Lectin Receptor-like Kinase Signaling during Engineered Ectomycorrhiza Colonization

Shrestha, Him K.; Yao, Tao; Qiao, Zhenzhen; Muchero, Wellington; Hettich, Robert (Bob) L.; Chen, Jin-Gui (Jay); Abraham, Paul E.

doi:10.3390/cells12071082

Lectin Receptor-like Kinase Signaling during Engineered Ectomycorrhiza Colonization

Journal Article · Tue Apr 04 00:00:00 EDT 2023 · Cells

DOI:https://doi.org/10.3390/cells12071082· OSTI ID:1973326

^[1]; ^[2]; Qiao, Zhenzhen ^[2]; ^[2]; ^[1]; ^[2]; ^[1]

Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

Mutualistic association can improve a plant’s health and productivity. G-type lectin receptor-like kinase (PtLecRLK1) is a susceptibility factor in Populus trichocarpa that permits root colonization by a beneficial fungus, Laccaria bicolor. Engineering PtLecRLK1 also permits L. bicolor root colonization in non-host plants similar to Populus trichocarpa. The intracellular signaling reprogramed by PtLecRLK1 upon recognition of L. bicolor to allow for the development and maintenance of symbiosis is yet to be determined. In this study, phosphoproteomics was utilized to identify phosphorylation-based relevant signaling pathways associated with PtLecRLK1 recognition of L. bicolor in transgenic switchgrass roots. Our finding shows that PtLecRLK1 in transgenic plants modifies the chitin-triggered plant defense and MAPK signaling along with a significant adjustment in phytohormone signaling, ROS balance, endocytosis, cytoskeleton movement, and proteasomal degradation in order to facilitate the establishment and maintenance of L. bicolor colonization. Moreover, protein–protein interaction data implicate a cGMP-dependent protein kinase as a potential substrate of PtLecRLK1.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1973326

Journal Information:: Cells, Journal Name: Cells Journal Issue: 7 Vol. 12; ISSN 2073-4409

Publisher:: MDPICopyright Statement

Country of Publication:: United States

Language:: English

References (33)

Inactivation of a wheat protein kinase gene confers broad-spectrum resistance to rust fungi Wang, Ning; Tang, Chunlei; Fan, Xin Cell, Vol. 185, Issue 16 https://doi.org/10.1016/j.cell.2022.06.027	journal	August 2022
Comparison of protein precipitation methods for sample preparation prior to proteomic analysis Jiang, Lei; He, Lin; Fountoulakis, Michael Journal of Chromatography A, Vol. 1023, Issue 2 https://doi.org/10.1016/j.chroma.2003.10.029	journal	January 2004
Arabidopsis CAP1 mediates ammonium-regulated root hair growth by influencing vesicle trafficking and the cytoskeletal arrangement in root hair cells Yu, Juanjuan; Ma, Xiaonan; Wang, Lianlian Journal of Genetics and Genomics, Vol. 49, Issue 10 https://doi.org/10.1016/j.jgg.2022.02.005	journal	October 2022
Engineering plant microbiomes by integrating eco-evolutionary principles into current strategies Morales Moreira, Zayda P.; Chen, Melissa Y.; Yanez Ortuno, Daniela L. Current Opinion in Plant Biology, Vol. 71 https://doi.org/10.1016/j.pbi.2022.102316	journal	February 2023
Microbial Inoculants: Silver Bullet or Microbial Jurassic Park? Jack, Chandra N.; Petipas, Renee H.; Cheeke, Tanya E. Trends in Microbiology, Vol. 29, Issue 4 https://doi.org/10.1016/j.tim.2020.11.006	journal	April 2021
MS Amanda, a Universal Identification Algorithm Optimized for High Accuracy Tandem Mass Spectra Dorfer, Viktoria; Pichler, Peter; Stranzl, Thomas Journal of Proteome Research, Vol. 13, Issue 8 https://doi.org/10.1021/pr500202e	journal	June 2014
Defining the core Arabidopsis thaliana root microbiome Lundberg, Derek S.; Lebeis, Sarah L.; Paredes, Sur Herrera Nature, Vol. 488, Issue 7409 https://doi.org/10.1038/nature11237	journal	August 2012
Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota Bulgarelli, Davide; Rott, Matthias; Schlaeppi, Klaus Nature, Vol. 488, Issue 7409 https://doi.org/10.1038/nature11336	journal	August 2012
Plant signalling in symbiosis and immunity Zipfel, Cyril; Oldroyd, Giles E. D. Nature, Vol. 543, Issue 7645 https://doi.org/10.1038/nature22009	journal	March 2017
The Perseus computational platform for comprehensive analysis of (prote)omics data Tyanova, Stefka; Temu, Tikira; Sinitcyn, Pavel Nature Methods, Vol. 13, Issue 9 https://doi.org/10.1038/nmeth.3901	journal	June 2016
Semi-supervised learning for peptide identification from shotgun proteomics datasets Käll, Lukas; Canterbury, Jesse D.; Weston, Jason Nature Methods, Vol. 4, Issue 11 https://doi.org/10.1038/nmeth1113	journal	October 2007
Mediation of plant–mycorrhizal interaction by a lectin receptor-like kinase Labbé, Jessy; Muchero, Wellington; Czarnecki, Olaf Nature Plants, Vol. 5, Issue 7 https://doi.org/10.1038/s41477-019-0469-x	journal	July 2019
Genome-wide Identification of PP2C Genes and Their Expression Profiling in Response to Drought and Cold Stresses in Medicago truncatula Yang, Qi; Liu, Kun; Niu, Xiaocui Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-29627-9	journal	August 2018
CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis Miya, A.; Albert, P.; Shinya, T. Proceedings of the National Academy of Sciences, Vol. 104, Issue 49 https://doi.org/10.1073/pnas.0705147104	journal	November 2007
Structure, variation, and assembly of the root-associated microbiomes of rice Edwards, Joseph; Johnson, Cameron; Santos-Medellín, Christian Proceedings of the National Academy of Sciences, Vol. 112, Issue 8 https://doi.org/10.1073/pnas.1414592112	journal	January 2015
The Lysin Motif Receptor-like Kinase (LysM-RLK) CERK1 Is a Major Chitin-binding Protein in Arabidopsis thaliana and Subject to Chitin-induced Phosphorylation Petutschnig, Elena K.; Jones, Alexandra M. E.; Serazetdinova, Liliya Journal of Biological Chemistry, Vol. 285, Issue 37 https://doi.org/10.1074/jbc.M110.116657	journal	July 2010
DAnTE: a statistical tool for quantitative analysis of -omics data Polpitiya, A. D.; Qian, W. -J.; Jaitly, N. Bioinformatics, Vol. 24, Issue 13 https://doi.org/10.1093/bioinformatics/btn217	journal	May 2008
The STRING database in 2021: customizable protein–protein networks, and functional characterization of user-uploaded gene/measurement sets Szklarczyk, Damian; Gable, Annika L.; Nastou, Katerina C. Nucleic Acids Research, Vol. 49, Issue D1 https://doi.org/10.1093/nar/gkaa1074	journal	November 2020
STRING: a database of predicted functional associations between proteins Mering, C. v. Nucleic Acids Research, Vol. 31, Issue 1 https://doi.org/10.1093/nar/gkg034	journal	January 2003
The S-Domain Receptor Kinase Arabidopsis Receptor Kinase2 and the U Box/Armadillo Repeat-Containing E3 Ubiquitin Ligase9 Module Mediates Lateral Root Development under Phosphate Starvation in Arabidopsis Deb, Srijani; Sankaranarayanan, Subramanian; Wewala, Gayathri Plant Physiology, Vol. 165, Issue 4 https://doi.org/10.1104/pp.114.244376	journal	June 2014
Dual Activities of Plant cGMP-Dependent Protein Kinase and Its Roles in Gibberellin Signaling and Salt Stress Shen, Qingwen; Zhan, Xinqiao; Yang, Pei The Plant Cell, Vol. 31, Issue 12 https://doi.org/10.1105/tpc.19.00510	journal	October 2019
Knowing your friends and foes - plant receptor-like kinases as initiators of symbiosis or defence Antolín-Llovera, Meritxell; Petutsching, Elena Kristin; Ried, Martina Katharina New Phytologist, Vol. 204, Issue 4 https://doi.org/10.1111/nph.13117	journal	November 2014
The rice LysM receptor-like kinase Os CERK1 is required for the perception of short-chain chitin oligomers in arbuscular mycorrhizal signaling Carotenuto, Gennaro; Chabaud, Mireille; Miyata, Kana New Phytologist, Vol. 214, Issue 4 https://doi.org/10.1111/nph.14539	journal	March 2017
Ecosystem consequences of introducing plant growth promoting rhizobacteria to managed systems and potential legacy effects Moore, Jessica A. M.; Abraham, Paul E.; Michener, Joshua K. New Phytologist, Vol. 234, Issue 6 https://doi.org/10.1111/nph.18010	journal	March 2022
Overexpression of a Prefoldin β subunit gene reduces biomass recalcitrance in the bioenergy crop Populus Zhang, Jin; Xie, Meng; Li, Mi Plant Biotechnology Journal, Vol. 18, Issue 3 https://doi.org/10.1111/pbi.13254	journal	September 2019
Towards engineering ectomycorrhization into switchgrass bioenergy crops via a lectin receptor‐like kinase Qiao, Zhenzhen; Yates, Timothy B.; Shrestha, Him K. Plant Biotechnology Journal, Vol. 19, Issue 12 https://doi.org/10.1111/pbi.13671	journal	August 2021
A pair of receptor-like kinases is responsible for natural variation in shoot growth response to mannitol treatment inArabidopsis thaliana Trontin, Charlotte; Kiani, Seifollah; Corwin, Jason A. The Plant Journal, Vol. 78, Issue 1 https://doi.org/10.1111/tpj.12454	journal	March 2014
The receptor kinase CERK1 has dual functions in symbiosis and immunity signalling Zhang, Xiaowei; Dong, Wentao; Sun, Jongho The Plant Journal, Vol. 81, Issue 2 https://doi.org/10.1111/tpj.12723	journal	December 2014
Decoding the Patterns of Self and Nonself by the Innate Immune System Medzhitov, Ruslan; Janeway, Charles A. Science, Vol. 296, Issue 5566 https://doi.org/10.1126/science.1068883	journal	April 2002
Comparative Metagenomics of Microbial Communities Tringe, S. G. Science, Vol. 308, Issue 5721 https://doi.org/10.1126/science.1107851	journal	April 2005
Phosphorylation of Glutamine Synthetase on Threonine 301 Contributes to Its Inactivation During Epilepsy Huyghe, Deborah; Denninger, Andrew R.; Voss, Caroline M. Frontiers in Molecular Neuroscience, Vol. 12 https://doi.org/10.3389/fnmol.2019.00120	journal	May 2019
Adjusting ammonium uptake via phosphorylation Lanquar, Viviane; Frommer, Wolf B. Plant Signaling & Behavior, Vol. 5, Issue 6 https://doi.org/10.4161/psb.5.6.11696	journal	June 2010
The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1 Cao, Yangrong; Liang, Yan; Tanaka, Kiwamu eLife, Vol. 3 https://doi.org/10.7554/eLife.03766	journal	October 2014

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59 BASIC BIOLOGICAL SCIENCES
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Lectin Receptor-like Kinase Signaling during Engineered Ectomycorrhiza Colonization

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