Pseudomonas syringae

Last updated

Pseudomonas syringae
Pseudomonas syringae cultures.jpg
Cultures of Pseudomonas syringae
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Bacteria
Phylum: Pseudomonadota
Class: Gammaproteobacteria
Order: Pseudomonadales
Family: Pseudomonadaceae
Genus: Pseudomonas
Species:
P. syringae
Binomial name
Pseudomonas syringae
Van Hall, 1904
Type strain
ATCC 19310

CCUG 14279
CFBP 1392
CIP 106698
ICMP 3023
LMG 1247
NCAIM B.01398
NCPPB 281
NRRL B-1631

Contents

Pathovars

P. s. pv. aceris
P. s. pv. aptata
P. s. pv. atrofaciens
P. s. pv. dysoxylis
P. s. pv. japonica
P. s. pv. lapsa
P. s. pv. panici
P. s. pv. papulans
P. s. pv. persicae(Prunier, Luisetti &. Gardan) Young, Dye & Wilkie [1]
P. s. pv. pisi
P. s. pv. syringae
P. s. pv. morsprunorum

Pseudomonas syringae is a rod-shaped, Gram-negative bacterium with polar flagella. As a plant pathogen, it can infect a wide range of species, and exists as over 50 different pathovars, [2] all of which are available to researchers from international culture collections such as the NCPPB, ICMP, and others.

Pseudomonas syringae is a member of the genus Pseudomonas , and based on 16S rRNA analysis, it has been placed in the P. syringae group. [3] It is named after the lilac tree ( Syringa vulgaris ), from which it was first isolated. [4]

A phylogenomic analysis of 494 complete genomes from the entire Pseudomonas genus showed that P. syringae does not form a monophyletic species in the strict sense, but a wider evolutionary group that also included other species as well, such as P. avellanae, P. savastanoi, P. amygdali, and P. cerasi. [5]

Pseudomonas syringae tests negative for arginine dihydrolase and oxidase activity, and forms the polymer levan on sucrose nutrient agar. Many, but not all, strains secrete the lipodepsinonapeptide plant toxin syringomycin, [6] and it owes its yellow fluorescent appearance when cultured in vitro on King's B medium to production of the siderophore pyoverdin. [7]

Pseudomonas syringae also produces ice nucleation active (INA) proteins which cause water (in plants) to freeze at fairly high temperatures (−1.8 to −3.8 °C (28.8 to 25.2 °F)), resulting in injury. [8] Since the 1970s, P. syringae has been implicated as an atmospheric biological ice nucleator, with airborne bacteria serving as cloud condensation nuclei. Recent evidence has suggested the species plays a larger role than previously thought in producing rain and snow. They have also been found in the cores of hailstones, aiding in bioprecipitation. [9] These INA proteins are also used in making artificial snow. [10]

Pseudomonas syringae pathogenesis is dependent on effector proteins secreted into the plant cell by the bacterial type III secretion system. Nearly 60 different type III effector families encoded by hop genes have been identified in P. syringae. [11] Type III effectors contribute to pathogenesis chiefly through their role in suppressing plant defense. Owing to early availability of the genome sequence for three P. syringae strains and the ability of selected strains to cause disease on well-characterized host plants, including Arabidopsis thaliana , Nicotiana benthamiana , and the tomato, P. syringae has come to represent an important model system for experimental characterization of the molecular dynamics of plant-pathogen interactions. [12]

Bacterial speck on tomato in Upstate New York Smart-tomato-speck.JPG
Bacterial speck on tomato in Upstate New York
Tomato plant leaf infected with bacterial speck Collmer leaf speck3.jpg
Tomato plant leaf infected with bacterial speck

History

In 1961, Paul Hoppe of the U.S. Department of Agriculture studied a corn fungus by grinding up infected leaves each season, then applying the powder to test corn for the following season to track the disease. [13] A surprise frost occurred that year, leaving peculiar results. Only plants infected with the diseased powder incurred frost damage, leaving healthy plants unfrozen. This phenomenon baffled scientists until graduate student Steven E. Lindow of the University of Wisconsin–Madison with D.C. Arny and C. Upper found a bacterium in the dried leaf powder in the early 1970s. [14] Steven E. Lindow, now a plant pathologist at the University of California, Berkeley, found that when this particular bacterium was introduced to plants where it is originally absent, the plants became very vulnerable to frost damage. He went on to identify the bacterium as P. syringae, investigate the role of P. syringae in ice nucleation and in 1977, discover the mutant ice-minus strain. He was later successful at producing the ice-minus strain of P. syringae through recombinant DNA technology, as well. [15]

Genomics

Based on a comparative genomic and phylogenomic analysis of 494 complete genomes from the entire Pseudomonas genus, P. syringae does not form a monophyletic species in the strict sense, but a wider evolutionary group (34 genomes in total, organized into 3 subgroups) that includes other species as well. [5] The core proteome of the P. syringae group comprised 2944 proteins, whereas the protein count and GC content of the strains of this group ranged between 4973 and 6026 (average: 5465) and between 58 and 59.3% (average: 58.6%), respectively. [5]

Disease cycle

Pseudomonas syringae overwinters on infected plant tissues such as regions of necrosis or gummosis (sap oozing from wounds on the tree) but can also overwinter in healthy looking plant tissues. In the spring, water from rain or other sources will wash the bacteria onto leaves/blossoms where it will grow and survive throughout the summer. [16] This is the epiphyte phase of P. syringae’s life cycle where it will multiply and spread but will not cause a disease. Once it enters the plant through a leaf's stomata or necrotic spots on either leaves or woody tissue then the disease will start. [17] The pathogen will then exploit and grow in intercellular space causing the leaf spots and cankers. P. syringae can also survive in temperatures slightly below freezing. These below freezing temperatures increase the severity of infection within trees like sour cherry, apricot, and peach. [16]

Epidemiology

Diseases caused by P. syringae tend to be favoured by wet, cool conditions—optimum temperatures for disease tend to be around 12–25 °C (54–77 °F), although this can vary according to the pathovar involved. The bacteria tend to be seed-borne, and are dispersed between plants by rain splash. [18]

Although it is a plant pathogen, it can also live as a saprotroph in the phyllosphere when conditions are not favourable for disease. [19] Some saprotrophic strains of P. syringae have been used as biocontrol agents against postharvest rots. [20]

Mechanisms of pathogenicity

The mechanisms of P. syringae pathogenicity can be separated into several categories: ability to invade a plant, ability to overcome host resistance, biofilm formation, and production of proteins with ice-nucleating properties. [21]

Ability to invade plants

Planktonic P. syringae is able to enter plants using its flagella and pili to swim towards a target host. It enters the plant via wounds of natural opening sites, as it is not able to breach the plant cell wall. An example of this is the partnership with the leaf-mining fly Scaptomyza flava , which creates holes in leaves during oviposition that the pathogen can take advantage of. [22] The role of taxis in P. syringae has not been well-studied, but the bacteria are thought to use chemical signals released by the plant to find their host and cause infection. [21]

Overcoming host resistance

Effectors

Pseudomonas syringae isolates carry a range of virulence factors called type III secretion system (T3SS) effector proteins. These proteins primarily function to cause disease symptoms and manipulate the host's immune response to facilitate infection. The major family of T3SS effectors in P. syringae is the hrp gene cluster, coding for the Hrp secretion apparatus. [21]

Hop effectors

HopZ1s are type III effectors which interfere with the Glycine max 2-hydroxyisoflavanone dehydratase ( GmHID1 ). HopZ1b degrades daidzein after production, reducing concentrations and thus reducing the immunity it provides the plant. [23]

Phytotoxins

The pathogens also produce phytotoxins which injure the plant and can suppress the host immune system. One such phytotoxin is coronatine, found in pathovars Pto and Pgl. [21]

Elicitors

Pst DC3000 produces a PsINF1 , the INF1 in P. syringae. Hosts respond with autophagy upon detection of this elicitor. Liu et al. 2005 finds this to be the only alternative to mass hypersensitivity leading to mass programmed cell death. [24]

Biofilm formation

Pseudomonas syringae produces polysaccharides which allow it to adhere to the surface of plant cells. It also releases quorum sensing molecules, which allows it to sense the presence of other bacterial cells nearby. If these molecules pass a threshold level, the bacteria change their pattern of gene expression to form a biofilm and begin expression of virulence-related genes. The bacteria secrete highly viscous compounds such as polysaccharides and DNA to create a protective environment in which to grow. [21]

Ice-nucleating properties

Pseudomonas syringae—more than any mineral or other organism—is responsible for the surface frost damage in plants [25] exposed to the environment. For plants without antifreeze proteins, frost damage usually occurs between −4 and −12 °C (25 and 10 °F) as the water in plant tissue can remain in a supercooled liquid state. P. syringae can cause water to freeze at temperatures as high as −1.8 °C (28.8 °F), [26] but strains causing ice nucleation at lower temperatures (down to −8 °C (18 °F)) are more common. [27] The freezing causes injuries in the epithelia and makes the nutrients in the underlying plant tissues available to the bacteria.[ citation needed ]

Pseudomonas syringae has ina (ice nucleation-active) genes that make INA proteins which translocate to the outer bacterial membrane on the surface of the bacteria, where the proteins act as nuclei for ice formation. [27] Artificial strains of P. syringae known as ice-minus bacteria have been created to reduce frost damage.[ citation needed ]

Pseudomonas syringae has been found in the center of hailstones, suggesting the bacterium may play a role in Earth's hydrological cycle. [9]

Management

Currently there is not a 100% effective way to eradicate P. syringae from a field. The most common way to control this pathogen is to spray bactericides with copper compounds or other heavy metals that can be combined with fungicides or other pest control chemicals. Chemical treatments with fixed copper such as Bordeaux, copper hydroxide, and cupric sulfate are used to stop the spread of P. syringae by killing the bacteria while it is in the epiphyte stage on leaves, or woody parts of trees - however resistant P. syringae strains do exist. [28] Spraying antibiotics such as streptomycin and organic bactericides is another way to control P. syringae but is less common than the methods listed above. [29]  

New research has shown that adding ammonium (NH4+) nutrition to tomato plants can cause a metabolic change leading to resistance against Pseudomonas syringae. This "ammonium syndrome" causes nutrient imbalances in the plant and therefore triggers a defense response against the pathogen. [30]

Strict hygiene practices used in orchards along with pruning in early spring and summer were proven to make the trees more resistant to P. syringae. Cauterizing cankers found on orchard trees can save the tree's life by stopping the infection from spreading. [31]

Breeding plants for resistance is another somewhat effective way to avoid P. syringae. It has been successful in the cherry rootstock with Pseudomonas syringae pv. syringae, but so far, no other species are 100% resistant to this pathogen. Resistance breeding is a slow process, especially in trees. Unfortunately, P. syringae bacteria can adapt genetically to infect resistant plants, and the process for resistance breeding has to start over again.

A combination treatment of bacteriophage and carvacrol shows promise in control of both the planktonic and biofilm forms. [32]

Pathovars

Following ribotype analysis, incorporation of several pathovars of P. syringae into other species was proposed [33] (see P. amygdali , 'P. tomato' , P. coronafaciens , P. avellanae , 'P. helianthi' , P. tremae , P. cannabina , and P. viridiflava ). According to this schema, the remaining pathovars are:

However, many of the strains for which new species groupings were proposed continue to be referred to in the scientific literature as pathovars of P. syringae, including pathovars tomato, phaseolicola, and maculicola. Pseudomonas savastanoi was once considered a pathovar or subspecies of P. syringae, and in many places continues to be referred to as P. s. pv. savastanoi, although as a result of DNA-relatedness studies, it has been instated as a new species. [33] It has three host-specific pathovars: P. s.fraxini (which causes ash canker), P. s.nerii (which attacks oleander), and P. s.oleae (which causes olive knot).

Determinants of host specificity

A combination of the pathogen's effector genes and the plant's resistance genes is thought to determine which species a particular pathovar can infect. Plants can develop resistance to a pathovar by recognising pathogen-associated molecular patterns (PAMPs) and launching an immune response. These PAMPs are necessary for the microbe to function, so cannot be lost, but the pathogen may find ways to suppress this immune response, leading to an evolutionary arms race between the pathogen and the host. [21] [38]

Pseudomonas syringae as a model system

Owing to early availability of genome sequences for P. syringae pv. tomato strain DC3000, P. syringae pv. syringae strain B728a, and P. syringae pv. phaseolicola strain 1448A, together with the ability of selected strains to cause disease on well-characterized host plants such as Arabidopsis thaliana , Nicotiana benthamiana , and tomato, P. syringae has come to represent an important model system for experimental characterization of the molecular dynamics of plant-pathogen interactions. [39] The P. syringae experimental system has been a source of pioneering evidence for the important role of pathogen gene products in suppressing plant defense. The nomenclature system developed for P. syringae effectors has been adopted by researchers characterizing effector repertoires in other bacteria, [40] and methods used for bioinformatic effector identification have been adapted for other organisms. In addition, researchers working with P. syringae have played an integral role in the Plant-Associated Microbe Gene Ontology working group, aimed at developing gene ontology terms that capture biological processes occurring during the interactions between organisms, and using the terms for annotation of gene products. [41]

Pseudomonas syringae pv. tomato strain DC3000 and Arabidopsis thaliana

As mentioned above, the genome of P. syringae pv. tomato DC3000 has been sequenced, [42] and approximately 40 Hop (Hrp Outer Protein) effectors - pathogenic proteins that attenuate the host cell - have been identified. [43] These 40 effectors are not recognized by A. thaliana thus making P. syringae pv. tomato DC3000 virulent against it - that is, P. syringae pv. tomato DC3000 is able to infect A. thaliana - thus A. thaliana is susceptible to this pathogen.[ citation needed ]

Many gene-for-gene relationships have been identified using the two model organisms, P. syringae pv. tomato strain DC3000 and Arabidopsis. The gene-for-gene relationship describes the recognition of pathogenic avirulence (avr) genes by host resistance genes (R-genes). P. syringae pv. tomato DC3000 is a useful tool for studying avr: R-gene interactions in A. thaliana because it can be transformed with avr genes from other bacterial pathogens, and furthermore, because none of the endogenous hops genes is recognized by A. thaliana, any observed avr recognition identified using this model can be attributed to recognition of the introduced avr by A. thaliana. [44] The transformation of P. syringae pv. tomato DC3000 with effectors from other pathogens have led to the identification of many R-genes in Arabidopsis to further advance knowledge of plant pathogen interactions.

Examples of avr genes in P. syringae DC3000 and A. thaliana R-genes that recognize them
Avr geneA. thaliana R-gene
AvrB RPM1
AvrRpm1RPM1
AvrRpt2 RPS2
AvrRps4RPS4
AvrRps6RPS6
AvrPphB [45] [46] RPS5/RESISTANCE TO PSEUDOMONAS SYRINGAE 5 (see also Arabidopsis thaliana § RPS5) [45] [47] [46]

The Dynamin-related protein 2b/drp2b gene in A. thaliana is not directly an immunity gene, but by helping move external material into the intracellular network is indirectly related, and some mutants increase susceptibility. [48]

Pseudomonas syringae pv. tomato strain DC3000, its derivatives, and its tomato host

As its name suggests, P. syringae pv. tomato DC3000 (Pst DC3000) is virulent to tomato ( Solanum lycopersicum ). However, the tomato cultivar Rio Grande-PtoR (RG-PtoR), harboring the resistance gene Pto, recognizes key effectors secreted by Pst DC3000, making it resistant to the bacteria. [49] Studying the interactions between the Pto-expressing tomato lines and Pst DC3000 and its pathovars is a powerful system for understanding plant-microbe interactions. [50] [51]

Like other plants, the tomato has a two-tier pathogen defense system. The first and more universal line of plant defense, pattern-triggered immunity (PTI), is activated when plant pattern recognition receptors (PRRs) on the cell surface bind to pathogen-associated molecular patterns (PAMPs). [52] The other branch of plant immunity, effector-triggered immunity (ETI), is triggered when intracellular (Nucleotide-binding site, Leucine-rich repeat) NB-LRR proteins bind to an effector, a molecule specific to a particular pathogen. ETI is generally more severe than PTI, and when a threshold of defense activation is reached, it can trigger a hypersensitive response (HR), which is purposeful death of host tissue to prevent the spread of infection. [52] Two key effectors secreted by Pst DC3000 are AvrPto and AvrPtoB, which initiate ETI by binding the Pto/Prf receptor complex in Pto-expressing tomato lines like RG-PtoR. [53]

Pst DC3000 has been modified to create the mutant strain Pst DC3000∆avrPto∆avrPtoB (Pst DC3000∆∆), which expresses neither AvrPto nor AvrPtoB. By infecting RG-PtoR with Pst DC3000∆∆, ETI to the pathogen is not triggered due to the absence of the main effectors recognized by the Pto/Prf complex. [54] [55] In the lab this is highly valuable, as using Pst DC3000∆∆ allows researchers to study the function of PTI-candidate genes in RG-PtoR, which would otherwise be masked by ETI. [53] [56]

Another useful DC3000 derivative is Pst DC3000∆avrPto∆avrPtoB∆fliC (Pst DC3000∆∆∆). Like Pst DC3000∆∆, this strain does not express AvrPto and AvrPtoB, but it also has an additional knock-out for fliC, the gene encoding flagellin, whose fragments serve as main PAMPs required for tomato PTI. [57] [58] By comparing plants within the same line that have been infected with either Pst DC3000∆∆ or Pst DC3000∆∆∆, researchers can determine if genes of interest are important to the flagellin recognition pathway of PTI. [58]

By treating CRISPR-induced tomato knockout mutants (in a RG-PtoR background) with Pst DC3000, Pst DC3000∆avrPto∆avrPtoB, or Pst DC3000∆avrPto∆avrPtoB∆fliC has led to the characterization of key components of the tomato immune system and continues to be used to further the field of tomato pathology.

Importance

Pseudomonas syringae has impacted many crop and orchard industries with its various pathovars.

P. s. pv. actinidiae

Mesarich et al. 2017 provides several libraries for transposon insertion sequencing of mutants of P. s. a. [59]

The kiwifruit industry in New Zealand has suffered catastrophic losses since their first known outbreak in 2007 from P. syringae pv. actinidiae. [34] New Zealand is second to Italy in the total volume of kiwifruit exports making an annual revenue of $NZ 1 billion, making it the most economically valuable export in the country. In 2014 the loss of exports alone was as high as NZ$930 million. [60] Growers had to pay for treatments, and removal of infected vines along with suffering the loss of capital value in their orchards. For some, the orchard values went from NZ$450,000/ha to $70,000/ha after the outbreak, which is the price of bare land. The total loss of equity for the country of New Zealand was as high as NZ$2 billion. [61]

Between 2010 and 2012 over 2,000 hectares (4,900 acres) of Italian kiwifruit orchards either were killed by P. syringae pv. actinidiae or were killed to contain the disease. The financial consequences for growers and their suppliers were severe, as were the economic consequences more widely. [62]

See also

Related Research Articles

<i>Arabidopsis thaliana</i> Model plant species in the family Brassicaceae

Arabidopsis thaliana, the thale cress, mouse-ear cress or arabidopsis, is a small plant from the mustard family (Brassicaceae), native to Eurasia and Africa. Commonly found along the shoulders of roads and in disturbed land, it is generally considered a weed.

<i>Pseudomonas</i> Genus of Gram-negative bacteria

Pseudomonas is a genus of Gram-negative bacteria belonging to the family Pseudomonadaceae in the class Gammaproteobacteria. The 313 members of the genus demonstrate a great deal of metabolic diversity and consequently are able to colonize a wide range of niches. Their ease of culture in vitro and availability of an increasing number of Pseudomonas strain genome sequences has made the genus an excellent focus for scientific research; the best studied species include P. aeruginosa in its role as an opportunistic human pathogen, the plant pathogen P. syringae, the soil bacterium P. putida, and the plant growth-promoting P. fluorescens, P. lini, P. migulae, and P. graminis.

Phytotoxins are substances that are poisonous or toxic to the growth of plants. Phytotoxic substances may result from human activity, as with herbicides, or they may be produced by plants, by microorganisms, or by naturally occurring chemical reactions.

The gene-for-gene relationship is a concept in plant pathology that plants and their diseases each have single genes that interact with each other during an infection. It was proposed by Harold Henry Flor who was working with rust (Melampsora lini) of flax (Linum usitatissimum). Flor showed that the inheritance of both resistance in the host and parasite ability to cause disease is controlled by pairs of matching genes. One is a plant gene called the resistance (R) gene. The other is a parasite gene called the avirulence (Avr) gene. Plants producing a specific R gene product are resistant towards a pathogen that produces the corresponding Avr gene product. Gene-for-gene relationships are a widespread and very important aspect of plant disease resistance. Another example can be seen with Lactuca serriola versus Bremia lactucae.

<i>Xanthomonas campestris</i> Species of bacterium

Xanthomonas campestris is a gram-negative, obligate aerobic bacterium that is a member of the Xanthomonas genus, which is a group of bacteria that are commonly known for their association with plant disease. This species includes Xanthomonas campestris pv. campestris the cause of black rot of brassicas, one of the most important diseases of brasicas worldwide.

<i>Pseudomonas savastanoi</i> Species of bacterium

Pseudomonas savastanoi is a gram-negative plant pathogenic bacterium that infects a variety of plants. It was once considered a pathovar of Pseudomonas syringae, but following DNA-relatedness studies, it was instated as a new species. It is named after Savastano, a worker who proved between 1887 and 1898 that olive knot are caused by bacteria.

Pseudomonas viridiflava is a fluorescent, Gram-negative, soil bacterium that is pathogenic to plants. It was originally isolated from the dwarf or runner bean, in Switzerland. Based on 16S rRNA analysis, P. viridiflava has been placed in the P. syringae group. Following ribotypical analysis misidentified strains of Pseudomonas syringae pv. ribicola and Pseudomonas syringae pv. primulae were incorporated into this species. This pathogen causes bacterial blight of Kiwifruit.

Pseudomonas amygdali is a Gram-negative plant pathogenic bacterium. It is named after its ability to cause disease on almond trees. Different analyses, including 16S rRNA analysis, DNA-DNA hybridization, and MLST clearly placed P. amygdali in the P. syringae group together with the species Pseudomonas ficuserectae and Pseudomonas meliae, and 27 pathovars of Pseudomonas syringae/Pseudomonas savastanoi, constituting a single, well-defined phylogenetic group which should be considered as a single species. This phylogenetic group has not been formally named because of the lack of reliable means to differentiate it phenotypically from closely related species, and it is currently known as either genomospecies 2 or phylogroup 3. When it is formally named, the correct name for this new species should be Pseudomonas amygdali, which takes precedence over all the other names of taxa from this group, including Pseudomonas savastanoi, which is and inadequate and confusing name whose use is not recommended.

<i>Pseudomonas cannabina</i> Species of bacterium

Pseudomonas cannabina is a gray, Gram-negative, fluorescent, motile, flagellated, aerobic bacterium that causes leaf and stem rot of hemp, from which it derives its name. It was formerly classified as a pathovar of Pseudomonas syringae, but following ribotypical analysis, it was reinstated as a species. The type strain is CFBP 2341.

<i>Ralstonia solanacearum</i> Disease bacteria of tomato family, others

Ralstonia solanacearum is an aerobic non-spore-forming, Gram-negative, plant pathogenic bacterium. R. solanacearum is soil-borne and motile with a polar flagellar tuft. It colonises the xylem, causing bacterial wilt in a very wide range of potential host plants. It is known as Granville wilt when it occurs in tobacco. Bacterial wilts of tomato, pepper, eggplant, and Irish potato caused by R. solanacearum were among the first diseases that Erwin Frink Smith proved to be caused by a bacterial pathogen. Because of its devastating lethality, R. solanacearum is now one of the more intensively studied phytopathogenic bacteria, and bacterial wilt of tomato is a model system for investigating mechanisms of pathogenesis. Ralstonia was until recently classified as Pseudomonas, with similarity in most aspects, except that it does not produce fluorescent pigment like Pseudomonas. The genomes from different strains vary from 5.5 Mb up to 6 Mb, roughly being 3.5 Mb of a chromosome and 2 Mb of a megaplasmid. While the strain GMI1000 was one of the first phytopathogenic bacteria to have its genome completed, the strain UY031 was the first R. solanacearum to have its methylome reported. Within the R. solanacearum species complex, the four major monophyletic clusters of strains are termed phylotypes, that are geographically distinct: phylotypes I-IV are found in Asia, the Americas, Africa, and Oceania, respectively.

<i>Xanthomonas</i> Genus of bacteria

Xanthomonas is a genus of bacteria, many of which cause plant diseases. There are at least 27 plant associated Xanthomonas spp., that all together infect at least 400 plant species. Different species typically have specific host and/or tissue range and colonization strategies.

<i>Pseudomonas tomato</i> Species of bacterium

"Pseudomonas tomato" is a Gram-negative plant pathogenic bacterium that infects a variety of plants. It was once considered a pathovar of Pseudomonas syringae, but following DNA-relatedness studies, it was recognized as a separate species and several other former P. syringae pathovars were incorporated into it. Since no official name has yet been given, it is referred to by the epithet 'Pseudomonas tomato' .

Bioprecipitation is the concept of rain-making bacteria and was proposed by David Sands from Montana State University in the 1970s. This is precipitation that is beneficial for microbial and plant growth, it is a feedback cycle beginning with land plants generating small air-borne particles call aerosols that contain microorganisms that influences the formation of clouds by their ice nucleation properties. The formation of ice in clouds is required for snow and most rainfall. Dust and soot particles can serve as ice nuclei, but biological ice nuclei are capable of catalyzing freezing at much warmer temperatures. The ice-nucleating bacteria currently known are mostly plant pathogens. Recent research suggests that bacteria may be present in clouds as part of an evolved process of dispersal.

<span class="mw-page-title-main">Plant disease resistance</span> Ability of a plant to stand up to trouble

Plant disease resistance protects plants from pathogens in two ways: by pre-formed structures and chemicals, and by infection-induced responses of the immune system. Relative to a susceptible plant, disease resistance is the reduction of pathogen growth on or in the plant, while the term disease tolerance describes plants that exhibit little disease damage despite substantial pathogen levels. Disease outcome is determined by the three-way interaction of the pathogen, the plant and the environmental conditions.

<span class="mw-page-title-main">GyrA RNA motif</span>

The gyrA RNA motif is a conserved RNA structure identified by bioinformatics. The RNAs are present in multiple species of bacteria within the order Pseudomonadales. This order contains the genus Pseudomonas, which includes the opportunistic human pathogen Pseudomonas aeruginosa and Pseudomonas syringae, a plant pathogen.

<span class="mw-page-title-main">RsmX</span>

The rsmX gene is part of the Rsm/Csr family of non-coding RNAs (ncRNAs). Members of the Rsm/Csr family are present in a diverse range of bacteria, including Escherichia coli, Erwinia, Salmonella, Vibrio and Pseudomonas. These ncRNAs act by sequestering translational repressor proteins, called RsmA, activating expression of downstream genes that would normally be blocked by the repressors. Sequestering of target proteins is dependent upon exposed GGA motifs in the stem loops of the ncRNAs. Typically, the activated genes are involved in secondary metabolism, biofilm formation and motility.

<span class="mw-page-title-main">CrcZ</span>

CrcZ is a small RNA found in Pseudomonas bacteria, which acts as a global regulator of carbon catabolite repression. In P. aeruginosa, CrcZ is responsible for sequestering the protein Crc. Crc is an RNA-binding global regulator, which acts by inhibiting the translation of the transcriptional regulator AlkS.

Guard theory is a branch of immunology which concerns the innate sensing of stereotypical consequences of a virulence factor or pathogen. This is in contrast to the classical understanding of recognition by the innate immune system, which involves recognition of distinct microbial structures- pathogen-associated molecular patterns (PAMPs)- with pattern recognition receptors (PRRs). Some of these stereotypical consequences of virulence factors and pathogens may include altered endosomal trafficking and changes in the cytoskeleton. These recognition mechanisms would work to complement classical pattern recognition mechanisms.

<span class="mw-page-title-main">Bacterial blight of soybean</span> Bacterial plant disease

Bacterial blight of soybean is a widespread disease of soybeans caused by Pseudomonas syringaepv. glycinea.

AvrPphB SUSCEPTIBLE 1/PBS1 is a protein kinase acting upon serine and threonine. It is a receptor-like cytoplasmic kinase, of Subfamily VII. It is the guardee of RESISTANCE TO PSEUDOMONAS SYRINGAE 5/RPS5. PBS1 is cleaved by an effector, AvrPphB, used by Pseudomonas syringae pv. phaseolicola, serving as an immunological decoy to signal RPS5 that an attack is underway as reviewed by Kourelis et al. 2016.

References

  1. 1 2 "Pseudomonas syringae pv. persicae (PSDMPE)[Overview]". Global Database. EPPO (European and Mediterranean Plant Protection Organization). 28 January 2001. Retrieved 22 March 2022.
  2. ↑ Arnold, DL; Preston, GM (2019). "Pseudomonas syringae: enterprising epiphyte and stealthy parasite". Microbiology. 165 (3): 251–53. doi: 10.1099/mic.0.000715 . PMID   30427303.
  3. ↑ Anzai, Y; Kim, H; Park, JY; Wakabayashi, H; Oyaizu, H (2000). "Phylogenetic affiliation of the pseudomonads based on 16S rRNA sequence". International Journal of Systematic and Evolutionary Microbiology. 50 (4): 1563–89. doi:10.1099/00207713-50-4-1563. PMID   10939664.
  4. ↑ Kreig, N. R.; Holt, J. G., eds. (1984). Bergey's Manual of Systematic Biology. Baltimore: Williams and Wilkins. pp. 141–99.
  5. 1 2 3 Nikolaidis, Marios; Mossialos, Dimitris; Oliver, Stephen G.; Amoutzias, Grigorios D. (August 2020). "Comparative Analysis of the Core Proteomes among the Pseudomonas Major Evolutionary Groups Reveals Species-Specific Adaptations for Pseudomonas aeruginosa and Pseudomonas chlororaphis". Diversity. 12 (8): 289. doi: 10.3390/d12080289 .
  6. ↑ Scholz-Schroeder, Brenda K.; Soule, Jonathan D.; Gross, Dennis C. (2003). "The sypA, sypB, and sypC Synthetase Genes Encode Twenty-Two Modules Involved in the Nonribosomal Peptide Synthesis of Syringopeptin by Pseudomonas syringae pv. syringae B301D". Molecular Plant-Microbe Interactions. 16 (4): 271–80. doi: 10.1094/MPMI.2003.16.4.271 . PMID   12744455.
  7. ↑ Cody, YS; Gross, DC (1987). "Characterization of Pyoverdin(pss), the Fluorescent Siderophore Produced by Pseudomonas syringae pv. syringae". Applied and Environmental Microbiology. 53 (5): 928–34. Bibcode:1987ApEnM..53..928C. doi:10.1128/AEM.53.5.928-934.1987. PMC   203788 . PMID   16347352.
  8. ↑ Maki, Leroy (September 1974). "Ice Nucleation Induced by Pseudomonas syringae". Applied Microbiology. 28 (3): 456–59. doi:10.1128/AEM.28.3.456-459.1974. PMC   186742 . PMID   4371331.
  9. 1 2 Palmer, Jason (25 May 2011). "Bacteria-rich hailstones add to 'bioprecipitation' idea". BBC News.
  10. ↑ Robbins, Jim (24 May 2010). "From Trees and Grass, Bacteria That Cause Snow and Rain". The New York Times.
  11. ↑ "PPI home – Pseudomonas-Plant Interaction – Pseudomonas syringae Genome Resources Home Page". Cornell University & National Science Foundation & USDA ARS. 3 September 2010. Retrieved 22 March 2022.
  12. ↑ Mansfield, John (2012). "Top 10 plant pathogenic bacteria in molecular plant pathology". Molecular Plant Pathology. 13 (6): 614–29. doi:10.1111/j.1364-3703.2012.00804.x. PMC   6638704 . PMID   22672649.
  13. ↑ Parrott, Carolyn C. (1993). "Recombinant DNA to Protect Crops". Archived from the original on 18 September 2012.
  14. ↑ Lindow, Steven E.; Arny, Deane C.; Upper, Christen D. (1 October 1982). "Bacterial Ice Nucleation: A Factor in Frost Injury to Plants". Plant Physiology. 70 (4). American Society of Plant Biologists (ASPB): 1084–1089. doi:10.1104/pp.70.4.1084. ISSN   0032-0889. PMC   1065830 . PMID   16662618.
  15. ↑ Hynes, H. Patricia (1989). "Biotechnology in agriculture: an analysis of selected technologies and policy in the United States" (PDF). Reproductive and Genetic Engineering. 2 (1): 39–49. Archived from the original (PDF) on 4 December 2014. Retrieved 3 September 2012.
  16. 1 2 Kennelly, Megan M.; Cazorla, Francisco M.; de Vicente, Antonio; Ramos, Cayo; Sundin, George W. (January 2007). "Pseudomonas syringae Diseases of Fruit Trees: Progress Toward Understanding and Control". Plant Disease. 91 (1): 4–17. doi: 10.1094/PD-91-0004 . ISSN   0191-2917. PMID   30781059.
  17. ↑ Jeong, R.-D.; Chu, E.-H.; Lee, G.W.; Park, J.M.; Park, H.-J. (24 March 2016). "Effect of gamma irradiation on Pseudomonas syringae pv. tomato DC3000 – short communication". Plant Protection Science. 52 (2): 107–12. doi: 10.17221/68/2015-pps . ISSN   1212-2580.
  18. ↑ Hirano, S S; Upper, C D (1990). "Population Biology and Epidemiology of Pseudomonas Syringae". Annual Review of Phytopathology. 28: 155–77. doi:10.1146/annurev.py.28.090190.001103.
  19. ↑ Hirano, S. S.; Upper, C. D. (2000). "Bacteria in the Leaf Ecosystem with Emphasis on Pseudomonas syringae---a Pathogen, Ice Nucleus, and Epiphyte". Microbiology and Molecular Biology Reviews. 64 (3): 624–53. doi:10.1128/MMBR.64.3.624-653.2000. PMC   99007 . PMID   10974129.
  20. ↑ Janisiewicz WJ, Marchi A (1992). "Control of Storage Rots on Various Pear Cultivars with a Saprophytic Strain of Pseudomonas syringae". Plant Disease. 76 (6): 555–60. doi:10.1094/pd-76-0555.
  21. 1 2 3 4 5 6 Ichinose, Yuki; Taguchi, Fumiko; Mukaihara, Takafumi (2013). "Pathogenicity and virulence factors of Pseudomonas syringae". J Gen Plant Pathol. 79 (5): 285–296. doi:10.1007/s10327-013-0452-8. S2CID   17519705.
  22. ↑ Groen, Simon C.; Humphrey, Parris T.; Chevasco, Daniela; Ausubel, Frederick M.; Pierce, Naomi E.; Whiteman, Noah K. (1 January 2016). "Pseudomonas syringae enhances herbivory by suppressing the reactive oxygen burst in Arabidopsis". Journal of Insect Physiology. plant-reprogramming insects: from effector molecules to ecosystem engineering. 84: 90–102. doi:10.1016/j.jinsphys.2015.07.011. ISSN   0022-1910. PMC   4721946 . PMID   26205072.
  23. ↑ Bauters, Lander; Stojilković, Boris; Gheysen, Godelieve (19 August 2021). "Pathogens pulling the strings: Effectors manipulating salicylic acid and phenylpropanoid biosynthesis in plants". Molecular Plant Pathology . 22 (11): 1436–1448. doi: 10.1111/mpp.13123 . ISSN   1464-6722. PMC   8518561 . PMID   34414650.
  24. ↑ Yang, Meng; Ismayil, Asigul; Liu, Yule (29 September 2020). "Autophagy in Plant-Virus Interactions". Annual Review of Virology . 7 (1). Annual Reviews: 403–419. doi:10.1146/annurev-virology-010220-054709. ISSN   2327-056X. PMID   32530794. S2CID   219621432.
  25. ↑ Hirano, Susan S.; Upper, Christen D. (1995). "Ecology of Ice Nucleation – Active Bacteria". In Lee, Richard E.; Warren, Gareth J.; Gusta, L. V. (eds.). Biological Ice Nucleation and Its Applications. St. Paul, Minnesota: American Phytopathological Society. pp. 41–61. ISBN   978-0-89054-172-2.
  26. ↑ Maki, LR; Galyan, EL; Chang-Chien, MM; Caldwell, DR (1974). "Ice nucleation induced by Pseudomonas syringae". Applied Microbiology. 28 (3): 456–59. doi:10.1128/AEM.28.3.456-459.1974. PMC   186742 . PMID   4371331.
  27. 1 2 Fall, Ray; Wolber, Paul K. (1995). "Biochemistry of Bacterial Ice Nuclei". In Lee, Richard E.; Warren, Gareth J.; Gusta, L. V. (eds.). Biological Ice Nucleation and Its Applications. St. Paul, Minnesota: American Phytopathological Society. pp. 63–83. ISBN   978-0-89054-172-2.
  28. ↑ Cazorla, Francisco M.; Arrebola, Eva; Sesma, Ane; Pérez-García, Alejandro; Codina, Juan C.; Murillo, Jesús; de Vicente, Antonio (2002). "Copper Resistance in Pseudomonas syringae Strains Isolated from Mango Is Encoded Mainly by Plasmids". Phytopathology. 92 (8). Scientific Societies: 909–916. doi: 10.1094/phyto.2002.92.8.909 . ISSN   0031-949X. PMID   18942971.
  29. ↑ Bashan, Yoav (1997), "Alternative Strategies for Controlling Plant Diseases Caused by Pseudomonas syringae", in Rudolph, K.; Burr, T. J.; Mansfield, J. W.; Stead, D. (eds.), Pseudomonas Syringae Pathovars and Related Pathogens, Developments in Plant Pathology, vol. 9, Springer Netherlands, pp. 575–83, doi:10.1007/978-94-011-5472-7_105, ISBN   978-94-010-6301-2
  30. ↑ González-Hernández, Ana Isabel; Fernández-Crespo, Emma; Scalschi, Loredana; Hajirezaei, Mohammad-Reza; von Wirén, Nicolaus; García-Agustín, Pilar; Camañes, Gemma (August 2019). "Ammonium mediated changes in carbon and nitrogen metabolisms induce resistance against Pseudomonas syringae in tomato plants". Journal of Plant Physiology. 239: 28–37. doi:10.1016/j.jplph.2019.05.009. PMID   31177028. S2CID   182543294.
  31. ↑ "Diseases Caused by Pseudomonas syringe". Pacific Northwest Pest Management Handbooks. 10 September 2015. Retrieved 11 December 2019.
  32. ↑ Ni, Peien; Wang, Lei; Deng, Bohan; Jiu, Songtao; Ma, Chao; Zhang, Caixi; Almeida, Adelaide; Wang, Dapeng; Xu, Wenping; Wang, Shiping (2 June 2020). "Combined Application of Bacteriophages and Carvacrol in the Control of Pseudomonas syringae pv. actinidiae Planktonic and Biofilm Forms". Microorganisms. 8 (6). MDPI AG: 837. doi: 10.3390/microorganisms8060837 . ISSN   2076-2607. PMC   7356356 . PMID   32498472.
  33. 1 2 Gardan, L.; Shafik, H.; Belouin, S.; Broch, R.; Grimont, F.; Grimont, P. A. D. (1999). "DNA relatedness among the pathovars of Pseudomonas syringae and description of Pseudomonas tremae sp. nov. and Pseudomonas cannabina sp. nov. (ex Sutic and Dowson 1959)". International Journal of Systematic Bacteriology. 49 (2): 469–78. doi: 10.1099/00207713-49-2-469 . PMID   10319466.
  34. 1 2 "Pseudomonas syringae pv. actinidiae (PSDMAK)[Overview]". Global Database. EPPO (European and Mediterranean Plant Protection Organization). 7 February 2008. Retrieved 13 July 2021.
  35. ↑ Di Lallo G, Evangelisti M, Mancuso F, Ferrante P, Marcelletti S, Tinari A, Superti F, Migliore L, D'Addabbo P, Frezza D, Scortichini M, Thaller MC (2014). "Isolation and partial characterization of bacteriophages infecting Pseudomonas syringae pv. actinidiae, causal agent of kiwifruit bacterial canker" (PDF). J. Basic Microbiol. 54 (11): 1210–21. doi:10.1002/jobm.201300951. hdl: 2108/92348 . PMID   24810619. S2CID   11456671.
  36. ↑ "Bleeding Canker of Horse Chestnut". UK Forestry Commission. Archived from the original on 17 December 2010. Retrieved 24 January 2011.
  37. ↑ Bennett, J. Michael; Hicks, Dale R.; Naeve, Seth L.; Bennett, Nancy Bush (2014). The Minnesota Soybean Field Book (PDF). St Paul, MN: University of Minnesota Extension. p. 84. Archived from the original (PDF) on 30 September 2013. Retrieved 21 February 2016.
  38. ↑ Baltrus, David; Nishimura, Marc; Dougherty, Kevin; Biswas, Surojit; Mukhtar, M. Shahid; Vicente, Joana; Holub, Eric; Jeffery, Dangl (2012). "The Molecular Basis of Host Specialization in Bean Pathovars of Pseudomonas syringae" (PDF). Molecular Plant-Microbe Interactions . 25 (7): 877–88. doi: 10.1094/mpmi-08-11-0218 . PMID   22414441.
  39. ↑ Mansfield, John W. (2009). "From bacterial avirulence genes to effector functions via thehrpdelivery system: an overview of 25 years of progress in our understanding of plant innate immunity". Molecular Plant Pathology. 10 (6): 721–34. doi:10.1111/j.1364-3703.2009.00576.x. PMC   6640528 . PMID   19849780.
  40. ↑ Tobe, T.; Beatson, S. A.; Taniguchi, H.; Abe, H.; Bailey, C. M.; Fivian, A.; Younis, R.; Matthews, S.; et al. (2006). "An extensive repertoire of type III secretion effectors in Escherichia coli O157 and the role of lambdoid phages in their dissemination". Proceedings of the National Academy of Sciences. 103 (40): 14941–6. Bibcode:2006PNAS..10314941T. doi: 10.1073/pnas.0604891103 . PMC   1595455 . PMID   16990433.
  41. ↑ Torto-Alalibo, T.; Collmer, C. W.; Gwinn-Giglio, M.; Lindeberg, M.; Meng, S.; Chibucos, M. C.; Tseng, T.-T.; Lomax, J.; et al. (2010). "Unifying Themes in Microbial Associations with Animal and Plant Hosts Described Using the Gene Ontology". Microbiology and Molecular Biology Reviews. 74 (4): 479–503. doi:10.1128/MMBR.00017-10. PMC   3008171 . PMID   21119014.
  42. ↑ Buell CR, Joardar V, Lindeberg M, Selengut J, Paulsen IT, Gwinn ML, et al. (2003). "The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000". Proc. Natl. Acad. Sci. U.S.A. 100 (18): 10181–86. Bibcode:2003PNAS..10010181B. doi: 10.1073/pnas.1731982100 . PMC   193536 . PMID   12928499.
  43. ↑ Petnicki-Ocwieja T, Schneider DJ, Tam VC, Chancey ST, Shan L, Jamir Y, Schechter LM, Janes MD, Buell CR, Tang X, Collmer A, Alfano JR (2002). "Genomewide identification of proteins secreted by the Hrp type III protein secretion system of Pseudomonas syringae pv. tomato DC3000". Proc. Natl. Acad. Sci. U.S.A. 99 (11): 7652–57. Bibcode:2002PNAS...99.7652P. doi: 10.1073/pnas.112183899 . PMC   124312 . PMID   12032338.
  44. ↑ Hinsch, M; Staskawicz B. (9 January 1996). "Identification of a new Arabidopsis disease resistance locus, RPs4, and cloning of the corresponding avirulence gene, avrRps4, from Pseudomonas syringae pv. pisi". Molecular Plant-Microbe Interactions . 9 (1): 55–61. doi:10.1094/mpmi-9-0055. PMID   8589423.
  45. 1 2 Weigel, Detlef; Nordborg, Magnus (23 November 2015). "Population Genomics for Understanding Adaptation in Wild Plant Species". Annual Review of Genetics . 49 (1). Annual Reviews: 315–338. doi:10.1146/annurev-genet-120213-092110. ISSN   0066-4197. PMID   26436459.
  46. 1 2 Pottinger, Sarah E.; Innes, Roger W. (25 August 2020). "RPS5-Mediated Disease Resistance: Fundamental Insights and Translational Applications". Annual Review of Phytopathology . 58 (1). Annual Reviews: 139–160. doi: 10.1146/annurev-phyto-010820-012733 . ISSN   0066-4286. PMID   32284014. S2CID   215757180.
  47. ↑ Wang, Yan; Tyler, Brett M.; Wang, Yuanchao (8 September 2019). "Defense and Counterdefense During Plant-Pathogenic Oomycete Infection". Annual Review of Microbiology . 73 (1). Annual Reviews: 667–696. doi:10.1146/annurev-micro-020518-120022. ISSN   0066-4227. PMID   31226025. S2CID   195259901.
  48. ↑ Ben Khaled, Sara; Postma, Jelle; Robatzek, Silke (4 August 2015). "A Moving View: Subcellular Trafficking Processes in Pattern Recognition Receptor–Triggered Plant Immunity". Annual Review of Phytopathology . 53 (1). Annual Reviews: 379–402. doi:10.1146/annurev-phyto-080614-120347. ISSN   0066-4286. PMID   26243727.
  49. ↑ Martin GB, Williams JG, Tanksley SD (1991). "Rapid identification of markers linked to a Pseudomonas resistance gene in tomato by using random primers and near-isogenic lines". Proc. Natl. Acad. Sci. 88 (6): 2336–40. Bibcode:1991PNAS...88.2336M. doi: 10.1073/pnas.88.6.2336 . PMC   51226 . PMID   2006172.
  50. ↑ Schwizer S, Kraus CM, Dunham DM, Zheng Y, Fernandez-Pozo N, Pombo MA, et al. (2017). "The tomato kinase Pti1 contributes to production of reactive oxygen species in response to two flagellin-derived peptides and promotes resistance to Pseudomonas syringae infection" (PDF). Molecular Plant-Microbe Interactions. 30 (9): 725–38. doi: 10.1094/MPMI-03-17-0056-R . PMID   28535079.
  51. ↑ Xiu-Fang X, He SY (2013). "Pseudomonas syringae pv. Tomato DC3000: A Model Pathogen for Probing Disease Susceptibility and Hormone Signaling in Plants". Annu. Rev. Phytopathol. 51: 473–98. doi:10.1146/annurev-phyto-082712-102321. PMID   23725467.
  52. 1 2 Jones JD, Dangl J (2006). "The plant immune system". Nature. 444 (7117): 323–29. Bibcode:2006Natur.444..391Y. doi:10.1038/nature05281. PMID   17051149. S2CID   4419198.
  53. 1 2 Kim YJ, Lin NC, Martin GB (2002). "Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity". Cell. 109 (5): 589–598. doi: 10.1016/S0092-8674(02)00743-2 . PMID   12062102. S2CID   16848405.
  54. ↑ Lin N, Martin GB (2005). "An avrPto/avrPtoB Mutant of Pseudomonas syringae pv. tomato DC3000 Does Not Elicit Pto-Mediated Resistance and Is Less Virulent on Tomato". Molecular Plant-Microbe Interactions . 18 (1): 43–51. doi: 10.1094/MPMI-18-0043 . PMID   15672817.
  55. ↑ Martin GB (2011). "Suppression and Activation of the Plant Immune System by Pseudomonas syringae Effectors AvrPto and AvrPtoB". Effectors in Plant–Microbe Interactions. pp. 123–54. ISBN   9781119949138.
  56. ↑ Roberts R, Mainiero S, Powell AF, Liu AE, Shi K, Hind SR, et al. (2019). "Natural variation for unusual host responses and flagellin mediated immunity against Pseudomonas syringae in genetically diverse tomato accessions". New Phytologist. 223 (1): 447–61. doi: 10.1111/nph.15788 . PMID   30861136.
  57. ↑ Rosli HG, Zheng Y, Pombo MA, Zhong S, Bombarely A, Fei Z, et al. (2013). "Transcriptomics-based screen for genes induced by flagellin and repressed by pathogen effectors identifies a cell wall-associated kinase involved in plant immunity". Genome Biology. 14 (12): R139. doi: 10.1186/gb-2013-14-12-r139 . PMC   4053735 . PMID   24359686.
  58. 1 2 Kvitko BH, Park DH, Velasquez AC, Wei CF, Russell A, Martin GB, et al. (2009). "Deletions in the repertoire of Pseudomonas syringae pv. tomato DC3000 type III secretion effector genes reveal functional overlap among effectors". PLOS Pathogens. 5 (4): e1000388. doi: 10.1371/journal.ppat.1000388 . PMC   2663052 . PMID   19381254.
  59. ↑ van Opijnen, Tim; Levin, Henry L. (23 November 2020). "Transposon Insertion Sequencing, a Global Measure of Gene Function". Annual Review of Genetics . 54 (1). Annual Reviews: 337–365. doi:10.1146/annurev-genet-112618-043838. ISSN   0066-4197. PMC   9488914 . PMID   32886545. S2CID   221504442.
  60. ↑ Cameron, A.; Sarojini, V. (February 2014). "Pseudomonas syringae pv. actinidiae : chemical control, resistance mechanisms and possible alternatives". Plant Pathology. 63 (1): 1–11. doi: 10.1111/ppa.12066 .
  61. ↑ Vanneste, Joel L. (4 August 2017). "The Scientific, Economic, and Social Impacts of the New Zealand Outbreak of Bacterial Canker of Kiwifruit (Pseudomonas syringae pv. actinidiae)". Annual Review of Phytopathology. 55 (1): 377–99. doi:10.1146/annurev-phyto-080516-035530. ISSN   0066-4286. PMID   28613977.
  62. ↑ Donati, Irene; Cellini, Antonio; Sangiorgio, Daniela; Vanneste, Joel L.; Scortichini, Marco; Balestra, Giorgio M.; Spinelli, Francesco (3 January 2020). "Pseudomonas syringae pv. actinidiae: Ecology, Infection Dynamics and Disease Epidemiology". Microbial Ecology. 80 (1). Springer Science and Business Media LLC: 81–102. doi:10.1007/s00248-019-01459-8. ISSN   0095-3628. PMC   7223186 . PMID   31897570. S2CID   209542819.
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.