Expression of a Fungal Lectin in Arabidopsis Enhances Plant Growth and Resistance Toward Microbial Pathogens and a Plant-Parasitic Nematode

Abstract

Coprinopsis cinerea lectin 2 (CCL2) is a fucoside-binding lectin from the basidiomycete C. cinerea that is toxic to the bacterivorous nematode Caenorhabditis elegans as well as animal-parasitic and fungivorous nematodes. We expressed CCL2 in Arabidopsis to assess its protective potential toward plant-parasitic nematodes. Our results demonstrate that expression of CCL2 enhances host resistance against the cyst nematode Heterodera schachtii. Surprisingly, CCL2-expressing plants were also more resistant to fungal pathogens including Botrytis cinerea, and the phytopathogenic bacterium Pseudomonas syringae. In addition, CCL2 expression positively affected plant growth indicating that CCL2 has the potential to improve two important agricultural parameters namely biomass production and general disease resistance. The mechanism of the CCL2-mediated enhancement of plant disease resistance depended on fucoside-binding by CCL2 as transgenic plants expressing a mutant version of CCL2 (Y92A), compromised in fucoside-binding, exhibited wild type (WT) disease susceptibility. The protective effect of CCL2 did not seem to be direct as the lectin showed no growth-inhibition toward B. cinerea in in vitro assays. We detected, however, a significantly enhanced transcriptional induction of plant defense genes in CCL2- but not CCL2-Y92A-expressing lines in response to infection with B. cinerea compared to WT plants. This study demonstrates a potential of fungal defense lectins in plant protection beyond their use as toxins.

Functional Characterization of an Amaranth Natterin-4-Like-1 Gene in Arabidopsis thaliana

“…The negative effect on vegetative and reproductive growth caused by the overexpression of this gene in A. thaliana was also an unexpected outcome considering that is was contrary to published data describing lectin-induced mitosis in some root apical meristem tissues (Bonner, 2009) and to lectindependent modulation of sugar metabolism and/or signaling leading to increased plant productivity (Nonomura et al, 2020;Moradi et al, 2021). On the other hand, it was in agreement with a study in which detrimental effects on plant growth and development were reported in A. thaliana plants overexpressing a lectin receptor kinase used as a sensor for extracellular nicotinamide adenine dinucleotide and with the suppressed growth observed in A. cruentus hairy roots transformed with AhN4L-2, an homolog of AhN4L-1 (Castellanos-Arévalo, 2020).…”

β-D-XYLOSIDASE 4 modulates systemic immune signaling in Arabidopsis thaliana

“…G3P is one of several putative long-distance signals of SAR ( Chanda et al., 2011 ; Gao et al., 2015 ; Vlot et al., 2021 ). Notably, Moradi et al. (2021) described that a local treatment with an exogenously applied fungal, fucose-binding lectin protein induced SAR against Pst .…”

“…(2021) described that a local treatment with an exogenously applied fungal, fucose-binding lectin protein induced SAR against Pst . Concomitantly, transcripts of genes, including the G3P biosynthetic enzyme GLY1 as well as PR-1 and RESPIRATORY BURST OXIDASE HOMOLOGS D and F ( RBOHD and F ) were induced in the lectin-inoculated leaves ( Moradi et al., 2021 ). This suggests that fucose-associated signals may promote the enrichment of G3P while also boosting local ROS signals.…”

TIR1/AFB proteins: Active players in abiotic and biotic stress signaling

“…Nematodes are pathogens of Arabidopsis ( Moradi et al., 2021 ), apple ( Fallahi et al., 1998 ), tomato ( Khan and Khan, 1995 ), and wheat ( Cortese et al., 2003 ), these species could move through roots and be vector of some virus, caused root damage, yield loss. The tomato Mi-1 gene confers isolate-specific resistance against root-knot nematodes ( Seah et al., 2007 ).…”