BcXYG1, a Secreted Xyloglucanase from Botrytis cinerea, Triggers Both Cell Death and Plant Immune Responses

Abstract

In search of cell death-inducing proteins, we found a xyloglucanase (BcXYG1) that induced strong necrosis and a resistance response in dicot plants. Expression of the gene was strongly induced during the first 12 h post inoculation, and analysis of disease dynamics using PathTrack showed that a strain overexpressing produced early local necrosis, supporting a role of BcXYG1 as an early cell death-inducing factor. The xyloglucanase activity of BcXYG1 was not necessary for the induction of necrosis and plant resistance, as a mutant of BcXYG1 lacking the xyloglucanase enzymatic activity retained both functions. Residues in two exposed loops on the surface of BcXYG1 were found to be necessary for the induction of cell death but not to induce plant resistance. Further analyses showed that BcXYG1 is apoplastic and possibly interacts with the proteins of the plant cell membrane and also that the BcXYG1 cell death-promoting signal is mediated by the leucine-rich repeat receptor-like kinases BAK1 and SOBIR1. Our findings support the role of cell death-inducing proteins in establishing the infection of necrotrophic pathogens and highlight the recognition of fungal apoplastic proteins by the plant immune system as an important mechanism of resistance against this class of pathogens.

Rapid identification of an Arabidopsis NLR gene as a candidate conferring susceptibility to Sclerotinia sclerotiorum using time‐resolved automated phenotyping

“…Several molecules secreted by broad host range necrotrophic fungi trigger cell death in plants. Examples include B. cinerea endo-arabinase BcAra1 (Nafisi et al, 2014), xyloglucanase BcXYG1 (Zhu et al, 2017), the S. sclerotiorum necrosis, and ethylene-inducing peptide SsNEP1 (Dallal Bashi et al, 2010) or Alternaria tenuissima Hrip1 protein elicitor (Kulye et al, 2012). Cell death induction by these elicitors is often due to direct toxic effects on plant cells independently of the manipulation of plant programmed cell death (Lenar ci c et al, 2017).…”

The Botrytis cinerea Xylanase BcXyl1 Modulates Plant Immunity

“…For instance, VdEG1, VdEG3 and VdVUT11 from Verticillium dahliae , XEG1 from Phytophthora sojae and BcXYG1, a secreted xyloglucanase from B. cinerea contributed to virulence and triggered plant immunity as PAMPs simultaneously ( Ma et al, 2015 ; Gui Y. et al, 2017 ; Gui Y.-J. et al, 2017 ; Zhu et al, 2017 ).…”

A Verticillium dahliae Pectate Lyase Induces Plant Immune Responses and Contributes to Virulence

“…Previous studies showed that many fungal CWDEs, including xyloglucanases, glucanases, and cellulases, can trigger cell-death responses independent of their enzymatic activity ( Ma et al, 2014 , 2015 ; Gui Y.-J. et al, 2017 ; Zhu et al, 2017a ). Endopolygalacturonase 1 (EG1) has two biological activities (enzymatic activity and elicitor activity) that are independent of each other in B. cinerea ( Poinssot et al, 2003 ).…”

“…Recently, it was widely reported that glycoside hydrolase 12 (GH12) proteins, VdEG1 and VdEG3 from Verticillium dahliae , XEG1 from Phytophthora sojae and BcXYG1, a secreted xyloglucanase from B. cinerea contributed to virulence and simultaneously triggered plant immunity as PAMPs ( Gui Y.-J. et al, 2017 ; Zhu et al, 2017a , b ). Oligogalacturonides (OGs) were regarded as DAMPs to activate the plant immune responses ( De Lorenzo et al, 2011 ).…”