A Novel Family of Lectins Evolutionarily Related to Class V Chitinases: An Example of Neofunctionalization in Legumes

Damme, Els J.M. Van; Culerrier, Raphaël; Barre, Annick; Alvarez, Richard A.; Rougé, Pierre; Peumans, Willy J.

doi:10.1104/pp.106.087981

Cited by 57 publications

(47 citation statements)

References 38 publications

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“…BLAST searches on the genome of the nematode C. elegans reveal several genes likely to encode chi-lectins, yet phylogenetic analyses again show none of them to group within the tree (results not shown). Recently, the occurrence in several plant species of chi-lectins homologous to chitinases has also been reported (van Damme et al 2006). Mutations resulting in loss of chitinolytic activity have apparently occurred independently in a variety of lineages.…”

Section: Discussionmentioning

confidence: 99%

Evolution of Mammalian Chitinase(-Like) Members of Family 18 Glycosyl Hydrolases

et al. 2007

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Family 18 of glycosyl hydrolases encompasses chitinases and so-called chi-lectins lacking enzymatic activity due to amino acid substitutions in their active site. Both types of proteins widely occur in mammals although these organisms lack endogenous chitin. Their physiological function(s) as well as evolutionary relationships are still largely enigmatic. An overview of all family members is presented and their relationships are described. Molecular phylogenetic analyses suggest that both active chitinases (chitotriosidase and AMCase) result from an early gene duplication event. Further duplication events, followed by mutations leading to loss of chitinase activity, allowed evolution of the chi-lectins. The homologous genes encoding chitinase(-like) proteins are clustered in two distinct loci that display a high degree of synteny among mammals. Despite the shared chromosomal location and high homology, individual genes have evolved independently. Orthologs are more closely related than paralogues, and calculated substitution rate ratios indicate that protein-coding sequences underwent purifying selection. Substantial gene specialization has occurred in time, allowing for tissue-specific expression of pH optimized chitinases and chilectins. Finally, several family 18 chitinase-like proteins are present only in certain lineages of mammals, exemplifying recent evolutionary events in the chitinase protein family.

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Section: Discussionmentioning

confidence: 99%

Evolution of Mammalian Chitinase(-Like) Members of Family 18 Glycosyl Hydrolases

et al. 2007

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“…S1) were also cloned and expressed in E. coli. The Mt75352 sequence encodes a putative class V chitinase, whereas MtCRA is related to the previously characterized lectin RobpsCRA of R. pseudoacacia (Van Damme et al, 2007). For comparison, the class V chitinases AtChiC of Arabidopsis (Ohnuma et al, 2011a) and NtChiV of tobacco (Ohnuma et al, 2011b) were cloned and expressed in a similar way.…”

Section: Mtnfh1 Encodes An Nf-cleaving Enzymementioning

confidence: 99%

“…In addition to these enzymes, a class V chitinase-related lectin (RobpsCRA) from the legume tree Robinia pseudoacacia has been characterized. This protein binds to high-Man N-glycans but lacks catalytic activity (Van Damme et al, 2007). Similarly, the extracellular domain of the chitinase-related receptor-like kinase 1 of tobacco is related to class V chitinases (Kim et al, 2000).…”

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confidence: 99%

The Nodulation Factor Hydrolase of Medicago truncatula: Characterization of an Enzyme Specifically Cleaving Rhizobial Nodulation Signals

et al. 2013

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Nodule formation induced by nitrogen-fixing rhizobia depends on bacterial nodulation factors (NFs), modified chitin oligosaccharides with a fatty acid moiety. Certain NFs can be cleaved and inactivated by plant chitinases. However, the most abundant NF of Sinorhizobium meliloti, an O-acetylated and sulfated tetramer, is resistant to hydrolysis by all plant chitinases tested so far. Nevertheless, this NF is rapidly degraded in the host rhizosphere. Here, we identify and characterize MtNFH1 (for Medicago truncatula Nod factor hydrolase 1), a legume enzyme structurally related to defense-related class V chitinases (glycoside hydrolase family 18). MtNFH1 lacks chitinase activity but efficiently hydrolyzes all tested NFs of S. meliloti. The enzyme shows a high cleavage preference, releasing exclusively lipodisaccharides from NFs. Substrate specificity and kinetic properties of MtNFH1 were compared with those of class V chitinases from Arabidopsis (Arabidopsis thaliana) and tobacco (Nicotiana tabacum), which cannot hydrolyze tetrameric NFs of S. meliloti. The Michaelis-Menten constants of MtNFH1 for NFs are in the micromolar concentration range, whereas nonmodified chitin oligosaccharides represent neither substrates nor inhibitors for MtNFH1. The three-dimensional structure of MtNFH1 was modeled on the basis of the known structure of class V chitinases. Docking simulation of NFs to MtNFH1 predicted a distinct binding cleft for the fatty acid moiety, which is absent in the class V chitinases. Point mutation analysis confirmed the modeled NF-MtNFH1 interaction. Silencing of MtNFH1 by RNA interference resulted in reduced NF degradation in the rhizosphere of M. truncatula. In conclusion, we have found a novel legume hydrolase that specifically inactivates NFs.

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“…Plant lectins, also referred to as ''agglutinins,'' are a heterogenous group of carbohydratebinding proteins that are able to reversibly bind simple sugars and/or complex carbohydrates (for review, see Van Damme et al, 1998). However, over the past few years, novel sugar-binding domains have been identified (Kaku et al, 2006;Peumans et al, 2007;Van Damme et al, 2007a) that necessitated redefining the families of plant lectins.…”

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confidence: 99%

Functional Characterization of HFR1, a High-MannoseN-Glycan-Specific Wheat Lectin Induced by Hessian Fly Larvae

et al. 2008

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We previously cloned and characterized a novel jacalin-like lectin gene from wheat (Triticum aestivum) plants that responds to infestation by Hessian fly (Mayetiola destructor) larvae, a major dipteran pest of this crop. The infested resistant plants accumulated higher levels of Hfr-1 (for Hessian fly-responsive gene 1) transcripts compared with uninfested or susceptible plants. Here, we characterize the soluble and active recombinant His 6 -HFR1 protein isolated from Escherichia coli. Functional characterization of the protein using hemagglutination assays revealed lectin activity. Glycan microarray-binding assays indicated strong affinity of His 6 -HFR1 to Mana1-6(Mana1-3)Man trisaccharide structures. Resistant wheat plants accumulated high levels of HFR1 at the larval feeding sites, as revealed by immunodetection, but the avirulent larvae were deterred from feeding and consumed only small amounts of the lectin. Behavioral studies revealed that avirulent Hessian fly larvae on resistant plants exhibited prolonged searching and writhing behaviors as they unsuccessfully attempted to establish feeding sites. During His 6 -HFR1 feeding bioassays, Drosophila melanogaster larvae experienced significant delays in growth and pupation, while percentage mortality increased with progressively higher concentrations of His 6 -HFR1 in the diet. Thus, HFR1 is an antinutrient to dipteran larvae and may play a significant role in deterring Hessian fly larvae from feeding on resistant wheat plants.

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A Novel Family of Lectins Evolutionarily Related to Class V Chitinases: An Example of Neofunctionalization in Legumes

Cited by 57 publications

References 38 publications

Evolution of Mammalian Chitinase(-Like) Members of Family 18 Glycosyl Hydrolases

Evolution of Mammalian Chitinase(-Like) Members of Family 18 Glycosyl Hydrolases

The Nodulation Factor Hydrolase of Medicago truncatula: Characterization of an Enzyme Specifically Cleaving Rhizobial Nodulation Signals

Functional Characterization of HFR1, a High-MannoseN-Glycan-Specific Wheat Lectin Induced by Hessian Fly Larvae

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