. Van Overbeek & van Elsas (2008) demonstrated that among the three main factors affecting bacterial communities, potato growth stage and experimental conditions (field and year) were significantly more influential than potato genotype. These authors underlined the impact of these factors, including the potato cultivar and the breeding line to select and favour antagonists. The control of substances secreted by the roots using either specific cultivars or genetically modified plants seems relevant for biological control, and help to overcome the influence of environmental parameters. This view was confirmed by the work of Becker *et al.* (2008) who compared the rhizosphere and phyllosphere communities of transgenic potatoes producing fructan with isogenic controls in field experiments. Over a period of 3 years, they showed that the structure of the rhizosphere bacterial community was affected to a greater extent by soil conditions within the field site than by the different potato genotypes tested. In contrast, the phyllosphere communities, without contact with the soil, were strongly modified by the transgenic plants. Considering the metabolic potential of the *Solanaceae* (e.g. biosynthesis of glycaloides, starch or proteins of pharmaceutical interest), the use of transgenic potato plants has already been considered. In 2010, Amflora® was the first variety authorized to be cultivated on European soil, provided that its tubers would be intended exclusively for industrial use. This transgenic potato is affected in its ability to synthesize amylose and consequently produces a starch with a very high proportion of amylopectin, a component of interest in paper and adhesive synthesis (http://www.basf.com/group/corporate/en/products-and-industries/biotechnology/plant-biotechnology/amflora). However, due to potential environmental risks and negative public opinion, the production of transgenic plants has remained minimal in Europe (Myskja, 2006; Varzakas *et al.*, 2007).

Since the 1990s, several transgenic potato lineages have been constructed to reduce *P. atrosepticum* infections by expressing antibacterial enzymes and peptides produced by the T4 phage or the silkworm (Düring *et al.*, 1993; Rasche *et al.*, 2006a,b). On the other hand, Wegener *et al.* (1996) expressed a *P. atrosepticum* pectate lyase in potato plants to induce host defence pathways and the resistance of potato tubers to soft rot. These transgenic lines increase the release of specific oligogalacturonates and consequently levels of enzymes involved in plant defence (Wegener & Olsen, 2004). In order to rate the ecological risk presented by these genetically modified potatoes, their impact on the associated microbial communities was assessed. Lysozyme produced by transgenic potatoes had no effect on bacterial populations or on the antagonist proportion of potato pathogens. The impact on the diversity of antagonistic strains was equivalent to the influence of plant growth stage or negligible relative to natural factors (Lottmann *et al.*, 1999; Heuer

*et al.*, 2002). Similar results were obtained by Rasche *et al.* (2006a, b), while assessing the impact of transgenic potato plants producing lysozyme, attacin or cecropin. However, when a lysozyme-resistant biocontrol agent is introduced to the potato rhizosphere, its persistence was shown to be greater in the vicinity of lysozyme-producing transgenic potato plants than in wild-type ones (Lottmann *et al.*, 2000).

In addition to the secretion of root exudates, the rhizosphere is also the place where microorganisms can exchange signals. The most studied model relies on both synthesis and perception of N-acyl-homoserine lactone (NAHSL)-signaling molecules leading coordinated gene expression in a bacterial population. Right now, a dozen plant-associated bacterial genera have been described to regulate virulence functions by NAHSL-based quorum sensing, including potato pathogens such as *Dickeya*, *Pectobacterium* and *Ralstonia* species (Cha *et al.*, 1998; Nasser *et al.*, 1998; Diallo *et al.*, 2009). The means of communication used by these plant pathogenic bacteria has emerged as a target for the development of new biocontrol methods at the beginning of the decade. *Pectobacterium* spp. and its quorum-sensing system were chosen as the main plant pathogen model for quorum-quenching strategies. A first proposed control method was the expression of a NAHSL-degrading enzyme by the plant, which provided good protection levels (Dong *et al.*, 2000). Then an interference method with extra NAHSL production was considered in order to generate a premature attack by an insufficient amount of soft-rot bacteria (Fray *et al.*, 1999; Maë *et al.*, 2001). This led to contrasting results in tobacco and potato plants. The treatment is more effective to tobacco, probably due to differences in the defence systems, which are more efficient in tobacco than in potato. This could also be due to the primary role of this cellular signalling, which would lead to a massive secretion of lytic enzymes perhaps not sufficient to overwhelm plant defences, but could provide the nutrients needed under conditions of high population density (Toth *et al.*, 2004).

As the rhizosphere also hosts signal-degrading bacteria (D'Angelo-Picard *et al.*, 2005; Jafra *et al.*, 2006), the principle of quorum quenching was broadened to include the use of NAHSL-degrading bacteria that can protect potato against *P. atrosepticum* (Smadja *et al.*, 2004) or *P. carotovorum* maceration symptoms (Dong *et al.*, 2000; Molina *et al.*, 2003; Uroz *et al.*, 2003; Jafra *et al.*, 2006). Quenching bacteria isolated from the potato rhizosphere belong mainly to *Agrobacterium*, *Bacillus*, *Pseudomonas*, *Delftia*, *Ochrobactrum* and *Rhodococcus* genera (Jafra *et al.*, 2006; Cirou *et al.*, 2007). These biocontrol methods were not aimed at eradiating the pathogen, but targeted at reducing the expression of virulence systems (Faure & Dessaux, 2007). These treatments are considered more respectful of microbial balance. However, interference with quorum sensing might modify
the bacterial density and diversity. This hypothesis was first
tested with potato crops in hydroponic systems where the
potato microbial community can be modified in order to
promote NAHSL-degrading communities by adding biosti-
mulating molecules. These biostimulating molecules show
structural similarities to NAHSLs and are not persistent in
the environment. They tend to favour transient elevation of
bacterial communities, which are able to metabolize both
molecules. In contrast, NAHSL-signal producing bacteria do
not seem affected by these changes (Cirou et al., 2007). On
the whole, these traits seem to be favourable indicators for
the use of structural analogues of quorum-sensing signals to
biocontrol application.

The expansion of potato cultivation will accommodate
new constraints encountered in the tropical zone, where
potatoes will be grown in low-input cropping systems and
potato blight and rots are major causes for losses in crop
yield. For plants such as the potato, which have a low root
density and high growth potential, the arbuscular mycor-
rhizal symbiosis may be of particular significance in coping
with phosphorus and water deficiency stress in tropical soils.
One way to improve biocontrol would be to use multiple
antagonists in effective combinations particularly to control
aerial diseases such as the late blight due to P. infestans.
Indeed, this devastating oomycete presents a remarkable
speed of adaptation to control strategies such as genetically
resistant cultivars and chemical treatments (Montarry et al.,
2008; Haas et al., 2009). Management of the potato mycor-
rhizosphere should include the use of mycorrhizal fungi
promoting the root colonization of microorganisms that
induce systemic resistance to P. infestans (as those cited in
Table 2) or should combine the use of compatible mycor-
rhizal fungi with these microorganisms.

Conclusion

The qualities of the potato define it as a strategic food-
producing crop. However, this Solanaceous plant is suscep-
tible to many pathogens. Its genetic complexity combined
with its small number of resistance genes limits genetic
control methods to a few cryptogamic or viral diseases
(Priou & Jouan, 1996; Gebhardt & Valkonen, 2001). Conse-
quently, up to this point the potato's prosperity relies mainly
on sanitary and phytosanitary measures, and the develop-
ment of microbiological control is a worthy and challenging
alternative (Latour et al., 2008). It relies on the development
and use of environmentally risk-free strains, which are able
to colonize the potato plant and express antagonism under
every cultivation condition.

The rhizosphere is the site of complex plant–microorgan-
ism interactions and is of interest from multiple environ-
mental perspectives, including the protection of plants. It is
the subject of a European cooperation in the field of scientific

and technical research (Wenzel, 2005; http://www.rhizo.at/
cost631) and an international conference (Hartmann, 2008;
http://rhizosphere3.com) specifically dedicated to it. Because
of the importance of underground parts in the S. tuberosum
species and its proximity with telluric pathogens, the potato
rhizosphere is the main target in biocontrol studies. Histori-
cally, the first potential biocontrol agents were investigated in
relation to the potato rhizosphere (Burr et al., 1978; Kloepper
et al., 1980). In these pioneer works, antagonist activities were
mainly shown to rely on antibiosis and competition, and the
bacteria used belonged to the fluorescent pseudomonads.
Unfortunately, due to insufficient expression of antagonistic
activities, the first large-scale protection trials failed (Gross,
1988). So far, the diversity of bacteria associated with potato
roots has motivated intensive research mainly conducted by
teams from countries traditionally involved in potato pro-
duction. It has also permitted evaluation of different biocon-
trol techniques. Potato roots host a highly diverse and dense
microbial community where various candidate antagonistic
bacteria and fungi can potentially be used. Furthermore,
antibiotic production by biocontrol agents can not only affect
the pathogen but also plant development (Brazelton et al.,
2008). Consequently, current investigations are aimed at
screening for new protectors, and new antagonistic properties
that target pathogen properties, but not the plant. Another
innovative strategy consists of influencing the potato rhizo-
sphere chemical environment, via the use of transgenic plants,
or the use of molecules leading to interference with the
pathogen communication system (Fray, 2002; Faure & Des-
saux, 2007). Yet, the fact that numerous signal-degrading
bacteria belong to the main potato-colonizing bacteria genera
(Table 1) could lead us to hope that a massive installation of
these bacteria in the potato rhizosphere would protect it
effectively. Finally, the recent registration and commercializa-
tion of the first phage formulation for plant disease control
should provide new solutions to farmers. This formulation,
based on phages targeting Xanthomonas campestris pv. vesi-
catoria, is used on tomatoes in greenhouses and production
fields as a part of a standard integrated management program
to control tomato bacterial spot in Florida (Jones et al., 2007;
Evans et al., 2010). This concrete application and the isolation
of new phages that target potato pathogens are promising for
effective use of this alternative therapy against bacterial
diseases of the potato.

Because of major losses caused by cryptogamic diseases
harming potato crops, biocontrol methods using fungal
protection agents should be developed in the future. These
microorganisms can compete with taxonomically related
pathogenic fungi, act in synergy with PGPR and harbour
signal-degrading activities that are similar to quorum-
quenching activities (Alabouvette & Lemanceau, 1996; Pieta
& Patkowska, 2003; Brewer & Larkin, 2005; Uroz & Heinon-
salo, 2008). Further avenues should include the evaluation
of mycorrhizal fungi. *Glomus intraradices* and *G. mosseae* isolates could be considered as examples of new candidates in biological control studies, due to their intimacy with potato roots and their antagonistic effect on some major potato pathogens (Garcia-Garrido & Ocampo, 1988; Pozo *et al.*, 2002; Bharadwaj *et al.*, 2008; Cesaro *et al.*, 2008).

Considering the diversity of mechanisms and recent advances involved in plant growth promotion and microbial protection, the potato rhizosphere constitutes both a historical and a relevant model for developing biocontrol strategies.

## Acknowledgements

This work was supported by grants from Conseil Régional de Haute-Normandie & Ministère délégué à l'Enseignement Supérieur et à la Recherche, the National Association of Technical Research (ANRT-CIFRE), GRR VATA & FEDER (European Union) and by the national grant CAS-DAR AAP No. 7124. We also thank Christine Farmer for linguistic support.

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