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SUMMARY

  1. Top of page
  2. SUMMARY
  3. INTRODUCTION
  4. 1. PSEUDOMONAS SYRINGAE PATHOVARS
  5. 2. RALSTONIA SOLANACEARUM
  6. 3. AGROBACTERIUM TUMEFACIENS
  7. 4. XANTHOMONAS ORYZAE (ORYZAE)
  8. 5. XANTHOMONAS CAMPESTRIS PATHOVARS
  9. 6. XANTHOMONAS AXONOPODIS
  10. 7. ERWINIA AMYLOVORA
  11. 8. XYLELLA FASTIDIOSA
  12. 9. DICKEYA (DADANTII AND SOLANI)
  13. 10. PECTOBACTERIUM CAROTOVORUM (AND P. ATROSEPTICUM)
  14. ACKNOWLEDGEMENTS
  15. REFERENCES

Many plant bacteriologists, if not all, feel that their particular microbe should appear in any list of the most important bacterial plant pathogens. However, to our knowledge, no such list exists. The aim of this review was to survey all bacterial pathologists with an association with the journal Molecular Plant Pathology and ask them to nominate the bacterial pathogens they would place in a ‘Top 10’ based on scientific/economic importance. The survey generated 458 votes from the international community, and allowed the construction of a Top 10 bacterial plant pathogen list. The list includes, in rank order: (1) Pseudomonas syringae pathovars; (2) Ralstonia solanacearum; (3) Agrobacterium tumefaciens; (4) Xanthomonas oryzae pv. oryzae; (5) Xanthomonas campestris pathovars; (6) Xanthomonas axonopodis pathovars; (7) Erwinia amylovora; (8) Xylella fastidiosa; (9) Dickeya (dadantii and solani); (10) Pectobacterium carotovorum (and Pectobacterium atrosepticum). Bacteria garnering honourable mentions for just missing out on the Top 10 include Clavibacter michiganensis (michiganensis and sepedonicus), Pseudomonas savastanoi and Candidatus Liberibacter asiaticus. This review article presents a short section on each bacterium in the Top 10 list and its importance, with the intention of initiating discussion and debate amongst the plant bacteriology community, as well as laying down a benchmark. It will be interesting to see, in future years, how perceptions change and which bacterial pathogens enter and leave the Top 10.


INTRODUCTION

  1. Top of page
  2. SUMMARY
  3. INTRODUCTION
  4. 1. PSEUDOMONAS SYRINGAE PATHOVARS
  5. 2. RALSTONIA SOLANACEARUM
  6. 3. AGROBACTERIUM TUMEFACIENS
  7. 4. XANTHOMONAS ORYZAE (ORYZAE)
  8. 5. XANTHOMONAS CAMPESTRIS PATHOVARS
  9. 6. XANTHOMONAS AXONOPODIS
  10. 7. ERWINIA AMYLOVORA
  11. 8. XYLELLA FASTIDIOSA
  12. 9. DICKEYA (DADANTII AND SOLANI)
  13. 10. PECTOBACTERIUM CAROTOVORUM (AND P. ATROSEPTICUM)
  14. ACKNOWLEDGEMENTS
  15. REFERENCES

Recently, the journal Molecular Plant Pathology considered which viruses would appear in a Top 10 of plant viruses based on their perceived importance, scientifically or economically, in terms of the views of the contributors to the journal (Scholthof et al., 2011). This was followed by a similar review on fungi (Dean et al., 2012). These surveys were carried out as many papers, reviews and grant applications claim that a particular plant virus or fungal pathogen is of huge importance, and this is probably rightly so.

As a result of the interest generated by the plant virus and fungal pathogen surveys, a similar survey was carried out for plant pathogenic bacteria and, as before, bacterial pathologists with an association with the journal Molecular Plant Pathology were contacted and asked to nominate three plant pathogenic bacteria that they would expect to see in a list of the most scientifically/economically important bacterial pathogens. The review, by its very nature, is similar in format and layout to the Top 10 Virus and Top 10 Fungal Reviews (Dean et al., 2012; Scholthof et al., 2011).

The survey generated 458 votes from the international community, and allowed the construction of a Top 10 bacterial plant pathogen list for the journal Molecular Plant Pathology (see Table 1).

Table 1.  Top 10 bacterial plant pathogens. The table represents the ranked list of bacteria as voted for by plant bacteriologists associated with the journal Molecular Plant Pathology.
RankBacterial pathogenAuthor of bacterial description
 1Pseudomonas syringae pathovarsJohn Mansfield
 2Ralstonia solanacearumStéphane Genin
 3Agrobacterium tumefaciensShimpei Magori, Vitaly Citovsky
 4Xanthomonas oryzae pv. oryzaeMalinee Sriariyanum, Pamela Ronald
 5Xanthomonas campestris pathovarsMax Dow
 6Xanthomonas axonopodis pv. manihotisValérie Verdier
 7Erwinia amylovoraSteven V. Beer
 8Xylella fastidiosaMarcos A. Machado
 9Dickeya (dadantii and solani)Ian Toth
10Pectobacterium carotovorum (and P. atrosepticum)George Salmond

The bacterium, or group of pathovars, making the strongest appearance on scientific and economic grounds is Pseudomonas syringae, with many voters grouping the various pathovars together, and others voting for individual pathovars. It is clear that P. syringae has had a huge impact on our scientific understanding of microbial pathogenicity, and continues to cause economically important plant diseases.

In second place is Ralstonia solanacearum, which rates very highly on economic importance worldwide, especially as it has a very broad host range, with affected crops ranging from potato to banana.

In third position is Agrobacterium tumefaciens, making a very strong appearance based primarily on its scientific importance. Although this bacterium can cause significant damage in particular crops, its role in scientific breakthroughs and applications clearly attracted votes.

In fourth, fifth and sixth positions are Xanthomonas species, all clearly distinctive in their pathology and host targets, with each attracting significant votes as individuals. In fourth and sixth positions are xanthomonads with relatively specific crop targets, namely Xanthomonas oryzae pv. oryzae, one of the most serious pathogens of rice, and Xanthomonas axonopodis pv. manihotis, the causal agent of cassava bacterial blight (CBB). Xanthomonas campestris pathovars, which cause diseases in a range of crops worldwide, reached fifth position.

In seventh position comes Erwinia amylovora, which causes the well-known fire blight disease of ornamentals, fruit trees and bushes. This disease has significant scientific history and is of continuing economic importance.

Xylella fastidiosa rightly has a place in the Top 10 in eighth position, as it is associated with several important diseases of crops and trees. It also has the important scientific claim of being the first phytopathogen (outside of plant viruses) to have had its genome sequenced.

For the entry in ninth position, it was decided to group two species of Dickeya together, namely Dickeya dadantii and solani, as Dickeya attracted significant votes, many of which were simply referred to as Dickeya spp. This is perhaps understandable as the taxonomy of these bacteria may be described as being in a state of flux. Indeed, the name Dickeya solani has not been officially accepted, but it is clear that Dickeya spp. cause economically important diseases, particularly in potato.

The final entry in tenth place is Pectobacterium carotovorum (also covering P. atrosepticum), meriting a place in the Top 10 because of the economic losses linked with the soft rot diseases, but also being responsible for several scientific milestones. This is in addition to some long-standing translational breakthroughs, such as involvement in the treatment of some leukaemias.

Although the aim of this review article was to identify the views of contributors to Molecular Plant Pathology with regard to the Top 10 most important plant pathogenic bacteria, the authors are very much aware that importance and priorities can vary locally across continents and disciplines. We are also aware that not all bacteria can make it into any Top 10, for obvious numerical limits, although such bacteria can still be regarded as hugely important. We therefore felt it appropriate to make honourable mentions to bacteria just missing out on the Top 10 list, including Clavibacter michiganensis (michiganensis and sepedonicus) (Eichenlaub and Gartemann, 2011), Pseudomonas savastanoi (Rodríguez-Palenzuela et al., 2010) and Candidatus Liberibacter (pv. asiaticus) (Duan et al., 2009), all clearly important.

This review contains single-page descriptions of the Top 10, including illustrative figures and key references for further reading. We hope that the review triggers discussion and debate amongst the plant bacteriology community, as well as laying down a benchmark. It will be interesting to see how perceptions change in future years and which bacteria enter and leave the Top 10 list.

1. PSEUDOMONAS SYRINGAE PATHOVARS

  1. Top of page
  2. SUMMARY
  3. INTRODUCTION
  4. 1. PSEUDOMONAS SYRINGAE PATHOVARS
  5. 2. RALSTONIA SOLANACEARUM
  6. 3. AGROBACTERIUM TUMEFACIENS
  7. 4. XANTHOMONAS ORYZAE (ORYZAE)
  8. 5. XANTHOMONAS CAMPESTRIS PATHOVARS
  9. 6. XANTHOMONAS AXONOPODIS
  10. 7. ERWINIA AMYLOVORA
  11. 8. XYLELLA FASTIDIOSA
  12. 9. DICKEYA (DADANTII AND SOLANI)
  13. 10. PECTOBACTERIUM CAROTOVORUM (AND P. ATROSEPTICUM)
  14. ACKNOWLEDGEMENTS
  15. REFERENCES

It seems a little unfair that a team of pathovars has been voted for an award, a bit like a relay team winning the 400-m individual Olympic gold medal. It may of course be argued that the pathovar designation is really unjustified and that we are dealing with one remarkably versatile single species, Pseudomonas syringae. This debate is now being resurrected by the emerging detail from genomic sequencing. The criteria for this award were importance to basic science and impact on food production and/or the environment—P. syringae scores heavily on all counts.

The economic impact of P. syringae is increasing, with a resurgence of old diseases, including bacterial speck of tomato (pv. tomato; Shenge et al., 2007), and the emergence of new infections of importance worldwide, such as bleeding canker of horse-chestnut (pv. aesculi; Green et al., 2010). The European Handbook of Plant Diseases (Smith et al., 1988) describes 28 pathovars, each attacking a different host species. We can now add pv. aesculi to this list. Several pathovars cause long-term problems in trees, often through the production of distortions and cankers (e.g. pathovars savastanoi and morsprunorum). Infections of annual crops are more sporadic, and outbreaks are often caused by sowing contaminated seed. Many reports highlight the seed-borne nature of P. syringae, but it is a remarkably adaptive pathogen, emerging in some apparently bizarre sites, such as snow melt waters (Morris et al., 2007). Once new infections have established, given favourable conditions of rainfall and temperatures, disease outbreaks are often devastating, as observed with bean halo blight caused by pv. phaseolicola (Murillo et al., 2010).

Research into the molecular biology of virulence and plant defence against P. syringae has opened up new insights into microbial pathogenicity, not only with regard to plants but also with more general significance to human diseases. Pathovars phaseolicola and tomato have emerged as excellent models for fundamental studies on bacterial attack and plant defence (Arnold et al., 2011; Preston, 2000). Notable examples are discoveries concerning the hypersensitive response and pathogenicity (hrp) gene cluster encoding the type III secretion system (see Fig. 1), effector trafficking and host targets for defence suppression (Huynh et al., 1989; Jovanovic et al., 2011; Kvitko et al., 2009; Li et al., 2002; Zhang et al., 2010).

image

Figure 1. The type III secretion system (T3SS) of Pseudomonas syringae pv. tomato. (A) Putative basal body of the T3SS released from membrane preparations after growth in hrp inducing medium. The arrow marks the attachment point of the Hrp pilus. Bar, 25 nm. (B) False colour image of the Hrp pilus gold labelled with antibodies to the subunit protein HrpA, emerging from the bacterial surface. Bar, 50 nm. Both images kindly provided by Ian Brown (University of Kent).

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Pseudomonas syringae leads the field in the impact of high-throughput sequencing technologies on our understanding of pathogenicity. Remarkably, the prediction by O'Brien et al. (2011) that, ‘. . .  at least two dozen new P. syringae genomes will be released this year’, has been proven to be correct with the publication of the landmark study by Baltrus et al. (2011). So far, a perhaps unexpected feature is that pathovars colonizing strongly unrelated plants are being closely grouped together, for example pv. savastanoi (olive) and pv. phaseolicola (bean) both lie within the same clade. Genomic analysis, initiated by Joardar et al. (2005) and Lindeberg et al. (2008), has perhaps the most potential for unravelling the determinants of host specificity. As more genomic sequences are completed, further insight should be gained into the still puzzling role of effector proteins and toxins in defining host range within the species.

Pseudomonas syringae pathovars represent not only the premier plant pathogenic bacterial grouping, but would also probably top the all time pathogen charts including fungi and oomycetes. Research on the effector biology of the filamentous pathogens is very much following in the wake of advances made with P. syringae (Cunnac et al., 2009; Hann et al., 2010; Oliva et al., 2010).

2. RALSTONIA SOLANACEARUM

  1. Top of page
  2. SUMMARY
  3. INTRODUCTION
  4. 1. PSEUDOMONAS SYRINGAE PATHOVARS
  5. 2. RALSTONIA SOLANACEARUM
  6. 3. AGROBACTERIUM TUMEFACIENS
  7. 4. XANTHOMONAS ORYZAE (ORYZAE)
  8. 5. XANTHOMONAS CAMPESTRIS PATHOVARS
  9. 6. XANTHOMONAS AXONOPODIS
  10. 7. ERWINIA AMYLOVORA
  11. 8. XYLELLA FASTIDIOSA
  12. 9. DICKEYA (DADANTII AND SOLANI)
  13. 10. PECTOBACTERIUM CAROTOVORUM (AND P. ATROSEPTICUM)
  14. ACKNOWLEDGEMENTS
  15. REFERENCES

Ralstonia solanacearum is probably the most destructive plant pathogenic bacterium worldwide. One of the reasons for this is that the R. solanacearum species is composed of a very large group of strains varying in their geographical origin, host range and pathogenic behaviour (Denny, 2006; Genin, 2010). This heterogeneous group is nowadays recognized as a ‘species complex’ which has been divided into four main phylotypes (phylogenetic grouping of strains). The species as a whole has a very broad host range, infecting 200 plant species in over 50 families, and is the causal agent of potato brown rot, bacterial wilt of tomato, tobacco, eggplant and some ornamentals, as well as Moko disease of banana.

Ralstonia solanacearum is a soil-borne pathogen that infects plants via wounds, root tips or cracks at the sites of lateral root emergence. The bacterium subsequently colonizes the root cortex, invades the xylem vessels and reaches the stem and aerial parts of the plant through the vascular system (Fig. 2). Ralstonia solanacearum can rapidly multiply in the xylem up to very high cell densities, leading to wilting symptoms and plant death.

image

Figure 2. Ralstonia solanacearum (A, photograph J. Vasse) and disease wilting symptoms on tomato (B) with bacteria oozing from the vascular system after stem section (C).

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The direct economic impact of R. solanacearum is difficult to quantify, but the pathogen is extremely damaging because of its wide geographical distribution and host range; on potato alone, it is responsible for an estimated US$1 billion in losses each year worldwide (Elphinstone, 2005). The incidence of the disease is particularly dramatic for agriculture in many developing countries in inter-tropical regions in which R. solanacearum is endemic. In areas in which the organism has quarantine status, it is also responsible for important losses because of regulatory eradication measures and restrictions on further production on contaminated land. Disease management remains limited and is hampered by the faculty of the pathogen to survive for years in wet soil, water ponds, on plant debris or in asymptomatic weed hosts, which act as inoculum reservoirs. Breeding for resistance, although effective in a few cases, is hampered by the broad diversity of the pathogenic strains.

As a root and vascular pathogen, R. solanacearum is a model system for the study of bacterial pathogenicity. The bacterium was one of the first plant pathogen genomes to be entirely sequenced (Salanoubat et al., 2002), and the development of pathosystems with model plants, such as Arabidopsis, or the legume Medicago truncatula has facilitated genetic and molecular studies on both the plant and bacterial partners. The pathogenicity of R. solanacearum relies on a type III secretion system, and many studies have been conducted on this topic since the first description of a hrp mutant phenotype by Boucher et al. (1985). Many other pathogenicity factors have been identified and characterized, whose expression is orchestrated by an atypical quorum-sensing molecule structurally related to the diffusible signal factor (DSF) family (Flavier et al., 1997).

Future research in this field will include a better understanding of the molecular bases underlying the adaptation of this versatile group of strains to such a diverse range of hosts. Another major task to address is how our increasing knowledge of the sophisticated mechanisms developed by R. solanacearum to promote plant susceptibility could be used to engineer novel and durable protection strategies to fight this devastating disease.

3. AGROBACTERIUM TUMEFACIENS

  1. Top of page
  2. SUMMARY
  3. INTRODUCTION
  4. 1. PSEUDOMONAS SYRINGAE PATHOVARS
  5. 2. RALSTONIA SOLANACEARUM
  6. 3. AGROBACTERIUM TUMEFACIENS
  7. 4. XANTHOMONAS ORYZAE (ORYZAE)
  8. 5. XANTHOMONAS CAMPESTRIS PATHOVARS
  9. 6. XANTHOMONAS AXONOPODIS
  10. 7. ERWINIA AMYLOVORA
  11. 8. XYLELLA FASTIDIOSA
  12. 9. DICKEYA (DADANTII AND SOLANI)
  13. 10. PECTOBACTERIUM CAROTOVORUM (AND P. ATROSEPTICUM)
  14. ACKNOWLEDGEMENTS
  15. REFERENCES

More than a century ago, Smith and Townsend (1907) identified Agrobacterium tumefaciens as the causative agent of crown gall tumour, one of the most serious plant diseases affecting various crop species worldwide. In nature, this soil-borne bacterium induces neoplastic growths (Fig. 3) at wound sites on host plants and severely limits crop yield and growth vigour. This deleterious effect of A. tumefaciens has unquestionably contributed to a driving force behind long-lasting Agrobacterium research. However, A. tumefaciens is not just another phytopathogen, but possesses a very rare feature: the ability for genetic transformation.

image

Figure 3. A crown gall on cherry trunk caused by Agrobacterium tumefaciens.

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The ‘Eureka’ moment came in the late 1970s when Mary-Dell Chilton and Eugene Nester with their colleagues demonstrated that the specific DNA segment (now known as the T-DNA) of the bacterial tumour-inducing (Ti) plasmid was present in the genome of infected plant cells (Chilton et al., 1977). This landmark discovery cast the spotlight on Agrobacterium as the first organism capable of trans-kingdom gene transfer. Since then, a great deal has been learned about the molecular mechanisms underlying A. tumefaciens-mediated genetic transformation, which has emerged as a highly complex process regulated by numerous bacterial and host factors (reviewed by Gelvin, 2010; Pitzschke and Hirt, 2010; Tzfira and Citovsky, 2002; Zupan et al., 2000). Briefly, A. tumefaciens perceives phenolic compounds exuded from plant wound tissues and activates the expression of several effectors, termed virulence (Vir) proteins. Some of these factors mediate the generation of a single-stranded copy of T-DNA (T-strand) and its transport into the host cell through a type IV secretion system. In addition to the T-strand, several Vir proteins are also translocated into plant cells. These exported effectors, together with multiple host factors, facilitate the nuclear import of the T-strand and its subsequent integration into the host genome. Finally, genes involved in auxin and cytokinin biosynthesis are expressed from the integrated T-DNA, leading to abnormal cell proliferation in the infected tissues and the formation of tumours, i.e. crown galls (Fig. 3).

Although the details on its molecular basis are still emerging, the discovery of the Agrobacterium-mediated genetic transformation of plants ushered in a new era of plant molecular biology. In 1983, Chilton and colleagues reported that an engineered T-DNA carrying a foreign gene could be transferred to tobacco plants and maintained through regeneration (Barton et al., 1983). Since this first demonstration of transgenic plants, substantial conceptual and technical advances have been achieved to make the Agrobacterium-mediated genetic engineering of plants more feasible in the daily practice of basic research as well as biotechnology (Fig. 4). For example, the advent of binary vectors, a system of two separate replicons that house the T-DNA and virulence genes and function in both Escherichia coli and A. tumefaciens, has made it much easier to manipulate the T-DNA. Owing to its incredibly wide host range, which, under laboratory conditions, includes most eukaryotic organisms (Lacroix et al., 2006), high efficiency and sophisticated modern transformation technology, A. tumefaciens is now a transformation vehicle of choice for the genetic manipulation of most plant species, including the model plant Arabidopsis thaliana, as well as numerous fungal species.

image

Figure 4. Wild-type tomato plant developing crown gall tumours (left) and Agrobacterium tumefaciens-resistant transgenic tomato plant generated by A. tumefaciens-mediated genetic transformation (right) illustrate two important aspects of A. tumefaciens: one as a pathogen and another as a tool for genetic engineering (reproduced with permission from Escobar et al., 2001).

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Agrobacterium tumefaciens never ceases to amaze plant biologists and pathologists. Even after 100 years of research, we are still discovering novel mechanisms that underlie the interactions of A. tumefaciens with its hosts, and are only beginning to understand how truly clever this pathogen is. For instance, recent studies have revealed that A. tumefaciens can subvert the host defence machinery for the active promotion of infection (Djamei et al., 2007; Zaltsman et al., 2010). In the foreseeable future, therefore, A. tumefaciens will continue to serve not only as a powerful tool for plant genetic engineering, but also as an excellent model organism to decipher host–pathogen interactions.

4. XANTHOMONAS ORYZAE (ORYZAE)

  1. Top of page
  2. SUMMARY
  3. INTRODUCTION
  4. 1. PSEUDOMONAS SYRINGAE PATHOVARS
  5. 2. RALSTONIA SOLANACEARUM
  6. 3. AGROBACTERIUM TUMEFACIENS
  7. 4. XANTHOMONAS ORYZAE (ORYZAE)
  8. 5. XANTHOMONAS CAMPESTRIS PATHOVARS
  9. 6. XANTHOMONAS AXONOPODIS
  10. 7. ERWINIA AMYLOVORA
  11. 8. XYLELLA FASTIDIOSA
  12. 9. DICKEYA (DADANTII AND SOLANI)
  13. 10. PECTOBACTERIUM CAROTOVORUM (AND P. ATROSEPTICUM)
  14. ACKNOWLEDGEMENTS
  15. REFERENCES

Bacterial leaf blight (BLB), caused by Xanthomonas oryzae pv. oryzae (Xoo), is found in both tropical and temperate regions. BLB also occurs in Australia, Africa, Latin America, the Caribbean and the USA (Mew et al., 1993; Mizukami and Wakimoto, 1969). Yield losses of 10%–50% from BLB have been reported (Ou, 1972). Outbreaks of BLB are most common during the monsoon season in South-East Asia and India (Mew et al., 1993). Rice was introduced for cultivation into the USA (North Carolina) more than 200 years ago and has been cultivated in other parts of the USA for over 100 years. Although many rice diseases have either been introduced or developed on rice during the history of its cultivation in the USA, Xoo has not established in the USA. The climates of rice-producing areas in the USA and USA rice cultivation practices are not conducive to the long-term survival or spread of Xoo. For these reasons, Xoo is of low risk to US agriculture.

BLB is efficiently controlled by the use of resistant rice cultivars. However, because Xoo has the capacity to express effectors that suppress some host defence responses, often this resistance is eventually overcome (Verdier et al., 2011). Resistance genes of the non-RD pattern recognition receptor class typically confer long-lasting resistance because they recognize conserved microbial signatures, which, when mutated, cripple the virulence of the pathogen (Han et al., 2011; Ronald and Beutler, 2010; Schwessinger and Ronald, 2012). Control of the disease with copper compounds, antibiotics and other chemicals has not proven to be effective (Mew, 1989; Singh et al., 1980).

Xanthomonas oryzae pv. oryzae is a rod-shaped, Gram-negative bacterium. It produces a yellow soluble pigment, called xanthomonadin (Fig. 5), and extracellular polysaccharide (EPS). EPS is important in the protection of bacteria from desiccation and for the attenuation of wind- and rain-borne dispersal (Ou, 1972; Swings et al., 1990). Xoo is disseminated by irrigation water systems, splashing or wind-blown rain, as well as by contaminated rice stubble from the previous crop season, which is the most important source of primary inoculum (Mizukami and Wakimoto, 1969; Murthy and Devadath, 1984). Xoo infects the rice leaf typically through hydathodes at the leaf tip, broken trichomes, leaf margins and wounds in the leaves or roots, multiplies in the intercellular spaces and enters into xylem vessels (Fig. 5) (Noda and Kaku, 1999; Ou, 1985; Park et al., 2010). Within a few days of infection, bacterial cells and EPS fill the xylem vessels and ooze out from the hydathodes, and form beads of exudate on the leaf surface, a characteristic sign of the disease and a source of secondary inoculum (Mew et al., 1993).

image

Figure 5. Visualization of Xanthomonas oryzae pv. oryzae (Xoo) in rice plants. (A, B) Transverse leaf sections of rice infected with Xoo strain PXO99 expressing the green fluorescence of rice cultivar TP309 (susceptible) (A) and TP309-XA21 (resistant) (B). Images were observed with excitation from 450 to 490 nm and emitted light collected at 520 nm at 40× magnification using a Zeiss Axiophot fluorescence microscope, 12 days after inoculation. The bars in (A) and (B) represent 50 µm. (C) Scanning electron micrograph of Xoo cells in the xylem vessel of a rice leaf. (D) Close-up of Xoo-infected rice leaf. Bacterial cells fill the xylem vessels and ooze out at hydathodes, forming beads or strands of exudate on the leaf surface, a characteristic sign of the disease. Photographs in (A) and (B) courtesy of S. W. Han (reprinted from BMC Microbiol. 2008; 8: 164). Photograph in (C) courtesy of J. Leach (reprinted from Mol. Plant Pathol. 2006; 7(5): 303–324). Photograph in (D) courtesy of the Bureau of Rice Research and Development, Thailand (http://www.brrd.in.th).

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Similar to Xanthomonas campestris pv. campestris (Xcc), Xoo also produces a range of virulence factors, including EPS, extracellular enzyme and type III effectors, which are essential for virulence (Mole et al., 2007). Xoo employs two different types of quorum-sensing factors, DSF and Ax21 (activator of Ax21-mediated immunity), a small, N-terminally processed, type I secreted protein (Han et al., 2011; He et al., 2010). A dual role for Ax21 in quorum sensing and in the activation of the host innate immune response has recently been demonstrated (Han et al., 2011). Ax21 mediates biofilm formation, motility and virulence. Whereas the rpf (regulation of pathogenicity factors) gene cluster is required for DSF-mediated quorum sensing (Jeong et al., 2008), rax genes are required for Ax21-mediated quorum sensing (Lee et al., 2006). Ax21 is broadly conserved in all Xanthomonas species and in related genera, and some of these orthologues can also activate XA21-mediated immunity (Lee et al., 2009).

The genome sequences of three Xoo strains (MAFF311018, KACC10331, PXO99A) have been completed (Lee et al., 2005; Ochiai et al., 2005; Salzberg et al., 2008) and the genome sequencing of eight additional Xoo strains is underway (Verdier et al., 2011). Comparative genomic analysis of different Xoo strains has revealed a large number of genomic rearrangements and transcriptional activator-like (TAL) effector gene recombinations, as well as a large number of insertion sequence (IS) elements (Ochiai et al., 2005; Ryan et al., 2011; Salzberg et al., 2008). Several genetic studies have suggested that the activity of IS elements and recombination among TAL effector genes have contributed to the diverse race structure within Xoo (Ochiai et al., 2005; Ponciano et al., 2004; Rajeshwari and Sonti, 2000). The comparative analysis of the genomic sequence has facilitated an understanding of the diversity and evolution of Xoo (Salzberg et al., 2008). Complete genome sequences have also facilitated the development of markers that are useful for epidemiological studies.

5. XANTHOMONAS CAMPESTRIS PATHOVARS

  1. Top of page
  2. SUMMARY
  3. INTRODUCTION
  4. 1. PSEUDOMONAS SYRINGAE PATHOVARS
  5. 2. RALSTONIA SOLANACEARUM
  6. 3. AGROBACTERIUM TUMEFACIENS
  7. 4. XANTHOMONAS ORYZAE (ORYZAE)
  8. 5. XANTHOMONAS CAMPESTRIS PATHOVARS
  9. 6. XANTHOMONAS AXONOPODIS
  10. 7. ERWINIA AMYLOVORA
  11. 8. XYLELLA FASTIDIOSA
  12. 9. DICKEYA (DADANTII AND SOLANI)
  13. 10. PECTOBACTERIUM CAROTOVORUM (AND P. ATROSEPTICUM)
  14. ACKNOWLEDGEMENTS
  15. REFERENCES

Pathovars of Xanthomonas campestris cause diseases of agronomic importance throughout the world. Among the most notable of these pathogens are Xanthomonas campestris pv. campestris (Xcc), the causal agent of black rot of crucifers that affects all cultivated brassicas, X. campestris pv. vesicatoria (Xcv), now reclassified as X. euvesicatoria, the causal agent of bacterial spot of pepper and tomato, and X. campestris pv. malvacearum (Xcm, now X. axonopodis pv. malvacearum), which causes angular leaf spot of cotton. The diseases caused by these bacteria are particularly severe in regions with a warm and humid climate, although black rot is also economically important in temperate regions, e.g. in Cornwall and other western areas of the UK. Xcc is also important as a producer of the EPS xanthan, which is used as a food additive and in the pharmaceutical and oil-drilling industries.

Studies of these bacteria have had considerable scientific impact, which has not been restricted to the discipline of molecular plant pathology. Work on Xcm provided the first demonstration for the hypothesis that a gene-for-gene pattern governs interactions between bacterial pathogens and plants (Gabriel et al., 1986). Work on Xcv established the genetic basis of the triggering of disease resistance in pepper, leading to the isolation of genes specifying avirulence on pepper cultivars containing the Bs1, Bs2 or Bs3 (for bacterial spot) resistance genes (Boch and Bonas, 2010; Minsavage et al., 1990). AvrBs3 is the paradigm member of the large family of TAL type III effector proteins in Xanthomonas spp. It was subsequently established that this effector is translocated to the nucleus of the plant cell, where it influences gene expression by binding to plant promoters (Boch and Bonas, 2010). The ‘code’ governing promoter recognition by the majority of effectors of this family has been determined (Fig. 6). The knowledge of this code affords great potential for biotechnology, e.g. by engineering promoters with boxes for TAL effectors to drive the expression of resistance genes or by allowing the generation of custom-designed DNA-binding specificities.

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Figure 6. (A) Black rot disease symptoms on cabbage caused by Xanthomonas campestris pv. campestris, showing the characteristic blackening of the leaf veins (image kindly provided by Sarah Schatschneider and Karsten Niehaus, University of Bielefeld). (B) Domain architecture of the AvrBs3 effector showing the variations at positions 12 and 13 in the repeats and the nucleotides recognized in the consensus UPA (upregulated by AvrBs3) box (see Boch and Bonas, 2010).

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Work on Xcc led to the identification of the genes involved in xanthan biosynthesis (Capage et al., 1987; Vorhölter et al., 2008) and the rpf gene cluster, which acts to control the synthesis of extracellular enzymes and xanthan, and contributes to virulence. Studies of the function of the Rpf gene products led to the discovery of the cell–cell signalling system mediated by DSF, which was subsequently identified as a cis-unsaturated fatty acid (Ryan and Dow, 2011). The rpf genes involved in DSF synthesis and perception are conserved in all xanthomonads, including Xylella fastidiosa and Stenotrophomonas spp., some strains of which are nosocomial human pathogens. Furthermore, DSF signalling controls virulence in some, but not all, of these bacteria, although the precise role differs between organisms (Ryan and Dow, 2011). RpfG, the regulatory protein involved in DSF signal transduction, contains a histidine-aspartic acid-glycine-tyrosine-proline (HD-GYP) domain. Studies in Xcc were the first to establish the regulatory function of an HD-GYP domain regulator and its enzymatic activity as a phosphodiesterase degrading the second messenger cyclic di-guanosine monophosphate (di-GMP) (Ryan et al., 2006). These observations have contributed to an understanding of cyclic di-GMP signalling in many organisms, as the HD-GYP domain is widely conserved in bacteria, including plant, animal and human pathogens.

6. XANTHOMONAS AXONOPODIS

  1. Top of page
  2. SUMMARY
  3. INTRODUCTION
  4. 1. PSEUDOMONAS SYRINGAE PATHOVARS
  5. 2. RALSTONIA SOLANACEARUM
  6. 3. AGROBACTERIUM TUMEFACIENS
  7. 4. XANTHOMONAS ORYZAE (ORYZAE)
  8. 5. XANTHOMONAS CAMPESTRIS PATHOVARS
  9. 6. XANTHOMONAS AXONOPODIS
  10. 7. ERWINIA AMYLOVORA
  11. 8. XYLELLA FASTIDIOSA
  12. 9. DICKEYA (DADANTII AND SOLANI)
  13. 10. PECTOBACTERIUM CAROTOVORUM (AND P. ATROSEPTICUM)
  14. ACKNOWLEDGEMENTS
  15. REFERENCES

Xanthomonas axonopodis pv. manihotis

The genus Xanthomonas currently consists of 20 species including X. axonopodis (Vauterin et al., 2000). Six distinct genomic groups have been defined within X. axonopodis, with many pathovars causing economically important diseases on different host plants of agronomic significance (Rademaker et al., 2005; Young et al., 2008).

Cassava (Manihot esculenta) is the staple food of nearly 600 million people in the world's tropical regions. Xanthomonas axonopodis pv. manihotis (Xam) is the causal agent of CBB, a major disease, endemic in tropical and subtropical areas. This foliar and vascular disease severely affects cassava production worldwide. Losses of between 12% and 100% affect both yield and planting material (Lozano, 1986; Verdier et al., 2004). Over recent years, a significant recurrence of the disease has been reported in different regions in Africa and Asia. Xam induces a wide combination of symptoms, including angular leaf lesions, blight, wilt, stem exudates and stem canker (Figs. 7 and 8). Host resistance is still the most effective way to control this disease. However, no breeding strategy is being developed for the control of CBB disease. Only two cassava CBB resistance genes have been identified so far (C. Lopez, personal communication, Universidad Nacional, Bogota, Colombia). Plant defence responses to Xam have been well characterized (Fig. 9) (Boher and Verdier, 1995; Boher et al., 1997; Kpémoua et al., 1996). Genomic tools for cassava, such as a large expressed sequence tag (EST) database and a cassava microarray, have been developed and used for Xam–plant expression studies (Lopez et al., 2004, 2005).

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Figure 7. Bacterial blight symptoms caused by Xanthomonas axonopodis pv. manihotis: (A) angular leaf spots (Courtesy of V. Verdier, IRD Montpellier, France); (B) leaf wilting (courtesy of B. Boher, IRD Montpellier, France).

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Figure 8. Scanning electron microscopy showing a large amount of bacteria near the stomata (Courtesy of V. Verdier, IRD Montpellier, France).

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Figure 9. Xanthomonas axonopodis pv. manihotis in xylem vessels (courtesy of B. Boher, IRD Montpellier, France).

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The pathogenicity of Xam relies, in part, on a type III secretion system which translocates effectors into plant cells. A strong effect in Xam pathogenicity has been demonstrated for a small number of effectors, including transcriptional activator-like effector (A. Bernal, personal communication, Universidad de Los Andes, Bogota, Colombia). Different pathotypes of Xam have been reported in different countries in Africa and South America (Restrepo et al., 2000a; Wydra et al., 2004), and studies using DNA fingerprinting methods have shown that Xam pathogen populations are variable both within and across Africa, South America and Asia (Restrepo and Verdier, 1997; Restrepo et al., 2000b; Verdier et al., 1993). In Colombia, the existence of a geographical differentiation of Xam strains in different ecozones has been shown (Restrepo and Verdier, 1997). The exchange of contaminated cassava materials has contributed to the migration of strains and, consequently, has influenced the genetic structure of Xam populations. Climate changes may also influence the genetic diversity and population structure of Xam (Restrepo et al., 2000b).

Xam is considered as a quarantine organism in all countries that grow cassava. A simple and fast procedure has been employed to rapidly identify Xam strains (Ojeda and Verdier, 2000; Verdier et al., 1998), and can easily be implemented to certify plant materials.

Recently, the sequencing of a Xam genome (Colombian strain CIO151) was completed at the Universidad de los Andes (Bogota, Colombia) and the annotation is in progress through the French Xanthomonas consortium (http://www.reseau-xantho.org, http://www.xanthomonas.org). Access to this and subsequent Xam genomes should open up new applications for the comparative and functional genomics of Xam, and will accelerate the development of new molecular typing techniques useful for epidemiological and phylogenetic studies of Xam, as well as diagnostic primers. Much remains to be carried out to improve our ability to combat this economically important plant disease.

7. ERWINIA AMYLOVORA

  1. Top of page
  2. SUMMARY
  3. INTRODUCTION
  4. 1. PSEUDOMONAS SYRINGAE PATHOVARS
  5. 2. RALSTONIA SOLANACEARUM
  6. 3. AGROBACTERIUM TUMEFACIENS
  7. 4. XANTHOMONAS ORYZAE (ORYZAE)
  8. 5. XANTHOMONAS CAMPESTRIS PATHOVARS
  9. 6. XANTHOMONAS AXONOPODIS
  10. 7. ERWINIA AMYLOVORA
  11. 8. XYLELLA FASTIDIOSA
  12. 9. DICKEYA (DADANTII AND SOLANI)
  13. 10. PECTOBACTERIUM CAROTOVORUM (AND P. ATROSEPTICUM)
  14. ACKNOWLEDGEMENTS
  15. REFERENCES

Erwinia amylovora causes fire blight disease of apple, pear, quince, blackberry, raspberry and many wild and cultivated rosaceous ornamentals (Vanneste, 2000). The disease develops sporadically, but, occasionally, it is highly destructive, especially to young fruit trees that may be killed outright by infections that girdle the trunk or the rootstock. The pathogen is distributed widely in temperate regions in which rosaceous plants thrive. It was described initially as Micrococcus amylovorus, and then Bacillus amylovorus (Burrill), under the erroneous assumption that it destroys starch. It is Gram negative, rod shaped and motile with peritrichous flagella. It was renamed Erwinia amylovora (Burrill) Winslow et al. in the early 1900s and remains the type species of the genus (Lelliott and Dickey, 1984). Closely related bacteria that elicit symptoms reminiscent of fire blight, particularly, but not exclusively, in pear, have been described as new species, e.g. E. pyrifoliae (Kim et al., 1999) and E. piriflorinigrans (Lopez et al., 2011).

Erwinia amylovora is of great historical importance to phytobacteriologists in that it was the first bacterium clearly demonstrated to cause disease in plants shortly after the pioneering work of Pasteur and Koch on bacterial pathogens of humans and animals in the late 1800s (see Griffith et al., 2003 for the pioneering papers of Burrill, Arthur and Waite). Thus, E. amylovora is justifiably referred to as the ‘premier phytopathogenic bacterium’.

Symptoms of fire blight were first reported from orchards close to New York City. From there, the pathogen spread westward and across continents, particularly during the 20th century. Although E. amylovora is now widespread, stringent quarantine regulations against the movement of rosaceous plant materials continue, in effect, to prevent the introduction of E. amylovora into areas free, or potentially free, of the pathogen.

The management of fire blight is based on sanitation, cultural practices and the use of a limited number of bactericides and biological control products (Johnson and Stockwell, 1998), mainly to combat blossom blight. An analysis of materials tested for control in recent years in the eastern USA concluded that, in spite of more than two centuries of knowledge and ‘tremendous research efforts, effective control remains an elusive goal’ (Ngugi et al., 2011). Furthermore, streptomycin, which was introduced more than 50 years ago, remains the most effective control material in areas in which sensitive strains of E. amylovora are present. However, in many areas, resistant strains are prevalent or regulations against the use of antibiotics in plant agriculture preclude the use of streptomycin. The development of genetic resistance, particularly in apple rootstocks and scions, holds promise for the future (Norelli et al., 2003).

Interestingly, the genome of E. amylovora is amongst the smallest of the plant pathogenic bacteria sequenced so far, at only 3.89 Mb (Sebaihia et al., 2010). Its small size is consistent with its lack of plant cell-degrading tools, which are common to most other phytopathogenic bacteria, e.g. cell wall-degrading enzymes and low-molecular-weight toxins. Its most important pathological tools appear to be components of the hrp pathogenicity island and the exopolysaccharides amylovoran and levan (Oh and Beer, 2005). The type III secreted proteins DspA/E and HrpN are essential to pathogenicity (Bocsanczy et al., 2008), whereas approximately 20 additional proteins that secrete or regulate the expression of Hrp proteins also play a role. Amylovoran and levan are involved in biofilm formation and pathogenicity (Koczan et al., 2009). Genomes of several strains and species closely related to E. amylovora have become available recently. Bioinformatic comparisons undoubtedly will reveal additional genetic bases for the virulence capability of the fire blight pathogen.

The developing fruits in Fig. 10 exhibit grey–green watersoaking typical of fire blight infection, which precedes necrosis, which is apparent on the dead blossoms at the bottom left and top right of the figure. Several drops of ooze exuding from infected blossoms and fruits, which contain billions of cells in a matrix of polysaccharides and plant sap, should be noted. Blossom cluster infection often leads to devastating losses to pome-fruit growers.

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Figure 10. Apple blossom cluster infected by Erwinia amylovora.

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In Fig. 11, the two outer circles depict the genes of E. amylovora on the forward (outermost) and complementary strands of chromosomal DNA, respectively. The genes in blue have predicted orthologues in E. coli K12, whereas the genes in red do not. Loci coloured orange, yellow and purple are RNA genes. The inner circles depict the predicted orthologous genes of related organisms. Purple and red indicate genes of enterobacterial plant pathogens, orange Yersinia, black E. coli, yellow Shigella, green Salmonella, dark blue enterobacterial endosymbionts (e.g. Sodalis glossinidius) and light blue Pseudomonas syringae. The absence of a particular colour indicates the absence of an orthologue. The innermost circle represents genome coordinates. The two plasmids inside the chromosomal diagram follow the same colour scheme as the two outer circles of the chromosome genome.

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Figure 11. Circular representation of the genome of Erwinia amylovora strain ATCC 49946 (Ea273) and comparison with related genomes. The figure and legend were provided courtesy of Bryan S. Biehl and Nicole T. Perna (University of Wisconsin, MI, USA), and Ana Maria Bocsanczy and Steven V. Beer (Cornell University, Ithaca, NY, USA).

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8. XYLELLA FASTIDIOSA

  1. Top of page
  2. SUMMARY
  3. INTRODUCTION
  4. 1. PSEUDOMONAS SYRINGAE PATHOVARS
  5. 2. RALSTONIA SOLANACEARUM
  6. 3. AGROBACTERIUM TUMEFACIENS
  7. 4. XANTHOMONAS ORYZAE (ORYZAE)
  8. 5. XANTHOMONAS CAMPESTRIS PATHOVARS
  9. 6. XANTHOMONAS AXONOPODIS
  10. 7. ERWINIA AMYLOVORA
  11. 8. XYLELLA FASTIDIOSA
  12. 9. DICKEYA (DADANTII AND SOLANI)
  13. 10. PECTOBACTERIUM CAROTOVORUM (AND P. ATROSEPTICUM)
  14. ACKNOWLEDGEMENTS
  15. REFERENCES

Xylella fastidiosa (Xanthomonadales, Xanthomonadaceae) is a Gram-negative, nonflagellate, xylem-limited and nutritional pathogenic bacterium associated with several important plant diseases, including Pierce's disease of grapevine (PD), citrus variegated chlorosis (CVC) and almond leaf scorch disease (ALSD). Elm, oak, oleander, maple, sycamore, coffee, peach, mulberry, plum, periwinkle, pear and pecan are also other host species of the bacterium. There is only a single species in the genus, but different strains have been well characterized as pathotypes, with cross-infections among different hosts and strains having been reported, but without the development of disease symptoms.

Xylella fastidiosa was the first phytopathogen to have its genome completely sequenced (Simpson et al., 2000). The genome size changes from 2475 to 2731 kb between strains, and consists of a circular chromosome and plasmids. In addition to the pathotype 9a5C (CVC), Temecula-1 (PD) and others (including Dixon, Ann1, M12, M23 and GB514) have now been sequenced completely. Genome-wide analyses among strains have revealed genes unique to each strain (60 of 9a5c, 54 of Dixon, 83 of Ann1 and nine of Temecula-1). Indels and strain-specific genes are the main source of variation among strains. The Pierce's disease strain Temecula-1 genome represents the ancestral genome of X. fastidiosa (Doddapaneni et al., 2006). Over the past 10 years, the increasing number of publications related to genomic information has considerably expanded our knowledge on the bacterium and its pathosystems (Chatterjee et al., 2008).

Xylella fastidiosa does not carry a type III secretion system, and it is therefore assumed that this pathogen does not translocate effectors into plant cells for the elicitation of a host response. This hypothesis is supported by the fact that, in the xylem vessels, there is only fibre and dead cells, and the pathogen is introduced into this tissue by its vector, the sharpshooter leafhopper (Homoptera, Cicadellidae). However, X. fastidiosa has active type I and type II secretion systems, which could be associated with the efflux pump and the secretion of hydrolytic enzymes, respectively, allowing lateral movement of the bacterium through pit membranes and the digestion of plant cell walls.

The development of symptoms in diseases caused by X. fastidiosa is strictly associated with the ability of the bacterium to spread, colonize and block xylem vessels. The colonies grow in biofilms, which can occlude xylem vessels, and reduce water and nutrient transport. The different virulences exhibited by strains of X. fastidiosa are often associated with differences in their abilities to spread, colonize and block xylem vessels. Type I and type IV pili are involved in twitching motility and migration, and attachment and biofilm formation, respectively. Biofilms are important for this pathogen to survive in environments with high turbulence, differential pressure and poor nutrient availability, such as xylem vessels and insect foreguts.12, 13

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Figure 12. Symptoms of citrus variegated chlorosis in leaves and plant of sweet orange (photograph Marcos A. Machado).

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Figure 13. (A, B) Biofilm of Xylella fastidiosa blocking the xylem vessels of sweet orange tree. Photographs in (A) by E.W. Kitajima (Escola Superior de Agricultura Luis de Queiróz, USP, Piracicaba, SP, Brazil) and in (B) by J.O. Lima (Citrulima Viveiros, São João da Boa Vista, SP, Brazil) and Marcos A. Machado.

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9. DICKEYA (DADANTII AND SOLANI)

  1. Top of page
  2. SUMMARY
  3. INTRODUCTION
  4. 1. PSEUDOMONAS SYRINGAE PATHOVARS
  5. 2. RALSTONIA SOLANACEARUM
  6. 3. AGROBACTERIUM TUMEFACIENS
  7. 4. XANTHOMONAS ORYZAE (ORYZAE)
  8. 5. XANTHOMONAS CAMPESTRIS PATHOVARS
  9. 6. XANTHOMONAS AXONOPODIS
  10. 7. ERWINIA AMYLOVORA
  11. 8. XYLELLA FASTIDIOSA
  12. 9. DICKEYA (DADANTII AND SOLANI)
  13. 10. PECTOBACTERIUM CAROTOVORUM (AND P. ATROSEPTICUM)
  14. ACKNOWLEDGEMENTS
  15. REFERENCES

In 1995, Erwinia chrysanthemi was transferred to the new genus Dickeya and divided into six species: D. dianthicola, D. dadantii, D. zeae, D. chrysanthemi, D. paradisiaca and D. dieffenbachiae (Samson et al., 2005). Since then, it has become clear that some strains do not fall into any of these species and may constitute new species, e.g. ‘D. solani’ (Parkinson et al., 2009; Sławiak et al., 2009). All Dickeya spp. cause economically important diseases on different plant hosts worldwide, including 10 monocot and 16 dicot families (Ma et al., 2007; Samson et al., 2005). However, D. dadantii and ‘D. solani’ have been selected here for two very different reasons.

Dickeya dadantii causes disease mainly in tropical and subtropical environments and has a wide host range, including Saintpaulia and potato (Samson et al., 2005) (Fig. 14). The reason for its inclusion is that D. dadantii strain 3937 (Dda3937) has been the Dickeya strain of choice for molecular studies for over 25 years (Diolez and Coleno, 1985). These studies have been instrumental in our understanding of bacterial plant pathogenesis, including the roles of exoenzymes and sugar catabolism, iron transport, secretion and regulation, complementing related studies in other ‘soft rot erwiniae’ (including Pectobacterium carotovorum and P. atrosepticum—see next section) (Hommais et al., 2008; Kazemi-Pour et al., 2004; Lemanceau et al., 2009; Rodionov et al., 2004; Toth et al., 2003; Venkatesh et al., 2006; Yang et al., 2002). Other recent areas of study include plant defence and pathogen response to defence (Antunez-Lamas et al., 2009; Fagard et al., 2007; Li et al., 2009; Segond et al., 2009; Yang et al., 2010), pathogenesis in the pea aphid (Costechareyre et al., 2010) and the interaction between phytopathogens and human pathogens on plants (Yamazaki et al., 2011). The availability of a genome sequence for Dda3937, annotated through an international consortium, combined with functional genomics and systems biology approaches, is furthering our knowledge of this and related pathogens (Babujee et al., 2007; Glasner et al., 2011; Kepseu et al., 2010; Yang et al., 2010) (Fig. 14).

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Figure 14. Artemis screenshot showing reciprocal best hit analysis of coding sequences (CDS) between Pectobacterium atrosepticum (top) and Dickeya dadantii 3937 (bottom). Coloured lines represent orthologues; red, same orientation; blue, opposite orientation.

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The name ‘D. solani’ has not yet been officially accepted. However, the sudden rise to prominence of this ‘species’ in European potato production has made it worthy of inclusion (Fig. 15). The ‘species’ was first recognized on potato around 2005, possibly transferring host from an ornamental plant, and has since spread to many potato-growing regions in Europe and beyond (Sławiak et al., 2009; Toth et al., 2011; Tsror (Lahkim) et al., 2009). Moreover, in some regions, it appears to have displaced existing ‘soft rot’ pathogens, possibly as a result of its increased aggressiveness and/or mode of infection (Czajkowski et al., 2010; Toth et al., 2011) (Fig. 16). In 2010, Scotland became the first country to introduce legislation in an attempt to keep its seed industry free from this pathogen; a strategy that has so far succeeded. ‘D. solani’ causes disease at a range of temperatures, conducive to the current European climate, but also shows increased aggressiveness in warmer conditions, raising concerns that climate change could lead to increased disease problems in the future (Sławiak et al., 2009; Tsror (Lahkim) et al., 2009). Little is known about the biology of ‘D. solani’, but scientists (including those studying Dda3937) are working together to better understand the biology of this pathogen and its control.

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Figure 15. Potato tuber rot caused by ‘Dickeya solani’. Fera crown copyright.

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Figure 16. Dickeya solani’ expressing green fluorescent protein (GFP) on potato roots (courtesy of J. van der Wolf, Plant Research International, Wageningen, the Netherlands).

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10. PECTOBACTERIUM CAROTOVORUM (AND P. ATROSEPTICUM)

  1. Top of page
  2. SUMMARY
  3. INTRODUCTION
  4. 1. PSEUDOMONAS SYRINGAE PATHOVARS
  5. 2. RALSTONIA SOLANACEARUM
  6. 3. AGROBACTERIUM TUMEFACIENS
  7. 4. XANTHOMONAS ORYZAE (ORYZAE)
  8. 5. XANTHOMONAS CAMPESTRIS PATHOVARS
  9. 6. XANTHOMONAS AXONOPODIS
  10. 7. ERWINIA AMYLOVORA
  11. 8. XYLELLA FASTIDIOSA
  12. 9. DICKEYA (DADANTII AND SOLANI)
  13. 10. PECTOBACTERIUM CAROTOVORUM (AND P. ATROSEPTICUM)
  14. ACKNOWLEDGEMENTS
  15. REFERENCES

Pectobacterium carotovorum (Pcc) and Pectobacterium atrosepticum (Pca) were originally classified as Erwinia carotovora subspecies carotovora and subspecies atroseptica, respectively. These species (or subspecies) were members of the soft rot group of erwinias and are taxonomically closely related to Erwinia chrysanthemi (recently reclassified as multiple Dickeya species; see previous section).

Pectobacterium carotovorum is geographically widely distributed, whereas Pca is largely confined to cooler climates (Pérombelon, 2002; Pérombelon and Kelman, 1980; Pérombelon and Salmond, 1995; Salmond, 1992; Toth et al., 2003). Pcc is the aetiological agent of soft rot diseases of several crop plants, and Pca is of particular importance in the commercially important blackleg disease of potato in temperate regions (Fig. 17) (Pérombelon, 2002; Pérombelon and Kelman, 1980). These soft rot pectobacteria were important ‘model’ pathogens in the early days of the genetic analysis of phytopathogenesis. Their taxonomic relatedness to E. coli (family Enterobacteriaceae) allowed the facile transfer, or development, of many genetic tools from E. coli to enable the molecular analysis of virulence (Fig. 18) (see, for example, Diolez and Coleno, 1985; Hinton et al., 1989; Kotoujansky, 1987; Mulholland and Salmond, 1995; Toth et al., 1993, 1997). This genetic tractability underpinned the first studies on the structure and virulence roles of plant cell wall-degrading enzymes (PCWDEs); particularly assorted pectinases, cellulases and proteases (Hinton et al., 1990; Kotoujansky, 1987; Liu et al., 1994). The central catabolic pathway for plant pectin degradation and assimilation by the pathogen was extensively investigated. Moreover, the analysis of the roles of PCWDEs in virulence led to the discovery of the enzyme secretion systems (type I and type II secretory pathways) and the fundamental appreciation that protein secretion systems operate by common mechanisms in molecular pathogenesis across plant and animal pathogens (Evans et al., 2009; Salmond, 1994; Wharam et al., 1995). This acknowledgement of common themes in plant and animal pathogens is now widespread.

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Figure 17. Blackleg disease of potato caused by Pectobacterium atrosepticum. Apparently healthy mother tubers can be seen, but stem rotting is also clear.

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Figure 18. Identification of Pectobacterium mutants affected in potato plant virulence (stem inoculation assays). Left, wild-type; others, reduced virulence.

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In addition to the role of PCWDE synthesis and secretion in virulence, the analysis of PCWDE regulation mechanisms in Pcc uncovered the phenomenon of ‘quorum sensing’ through which the pathogen controls the elaboration of the virulence determinants in concert with bacterial cell population density (Barnard et al., 2007; Coulthurst et al., 2007; Jones et al., 1993; Liu et al., 2008; Pirhonen et al., 1993; Whitehead et al., 2001). The crucial importance of quorum sensing pectobacterial pathogenesis was confirmed by studies on genetically engineered plants (Dong et al., 2001; Toth et al., 2004). Density-dependent control of virulence factors, modulated by freely diffusible N-acyl homoserine lactone intercellular signalling molecules, is now a well-established trait of various plant and animal pathogens (Waters and Bassler, 2005). Furthermore, Pcc was one of the first bacteria shown to produce 1-carbapen-2-em-3-carboxylic acid, a member of the carbapenem class of β-lactam antibiotics, and the production of this antibiotic is co-regulated with the PCWDE virulence factors via quorum sensing (Barnard et al., 2007; Coulthurst et al., 2005). It has been shown by in planta transcriptomic studies that quorum sensing plays an essential role during plant infection in the control of several hundred genes encoding diverse products impacting on the physiology of plant pathogenesis (Liu et al., 2008). These genes encode traits such as multiple protein secretion pathways (including type II, III, IV and VI machines), secondary metabolite production and an interesting selection of proteins of unknown function. Studies on PCWDE regulation have also demonstrated a key role for post-transcriptional control of gene expression via the RsmAB system (Liu et al., 1998; Mukherjee et al., 2000), another regulatory system that has been shown to occur in other plant and animal pathogens.

Pectobacterium atrosepticum was the first enterobacterial phytopathogen to be genomically sequenced and, at the time, this uncovered various unexpected predicted traits in the pathogen, including the possession of type IV and type VI secretion machines, the production of new secondary metabolite toxins and nitrogen fixation capability (Bell et al., 2004; Liu et al., 2008; Mattinen et al., 2008). Furthermore, the genome sequence highlighted fascinating evolutionary relationships between this enterobacterial plant pathogen and taxonomically related animal pathogens. In particular, Pca has been shown to carry a series of genomic islands, some of which are obvious loci for virulence, and ecological adaptation genes acquired by horizontal transfer. Genomic information is now available for Pcc strains and other ‘former Erwinia’ species now reclassified in the genus Dickeya (see previous section; Glasner et al., 2008; Ma et al., 2007).

Ecological studies of Pcc (and Pca) have been classically phenomenological (Pérombelon, 2002; Pérombelon and Kelman, 1980). However, recent studies have shown important roles for specific proteins in the possible ecological dissemination of Pcc by insect vectors, such as Drosophila. Interestingly, the fly also benefits from this interaction with the phytopathogen through a stimulation of the insect innate immune system (Basset et al., 2003; Muniz et al., 2007).

Finally, in addition to their agricultural impacts, we should not ignore the long-standing translational significance of Pectobacterium spp. For example, a periplasmic l-asparaginase from soft rotting Pcc is used clinically in the treatment of acute lymphocytic leukaemias and, historically, some related recombinant Erwinia spp have been considered as possible tools for the biotechnological manufacture of vitamin C (Robert-Baudouy, 1991).

REFERENCES

  1. Top of page
  2. SUMMARY
  3. INTRODUCTION
  4. 1. PSEUDOMONAS SYRINGAE PATHOVARS
  5. 2. RALSTONIA SOLANACEARUM
  6. 3. AGROBACTERIUM TUMEFACIENS
  7. 4. XANTHOMONAS ORYZAE (ORYZAE)
  8. 5. XANTHOMONAS CAMPESTRIS PATHOVARS
  9. 6. XANTHOMONAS AXONOPODIS
  10. 7. ERWINIA AMYLOVORA
  11. 8. XYLELLA FASTIDIOSA
  12. 9. DICKEYA (DADANTII AND SOLANI)
  13. 10. PECTOBACTERIUM CAROTOVORUM (AND P. ATROSEPTICUM)
  14. ACKNOWLEDGEMENTS
  15. REFERENCES
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