The cellulase encoded by the native plasmid of Clavibacter michiganensis ssp. sepedonicus plays a role in virulence and contains an expansin-like domain

Laine, M; Haapalainen, Minna; Wahlroos, Tony; Kankare, Katja; Nissinen, Riitta; Kassuwi, Shaaban; Metzler, Mary

doi:10.1006/pmpp.2000.0301

Cited by 78 publications

(53 citation statements)

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“…These proteins are required for virulence, have C-terminal expansin-like domains, and are found in many plant-associated microorganisms, including the phytopathogenic Actinobacteria organisms Clavibacter michiganensis subsp. sepedonicus (526,541). The S. scabiei expansin-like proteins exhibit 66% homology with each other at the amino acid level and are also closely related to putative expansin-like proteins from two nonpathogenic Streptomyces species.…”

Section: Interactions Between Actinobacteria and Plantsmentioning

confidence: 96%

“…michiganensis toward tomato plants can be modulated by three different mechanisms: loss of plasmids accompanied by the loss of the pathogenicity factors celA and pat-1, resulting in reduced virulence or even nonvirulence in a plasmid-free derivative; transfer of plasmids to plasmidfree C. michiganensis subsp. michiganensis derivatives, which restores full virulence; and loss of the pathogenicity island due to stress-activated recA-dependent recombination events, which leads to a low-titer colonizer that may carry the plasmids and the pathogenicity factors necessary for effective colonization but which can be considered a nonvirulent endophyte (526).…”

Section: Interactions Between Actinobacteria and Plantsmentioning

confidence: 99%

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Taxonomy, Physiology, and Natural Products of Actinobacteria

Barka

Vatsa

Sanchez

et al. 2016

Microbiol Mol Biol Rev

1,603

1,048

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SUMMARYActinobacteriaare Gram-positive bacteria with high G+C DNA content that constitute one of the largest bacterial phyla, and they are ubiquitously distributed in both aquatic and terrestrial ecosystems. ManyActinobacteriahave a mycelial lifestyle and undergo complex morphological differentiation. They also have an extensive secondary metabolism and produce about two-thirds of all naturally derived antibiotics in current clinical use, as well as many anticancer, anthelmintic, and antifungal compounds. Consequently, these bacteria are of major importance for biotechnology, medicine, and agriculture.Actinobacteriaplay diverse roles in their associations with various higher organisms, since their members have adopted different lifestyles, and the phylum includes pathogens (notably, species ofCorynebacterium,Mycobacterium,Nocardia,Propionibacterium, andTropheryma), soil inhabitants (e.g.,MicromonosporaandStreptomycesspecies), plant commensals (e.g.,Frankiaspp.), and gastrointestinal commensals (Bifidobacteriumspp.).Actinobacteriaalso play an important role as symbionts and as pathogens in plant-associated microbial communities. This review presents an update on the biology of this important bacterial phylum.

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Section: Interactions Between Actinobacteria and Plantsmentioning

confidence: 96%

Section: Interactions Between Actinobacteria and Plantsmentioning

confidence: 99%

Taxonomy, Physiology, and Natural Products of Actinobacteria

Barka

Vatsa

Sanchez

et al. 2016

Microbiol Mol Biol Rev

1,603

1,048

View full text Add to dashboard Cite

show abstract

“…Cellulase is an important determinant in C. michiganensis pathogenicity, so the disruption of celB is intriguing, although it should be noted that the plasmid-borne cellulase gene (celA), which is known to be involved in virulence in C. michiganensis subsp. michiganensis, appears to be intact (32,45,58). A gene encoding a 2,5-diketo-D-gluconic acid reductase is also disrupted.…”

Section: Resultsmentioning

confidence: 99%

Genome of the Actinomycete Plant Pathogen Clavibacter michiganensis subsp. sepedonicus Suggests Recent Niche Adaptation

et al. 2008

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Clavibacter michiganensis subsp. sepedonicus is a plant-pathogenic bacterium and the causative agent of bacterial ring rot, a devastating agricultural disease under strict quarantine control and zero tolerance in the seed potato industry. This organism appears to be largely restricted to an endophytic lifestyle, proliferating within plant tissues and unable to persist in the absence of plant material. Analysis of the genome sequence of C. michiganensis subsp. sepedonicus and comparison with the genome sequences of related plant pathogens revealed a dramatic recent evolutionary history. The genome contains 106 insertion sequence elements, which appear to have been active in extensive rearrangement of the chromosome compared to that of Clavibacter michiganensis subsp. michiganensis. There are 110 pseudogenes with overrepresentation in functions associated with carbohydrate metabolism, transcriptional regulation, and pathogenicity. Genome comparisons also indicated that there is substantial gene content diversity within the species, probably due to differential gene acquisition and loss. These genomic features and evolutionary dating suggest that there was recent adaptation for life in a restricted niche where nutrient diversity and perhaps competition are low, correlated with a reduced ability to exploit previously occupied complex niches outside the plant. Toleration of factors such as multiplication and integration of insertion sequence elements, genome rearrangements, and functional disruption of many genes and operons seems to indicate that there has been general relaxation of selective pressure on a large proportion of the genome.High-GϩC-content gram-positive coryneform bacteria cause economic losses in several crops worldwide, yet the relatively slow in vitro and in planta growth and general genetic intractability of these bacteria have long been deterrents to successful identification of the specific molecular mechanisms by which they cause diseases in plants. Consequently, there is a clear disparity between the amount of scientific research on plant-pathogenic coryneform bacteria and the amount of scientific research on their gramnegative counterparts. Recent advances in this field have coincided with the availability of transformation systems and complete genome sequences for representatives of the genera Clavibacter and Leifsonia, two of the major coryneform plant-pathogenic genera (14,32,48,56,74). Importantly, these advances allowed breakthrough identification of a novel set of pathogenicity-related genes in the tomato pathogen Clavibacter michiganensis subsp. michiganensis and identification of homologues in other coryneform plant pathogens (15, 27, 32; see the accompanying paper). Because methodologies created for functional analysis of C. michiganensis subsp. michiganensis are generally applicable to other members of the genus, additional advances in this field can be expected in the near future (40, 46).The genus Clavibacter provides an excellent resource for obtaining a more comprehensive underst...

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“…In a related vein, a modular endoglucanase with a domain distantly related to EXLX1 was found to be an important virulence factor for inducing symptoms during infection of tomato plants by Clavibacter michiganensis (29,30). Likewise, a recent study found that overexpression of ''swollenin,'' a fungal protein with an expansin-like domain, enhanced benign colonization of cucumber roots by Trichoderma reesei (31).…”

Section: Discussionmentioning

confidence: 98%

Crystal structure and activity of Bacillus subtilis YoaJ (EXLX1), a bacterial expansin that promotes root colonization

Kerff

Amoroso

Herman

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

185

291

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We solved the crystal structure of a secreted protein, EXLX1, encoded by the yoaJ gene of Bacillus subtilis. Its structure is remarkably similar to that of plant ␤-expansins (group 1 grass pollen allergens), consisting of 2 tightly packed domains (D1, D2) with a potential polysaccharide-binding surface spanning the 2 domains. Domain D1 has a double-␤-barrel fold with partial conservation of the catalytic site found in family 45 glycosyl hydrolases and in the MltA family of lytic transglycosylases. Domain D2 has an Ig-like fold similar to group 2/3 grass pollen allergens, with structural features similar to a type A carbohydratebinding domain. EXLX1 bound to plant cell walls, cellulose, and peptidoglycan, but it lacked lytic activity against a variety of plant cell wall polysaccharides and peptidoglycan. EXLX1 promoted plant cell wall extension similar to, but 10 times weaker than, plant ␤-expansins, which synergistically enhanced EXLX1 activity. Deletion of the gene encoding EXLX1 did not affect growth or peptidoglycan composition of B. subtilis in liquid medium, but slowed lysis upon osmotic shock and greatly reduced the ability of the bacterium to colonize maize roots. The presence of EXLX1 homologs in a small but diverse set of plant pathogens further supports a role in plant-bacterial interactions. Because plant expansins have proved difficult to express in active form in heterologous systems, the discovery of a bacterial homolog opens the door for detailed structural studies of expansin function.family 45 endoglucanase ͉ lytic transglycosylase ͉ peptidoglycan ͉ plant cell wall ͉ plant-microbe interactions B acterial and plant cell walls have similar functions but distinctive structures. Bacterial peptidoglycan forms a network of linear polysaccharide strands of alternating Nacetylglucosamine (GlcNAc) and N-acetylmuramic acid (MurNAc) residues cross-linked by short polypeptides. As a giant bag-shaped sacculus, peptidoglycan expands via the action of endopeptidases, amidases, and lytic transglycosylases that cleave covalent bonds and allow insertion of new subunits (1). In contrast, the growing plant cell wall is formed from a scaffold of cellulose microfibrils tethered together by branched glycans such as xyloglucan or arabinoxylan that bind noncovalently to cellulose surfaces. The cellulose-hemicellulose network enlarges via polymer slippage or ''creep,'' mechanically powered by turgorgenerated forces in the cell wall and catalyzed by expansins and other wall-loosening agents (2).Expansins are known principally from plants where they function in cell enlargement and other developmental events requiring cell wall loosening (3). Canonical expansins are small proteins (Ϸ26 kDa, Ϸ225 aa) consisting of 2 compact domains: D1 has a fold similar to that of family 45 glycosyl hydrolases (GH45), and D2 has a ␤-sandwich fold. Expansins facilitate cell wall creep without breakdown of wall polymers (3-5). Plant expansins consist of 2 major families: ␣-expansins, which preferentially loosen the cell walls of dicots compa...

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The cellulase encoded by the native plasmid of Clavibacter michiganensis ssp. sepedonicus plays a role in virulence and contains an expansin-like domain

Cited by 78 publications

References 50 publications

Taxonomy, Physiology, and Natural Products of Actinobacteria

Taxonomy, Physiology, and Natural Products of Actinobacteria

Genome of the Actinomycete Plant Pathogen Clavibacter michiganensis subsp. sepedonicus Suggests Recent Niche Adaptation

Crystal structure and activity of Bacillus subtilis YoaJ (EXLX1), a bacterial expansin that promotes root colonization

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