Plant lectins: the ties that bind in root symbiosis and plant defense

Abstract

Lectins are a diverse group of carbohydrate-binding proteins that are found within and associated with organisms from all kingdoms of life. Several different classes of plant lectins serve a diverse array of functions. The most prominent of these include participation in plant defense against predators and pathogens and involvement in symbiotic interactions between host plants and symbiotic microbes, including mycorrhizal fungi and nitrogen-fixing rhizobia. Extensive biological, biochemical, and molecular studies have shed light on the functions of plant lectins, and a plethora of uncharacterized lectin genes are being revealed at the genomic scale, suggesting unexplored and novel diversity in plant lectin structure and function. Integration of the results from these different types of research is beginning to yield a more detailed understanding of the function of lectins in symbiosis, defense, and plant biology in general.

Fig. 1

Lectin structures. a Structural model of the seed lectin monomer (doi:10.2210/pdb1LEM/pdb) from Lens culinaris, derived from co-crystallization of the protein and its ligand, at 3.00 Å resolution. This glucose/mannose binding lectin (see Loris et al. 1994) illustrates the typical L-legume fold with the flat β-sheet and β-strand dimerization interface (light blue, left side) and the structural elements (dark blue, right side) showing the “C” cup fold containing the sugar/metal co-factor interaction domains. Typical to most L-lectins is the direct interaction between the calcium co-factor and the target carbohydrate inside of the structurally conserved binding pocket. Atypical among most L-lectins (except PSL) is the internal proteolytic site on a portion of the polypeptide, shown as a red (middle) strand. This sequence makes up a component of the dimerization face as well as a support structure for the carbohydrate-binding domain. b Structural model of the homotetramer Lotus tetragonolobus seed lectin (LTA) (doi:10.2210/pdb2EIG/pdb), derived from co-crystallization of the protein and its ligands, at 2.00 Å resolution. This fucose-binding (see Moreno et al. 2008) lectin (here shown with N-acetyl-glucosamine residues) is structurally very similar to peanut (Arachis hypogaea) lectin at the level of the monomer, and thus serves as an example of the highly conserved monomeric structure of legume lectins. The unusual binding site of the carbohydrate (distal to the metal co-factors) is potentially influenced by the novel tetrameric arrangement of the monomers. This illustrates the importance of total structural characterization prior to assignment of definitive carbohydrate binding sites. Like other fucose-binding lectins, such as Ulex europaeus lectin II (doi:10.2210/pdb1QOO/pdb), LTA complexes with N-acetyl-glucosamine, as pictured. Structures were downloaded from the protein data bank (PDB) (http://www.rcsb.org/) through Chimera (Pettersen et al. 2004), oriented, and ray traced for visualization

Fig. 2

Neighbor-joining tree of selected lectin protein sequence alignment. Signal sequences have been removed. At Arabidopsis thaliana, Gm Glycine max, Lj Lotus japonicus, Ma Melilotus alba, Ms Medicago sativa, Mt Medicago truncatula, Nt Nicotiana tabacum, Ps Pisum sativum, Rp Robinia pseudoacacia, Vv Vitis vinifera. SignalP (Bendtsen et al. 2004) was used to predict the signal peptides, ClustalX (Larkin et al. 2007) to generate the alignments, and ATV (Zmasek and Eddy 2001) to visualize the data. Bootstrap values on the branches represent a repeat of 1,000 with a random start number of 111. Genbank IDs follow species/protein names. Names beginning with “chr” are contig identifiers in the Lotus japonicus genomic database (http://www.kazusa.or.jp/lotus/). See text for additional details

Fig. 3

a Hypothetical model to illustrate the perception of pathogenic, symbiotic, or commensal bacteria. A sugar/protein gradient is exuded from the root to permit the growth of potentially mutualistic organisms in the rhizosphere. Soluble lectin agglutinates most bacteria (illustrated) and fungus (not shown) along the root periphery. Those bacteria that elude this first line of defense, either through evasion or persistence, as well as isolated PAMPs or symbiont-associated molecular patterns (SAMPs); Hirsch 2004) bind to protein recognition receptors (PRRs) or lectins at the root surface. This binding activates kinase domains, triggering a cascade of MAP kinases leading to anti-pathogen responses or pro-symbiotic responses. Lectin kinases and soluble lectins agglutinate surface transmembrane proteins, helping to stabilize lipid rafts for enhanced downstream protein signaling. B-lectin kinases are diagrammed here with typical twin Pfam domains [usually a Pan/Apple (cd01098) and a S-locus (pfam00954)] proximal to the membrane from the lectin domain. L-lectin receptor kinases only contain a Pfam L-lectin domain in the extracellular space (not shown). Commensal bacteria either do not elicit a response, or lack symbiotic and pathogenic responses. b Enlargement of the mutualistic interaction with SAMP receptors (such as Nod factor receptor) responding to locally increased Nod factor concentrations due to localized agglutination of the compatible bacteria. c Enlargement of the pathogenic interaction showing soluble lectins and LecRKs agglutinating PAMP receptors. LecRK responses to pathogen effectors are known to occur on the cytoplasmic side of the membrane, as indicated. See text for additional details