Pathogen-induced Autophagy Regulates Monolignol Transport and Lignin Formation in Plant Immunity

Overview

Journal Autophagy

Specialty Cell Biology

Date 2022 Jun 2

PMID 35652914

Authors

Hwi Seong Jeon

Eunjeong Jang

Jinwoo Kim

Seu Ha Kim

Myoung-Hoon Lee

Myung Hee Nam

Yuki Tobimatsu

Ohkmae K Park

Affiliations

Soon will be listed here.

Abstract

The evolutionary plant-pathogen arms race has equipped plants with the immune system that can defend against pathogens. Pattern-triggered immunity and effector-triggered immunity are two major branches of innate immunity that share immune responses, including oxidative bursts, transcriptional reprogramming, and cell wall modifications such as lignin deposition. In a previous study, we reported that lignin rapidly accumulates in pathogen-infected leaves and acts as a mechanical barrier, spatially restricting pathogens and cell death. Lignin deposition into the cell wall is a three-step process: monolignol biosynthesis, transport, and polymerization. While monolignol biosynthesis and polymerization are relatively well understood, the mechanism of monolignol transport remains unclear. In this study, we show that macroautophagy/autophagy modulates pathogen-induced lignin formation. Lignification and other immune responses were impaired in autophagy-defective (autophagy-related) mutants. In microscopy analyses, monolignols formed punctate structures in response to pathogen infection and colocalized with autophagic vesicles. Furthermore, autophagic activity and lignin accumulation were both enhanced in (defense, no death 1) mutant with elevated disease resistance but no cell death and crossing with mutants resulted in a lignin deficit, further supporting that lignin formation requires autophagy. Collectively, these findings demonstrate that lignification, particularly monolignol transport, is achieved through autophagic membrane trafficking in plant immunity.: ABC transporter: ATP-binding cassette transporter; ACD2/AT4G37000: accelerated cell death 2; ATG: autophagy-related; C3'H/AT2G40890: -coumaroyl shikimate 3-hydroxylase; C4H/AT2G30490: cinnamate 4-hydroxylase; CA: coniferyl alcohol; CaMV: cauliflower mosaic virus; CASP: Casparian strip membrane domain protein; CASPL: CASP-like protein; CBB: Coomassie Brilliant Blue; CCoAOMT1/AT4G34050: caffeoyl-CoA -methyltransferase 1; CCR1/AT1G15950: cinnamoyl-CoA reductase 1; CFU: colony-forming unit; COMT1/AT5G54160: caffeic acid -methyltransferase 1; Con A: concanamycin A; DMAC: dimethylaminocoumarin; DND1/AT5G15410: defense, no death 1; CNGC2: cyclic nucleotide-gated channel 2; ER: endoplasmic reticulum; ESB1/AT2G28670/DIR10: enhanced suberin 1; ETI: effector-triggered immunity; EV: extracellular vesicle; F5H/AT4G36220: ferulate-5-hydroxylase; Fluo-3 AM: Fluo-3 acetoxymethyl ester; GFP: green fluorescent protein; HCT/AT5G48930: -hydroxycinnamoyl-CoA:quinate/shikimate -hydroxycinnamoyltransferase; HR: hypersensitive response; LAC: laccase; LTG: LysoTracker Green; LSD1/AT4G200380: lesion stimulating disease 1; PAL1/AT2G37040: phenylalanine ammonia-lyase 1; PAMP: pathogen-associated molecular patterns; PCD: programmed cell death; PE: phosphatidylethanolamine; PRX: peroxidase; DC3000: pv. DC3000; PTI: pattern-triggered immunity; SA: salicylic acid; SD: standard deviation; SID2/AT1G7410: SA induction-deficient 2; UGT: UDP-glucosyltransferase; UPLC: ultraperformance liquid chromatography; UPS: unconventional protein secretion; V-ATPase: vacuolar-type H-translocating ATPase.

Citing Articles

Mitigating Response of Induced by 2-Ethylfuran to Infection.

Ye H, Gao H, Li J, Lu L, Zheng S, Wu C Plants (Basel). 2025; 14(4).

PMID: 40006834 PMC: 11859901. DOI: 10.3390/plants14040575.

Establishment of an experimental system to analyse extracellular vesicles during apoplastic fungal pathogenesis.

Hearfield N, Brotherton D, Gao Z, Inal J, Stotz H J Extracell Biol. 2025; 4(2):e70029.

PMID: 39963377 PMC: 11831348. DOI: 10.1002/jex2.70029.

Proteasomes accumulate in the plant apoplast where they participate in microbe-associated molecular pattern (MAMP)-triggered pathogen defense.

Karimi H, Chen K, Karinshak M, Gu X, Sello J, Vierstra R Nat Commun. 2025; 16(1):1634.

PMID: 39952938 PMC: 11829042. DOI: 10.1038/s41467-025-56594-3.

The Mitochondrial Blueprint: Unlocking Secondary Metabolite Production.

Li Y, Zhang Y, He X, Guo Z, Yang N, Bai G Metabolites. 2024; 14(12).

PMID: 39728492 PMC: 11677534. DOI: 10.3390/metabo14120711.

The FERONIA-RESPONSIVE TO DESICCATION 26 module regulates vascular immunity to Ralstonia solanacearum.

Wang B, Luo C, Li X, Jimenez A, Cai J, Chen J Plant Cell. 2024; 37(1).

PMID: 39535787 PMC: 11663608. DOI: 10.1093/plcell/koae302.

References

Perkins M, Smith R, Samuels L . The transport of monomers during lignification in plants: anything goes but how?. Curr Opin Biotechnol. 2018; 56:69-74. DOI: 10.1016/j.copbio.2018.09.011. View

Takeuchi M, Kegasa T, Watanabe A, Tamura M, Tsutsumi Y . Expression analysis of transporter genes for screening candidate monolignol transporters using Arabidopsis thaliana cell suspensions during tracheary element differentiation. J Plant Res. 2017; 131(2):297-305. DOI: 10.1007/s10265-017-0979-4. View

Coll N, Epple P, Dangl J . Programmed cell death in the plant immune system. Cell Death Differ. 2011; 18(8):1247-56. PMC: 3172094. DOI: 10.1038/cdd.2011.37. View

Boerjan W, Ralph J, Baucher M . Lignin biosynthesis. Annu Rev Plant Biol. 2003; 54:519-46. DOI: 10.1146/annurev.arplant.54.031902.134938. View

Do T, Martinoia E, Lee Y . Functions of ABC transporters in plant growth and development. Curr Opin Plant Biol. 2017; 41:32-38. DOI: 10.1016/j.pbi.2017.08.003. View

Lee Y, Rubio M, Alassimone J, Geldner N . A mechanism for localized lignin deposition in the endodermis. Cell. 2013; 153(2):402-12. DOI: 10.1016/j.cell.2013.02.045. View

Cui H, Tsuda K, Parker J . Effector-triggered immunity: from pathogen perception to robust defense. Annu Rev Plant Biol. 2014; 66:487-511. DOI: 10.1146/annurev-arplant-050213-040012. View

Rabouille C . Pathways of Unconventional Protein Secretion. Trends Cell Biol. 2016; 27(3):230-240. DOI: 10.1016/j.tcb.2016.11.007. View

Zipfel C . Plant pattern-recognition receptors. Trends Immunol. 2014; 35(7):345-51. DOI: 10.1016/j.it.2014.05.004. View

10.

Tian W, Wang C, Gao Q, Li L, Luan S . Calcium spikes, waves and oscillations in plant development and biotic interactions. Nat Plants. 2020; 6(7):750-759. DOI: 10.1038/s41477-020-0667-6. View

11.

Sousa C, Biancur D, Wang X, Halbrook C, Sherman M, Zhang L . Pancreatic stellate cells support tumour metabolism through autophagic alanine secretion. Nature. 2016; 536(7617):479-83. PMC: 5228623. DOI: 10.1038/nature19084. View

12.

Jaini R, Wang P, Dudareva N, Chapple C, Morgan J . Targeted Metabolomics of the Phenylpropanoid Pathway in Arabidopsis thaliana using Reversed Phase Liquid Chromatography Coupled with Tandem Mass Spectrometry. Phytochem Anal. 2017; 28(4):267-276. DOI: 10.1002/pca.2672. View

13.

Liu C, Miao Y, Zhang K . Sequestration and transport of lignin monomeric precursors. Molecules. 2011; 16(1):710-27. PMC: 6259261. DOI: 10.3390/molecules16010710. View

14.

Cavalli G, Cenci S . Autophagy and Protein Secretion. J Mol Biol. 2020; 432(8):2525-2545. DOI: 10.1016/j.jmb.2020.01.015. View

15.

Alejandro S, Lee Y, Tohge T, Sudre D, Osorio S, Park J . AtABCG29 is a monolignol transporter involved in lignin biosynthesis. Curr Biol. 2012; 22(13):1207-12. DOI: 10.1016/j.cub.2012.04.064. View

16.

He B, Cai Q, Qiao L, Huang C, Wang S, Miao W . RNA-binding proteins contribute to small RNA loading in plant extracellular vesicles. Nat Plants. 2021; 7(3):342-352. PMC: 7979528. DOI: 10.1038/s41477-021-00863-8. View

17.

Tobimatsu Y, Schuetz M . Lignin polymerization: how do plants manage the chemistry so well?. Curr Opin Biotechnol. 2018; 56:75-81. DOI: 10.1016/j.copbio.2018.10.001. View

18.

Patel S, Dinesh-Kumar S . Arabidopsis ATG6 is required to limit the pathogen-associated cell death response. Autophagy. 2007; 4(1):20-7. DOI: 10.4161/auto.5056. View

19.

Foster C, Martin T, Pauly M . Comprehensive compositional analysis of plant cell walls (Lignocellulosic biomass) part I: lignin. J Vis Exp. 2010; (37). PMC: 3144576. DOI: 10.3791/1745. View

20.

Clough S, Fengler K, Yu I, Lippok B, Smith Jr R, Bent A . The Arabidopsis dnd1 "defense, no death" gene encodes a mutated cyclic nucleotide-gated ion channel. Proc Natl Acad Sci U S A. 2000; 97(16):9323-8. PMC: 16866. DOI: 10.1073/pnas.150005697. View