A Bacillus licheniformis Glycoside Hydrolase 43 Protein Is Recognized as a MAMP

Glycoside hydrolases from pathogens have often been reported as inducers of immune responses. However, the roles of glycoside hydrolase from plant-growth-promoting rhizobacteria (PGPR) in the resistance of plants against pathogens is not well studied. In this study, we identified a glycoside hydrolase 43 protein, H1AD43, produced by Bacillus licheniformis BL06 that can trigger defense responses, including cell death. Ion-exchange and size-exclusion chromatography were used for separation, and the amino acid sequence was identified by mass spectrometry. The recombinant protein generated by prokaryotic expression was able to elicit a hypersensitive response (HR) in Nicotiana benthamiana and trigger early defense responses, including reactive oxygen species (ROS) burst, callose accumulation, and the induction of defense genes. In addition, the protein could induce resistance in N. benthamiana, in which it inhibited infection by Phytophthora capsici Leonian and tobacco mosaic virus-green fluorescent protein (TMV-GFP) expression. H1AD43 thus represents a microbe-associated molecular pattern (MAMP) of PGPR that induces plant disease resistance and may provide a new method for the biological control of plant disease.

[1]  Cheng Zhou,et al.  Development of plant systemic resistance by beneficial rhizobacteria: Recognition, initiation, elicitation and regulation , 2022, Frontiers in Plant Science.

[2]  Haoran Peng,et al.  Nicotiana benthamiana asparagine synthetase associates with IP‐L and confers resistance against tobacco mosaic virus via the asparagine‐induced salicylic acid signalling pathway , 2021, Molecular plant pathology.

[3]  M. Barbetti,et al.  Pathogen Biocontrol Using Plant Growth-Promoting Bacteria (PGPR): Role of Bacterial Diversity , 2021, Microorganisms.

[4]  B. Galatis,et al.  Callose: a multifunctional (1, 3)-β–d-glucan involved in morphogenesis and function of angiosperm stomata , 2021, Journal of Biological Research-Thessaloniki.

[5]  H. Brumer,et al.  Mixed Linkage β-1,3/1,4-Glucan Oligosaccharides Induce Defense Responses in Hordeum vulgare and Arabidopsis thaliana , 2021, Frontiers in Plant Science.

[6]  Li Zheng,et al.  Cell wall integrity in Magnaporthe oryzae is weakened by proteins secreted by Bacillus licheniformis BL06 , 2021, Biological Control.

[7]  H. Zeng,et al.  FoEG1, a secreted glycoside hydrolase family 12 protein from Fusarium oxysporum, triggers cell death and modulates plant immunity , 2021, Molecular plant pathology.

[8]  Xiu-Fang Xin,et al.  PTI-ETI crosstalk: an integrative view of plant immunity. , 2021, Current opinion in plant biology.

[9]  D. Dou,et al.  Nicotiana benthamiana LRR-RLP NbEIX2 mediates the perception of an EIX-like protein from Verticillium dahliae. , 2020, Journal of integrative plant biology.

[10]  Guangya Zhang,et al.  Identification and Characterization of a Novel Thermostable and Salt-Tolerant β-1,3 Xylanase from Flammeovirga pacifica Strain WPAGA1 , 2020, Biomolecules.

[11]  Jesper Cairo Westergaard,et al.  Bacillus licheniformis FMCH001 Increases Water Use Efficiency via Growth Stimulation in Both Normal and Drought Conditions , 2020, Frontiers in Plant Science.

[12]  Baoyu Huai,et al.  A stripe rust effector Pst18363 targets and stabilizes TaNUDX23 that promotes stripe rust disease. , 2019, The New phytologist.

[13]  Ujjal J Phukan,et al.  Cell Death in Plant Immunity. , 2019, Cold Spring Harbor perspectives in biology.

[14]  P. Balint-Kurti,et al.  The plant hypersensitive response: concepts, control and consequences , 2019, Molecular plant pathology.

[15]  Celedonio González,et al.  A 25-Residue Peptide From Botrytis cinerea Xylanase BcXyn11A Elicits Plant Defenses , 2019, Front. Plant Sci..

[16]  Lili Huang,et al.  A small cysteine-rich protein from two kingdoms of microbes is recognized as a novel pathogen-associated molecular pattern. , 2019, The New phytologist.

[17]  Yijie Dong,et al.  The Botrytis cinerea Xylanase BcXyl1 Modulates Plant Immunity , 2018, Front. Microbiol..

[18]  Frank Van Breusegem,et al.  Reactive oxygen species in plant development , 2018, Development.

[19]  J. Kangasjärvi,et al.  Reactive Oxygen Species in Plant Signaling. , 2018, Annual review of plant biology.

[20]  Y. Saijo,et al.  Pattern recognition receptors and signaling in plant-microbe interactions. , 2018, The Plant journal : for cell and molecular biology.

[21]  A. Avrova,et al.  A new proteinaceous pathogen-associated molecular pattern (PAMP) identified in Ascomycete fungi induces cell death in Solanaceae. , 2017, The New phytologist.

[22]  F. Takken,et al.  Involvement of salicylic acid, ethylene and jasmonic acid signalling pathways in the susceptibility of tomato to Fusarium oxysporum , 2017, Molecular plant pathology.

[23]  Ningbo Wang,et al.  A Novel Protein Elicitor (PeBA1) from Bacillus amyloliquefaciens NC6 Induces Systemic Resistance in Tobacco , 2016, International journal of biological sciences.

[24]  C. Zipfel,et al.  Regulation of the NADPH Oxidase RBOHD During Plant Immunity. , 2015, Plant & cell physiology.

[25]  Yang Wang,et al.  A Phytophthora sojae Glycoside Hydrolase 12 Protein Is a Major Virulence Factor during Soybean Infection and Is Recognized as a PAMP[OPEN] , 2015, Plant Cell.

[26]  B. Poinssot,et al.  Perception of pathogenic or beneficial bacteria and their evasion of host immunity: pattern recognition receptors in the frontline , 2015, Front. Plant Sci..

[27]  H. Zeng,et al.  PeBL1, a Novel Protein Elicitor from Brevibacillus laterosporus Strain A60, Activates Defense Responses and Systemic Resistance in Nicotiana benthamiana , 2015, Applied and Environmental Microbiology.

[28]  N. L. Glass,et al.  Plant cell wall-degrading enzymes and their secretion in plant-pathogenic fungi. , 2014, Annual review of phytopathology.

[29]  W. Boerjan,et al.  The role of the secondary cell wall in plant resistance to pathogens , 2014, Front. Plant Sci..

[30]  Chengwei Li,et al.  A Rapid, Highly Efficient and Economical Method of Agrobacterium-Mediated In planta Transient Transformation in Living Onion Epidermis , 2014, PloS one.

[31]  S. Somerville,et al.  Differences in early callose deposition during adapted and non-adapted powdery mildew infection of resistant Arabidopsis lines , 2013, Plant signaling & behavior.

[32]  D. G. Naumoff.  Hierarchical classification of glycoside hydrolases , 2011, Biochemistry (Moscow).

[33]  Z. Mou,et al.  Salicylic acid and its function in plant immunity. , 2011, Journal of integrative plant biology.

[34]  Jian-Min Zhou,et al.  Plant immunity triggered by microbial molecular signatures. , 2010, Molecular plant.

[35]  C. Zipfel.  Early molecular events in PAMP-triggered immunity. , 2009, Current opinion in plant biology.

[36]  Yuanchao Wang,et al.  The role of respiratory burst oxidase homologues in elicitor-induced stomatal closure and hypersensitive response in Nicotiana benthamiana , 2009, Journal of experimental botany.

[37]  B. Joris,et al.  Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. , 2007, Environmental microbiology.

[38]  S. Chisholm,et al.  Host-Microbe Interactions: Shaping the Evolution of the Plant Immune Response , 2022 .

[39]  T. Boller,et al.  The Arabidopsis Receptor Kinase FLS2 Binds flg22 and Determines the Specificity of Flagellin Perception[W] , 2005, The Plant Cell Online.

[40]  D. Cosgrove.  Growth of the plant cell wall , 2005, Nature Reviews Molecular Cell Biology.

[41]  G. Stacey,et al.  Loss-of-Function Mutations in Chitin Responsive Genes Show Increased Susceptibility to the Powdery Mildew Pathogen Erysiphe cichoracearum1[w] , 2005, Plant Physiology.

[42]  K. Niehaus,et al.  The N Terminus of Bacterial Elongation Factor Tu Elicits Innate Immunity in Arabidopsis Plants , 2004, The Plant Cell Online.

[43]  A. Avni,et al.  A point mutation in the ethylene-inducing xylanase elicitor inhibits the beta-1-4-endoxylanase activity but not the elicitation activity. , 1999, Plant physiology.

[44]  David B. Collinge,et al.  Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley—powdery mildew interaction , 1997 .

[45]  T. Jabs,et al.  High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses , 1994, Cell.

[46]  Antje Heese,et al.  Staining and automated image quantification of callose in Arabidopsis cotyledons and leaves. , 2020, Methods in cell biology.

[47]  Caiji Gao,et al.  Using Fluorescent Protein Fusions to Study Protein Subcellular Localization and Dynamics in Plant Cells. , 2016, Methods in molecular biology.

[48]  M. Newman,et al.  The role of lipopolysaccharide and peptidoglycan, two glycosylated bacterial microbe-associated molecular patterns (MAMPs), in plant innate immunity. , 2012, Molecular plant pathology.

[49]  V. Citovsky,et al.  Biology of callose (β-1,3-glucan) turnover at plasmodesmata , 2010, Protoplasma.

[50]  T. Boller,et al.  Molecular Sensing of Bacteria in Plants THE HIGHLY CONSERVED RNA-BINDING MOTIF RNP-1 OF BACTERIAL COLD SHOCK PROTEINS IS RECOGNIZED AS AN ELICITOR SIGNAL IN TOBACCO*□S , 2003 .