Laccase GhLac1 Modulates Broad-Spectrum Biotic Stress Tolerance via Manipulating Phenylpropanoid Pathway and Jasmonic Acid Synthesis

Abstract

Plants are constantly challenged by a multitude of pathogens and pests, which causes massive yield and quality losses annually. A promising approach to reduce such losses is to enhance the immune system of plants through genetic engineering. Previous work has shown that laccases (p-diphenol:dioxygen oxidoreductase, EC 1.10.3.2) function as lignin polymerization enzymes. Here we demonstrate that transgenic manipulation of the expression of the laccase gene GhLac1 in cotton (Gossypium hirsutum) can confer an enhanced defense response to both pathogens and pests. Overexpression of GhLac1 leads to increased lignification, associated with increased tolerance to the fungal pathogen Verticillium dahliae and to the insect pests cotton bollworm (Helicoverpa armigera) and cotton aphid (Aphis gosypii). Suppression of GhLac1 expression leads to a redirection of metabolic flux in the phenylpropanoid pathway, causing the accumulation of JA and secondary metabolites that confer resistance to V. dahliae and cotton bollworm; it also leads to increased susceptibility to cotton aphid. Plant laccases therefore provide a new molecular tool to engineer pest and pathogen resistance in crops.

Melatonin enhances cotton immunity to Verticillium wilt via manipulating lignin and gossypol biosynthesis

“…Our transcriptome and metabolic studies show that melatonin pre‐treatment upregulated the expression of phenylpropanoid pathway genes and increased lignin accumulation in cotton seedlings after V. dahliae inoculation (Figures and S3). Consistently, overexpression of GhLac1 and GhLac15 , genes related to phenylpropanoid pathway and lignin biosynthesis, was previously found to enhance V. dahliae resistance in cotton (Hu et al ., ; Zhang et al ., ,b). Transcriptional and histochemical analysis of resistant cotton ( G. barbadense cv.…”

“…Verticillium wilt is one of the most destructive fungal diseases affecting plant species, and in cotton, it causes great reductions in yield and fiber quality (Xu et al, 2011;Hu et al, 2018). Understanding the mechanisms underlying cotton resistance to V. dahliae is critical for minimizing production loss in the cotton industry, and the related research questions have therefore drawn much interest.…”

“…Specifically, the pathway synthesizes monolignols, which are substrates of lignin polymerization (Boerjan et al, 2003;Mottiar et al, 2016). Before pathogen inoculation, lignin can enhance plant mechanical strength and thicken cell walls to form a physical barrier and inhibit pathogen invasion and colonization (Hu et al, 2018). At the same time, lignin accumulation in the infected cells not only inhibits the spread of pathogens and pathogen-produced toxins and enzymes but also prevents pathogens from extracting water and nutrients from host plants (Mottiar et al, 2016).…”

The cotton laccase gene GhLAC15 enhances Verticillium wilt resistance via an increase in defence‐induced lignification and lignin components in the cell walls of plants

“…The plant cell wall, composed of cellulose, hemicelluloses, lignin and pectic polysaccharides with minor structural proteins, is a dynamic structure that often determines the outcome of the interactions between plants and pathogens (Bellincampi et al, 2014;Xu et al, 2011). Lignin has been reported to be involved in multiple resistances, including cotton Verticillium wilt resistance (Bonello and Blodgett, 2003;Hu et al, 2018;Zhang et al, 2017). Previous studies have shown that plant laccases (LAC4, LAC11 and LAC17) are necessary and non-redundant with peroxidase for lignin polymerization in Arabidopsis (Berthet et al, 2011;Zhao et al, 2013), and that they oxidatively polymerize monolignols (p-coumaryl, coniferyl and sinapyl alcohols) into p-hydroxyphenyl (H), guaiacyl (G) and syringyl (S) lignin units (Wang et al, 2015).…”

“…Thus, it remains unclear whether the reduced resistance in PAL-deficient plants is the result of significant reductions in lignin, SA or both. Recently, Hu et al (2018) have reported that the overexpression of cotton GhLAC1 increases lignification and mediates jasmonic acid (JA) biosynthesis and the balance of the JA-SA defence response, resulting in a modulation of broad-spectrum biotic stress tolerance. However, whether the improved resistance of transgenic plants is the result of significant increases in lignin, SA, JA or all three still remains unclear.…”