Diverse Roles of Lysin-Motif (LysM) Proteins in Mediating Plant-Microbe Interactions
Lysin-motif (LysM) is a protein domain initially identified in a phage protein responsible for binding peptidoglycan, an important component of bacterial cell walls. LysM-containing proteins are distributed in diverse organisms, ranging from microbes to plants and animals (including human beings). Recent studies demonstrated that this group of proteins plays different roles in mediating plant-microbe interactions, leading to defense, symbiosis, or suppression of host defense. These roles are probably related to their potential ability to recognize and bind a specific signal molecule, such as chitooligosaccharides, peptidoglycan, nodulation factors (NFs), and mycorrhization factors (MFs).
AF Bent and D Mackey. Elicitors, effectors, and R genes: The new paradigm and a lifetime supply of questions. Annu. Rev. Phytopathol. 2007; 45, 399-36.
JD Jones and JL Dangl. The plant immune system. Nature 2006; 444, 323-9.
T Nurnberger and B Kemmerling. Receptor protein kinases: Pattern recognition receptors in plant immunity. Trend. Plant Sci. 2006; 11, 519-22.
B Schwessinger and C Zipfel. News from the frontline: Recent insights into PAMP-triggered immunity in plants. Curr. Opin. Plant Biol. 2008; 11, 389-95.
C Zipfel. Pattern-recognition receptors in plant innate immunity. Curr. Opin. Immunol. 2008; 20, 10-6.
T Boller and SY He. Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 2009; 324, 742-4.
NA Eckardt. BIK1 function in plant growth and defense signaling. Plant Cell 2011; 23, 2806.
K Laluk, H Luo, M Chai, R Dhawan, Z Lai and T Mengiste. Biochemical and genetic requirements for function of the immune response regulator Botrytis-induced kinase1 in plant growth, ethylene signaling, and PAMP-triggered immunity in Arabidopsis. Plant Cell 2011; 23, 2831-49.
D Lu, S Wu, X Gao, Y Zhang, L Shan and P He. A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. Proc. Natl. Acad. Sci. USA 2010; 107, 496-501.
M Roux, B Schwessinger, C Albrecht, D Chinchilla, A Jones, N Holton, FG Malinovsky, M Tor, S de Vries and C Zipfel. The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Plant Cell 2011; 23, 2440-55.
G Tena, M Boudsocq and J Sheen. Protein kinase signaling networks in plant innate immunity. Curr. Opin. Plant Biol. 2011; 14, 519-29.
T Boller and G Felix. A renaissance of elicitors: Perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 2009; 60, 379-406.
R Willmann, HM Lajunen, G Erbs, MA Newman, D Kolb, K Tsuda, F Katagiri, J Fliegmann, JJ Bono, JV Cullimore, AK Jehle, F Gotz, A Kulik, A Molinaro, V Lipka, AA Gust and T Nurnberger. Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection. Proc. Natl. Acad. Sci. USA 2011; 108, 19824-9.
E Iizasa, M Mitsutomi and Y Nagano. Direct binding of a plant LysM receptor-like kinase, LysM RLK1/CERK1, to chitin in vitro. J. Biol. Chem. 2010; 285, 2996-3004.
A Miya, P Albert, T Shinya, Y Desaki, K Ichimura, K Shirasu, Y Narusaka, N Kawakami, H Kaku and N Shibuya. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc. Natl. Acad. Sci. USA 2007; 104, 19613-8.
EK Petutschnig, AME Jones, L Serazetdinova, U Lipka and V Lipka. The Lysin Motif Receptor-like Kinase (LysM-RLK) CERK1 is a major chitin-binding protein in Arabidopsis thaliana and subject to chitin-induced phosphorylation. J. Biol. Chem. 2010; 285, 28902-11.
J Wan, XC Zhang, D Neece, KM Ramonell, S Clough, SY Kim, MG Stacey and G Stacey. A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 2008; 20, 471-81.
J Wan, XC Zhang and G Stacey. Chitin signaling and plant disease resistance. Plant Signal. Behav. 2008; 3, 831-3.
KJ Garvey, MS Saedi and J Ito. Nucleotide sequence of Bacillus phage phi 29 genes 14 and 15; homology of gene 15 with other phage lysozymes. Nucleic Acid. Res. 1986; 14, 10001-8.
MS Saedi, KJ Garvey and J Ito. Cloning and purification of a unique lysozyme produced by Bacillus phage phi 29. Proc. Natl. Acad. Sci. USA 1987; 84, 955-8.
C Eckert, M Lecerf, L Dubost, M Arthur and S Mesnage. Functional analysis of AtlA, the major N-acetylglucosaminidase of Enterococcus faecalis. J. Bacteriol. 2006; 188, 8513-9.
A Steen, G Buist, KJ Leenhouts, M El Khattabi, F Grijpstra, AL Zomer, G Venema, OP Kuipers and J Kok. Cell wall attachment of a widely distributed peptidoglycan binding domain is hindered by cell wall constituents. J. Biol. Chem. 2003; 278, 23874-81.
A Bateman and M Bycroft. The structure of a LysM domain from E. coli membrane-bound lytic murein transglycosylase D (MltD). J. Mol. Biol. 2000; 299, 1113-9.
G Buist, A Steen, J Kok and OP Kuipers. LysM, a widely distributed protein motif for binding to (peptido)glycans. Mol. Microbiol. 2008; 68, 838-47.
XC Zhang, X Wu, S Findley, J Wan, M Libault, HT Nguyen, SB Cannon and G Stacey. Molecular evolution of lysin motif-type receptor-like kinases in plants. Plant Physiol. 2007; 144, 623-36.
J Bielnicki, Y Devedjiev, U Derewenda, Z Dauter, A Joachimiak and ZS Derewenda. B. subtilis ykuD protein at 2.0 A resolution; insights into the structure and function of a novel, ubiquitous family of bacterial enzymes. Proteins 2006; 62, 144-51.
LM Koharudin, AR Viscomi, B Montanini, MJ Kershaw, NJ Talbot, S Ottonello and AM Gronenborn. Structure-function analysis of a CVNH-LysM lectin expressed during plant infection by the rice blast fungus Magnaporthe oryzae. Structure 2011; 19, 662-74.
T Liu, Z Liu, C Song, Y Hu, Z Han, J She, F Fan, J Wang, C Jin, J Chang, JM Zhou and J Chai. Chitin-induced dimerization activates a plant immune receptor. Science 2012; 336, 1160-4.
GJ Desbrosses and J Stougaard. Root nodulation: a paradigm for how plant-microbe symbiosis influences host developmental pathways. Cell Host Microbe 2011; 10, 348-58.
JE Huddleston. Symbiosis: market economics in plant-fungus relationships. Nat. Rev. Microbiol. 2011; 9, 698-9.
M Kawaguchi and K Minamisawa. Plant-microbe communications for symbiosis. Plant Cell Physiol. 2010; 51, 1377-80.
PT Lima, VG Faria, P Patraquim, AC Ramos, JA Feijo and E Sucena. Plant-microbe symbioses: new insights into common roots. Bioessays 2009; 31, 1233-44.
C van Ooij. Symbiosis: Fungus seeks plant. Nat. Rev. Microbiol. 2011; 9, 148.
J Dénarié, F Debellé and JC Promé. Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu. Rev. Biochem. 1996; 65, 503-35.
W D’Haeze and M Holsters. Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 2002; 12, 79R-105R.
F Maillet, V Poinsot, O Andre, V Puech-Pages, A Haouy, M Gueunier, L Cromer, D Giraudet, D Formey, A Niebel, EA Martinez, H Driguez, G Becard and J Denarie. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 2011; 469, 58-63.
C Gough and J Cullimore. Lipo-chitooligosaccharide signaling in endosymbiotic plant-microbe interactions. Mol. Plant Microbe Interact. 2011; 24, 867-78.
RB Abramovitch and GB Martin. Strategies used by bacterial pathogens to suppress plant defenses. Curr. Opin. Plant Biol. 2004; 7, 356-64.
L Da Cunha, MV Sreerekha and D Mackey. Defense suppression by virulence effectors of bacterial phytopathogens. Curr. Opin. Plant Biol. 2007; 10, 349-57.
P He, L Shan and J Sheen. Elicitation and suppression of microbe‐associated molecular pattern‐triggered immunity in plant-microbe interactions. Cell. Microbiol. 2007; 9, 1385-96.
S Hou, Y Yang and JM Zhou. The multilevel and dynamic interplay between plant and pathogen. Plant Signal. Behav. 2009; 4, 283.
MD Bolton, HP van Esse, JH Vossen, R de Jonge, I Stergiopoulos, IJ Stulemeijer, GC van den Berg, O Borras-Hidalgo, HL Dekker, CG de Koster, PJ de Wit, MH Joosten and BP Thomma. The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Mol. Microbiol. 2008; 69, 119-36.
R de Jonge and BP Thomma. Fungal LysM effectors: Extinguishers of host immunity? Trends Microbiol. 2009; 17, 151-7.
R de Jonge, HP van Esse, A Kombrink, T Shinya, Y Desaki, R Bours, S van der Krol, N Shibuya, MH Joosten and BP Thomma. Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 2010; 329, 953-5.
R Marshall, A Kombrink, J Motteram, E Loza-Reyes, J Lucas, KE Hammond-Kosack, BP Thomma and JJ Rudd. Analysis of two in planta expressed LysM effector homologs from the fungus Mycosphaerella graminicola reveals novel functional properties and varying contributions to virulence on wheat. Plant Physiol. 2011; 156, 756-69.
TA Mentlak, A Kombrink, T Shinya, LS Ryder, I Otomo, H Saitoh, R Terauchi, Y Nishizawa, N Shibuya and BPHJ Thomma. Effector-mediated suppression of chitin-triggered immunity by Magnaporthe oryzae is necessary for rice blast disease. Plant Cell 2012; 24, 322-35.
Y Liang, Y Cao, K Tanaka, S Thibivilliers, J Wan, J Choi, C Kang, J Qiu and G Stacey. Nonlegumes respond to rhizobial nod factors by suppressing the innate immune response. Science 2013; 341, 1384-7.
EB Madsen, LH Madsen, S Radutoiu, M Olbryt, M Rakwalska, K Szczyglowski, S Sato, T Kaneko, S Tabata, N Sandal and J Stougaard. A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 2003; 425; 637-40.
S Radutoiu, LH Madsen, EB Madsen, HH Felle, Y Umehara, M Gronlund, S Sato, Y Nakamura, S Tabata, N Sandal and J Stougaard. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 2003; 425, 585-92.
JF Arrighi, A Barre, B Ben Amor, A Bersoult, LC Soriano, R Mirabella, F de Carvalho-Niebel, EP Journet, M Ghérardi, T Huguet, R Geurts, J Dénarié, P Rougé and C Gough. The Medicago truncatula lysin motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol. 2006; 142, 265-79.
B Ben Amor, SL Shaw, GED Oldroyd, F Maillet, RV Penmetsa, DR Cook, C Gough, SR Long, J Dénarié and C Gough. The NFP locus of Medicago truncatula controls an early step of Nod factor signal transduction upstream of a rapid calcium flux and root hair deformation. Plant J. 2003; 34, 495-506.
E Limpens, C Franken, P Smit, J Willemse, T Bisseling and R Geurts. LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 2003; 302, 630-3.
A Indrasumunar and PM Gresshoff. Duplicated nod-factor receptor 5 (NFR5) genes are mutated in soybean (Glycine max L. Merr.). Plant Signal. Behav. 2010; 5, 535-6.
A Indrasumunar, A Kereszt, I Searle, M Miyagi, D Li, CD Nguyen, A Men, BJ Carroll and PM Gresshoff. Inactivation of duplicated nod factor receptor 5 (NFR5) genes in recessive loss-of-function non-nodulation mutants of allotetraploid soybean (Glycine max L. Merr.). Plant Cell Physiol. 2010; 51, 201-14.
V Zhukov, S Radutoiu, LH Madsen, T Rychagova, E Ovchinnikova, A Borisov, I Tikhonovich and J Stougaard. The pea Sym37 receptor kinase gene controls infection-thread initiation and nodule development. Mol. Plant Microbe Interact. 2008; 21, 1600-8.
A Broghammer, L Krusell, M Blaise, J Sauer, JT Sullivan, N Maolanon, M Vinther, A Lorentzen, EB Madsen, KJ Jensen, P Roepstorff, S Thirup, CW Ronson, MB Thygesen and J Stougaard. Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding. Proc. Natl. Acad. Sci. USA 2012; 109, 13859-64.
J Fliegmann, S Canova, C Lachaud, S Uhlenbroich, V Gasciolli, C Pichereaux, M Rossignol, C Rosenberg, M Cumener, D Pitorre, B Lefebvre, C Gough, E Samain, S Fort, H Driguez, B Vauzeilles, JM Beau, A Nurisso, A Imberty, J Cullimore and JJ Bono. Lipo-chitooligosaccharidic symbiotic signals are recognized by LysM receptor-like kinase LYR3 in the legume Medicago truncatula. ACS Chem. Biol. 2013; 8, 1900-6.
KK Sørensen, JB Simonsen, NN Maolanon, J Stougaard and KJ Jensen. Chemically synthesized 58-mer LysM domain binds lipochitin oligosaccharide. Chembiochem. 2014; 15, 2097-105.
R Op den Camp, A Streng, S De Mita, Q Cao, E Polone, W Liu, JS Ammiraju, D Kudrna, R Wing, A Untergasser, T Bisseling and R Geurts. LysM-type mycorrhizal receptor recruited for rhizobium symbiosis in nonlegume Parasponia. Science 2011; 331, 909-12.
K Miyata, T Kozaki, Y Kouzai, K Ozawa, K Ishii, E Asamizu, Y Okabe, Y Umehara, A Miyamoto, Y Kobae, K Akiyama, H Kaku, Y Nishizawa, N Shibuya and T Nakagawa. The bifunctional plant receptor, OsCERK1, regulates both chitin-triggered immunity and arbuscular mycorrhizal symbiosis in rice. Plant Cell Physiol. 2014; 55, 1864-72.
X Zhang, W Dong, J Sun, F Feng, Y Deng, Z He, GE Oldroyd and E Wang. The receptor kinase CERK1 has dual functions in symbiosis and immunity signalling. Plant J. 2015; 81, 258-67.
A Genre, M Chabaud, C Balzergue, V Puech-Pagès, M Novero, T Rey, J Fournier, S Rochange, G Bécard, P Bonfante and DG Barker. Short-chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytol. 2013; 198, 190-202.
LF Czaja, C Hogekamp, P Lamm, F Maillet, EA Martinez, E Samain, J Dénarié, H Küster and N Hohnjec. Transcriptional responses toward diffusible signals from symbiotic microbes reveal MtNFP- and MtDMI3-dependent reprogramming of host gene expression by arbuscular mycorrhizal fungal lipochitooligosaccharides. Plant Physiol. 2012; 159, 1671-85.
T Boller. Chemoperception of microbial signals in plant cells. Annu. Rev. Plant Biol. 1995; 46, 189-214.
PA Passarinho and SC de Vries. Arabidopsis chitinases: A genomic survey. The Arabidopsis Book. 2002; 1, 1-25.
N Shibuya and E Minami. Oligosaccharide signalling for defence responses in plant. Physiol. Mol. Plant Pathol. 2001; 59, 223-33.
G Stacey and N Shibuya. Chitin recognition in rice and legumes. Plant Soil 1997; 194, 161-9.
M Arlorio, A Ludwig, T Boller and P Bonfante. Inhibition of fungal growth by plant chitinases and β-1, 3-glucanases. Protoplasma 1992; 171, 34-43.
F Mauch, B Mauch-Mani and T Boller. Antifungal hydrolases in pea tissue: II. Inhibition of fungal growth by combinations of chitinase and β-1, 3-glucanase. Plant Physiol. 1988; 88, 936-42.
A Schlumbaum, F Mauch, U Vögeli and T Boller. Plant chitinases are potent inhibitors of fungal growth. Nature 1986; 324, 365-7.
S Tanabe, M Okada, Y Jikumaru, H Yamane, H Kaku, N Shibuya and E Minami. Induction of resistance against rice blast fungus in rice plants treated with a potent elicitor, N-acetylchitooligosaccharide. Biosci. Biotechnol. Biochem. 2006; 70, 1599-605.
H Kaku, Y Nishizawa, N Ishii-Minami, C Akimoto-Tomiyama, N Dohmae, K Takio, E Minami and N Shibuya. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc. Natl. Acad. Sci. USA 2006; 103, 11086-91.
S Tanaka, A Ichikawa, K Yamada, G Tsuji, T Nishiuchi, M Mori, H Koga, Y Nishizawa, R O'Connell and Y Kubo. HvCEBiP: A gene homologous to rice chitin receptor CEBiP, contributes to basal resistance of barley to Magnaporthe oryzae. BMC Plant Biol. 2010; 10, 288.
WS Lee, JJ RuddJ, KE Hammond-Kosack and K Kanyuka K. Mycosphaerella graminicola LysM effector-mediated stealth pathogenesis subverts recognition through both CERK1 and CEBiP homologues in wheat. Mol. Plant Microbe Interact. 2014; 27, 236-43.
T Shimizu, T Nakano, D Takamizawa, Y Desaki, N Ishii-Minami, Y Nishizawa, E Minami, K Okada, H Yamane, H Kaku and N Shibuya. Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J. 2010; 64, 204-14.
L Zeng, AC Velasquez, KR Munkvold, J Zhang and GB Martin. A tomato LysM receptor-like kinase promotes immunity and its kinase activity is inhibited by AvrPtoB. Plant J. 2012; 69, 92-103.
J Wan, K Tanaka, X Zhang, GH Son, L Brechenmacher, THN Nguyen and G Stacey. LYK4, a LysM receptor-like kinase, is important for chitin signaling and plant innate immunity in Arabidopsis. Plant Physiol. 2012; 160, 396-406.
B Liu, JF Li, Y Ao, J Qu, Z Li, J Su, Y Zhang, J Liu, D Feng, K Qi, Y He, J Wang and HB Wang. Lysin motif-containing proteins LYP4 and LYP6 play dual roles in peptidoglycan and chitin perception in rice innate immunity. Plant Cell 2012; 24, 3406-19.
S Gimenez-Ibanez, DR Hann, V Ntoukakis, E Petutschnig, V Lipka and JP Rathjen. AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Curr. Biol. 2009; 19, 423-9.
S Gimenez-Ibanez, V Ntoukakis and JP Rathjen. The LysM receptor kinase CERK1 mediates bacterial perception in Arabidopsis. Plant Signal. Behav. 2009; 4, 539-41.
Y Ao, Z Li, D Feng, F Xiong, J Liu, JF Li, M Wang, J Wang, B Liu and HB Wang. OsCERK1 and OsRLCK176 play important roles in peptidoglycan and chitin signaling in rice innate immunity. Plant J. 2014; 80, 1072-84.
Y Kouzai, S Mochizuki, K Nakajima, Y Desaki, M Hayafune, H Miyazaki, N Yokotani, K Ozawa, E Minami, H Kaku, N Shibuya and Y Nishizawa. Targeted gene disruption of OsCERK1 reveals its indispensable role in chitin perception and involvement in the peptidoglycan response and immunity in rice. Mol. Plant Microbe Interact. 2014; 27, 975-82.
T Boller and G Felix. A renaissance of elicitors; perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 2009; 60, 379-406.
A Collmer, JL Badel, AO Charkowski, WL Deng, DE Fouts, AR Ramos, AH Rehm, DM Anderson, O Schneewind, K van Dijk and JR Alfano. Pseudomonas syringae Hrp type III secretion system and effector proteins. Proc. Natl. Acad. Sci. USA 2000; 97, 8770-7.
H Cui, T Xiang and JM Zhou. Plant immunity: A lesson from pathogenic bacterial effector proteins. Cell Microbiol. 2009; 11, 1453-61.
M Guo, F Tian, Y Wamboldt and JR Alfano. The majority of the type III effector inventory of Pseudomonas syringae pv. tomato DC3000 can suppress plant immunity. Mol. Plant Microbe Interact. 2009; 22, 1069-80.
F Martin, A Aerts, D Ahren, A Brun, EG Danchin, F Duchaussoy, J Gibon, A Kohler, E Lindquist, V Pereda, A Salamov, HJ Shapiro, J Wuyts, D Blaudez, M Buee, P Brokstein, B Canback, D Cohen, PE Courty, PM Coutinho, C Delaruelle, JC Detter, A Deveau, S DiFazio, S Duplessis, L Fraissinet-Tachet, E Lucic, P Frey-Klett, C Fourrey, I Feussner, G Gay, J Grimwood, PJ Hoegger, P Jain, S Kilaru, J Labbe, YC Lin, V Legue, F Le Tacon, R Marmeisse, D Melayah, B Montanini, M Muratet, U Nehls, H Niculita-Hirzel, MP Oudot-Le Secq, M Peter, H Quesneville, B Rajashekar, M Reich, N Rouhier, J Schmutz, T Yin, M Chalot, B Henrissat, U Kues, S Lucas, Y Van de Peer, GK Podila , A Polle, PJ Pukkila, PM Richardson, P Rouze, IR Sanders, JE Stajich, A Tunlid, G Tuskan and IV Grigorie. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 2008; 452, 88-92.
E Giraud, L Moulin, D Vallenet, V Barbe, E Cytryn, JC Avarre, M Jaubert, D Simon, F Cartieaux, Y Prin, G Bena, L Hannibal, J Fardoux, M Kojadinovic, L Vuillet, A Lajus, S Cruveiller, Z Rouy, S Mangenot, B Segurens, C Dossat, WL Franck, WS Chang, E Saunders, D Bruce, P Richardson, P Normand, B Dreyfus, D Pignol, G Stacey, D Emerich, A Verméglio, C Médigue and M Sadowsky. Legumes symbioses: Absence of Nod genes in photosynthetic bradyrhizobia. Science 2007; 316, 1307-12.
C Gough and C Jacquet. Nod factor perception protein carries weight in biotic interactions. Trend. Plant Sci. 2013; 18, 566-74.
T Rey, A Nars, M Bonhomme, A Bottin, S Huguet, S Balzergue, MF Jardinaud, JJ Bono, J Cullimore, B Dumas, C Gough and C Jacquet. NFP, a LysM protein controlling Nod factor perception, also intervenes in Medicago truncatula resistance to pathogens. New Phytol. 2013; 198, 875-86.
Y Brotman, U Landau, S Pnini, J Lisec, S Balazadeh, B Mueller-Roeber, A Zilberstein, L Willmitzer, I Chet and A Viterbo. The LysM receptor-like kinase LysM RLK1 is required to activate defense and abiotic-stress responses induced by overexpression of fungal chitinases in Arabidopsis plants. Mol. Plant. 2012; 5, 1113-24.
C Paparella, DV Savatin, L Marti, G De Lorenzo and S Ferrari. The Arabidopsis Lysin motif-containing receptor-like kinase3 regulates the cross talk between immunity and abscisic acid responses. Plant Physiol. 2014; 165, 262-76.
J Wan and G Pentecost. Potential application of chitin signaling in engineering broad-spectrum disease resistance to fungal and bacterial pathogens in plants. Adv. Crop Sci. Tech. 2013; 1, 1000e103.