Cell wall associated immunity in plants

Jiangxue Wan, Min He, Qingqing Hou, Lijuan Zou, Yihua Yang, Yan Wei, Xuewei Chen

Stress Biology ›› 2021, Vol. 1 ›› Issue (1) : 3. DOI: 10.1007/s44154-021-00003-4
Review

Cell wall associated immunity in plants

Author information +
History +

Abstract

The plant cell wall is the first physical and defensive barrier against pathogens. The plant cell wall usually undergoes dynamic remodeling as an immune response to prevent infection by pathogens. In this review, we summarize advances on relationship between cell wall and immunity in plants. In particular, we outline current progresses regarding the regulation of the cell wall components, including cellulose, hemicellulose, pectin and lignin, on plant disease resistance. We also discuss the impacts of cell wall-derived cellodextrin, oligogalacturonic acid and xyloglucan/xylan oligosaccharides as potent elicitors or signal molecules to trigger plant immune response. We further propose future studies on dissecting the molecular regulation of cell wall on plant immunity, which have potentials in practical application of crop breeding aiming at improvement of plant disease resistance.

Keywords

Cell wall / Oligosaccharides / Elicitor / Plant immunity / Disease resistance

Cite this article

Download citation ▾
Jiangxue Wan, Min He, Qingqing Hou, Lijuan Zou, Yihua Yang, Yan Wei, Xuewei Chen. Cell wall associated immunity in plants. Stress Biology, 2021, 1(1): 3 https://doi.org/10.1007/s44154-021-00003-4

References

[1]
Aimanianda V, Clavaud C, Simenel C, Fontaine T, Delepierre M, Latge JP (2009) Cell wall β-(1,6)-glucan of Saccharomyces cerevisiae: structural characterization and in situ synthesis. J Biol Chem. 284(20):13401–13412. https://doi.org/10.1074/jbc.M807667200
[2]
AnSH, SohnKH, ChoiHW, HwangIS, LeeSC, HwangBK. Pepper pectin methylesterase inhibitor protein CaPMEI1 is required for antifungal activity, basal disease resistance and abiotic stress tolerance. Planta., 2008, 228(1):61-78
CrossRef Google scholar
[3]
AranaDM, PrietoD, RomanE, NombelaC, Alonso-MongeR, PlaJ. The role of the cell wall in fungal pathogenesis. Microb Biotechnol., 2009, 2(3):308-320
CrossRef Google scholar
[4]
AzizA, GauthierA, BezierA, PoinssotB, JoubertJM, PuginA, et al.. Elicitor and resistance-inducing activities of β-1,4 cellodextrins in grapevine, comparison with β-1,3 glucans and α-1,4 oligogalacturonides. J Exp Bot., 2007, 58(6):1463-1472
CrossRef Google scholar
[5]
AzizA, HeyraudA, LambertB. Oligogalacturonide signal transduction, induction of defense-related responses and protection of grapevine against Botrytis cinerea. Planta., 2004, 218(5):767-774
CrossRef Google scholar
[6]
Bacete L, Hamann T (2020) The Role of mechanoperception in plant cell wall integrity maintenance. Plants (Basel) 9(5). https://doi.org/10.3390/plants9050574
[7]
BaceteL, MelidaH, MiedesE, MolinaA. Plant cell wall-mediated immunity: cell wall changes trigger disease resistance responses. Plant J., 2018, 93(4):614-636
CrossRef Google scholar
[8]
BenedettiM, VerrascinaI, PontiggiaD, LocciF, MatteiB, De LorenzoG, et al.. Four Arabidopsis berberine bridge enzyme-like proteins are specific oxidases that inactivate the elicitor-active oligogalacturonides. Plant J., 2018, 94(2):260-273
CrossRef Google scholar
[9]
BethkeG, ThaoA, XiongG, LiB, SoltisNE, HatsugaiN, et al.. Pectin biosynthesis is critical for cell wall integrity and immunity in Arabidopsis thaliana. Plant Cell., 2016, 28(2):537-556
CrossRef Google scholar
[10]
Blanco-UlateB, Morales-CruzA, AmrineKC, LabavitchJM, PowellAL, CantuD. Genome-wide transcriptional profiling of Botrytis cinerea genes targeting plant cell walls during infections of different hosts. Front Plant Sci., 2014, 5: 435
CrossRef Google scholar
[11]
BordenaveM, GoldbergR, HuetJC, PernolletJC. A novel protein from mung bean hypocotyl cell walls with acetyl esterase activity. Phytochemistry., 1995, 38(2):315-319
CrossRef Google scholar
[12]
BrenyaE, TrusovY, DietzgenRG, BotellaJR. Heterotrimeric G-proteins facilitate resistance to plant pathogenic viruses in Arabidopsis thaliana (L.) Heynh. Plant Signal Behav, 2016, 11(8):e1212798
CrossRef Google scholar
[13]
BrownDM, ZeefLA, EllisJ, GoodacreR, TurnerSR. Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell., 2005, 17(8):2281-2295
CrossRef Google scholar
[14]
BrutusA, SiciliaF, MaconeA, CervoneF, De LorenzoG. A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc Natl Acad Sci USA., 2010, 107(20):9452-9457
CrossRef Google scholar
[15]
CaffallKH, MohnenD. The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res., 2009, 344(14):1879-1900
CrossRef Google scholar
[16]
Cao Y, Liang Y, Tanaka K, Nguyen CT, Jedrzejczak RP, Joachimiak A et al (2014) The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1. Elife. 3. https://doi.org/10.7554/eLife.03766
[17]
CarpitaNC, GibeautDM. Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J., 1993, 3(1):1-30
CrossRef Google scholar
[18]
CasasoliM, SpadoniS, LilleyKS, CervoneF, De LorenzoG, MatteiB. Identification by 2-D DIGE of apoplastic proteins regulated by oligogalacturonides in Arabidopsis thaliana. Proteomics., 2008, 8(5):1042-1054
CrossRef Google scholar
[19]
ChassotC, NawrathC, MetrauxJP. Cuticular defects lead to full immunity to a major plant pathogen. Plant J., 2007, 49(6):972-980
CrossRef Google scholar
[20]
ChassotC, NawrathC, MétrauxJP. The cuticle: not only a barrier for plant defence: A novel defence syndrome in plants with cuticular defects. Plant Signal Behav., 2008, 3(2):142-144
CrossRef Google scholar
[21]
ChenF, DixonRA. Lignin modification improves fermentable sugar yields for biofuel production. Nat Biotechnol., 2007, 25(7):759-761
CrossRef Google scholar
[22]
ChowdhuryJ, LuckS, RajaramanJ, DouchkovD, ShirleyNJ, SchwerdtJG, et al.. Altered expression of genes implicated in xylan biosynthesis affects penetration resistance against powdery mildew. Front Plant Sci., 2017, 8: 445
CrossRef Google scholar
[23]
ClaverieJ, BalaceyS, Lemaitre-GuillierC, BruleD, ChiltzA, GranetL, et al.. The cell wall-derived xyloglucan is a new DAMP triggering plant immunity in Vitis vinifera and Arabidopsis thaliana. Front Plant Sci., 2018, 9: 1725
CrossRef Google scholar
[24]
CosgroveDJ. Growth of the plant cell wall. Nat Rev Mol Cell Biol., 2005, 6(11):850-861
CrossRef Google scholar
[25]
Davidsson P, Broberg M, Kariola T, Sipari N, Pirhonen M, Palva ET (2017) Short oligogalacturonides induce pathogen resistance-associated gene expression in Arabidopsis thaliana. BMC Plant Biol. 17(1):19. https://doi.org/10.1186/s12870-016-0959-1
[26]
DavisKR, DarvillAG, AlbersheimP, DellA. Host-Pathogen Interactions. XXIX oligogalacturonides released from sodium polypectate by endopolygalacturonic acid lyase are elicitors of phytoalexins in soybean. Plant Physiol., 1986, 80(2):568-577
CrossRef Google scholar
[27]
DecreuxA, MessiaenJ. Wall-associated kinase WAK1 interacts with cell wall pectins in a calcium-induced conformation. Plant Cell Physiol., 2005, 46(2):268-278
CrossRef Google scholar
[28]
DecreuxA, ThomasA, SpiesB, BrasseurR, CutsemPV, MessiaenJ. In vitro characterization of the homogalacturonan-binding domain of the wall-associated kinase WAK1 using site-directed mutagenesis. Phytochemistry., 2006, 67(11):1068-1079
CrossRef Google scholar
[29]
Del HierroI, MelidaH, BroyartC, SantiagoJ, MolinaA. Computational prediction method to decipher receptor-glycoligand interactions in plant immunity. Plant J., 2021, 105(6):1710-1726
CrossRef Google scholar
[30]
Delgado-CerezoM, Sanchez-RodriguezC, EscuderoV, MiedesE, FernandezPV, JordaL, et al.. Arabidopsis heterotrimeric G-protein regulates cell wall defense and resistance to necrotrophic fungi. Mol Plant., 2012, 5(1):98-114
CrossRef Google scholar
[31]
DelteilA, GobbatoE, CayrolB, EstevanJ, Michel-RomitiC, DievartA, et al.. Several wall-associated kinases participate positively and negatively in basal defense against rice blast fungus. BMC Plant Biol., 2016, 16: 17
CrossRef Google scholar
[32]
DenouxC, GallettiR, MammarellaN, GopalanS, WerckD, De LorenzoG, et al.. Activation of defense response pathways by OGs and Flg22 elicitors in Arabidopsis seedlings. Mol Plant., 2008, 1(3):423-445
CrossRef Google scholar
[33]
DesprezT, JuraniecM, CrowellEF, JouyH, PochylovaZ, ParcyF, et al.. Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA., 2007, 104(39):15572
CrossRef Google scholar
[34]
DouchkovD, LueckS, HenselG, KumlehnJ, RajaramanJ, JohrdeA, et al.. The barley (Hordeum vulgare) cellulose synthase-like D2 gene (HvCslD2) mediates penetration resistance to host-adapted and nonhost isolates of the powdery mildew fungus. New Phytol., 2016, 212(2):421-433
CrossRef Google scholar
[35]
D'OvidioR, MatteiB, RobertiS, BellincampiD. Polygalacturonases, polygalacturonase-inhibiting proteins and pectic oligomers in plant-pathogen interactions. Biochim Biophys Acta., 2004, 1696(2):237-244
CrossRef Google scholar
[36]
EllisC, KarafyllidisI, WasternackC, TurnerJG. The Arabidopsis mutant cev1 links cell wall signaling to jasmonate and ethylene responses. Plant Cell., 2002, 14(7):1557-1566
CrossRef Google scholar
[37]
EngelsdorfT, HamannT. An update on receptor-like kinase involvement in the maintenance of plant cell wall integrity. Ann Bot., 2014, 114(6):1339-1347
CrossRef Google scholar
[38]
EngelsdorfT, WillC, HofmannJ, SchmittC, MerrittBB, RiegerL, et al.. Cell wall composition and penetration resistance against the fungal pathogen Colletotrichum higginsianum are affected by impaired starch turnover in Arabidopsis mutants. J Exp Bot., 2017, 68(3):701-713
CrossRef Google scholar
[39]
EscuderoV, JordáL, Sopeña-TorresS, MélidaH, MiedesE, Muñoz-BarriosA, et al.. Alteration of cell wall xylan acetylation triggers defense responses that counterbalance the immune deficiencies of plants impaired in the β-subunit of the heterotrimeric G-protein. Plant J., 2017, 92(3):386-399
CrossRef Google scholar
[40]
FerrariS, GallettiR, DenouxC, De LorenzoG, AusubelFM, DewdneyJ. Resistance to Botrytis cinerea induced in Arabidopsis by elicitors is independent of salicylic acid, ethylene, or jasmonate signaling but requires PHYTOALEXIN DEFICIENT3. Plant Physiol., 2007, 144(1):367-379
CrossRef Google scholar
[41]
FerrariS, GallettiR, PontiggiaD, ManfrediniC, LionettiV, BellincampiD, et al.. Transgenic expression of a fungal endo-polygalacturonase increases plant resistance to pathogens and reduces auxin sensitivity. Plant Physiol., 2008, 146(2):669-681
CrossRef Google scholar
[42]
FisherJF, MobasheryS. Constructing and deconstructing the bacterial cell wall. Protein Sci., 2020, 29(3):629-646
CrossRef Google scholar
[43]
FlorsV, Leyva MdeL, VicedoB, FinitiI, RealMD, Garcia-AgustinP, et al.. Absence of the endo-β-1,4-glucanases Cel1 and Cel2 reduces susceptibility to Botrytis cinerea in tomato. Plant J., 2007, 52(6):1027-1040
CrossRef Google scholar
[44]
Fontaine T, Simenel C, Dubreucq G, Adam O, Delepierre M, Lemoine J et al (2000) Molecular organization of the alkali-insoluble fraction of Aspergillus fumigatus cell wall. J Biol Chem. 275(36):27594–27607. https://doi.org/10.1074/jbc.M909975199
[45]
FreeSJ. Fungal cell wall organization and biosynthesis. Adv Genet., 2013, 81: 33-82
CrossRef Google scholar
[46]
Gallego-GiraldoL, JikumaruY, KamiyaY, TangY, DixonRA. Selective lignin downregulation leads to constitutive defense response expression in alfalfa (Medicago sativa L.). New Phytol., 2011, 190(3):627-639
CrossRef Google scholar
[47]
GallettiR, DenouxC, GambettaS, DewdneyJ, AusubelFM, De LorenzoG, et al.. The AtrbohD-mediated oxidative burst elicited by oligogalacturonides in Arabidopsis is dispensable for the activation of defense responses effective against Botrytis cinerea. Plant Physiol., 2008, 148(3):1695-1706
CrossRef Google scholar
[48]
GallettiR, FerrariS, De LorenzoG. Arabidopsis MPK3 and MPK6 play different roles in basal and oligogalacturonide- or flagellin-induced resistance against Botrytis cinerea. Plant Physiol., 2011, 157(2):804-814
CrossRef Google scholar
[49]
GaoY, HeC, ZhangD, LiuX, XuZ, TianY, et al.. Two trichome birefringence-like proteins mediate xylan acetylation, which is essential for leaf blight resistance in rice. Plant Physiol., 2017, 173(1):470-481
CrossRef Google scholar
[50]
Gigli-BiscegliaN, EngelsdorfT, HamannT. Plant cell wall integrity maintenance in model plants and crop species-relevant cell wall components and underlying guiding principles. Cell Mol Life Sci., 2020, 77(11):2049-2077
CrossRef Google scholar
[51]
GilleS, de SouzaA, XiongG, BenzM, ChengK, SchultinkA, et al.. O-acetylation of Arabidopsis hemicellulose xyloglucan requires AXY4 or AXY4L, proteins with a TBL and DUF231 domain. Plant Cell., 2011, 23(11):4041-4053
CrossRef Google scholar
[52]
GilleS, PaulyM. O-acetylation of plant cell wall polysaccharides. Front Plant Sci., 2012, 3: 12
CrossRef Google scholar
[53]
GlazebrookJ. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol., 2005, 43: 205-227
CrossRef Google scholar
[54]
Gomez-GomezE, IsabelM, RonceroG, Di PietroA, HeraC. Molecular characterization of a novel endo-β-1,4-xylanase gene from the vascular wilt fungus Fusarium oxysporum. Curr Genet., 2001, 40(4):268-275
CrossRef Google scholar
[55]
Gonzalez-PerezL, PerrottaL, AcostaA, OrellanaE, SpadaforaN, BrunoL, et al.. In tobacco BY-2 cells xyloglucan oligosaccharides alter the expression of genes involved in cell wall metabolism, signalling, stress responses, cell division and transcriptional control. Mol Biol Rep., 2014, 41(10):6803-6816
CrossRef Google scholar
[56]
GrunCH, HochstenbachF, HumbelBM, VerkleijAJ, SietsmaJH, KlisFM, et al.. The structure of cell wall alpha-glucan from fission yeast. Glycobiology., 2005, 15(3):245-257
CrossRef Google scholar
[57]
GuX, Bar-PeledM. The biosynthesis of UDP-galacturonic acid in plants. Functional cloning and characterization of Arabidopsis UDP-D-glucuronic acid 4-epimerase. Plant Physiol., 2004, 136(4):4256-4264
CrossRef Google scholar
[58]
HamannT, BennettM, MansfieldJ, SomervilleC. Identification of cell-wall stress as a hexose-dependent and osmosensitive regulator of plant responses. Plant J, 2009, 57(6):1015-1026
CrossRef Google scholar
[59]
HarholtJ, SuttangkakulA, VibeSH. Biosynthesis of pectin. Plant physiol., 2010, 153(2):384
CrossRef Google scholar
[60]
HarutaM, SabatG, SteckerK, MinkoffBB, SussmanMR. A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science., 2014, 343(6169):408-411
CrossRef Google scholar
[61]
HematyK, SadoPE, Van TuinenA, RochangeS, DesnosT, BalzergueS, et al.. A receptor-like kinase mediates the response of Arabidopsis cells to the inhibition of cellulose synthesis. Curr Biol., 2007, 17(11):922-931
CrossRef Google scholar
[62]
Hernandez-BlancoC, FengDX, HuJ, Sanchez-ValletA, DeslandesL, LlorenteF, et al.. Impairment of cellulose synthases required for Arabidopsis secondary cell wall formation enhances disease resistance. Plant Cell., 2007, 19(3):890-903
CrossRef Google scholar
[63]
HofteH, VoxeurA. Plant cell walls. Curr Biol., 2017, 27(17):R865-RR70
CrossRef Google scholar
[64]
HuangJ, GuM, LaiZ, FanB, ShiK, ZhouYH, et al.. Functional analysis of the Arabidopsis PAL gene family in plant growth, development, and response to environmental stress. Plant Physiol., 2010, 153(4):1526-1538
CrossRef Google scholar
[65]
HuckelhovenR. Cell wall-associated mechanisms of disease resistance and susceptibility. Annu Rev Phytopathol., 2007, 45: 101-127
CrossRef Google scholar
[66]
JinC. Protein glycosylation in Aspergillus fumigatus is essential for cell wall synthesis and serves as a promising model of multicellular eukaryotic development. Int J Microbiol., 2012, 2012: 654251
CrossRef Google scholar
[67]
JohnsonJM, ThurichJ, PetutschnigEK, AltschmiedL, MeichsnerD, SherametiI, et al.. A poly(A) ribonuclease controls the cellotriose-based interaction between Piriformospora indica and its host Arabidopsis. Plant Physiol., 2018, 176(3):2496-2514
CrossRef Google scholar
[68]
JonesJD, DanglJL. The plant immune system. Nature., 2006, 444(7117):323-329
CrossRef Google scholar
[69]
KlisFM, de GrootP, HellingwerfK. Molecular organization of the cell wall of Candida albicans. Med mycol., 2001, 39(Suppl 1):1-8
CrossRef Google scholar
[70]
KohornBD, JohansenS, ShishidoA, TodorovaT, MartinezR, DefeoE, et al.. Pectin activation of MAP kinase and gene expression is WAK2 dependent. Plant J., 2009, 60(6):974-982
CrossRef Google scholar
[71]
KohornBD, KohornSL. The cell wall-associated kinases, WAKs, as pectin receptors. Front Plant Sci., 2012, 3: 88
CrossRef Google scholar
[72]
KubicekCP, StarrTL, GlassNL. Plant cell wall-degrading enzymes and their secretion in plant-pathogenic fungi. Annu Rev Phytopathol., 2014, 52: 427-451
CrossRef Google scholar
[73]
LeeC, TengQ, ZhongR, YeZH. The four Arabidopsis reduced wall acetylation genes are expressed in secondary wall-containing cells and required for the acetylation of xylan. Plant Cell Physiol., 2011, 52(8):1289-1301
CrossRef Google scholar
[74]
LevS, HorwitzBA. A mitogen-activated protein kinase pathway modulates the expression of two cellulase genes in Cochliobolus heterostrophus during plant infection. Plant Cell., 2003, 15(4):835-844
CrossRef Google scholar
[75]
LiH, ZhouSY, ZhaoWS, SuSC, PengYL. A novel wall-associated receptor-like protein kinase gene, OsWAK1, plays important roles in rice blast disease resistance. Plant Mol Biol., 2009, 69(3):337-346
CrossRef Google scholar
[76]
Li Q, Fu J, Qin X, Yang W, Qi J, Li Z et al (2020a) Systematic analysis and functional validation of citrus pectin acetylesterases (CsPAEs) reveals that CsPAE2 negatively regulates citrus bacterial canker development. Int J Mol Sci 21(24). https://doi.org/10.3390/ijms21249429
[77]
LiW, WangK, ChernM, LiuY, ZhuZ, LiuJ, et al.. Sclerenchyma cell thickening through enhanced lignification induced by OsMYB30 prevents fungal penetration of rice leaves. New Phytol., 2020, 226(6):1850-1863
CrossRef Google scholar
[78]
Lin W, Tang W, Anderson CT, Yang Z (2018) FERONIA’s sensing of cell wall pectin activates ROP GTPase signaling in Arabidopsis. bioRxiv:269647. https://doi.org/10.1101/269647
[79]
LionettiV, CervoneF, BellincampiD. Methyl esterification of pectin plays a role during plant-pathogen interactions and affects plant resistance to diseases. J Plant Physiol., 2012, 169(16):1623-1630
CrossRef Google scholar
[80]
LionettiV, RaiolaA, CamardellaL, GiovaneA, ObelN, PaulyM, et al.. Overexpression of pectin methylesterase inhibitors in Arabidopsis restricts fungal infection by Botrytis cinerea. Plant Physiol., 2007, 143(4):1871-1880
CrossRef Google scholar
[81]
LionettiV, RaiolaA, CervoneF, BellincampiD. Transgenic expression of pectin methylesterase inhibitors limits tobamovirus spread in tobacco and Arabidopsis. Mol Plant Pathol., 2014, 15(3):265-274
CrossRef Google scholar
[82]
LiuN, SunY, PeiY, ZhangX, WangP, LiX, et al.. A pectin methylesterase inhibitor enhances resistance to Verticillium Wilt. Plant Physiol., 2018, 176(3):2202-2220
CrossRef Google scholar
[83]
LiuS, WangJ, HanZ, GongX, ZhangH, ChaiJ. Molecular mechanism for fungal cell wall recognition by rice chitin receptor OsCEBiP. Structure., 2016, 24(7):1192-1200
CrossRef Google scholar
[84]
LiuT, LiuZ, SongC, HuY, HanZ, SheJ, et al.. Chitin-induced dimerization activates a plant immune receptor. Science., 2012, 336(6085):1160-1164
CrossRef Google scholar
[85]
LocciF, BenedettiM, PontiggiaD, CittericoM, CaprariC, MatteiB, et al.. An Arabidopsis berberine bridge enzyme-like protein specifically oxidizes cellulose oligomers and plays a role in immunity. Plant J., 2019, 98(3):540-554
CrossRef Google scholar
[86]
LombardV, BernardT, RancurelC, BrumerH, CoutinhoPM, HenrissatB. A hierarchical classification of polysaccharide lyases for glycogenomics. Biochem J., 2010, 432(3):437-444
CrossRef Google scholar
[87]
Lopez-CruzJ, FinitiI, Fernandez-CrespoE, Crespo-SalvadorO, Garcia-AgustinP, Gonzalez-BoschC. Absence of endo-1,4-β-glucanase KOR1 alters the jasmonate-dependent defence response to Pseudomonas syringae in Arabidopsis. J Plant Physiol., 2014, 171(16):1524-1532
CrossRef Google scholar
[88]
LunaE, PastorV, RobertJ, FlorsV, Mauch-ManiB, TonJ. Callose deposition: a multifaceted plant defense response. Mol Plant Microbe Interact., 2010, 24(2):183-193
CrossRef Google scholar
[89]
MaZ, SongT, ZhuL, YeW, WangY, ShaoY, et al.. A phytophthora sojae glycoside hydrolase 12 protein is a major virulence factor during soybean infection and is recognized as a PAMP. Plant Cell., 2015, 27(7):2057-2072
CrossRef Google scholar
[90]
MaZ, ZhuL, SongT, WangY, ZhangQ, XiaY, et al.. A paralogous decoy protects Phytophthora sojae apoplastic effector PsXEG1 from a host inhibitor. Science., 2017, 355(6326):710-714
CrossRef Google scholar
[91]
ManabeY, NafisiM, VerhertbruggenY, OrfilaC, GilleS, RautengartenC, et al.. Loss-of-function mutation of REDUCED WALL ACETYLATION2 in Arabidopsis leads to reduced cell wall acetylation and increased resistance to Botrytis cinerea. Plant Physiol., 2011, 155(3):1068-1078
CrossRef Google scholar
[92]
ManabeY, VerhertbruggenY, GilleS, HarholtJ, ChongSL, PawarPM, et al.. Reduced wall acetylation proteins play vital and distinct roles in cell wall O-acetylation in Arabidopsis. Plant Physiol., 2013, 163(3):1107-1117
CrossRef Google scholar
[93]
MangH, FengB, HuZ, Boisson-DernierA, FranckCM, MengX, et al.. Differential regulation of two-tiered plant immunity and sexual reproduction by ANXUR receptor-like kinases. Plant Cell., 2017, 29(12):3140-3156
CrossRef Google scholar
[94]
Mary WanjiruW, ZhenshengK, BuchenauerH. Importance of cell wall degrading enzymes produced by Fusarium graminearum during infection of wheat heads. Eur J Plant Pathol., 2002, 108(8):803-810
CrossRef Google scholar
[95]
Masachis S, Segorbe D, Turrà D, Leon-Ruiz M, Fürst U, El Ghalid M et al (2016) A fungal pathogen secretes plant alkalinizing peptides to increase infection. Nat Microbiol 1(6). https://doi.org/10.1038/nmicrobiol.2016.43
[96]
McMillanGP, HedleyD, FyffeL, PérombelonMCM. Potato resistance to soft-rot erwinias is related to cell wall pectin esterification. Physiol Mol Plant P., 1993, 42(4):279-289
CrossRef Google scholar
[97]
MelidaH, BaceteL, RuprechtC, RebaqueD, Del HierroI, LopezG, et al.. Arabinoxylan-oligosaccharides act as damage associated molecular patterns in plants regulating disease resistance. Front Plant Sci., 2020, 11: 1210
CrossRef Google scholar
[98]
Mélida H, Largo-Gosens A, Novo-Uzal E, Santiago R, Pomar F, García P et al (2015) Ectopic lignification in primary cellulose-deficient cell walls of maize cell suspension cultures. J Integr Plant Biol. 57(4):357–372. https://doi.org/10.1111/jipb.12346
[99]
MelidaH, Sopena-TorresS, BaceteL, Garrido-ArandiaM, JordaL, LopezG, et al.. Non-branched β-1,3-glucan oligosaccharides trigger immune responses in Arabidopsis. Plant J., 2018, 93(1):34-49
CrossRef Google scholar
[100]
MertzRA, OlekAT, CarpitaNC. Alterations in cell-wall glycosyl linkage structure of Arabidopsis murus mutants. Carbohydrate Polymers., 2012, 89(2):331-339
CrossRef Google scholar
[101]
MiedesE, VanholmeR, BoerjanW, MolinaA. The role of the secondary cell wall in plant resistance to pathogens. Front Plant Sci., 2014, 5: 358
CrossRef Google scholar
[102]
NicaiseV, RouxM, ZipfelC. Recent advances in PAMP-triggered immunity against bacteria: pattern recognition receptors watch over and raise the alarm. Plant Physiol., 2009, 150(4):1638-1647
CrossRef Google scholar
[103]
NitureSK, KumarAR, PantA. Role of glucose in production and repression of polygalacturonase and pectate lyase from phytopathogenic fungus Fusarium moniliforme NCIM 1276. World J Microb and Biot., 2006, 22(9):893-899
CrossRef Google scholar
[104]
O'NeillM, AlbersheimP. DeyPM. Darvill A. 12 - The pectic polysaccharides of primary cell walls. Methods in Plant Biochemistry, 1990 Academic Press 415-441
CrossRef Google scholar
[105]
OsorioS, CastillejoC, QuesadaMA, Medina-EscobarN, BrownseyGJ, SuauR, et al.. Partial demethylation of oligogalacturonides by pectin methyl esterase 1 is required for eliciting defence responses in wild strawberry (Fragaria vesca). Plant J., 2008, 54(1):43-55
CrossRef Google scholar
[106]
PanstrugaR, ParkerJE, Schulze-LefertP. SnapShot: Plant immune response pathways. Cell, 2009, 136(5):978 e1-978 e3
CrossRef Google scholar
[107]
ParkYB, CosgroveDJ. Xyloglucan and its interactions with other components of the growing cell wall. Plant Cell Physiol., 2015, 56(2):180-194
CrossRef Google scholar
[108]
PaulyM, QinQ, GreeneH, AlbersheimP, DarvillA, YorkWS. Changes in the structure of xyloglucan during cell elongation. Planta., 2001, 212(5):842-850
CrossRef Google scholar
[109]
PaulyM, SchellerHV. O-Acetylation of plant cell wall polysaccharides: identification and partial characterization of a rhamnogalacturonan O-acetyl-transferase from potato suspension-cultured cells. Planta., 2000, 210(4):659-667
CrossRef Google scholar
[110]
PerssonS, ParedezA, CarrollA, PalsdottirH, DoblinM, PoindexterP, et al.. Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis. Proc Natl Acad Sci USA., 2007, 104(39):15566
CrossRef Google scholar
[111]
PhilippeF, PellouxJ, RayonC. Plant pectin acetylesterase structure and function: new insights from bioinformatic analysis. BMC Genomics., 2017, 18(1):456
CrossRef Google scholar
[112]
PogorelkoG, LionettiV, FursovaO, SundaramRM, QiM, WhithamSA, et al.. Arabidopsis and Brachypodium distachyon transgenic plants expressing Aspergillus nidulans acetylesterases have decreased degree of polysaccharide acetylation and increased resistance to pathogens. Plant Physiol., 2013, 162(1):9-23
CrossRef Google scholar
[113]
QuS, ZhangX, SongY, LinJ, ShanX. THESEUS1 positively modulates plant defense responses against Botrytis cinerea through GUANINE EXCHANGE FACTOR4 signaling. J Integr Plant Biol., 2017, 59(11):797-804
CrossRef Google scholar
[114]
RaesJ, RohdeA, ChristensenJH, Van de PeerY, BoerjanW. Genome-wide characterization of the lignification toolbox in Arabidopsis. Plant Physiol., 2003, 133(3):1051-1071
CrossRef Google scholar
[115]
RaiolaA, LionettiV, ElmaghrabyI, ImmerzeelP, MellerowiczEJ, SalviG, et al.. Pectin methylesterase is induced in Arabidopsis upon infection and is necessary for a successful colonization by necrotrophic pathogens. Mol Plant Microbe Interact., 2010, 24(4):432-440
CrossRef Google scholar
[116]
RamirezV, AgorioA, CoegoA, Garcia-AndradeJ, HernandezMJ, BalaguerB, et al.. MYB46 modulates disease susceptibility to Botrytis cinerea in Arabidopsis. Plant Physiol., 2011, 155(4):1920-1935
CrossRef Google scholar
[117]
RandouxB, Renard-MerlierD, MulardG, RossardS, DuymeF, SanssenéJ, et al.. Distinct defenses induced in wheat against powdery mildew by acetylated and nonacetylated oligogalacturonides. Phytopathology., 2010, 100(12):1352-1363
CrossRef Google scholar
[118]
Rebaque D, Del Hierro I, Lopez G, Bacete L, Vilaplana F, Dallabernardina P et al (2021) Cell wall-derived mixed-linked β-1,3/1,4-glucans trigger immune responses and disease resistance in plants. Plant J. https://doi.org/10.1111/tpj.15185
[119]
RidleyBL, O'NeillMA, MohnenD. Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry., 2001, 57(6):929-967
CrossRef Google scholar
[120]
RobertS, MouilleG, HöfteH. The mechanism and regulation of cellulose synthesis in primary walls: lessons from cellulose-deficient Arabidopsis mutants. Cellulose., 2004, 11(3):351-364
CrossRef Google scholar
[121]
RogersLA, DubosC, SurmanC, WillmentJ, CullisIF, MansfieldSD, et al.. Comparison of lignin deposition in three ectopic lignification mutants. New Phytol., 2005, 168(1):123-140
CrossRef Google scholar
[122]
RohdeA, MorreelK, RalphJ, GoeminneG, HostynV, De RyckeR, et al.. Molecular phenotyping of the pal1 and pal2 mutants of Arabidopsis thaliana reveals far-reaching consequences on phenylpropanoid, amino acid, and carbohydrate metabolism. Plant Cell., 2004, 16(10):2749-2771
CrossRef Google scholar
[123]
RovenichH, ZuccaroA, ThommaBP. Convergent evolution of filamentous microbes towards evasion of glycan-triggered immunity. New Phytol., 2016, 212(4):896-901
CrossRef Google scholar
[124]
Salvador P, Lasserre T (2010) Inventors; ELICITYL, assignee. Process for increasing plants resistance to an abiotic stress. 2010/08/03/Application date.
[125]
SampedroJ, PardoB, GianzoC, GuitianE, RevillaG, ZarraI. Lack of α-xylosidase activity in Arabidopsis alters xyloglucan composition and results in growth defects. Plant Physiol., 2010, 154(3):1105-1115
CrossRef Google scholar
[126]
SavatinDV, BiscegliaNG, MartiL, FabbriC, CervoneF, De LorenzoG. The Arabidopsis NUCLEUS- AND PHRAGMOPLAST-LOCALIZED KINASE1-related protein kinases are required for elicitor-induced oxidative burst and immunity. Plant Physiol., 2014, 165(3):1188-1202
CrossRef Google scholar
[127]
SchellerHV, UlvskovP. Hemicelluloses. Annu Rev Plant Biol., 2010, 61: 263-289
CrossRef Google scholar
[128]
SchultinkA, LiuL, ZhuL, PaulyM. Structural diversity and function of xyloglucan sidechain substituents. Plants (Basel)., 2014, 3(4):526-542
CrossRef Google scholar
[129]
SchulzeB, MentzelT, JehleAK, MuellerK, BeelerS, BollerT, et al.. Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1. J Biol Chem., 2010, 285(13):9444-9451
CrossRef Google scholar
[130]
ShakuM, EalandC, MatlhabeO, LalaR, KanaBD. Peptidoglycan biosynthesis and remodeling revisited. Adv Appl Microbiol., 2020, 112: 67-103
CrossRef Google scholar
[131]
ShimizuT, NakanoT, TakamizawaD, DesakiY, Ishii-MinamiN, NishizawaY, et al.. Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J., 2010, 64(2):204-214
CrossRef Google scholar
[132]
SieberP, SchorderetM, RyserU, BuchalaA, KolattukudyP, MétrauxJP, et al.. Transgenic Arabidopsis plants expressing a fungal cutinase show alterations in the structure and properties of the cuticle and postgenital organ fusions. Plant Cell., 2000, 12(5):721-738
CrossRef Google scholar
[133]
Silva-SanzanaC, Celiz-BalboaJ, GarzoE, MarcusSE, Parra-RojasJP, RojasB, et al.. Pectin methylesterases modulate plant homogalacturonan status in defenses against the Aphid Myzus persicae. Plant Cell., 2019, 31(8):1913-1929
CrossRef Google scholar
[134]
SimpsonSD, AshfordDA, HarveyDJ, BowlesDJ. Short chain oligogalacturonides induce ethylene production and expression of the gene encoding aminocyclopropane 1-carboxylic acid oxidase in tomato plants. Glycobiology., 1998, 8(6):579-583
CrossRef Google scholar
[135]
SmithCA. Structure, Structure, function and dynamics in the mur family of bacterial cell wall ligases. J Mol Biol., 2006, 362(4):640-655
CrossRef Google scholar
[136]
SomervilleC. Cellulose synthesis in higher plants. Annu Rev Cell Dev Biol., 2006, 22: 53-78
CrossRef Google scholar
[137]
SouzaCA, LiS, LinAZ, BoutrotF, GrossmannG, ZipfelC, et al.. Cellulose-derived oligomers act as damage-associated molecular patterns and trigger defense-like responses. Plant Physiol., 2017, 173(4):2383-2398
CrossRef Google scholar
[138]
StegmannM, MonaghanJ, Smakowska-LuzanE, RovenichH, LehnerA, HoltonN, et al.. The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling. Science., 2017, 355(6322):287-289
CrossRef Google scholar
[139]
SterlingJD, QuigleyHF, OrellanaA, MohnenD. The catalytic site of the pectin biosynthetic enzyme α-1,4-galacturonosyltransferase is located in the lumen of the Golgi. Plant Physiol., 2001, 127(1):360
CrossRef Google scholar
[140]
StranneM, RenY, FimognariL, BirdseyeD, YanJ, BardorM, et al.. TBL10 is required for O-acetylation of pectic rhamnogalacturonan-I in Arabidopsis thaliana. Plant J., 2018, 96(4):772-785
CrossRef Google scholar
[141]
SunA, YuB, ZhangQ, PengY, YangJ, SunY, et al.. MYC2-activated TRICHOME BIREFRINGENCE-LIKE37 acetylates cell walls and enhances herbivore resistance. Plant Physiol., 2020, 184(2):1083-1096
CrossRef Google scholar
[142]
TaylorNG. Cellulose biosynthesis and deposition in higher plants. New Phytol., 2008, 178(2):239-252
CrossRef Google scholar
[143]
TaylorNG, GardinerJC, WhitemanR, TurnerSR. Cellulose synthesis in the Arabidopsis secondary cell wall. Cellulose., 2004, 11(3):329-338
CrossRef Google scholar
[144]
TrusovY, RookesJE, ChakravortyD, ArmourD, SchenkPM, BotellaJR. Heterotrimeric G proteins facilitate Arabidopsis resistance to necrotrophic pathogens and are involved in jasmonate signaling. Plant Physiol., 2006, 140(1):210-220
CrossRef Google scholar
[145]
UnderwoodW. The plant cell wall: a dynamic barrier against pathogen invasion. Front Plant Sci., 2012, 3: 85
CrossRef Google scholar
[146]
UrbanowiczBR, PenaMJ, MonizHA, MoremenKW, YorkWS. Two Arabidopsis proteins synthesize acetylated xylan in vitro. Plant J., 2014, 80(2):197-206
CrossRef Google scholar
[147]
VaahteraL, SchulzJ, HamannT. Cell wall integrity maintenance during plant development and interaction with the environment. Nat Plants., 2019, 5(9):924-932
CrossRef Google scholar
[148]
van den BrinkJ, de VriesRP. Fungal enzyme sets for plant polysaccharide degradation. Appl Microbiol Biotechnol., 2011, 91(6):1477-1492
CrossRef Google scholar
[149]
Van der DoesD, BoutrotF, EngelsdorfT, RhodesJ, McKennaJF, VernhettesS, et al.. The Arabidopsis leucine-rich repeat receptor kinase MIK2/LRR-KISS connects cell wall integrity sensing, root growth and response to abiotic and biotic stresses. PLoS Genet., 2017, 13(6):e1006832
CrossRef Google scholar
[150]
VogelJP, RaabTK, SchiffC, SomervilleSC. PMR6, a pectate lyase-like gene required for powdery mildew susceptibility in Arabidopsis. Plant Cell., 2002, 14(9):2095-2106
CrossRef Google scholar
[151]
VogelJP, RaabTK, SomervilleCR, SomervilleSC. Mutations in PMR5 result in powdery mildew resistance and altered cell wall composition. Plant J., 2004, 40(6):968-978
CrossRef Google scholar
[152]
VollmerW, BlanotD, de PedroMA. Peptidoglycan structure and architecture. FEMS Microbiol Rev., 2008, 32(2):149-167
CrossRef Google scholar
[153]
VolpiC, JanniM, LionettiV, BellincampiD, FavaronF, D'OvidioR. The ectopic expression of a pectin methyl esterase inhibitor increases pectin methyl esterification and limits fungal diseases in wheat. Mol Plant Microbe Interact., 2011, 24(9):1012-1019
CrossRef Google scholar
[154]
VoxeurA, HabryloO, GueninS, MiartF, SoulieMC, RihoueyC, et al.. Oligogalacturonide production upon Arabidopsis thaliana-Botrytis cinerea interaction. Proc Natl Acad Sci USA., 2019, 116(39):19743-19752
CrossRef Google scholar
[155]
WangX, HouS, WuQ, LinM, AcharyaBR, WuD, et al.. IDL6-HAE/HSL2 impacts pectin degradation and resistance to Pseudomonas syringae pv tomato DC3000 in Arabidopsis leaves. Plant J., 2017, 89(2):250-263
CrossRef Google scholar
[156]
WangY, XuY, SunY, WangH, QiJ, WanB, et al.. Leucine-rich repeat receptor-like gene screen reveals that Nicotiana RXEG1 regulates glycoside hydrolase 12 MAMP detection. Nat Commun., 2018, 9(1):594
CrossRef Google scholar
[157]
WolfS, HématyK, HöfteH. G Growth control and cell wall signaling in plants. Annu Rev Plant Biol., 2012, 63(1):381-407
CrossRef Google scholar
[158]
WolfS, MouilleG, PellouxJ. Homogalacturonan methyl-esterification and plant development. Mol Plant., 2009, 2(5):851-860
CrossRef Google scholar
[159]
XiaoS, HuQ, ShenJ, LiuS, YangZ, ChenK, et al.. GhMYB4 downregulates lignin biosynthesis and enhances cotton resistance to Verticillium dahliae. Plant Cell Rep., 2021, 40(4):735-751
CrossRef Google scholar
[160]
XiongG, ChengK, PaulyM. Xylan O-acetylation impacts xylem development and enzymatic recalcitrance as indicated by the Arabidopsis mutant tbl29. Mol Plant., 2013, 6(4):1373-1375
CrossRef Google scholar
[161]
XuG, ZhongX, ShiY, LiuZ, JiangN, LiuJ, et al.. A fungal effector targets a heat shock-dynamin protein complex to modulate mitochondrial dynamics and reduce plant immunity. Sci Adv, 2020, 6(48):eabb7719
CrossRef Google scholar
[162]
YakobyN, KobilerI, DinoorA, PruskyD. pH regulation of pectate lyase secretion modulates the attack of Colletotrichum gloeosporioides on avocado fruits. Appl Environ Microbiol., 2000, 66(3):1026-1030
CrossRef Google scholar
[163]
Yang C, Liu R, Pang J, Ren B, Zhou H, Wang G et al (2021) Poaceae-specific cell wall-derived oligosaccharides activate plant immunity via OsCERK1 during Magnaporthe oryzae infection in rice. Nature Commun 12(1). https://doi.org/10.1038/s41467-021-22456-x\
[164]
YuanY, TengQ, ZhongR, YeZH. The Arabidopsis DUF231 domain-containing protein ESK1 mediates 2-O- and 3-O-acetylation of xylosyl residues in xylan. Plant Cell Physiol., 2013, 54(7):1186-1199
CrossRef Google scholar
[165]
ZhangL, KarsI, EssenstamB, LiebrandTW, WagemakersL, ElberseJ, et al.. Fungal endopolygalacturonases are recognized as microbe-associated molecular patterns by the arabidopsis receptor-like protein responsiveness to botrytis polygalacturonases1. Plant Physiol., 2014, 164(1):352-364
CrossRef Google scholar
[166]
ZhaoQ, DixonRA. Altering the cell wall and its impact on plant disease: from forage to bioenergy. Annu Rev Phytopathol., 2014, 52(1):69-91
CrossRef Google scholar
[167]
ZhongR, CuiD, YeZH. Secondary cell wall biosynthesis. New Phytol., 2019, 221(4):1703-1723
CrossRef Google scholar
[168]
ZhouF, EmonetA, Denervaud TendonV, MarhavyP, WuD, LahayeT, et al.. Co-incidence of damage and microbial patterns controls localized immune responses in roots. Cell., 2020, 180(3):440-453 e18
CrossRef Google scholar
[169]
ZhouX, LiaoH, ChernM, YinJ, ChenY, WangJ, et al.. Loss of function of a rice TPR-domain RNA-binding protein confers broad-spectrum disease resistance. Proc Natl Acad Sci USA., 2018, 115(12):3174
CrossRef Google scholar
Funding
National Natural Science Foundation of China(31871920); Key Research and Development Program from Sichuan Province(2018JZ0072); International Cooperation and Exchange Program of Sichuan Science and Technology Department(2020YFH0137)

Accesses

Citations

Detail

Sections
Recommended

/