Diversity and conservation of plant small secreted proteins associated with arbuscular mycorrhizal symbiosis

Hu, Xiao-Li; Zhang, Jin; Kaundal, Rakesh; Kataria, Raghav; Labbé, Jesse L.; Mitchell, Julie C.; Tschaplinski, Timothy J.; Tuskan, Gerald A.; Cheng, Zong-Ming (Max); Yang, Xiaohan

doi:10.1093/hr/uhac043

Title: Diversity and conservation of plant small secreted proteins associated with arbuscular mycorrhizal symbiosis

Journal Article · Sat Feb 19 00:00:00 UTC 2022 · Horticulture Research (online)

DOI: https://doi.org/10.1093/hr/uhac043 · OSTI ID:1873832

Hu, Xiao-Li ^[1]; Zhang, Jin ^[2]; Kaundal, Rakesh ^[3]; Kataria, Raghav ^[3];

^[4]; Mitchell, Julie C. ^[4];

^[5];

^[5]; Cheng, Zong-Ming (Max) ^[6];

^[7]

Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Zhejiang A&F Univ., Hangzhou (China). State Key Laboratory of Subtropical Silviculture
Utah State Univ., Logan, UT (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Bioenergy Innovation (CBI)
Univ. of Tennessee, Knoxville, TN (United States); Nanjing Agricultural Univ. (China)
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). Center for Bioenergy Innovation (CBI)

Arbuscular mycorrhizal symbiosis (AMS) is widespread mutualistic association between plants and fungi, which plays an essential role in nutrient exchange, enhancement in plant stress resistance, development of host, and ecosystem sustainability. Previous studies have shown that plant small secreted proteins (SSPs) are involved in beneficial symbiotic interactions. However, the role of SSPs in the evolution of AMS has not been well studied yet. In this study, we performed computational analysis of SSPs in 60 plant species and identified three AMS-specific ortholog groups containing SSPs only from at least 30% of the AMS species in this study and three AMS-preferential ortholog groups containing SSPs from both AMS and non-AMS species, with AMS species containing significantly more SSPs than non-AMS species. We found that independent lineages of monocot and eudicot plants contained genes in the AMS-specific ortholog groups and had significant expansion in the AMS-preferential ortholog groups. Also, two AMS-preferential ortholog groups showed convergent changes, between monocot and eudicot species, in gene expression in response to arbuscular mycorrhizal fungus Rhizophagus irregularis. Furthermore, conserved cis-elements were identified in the promoter regions of the genes showing convergent gene expression. We found that the SSPs, and their closely related homologs, in each of three AMS-preferential ortholog groups, had some local variations in the protein structural alignment. We also identified genes co-expressed with the Populus trichocarpa SSP genes in the AMS-preferential ortholog groups. This first plant kingdom-wide analysis on SSP provides insights on plant-AMS convergent evolution with specific SSP gene expression and local diversification of protein structures.

View Accepted Manuscript (DOE)

Cite

Export

Save

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

Sponsoring Organization:: National Natural Science Foundation of China (NSFC); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1873832

Journal Information:: Horticulture Research (online), Journal Name: Horticulture Research (online) Journal Issue: na Vol. 9; ISSN 2052-7276

Publisher:: Springer Nature - Nanjing Agricultural UniversityCopyright Statement

Country of Publication:: United States

Language:: English

References (68)

Phylogenetic distribution and evolution of mycorrhizas in land plants Wang, B.; Qiu, Y. -L. Mycorrhiza, Vol. 16, Issue 5 https://doi.org/10.1007/s00572-005-0033-6	journal	May 2006
Arbuscular mycorrhizal fungi and plant growth-promoting pseudomonads improve yield, quality and nutritional value of tomato: a field study Bona, Elisa; Cantamessa, Simone; Massa, Nadia Mycorrhiza, Vol. 27, Issue 1 https://doi.org/10.1007/s00572-016-0727-y	journal	August 2016
Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis Brundrett, Mark C. Plant and Soil, Vol. 320, Issue 1-2 https://doi.org/10.1007/s11104-008-9877-9	journal	February 2009
Predicting eukaryotic protein secretion without signals Nielsen, Henrik; Petsalaki, Eirini I.; Zhao, Linlin Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1867, Issue 12 https://doi.org/10.1016/j.bbapap.2018.11.011	journal	December 2019
Cold-Induced CBF–PIF3 Interaction Enhances Freezing Tolerance by Stabilizing the phyB Thermosensor in Arabidopsis Jiang, Bochen; Shi, Yiting; Peng, Yue Molecular Plant, Vol. 13, Issue 6 https://doi.org/10.1016/j.molp.2020.04.006	journal	June 2020
Advances and perspectives on the use of CRISPR/Cas9 systems in plant genomics research Liu, Degao; Hu, Rongbin; Palla, Kaitlin J. Current Opinion in Plant Biology, Vol. 30 https://doi.org/10.1016/j.pbi.2016.01.007	journal	April 2016
Construct design for CRISPR/Cas-based genome editing in plants Hassan, Md Mahmudul; Zhang, Yingxiao; Yuan, Guoliang Trends in Plant Science, Vol. 26, Issue 11 https://doi.org/10.1016/j.tplants.2021.06.015	journal	November 2021
The hunt for sORFs: A multidisciplinary strategy Peeters, Marlies K. R.; Menschaert, Gerben Experimental Cell Research, Vol. 391, Issue 1 https://doi.org/10.1016/j.yexcr.2020.111923	journal	June 2020
Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis Bonfante, Paola; Genre, Andrea Nature Communications, Vol. 1, Issue 1 https://doi.org/10.1038/ncomms1046	journal	July 2010
ModelFinder: fast model selection for accurate phylogenetic estimates Kalyaanamoorthy, Subha; Minh, Bui Quang; Wong, Thomas K. F. Nature Methods, Vol. 14, Issue 6 https://doi.org/10.1038/nmeth.4285	journal	May 2017
The Phyre2 web portal for protein modeling, prediction and analysis Kelley, Lawrence A.; Mezulis, Stefans; Yates, Christopher M. Nature Protocols, Vol. 10, Issue 6 https://doi.org/10.1038/nprot.2015.053	journal	May 2015
Advances and perspectives in discovery and functional analysis of small secreted proteins in plants Hu, Xiao-Li; Lu, Haiwei; Hassan, Md Mahmudul Horticulture Research, Vol. 8, Issue 1 https://doi.org/10.1038/s41438-021-00570-7	journal	June 2021
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
A small peptide modulates stomatal control via abscisic acid in long-distance signalling Takahashi, Fuminori; Suzuki, Takehiro; Osakabe, Yuriko Nature, Vol. 556, Issue 7700 https://doi.org/10.1038/s41586-018-0009-2	journal	April 2018
SignalP 5.0 improves signal peptide predictions using deep neural networks Almagro Armenteros, José Juan; Tsirigos, Konstantinos D.; Sønderby, Casper Kaae Nature Biotechnology, Vol. 37, Issue 4 https://doi.org/10.1038/s41587-019-0036-z	journal	February 2019
Populus trichocarpa encodes small, effector-like secreted proteins that are highly induced during mutualistic symbiosis Plett, Jonathan M.; Yin, Hengfu; Mewalal, Ritesh Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-00400-8	journal	March 2017
CLE-CLAVATA1 peptide-receptor signaling module regulates the expansion of plant root systems in a nitrogen-dependent manner Araya, Takao; Miyamoto, Mayu; Wibowo, Juliarni Proceedings of the National Academy of Sciences, Vol. 111, Issue 5 https://doi.org/10.1073/pnas.1319953111	journal	January 2014
Poplar Genomics: State of the Science Yang, Xiaohan; Kalluri, Udaya C.; DiFazio, Stephen P. Critical Reviews in Plant Sciences, Vol. 28, Issue 5 https://doi.org/10.1080/07352680903241014	journal	October 2009
Plant-mSubP: a computational framework for the prediction of single- and multi-target protein subcellular localization using integrated machine-learning approaches Sahu, Sitanshu S.; Loaiza, Cristian D.; Kaundal, Rakesh AoB PLANTS, Vol. 12, Issue 3 https://doi.org/10.1093/aobpla/plz068	journal	October 2019
DeepCPP: a deep neural network based on nucleotide bias information and minimum distribution similarity feature selection for RNA coding potential prediction Zhang, Yu; Jia, Cangzhi; Fullwood, Melissa Jane Briefings in Bioinformatics, Vol. 22, Issue 2 https://doi.org/10.1093/bib/bbaa039	journal	March 2020
MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization Katoh, Kazutaka; Rozewicki, John; Yamada, Kazunori D. Briefings in Bioinformatics, Vol. 20, Issue 4 https://doi.org/10.1093/bib/bbx108	journal	September 2017
Evaluation of methods for the prediction of membrane spanning regions Moller, S.; Croning, M. D. R.; Apweiler, R. Bioinformatics, Vol. 17, Issue 7 https://doi.org/10.1093/bioinformatics/17.7.646	journal	July 2001
sORF finder: a program package to identify small open reading frames with high coding potential Hanada, Kousuke; Akiyama, Kenji; Sakurai, Tetsuya Bioinformatics, Vol. 26, Issue 3 https://doi.org/10.1093/bioinformatics/btp688	journal	December 2009
STAR: ultrafast universal RNA-seq aligner Dobin, Alexander; Davis, Carrie A.; Schlesinger, Felix Bioinformatics, Vol. 29, Issue 1 https://doi.org/10.1093/bioinformatics/bts635	journal	October 2012
EBSeq: an empirical Bayes hierarchical model for inference in RNA-seq experiments Leng, Ning; Dawson, John A.; Thomson, James A. Bioinformatics, Vol. 29, Issue 8 https://doi.org/10.1093/bioinformatics/btt087	journal	February 2013
ASTRAL: genome-scale coalescent-based species tree estimation Mirarab, S.; Reaz, R.; Bayzid, Md. S. Bioinformatics, Vol. 30, Issue 17 https://doi.org/10.1093/bioinformatics/btu462	journal	August 2014
DeepLoc: prediction of protein subcellular localization using deep learning Almagro Armenteros, José Juan; Sønderby, Casper Kaae; Sønderby, Søren Kaae Bioinformatics, Vol. 33, Issue 21 https://doi.org/10.1093/bioinformatics/btx431	journal	July 2017
Characterization of Arabidopsis ZIM, a member of a novel plant-specific GATA factor gene family Shikata, M. Journal of Experimental Botany, Vol. 55, Issue 397 https://doi.org/10.1093/jxb/erh078	journal	January 2004
Novel MtCEP1 peptides produced in vivo differentially regulate root development in Medicago truncatula Mohd-Radzman, Nadiatul A.; Binos, Steve; Truong, Thy T. Journal of Experimental Botany, Vol. 66, Issue 17 https://doi.org/10.1093/jxb/erv008	journal	February 2015
Dirigent proteins in plants: modulating cell wall metabolism during abiotic and biotic stress exposure Paniagua, Candelas; Bilkova, Anna; Jackson, Phil Journal of Experimental Botany, Vol. 68, Issue 13 https://doi.org/10.1093/jxb/erx141	journal	May 2017
CRISPR/Cas9-mediated targeted mutagenesis for functional genomics research of crassulacean acid metabolism plants Liu, Degao; Chen, Mei; Mendoza, Brian Journal of Experimental Botany, Vol. 70, Issue 22 https://doi.org/10.1093/jxb/erz415	journal	September 2019
IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era Minh, Bui Quang; Schmidt, Heiko A.; Chernomor, Olga Molecular Biology and Evolution, Vol. 37, Issue 5 https://doi.org/10.1093/molbev/msaa015	journal	February 2020
Advantages of combined transmembrane topology and signal peptide prediction--the Phobius web server Kall, L.; Krogh, A.; Sonnhammer, E. L. L. Nucleic Acids Research, Vol. 35, Issue Web Server https://doi.org/10.1093/nar/gkm256	journal	May 2007
PlantPAN3.0: a new and updated resource for reconstructing transcriptional regulatory networks from ChIP-seq experiments in plants Chow, Chi-Nga; Lee, Tzong-Yi; Hung, Yu-Cheng Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky1081	journal	November 2018
BUSCA: an integrative web server to predict subcellular localization of proteins Savojardo, Castrense; Martelli, Pier Luigi; Fariselli, Piero Nucleic Acids Research, Vol. 46, Issue W1 https://doi.org/10.1093/nar/gky320	journal	April 2018
CNIT: a fast and accurate web tool for identifying protein-coding and long non-coding transcripts based on intrinsic sequence composition Guo, Jin-Cheng; Fang, Shuang-Sang; Wu, Yang Nucleic Acids Research, Vol. 47, Issue W1 https://doi.org/10.1093/nar/gkz400	journal	May 2019
RNA-seq Transcriptional Profiling of an Arbuscular Mycorrhiza Provides Insights into Regulated and Coordinated Gene Expression in Lotus japonicus and Rhizophagus irregularis Handa, Yoshihiro; Nishide, Hiroyo; Takeda, Naoya Plant and Cell Physiology, Vol. 56, Issue 8 https://doi.org/10.1093/pcp/pcv071	journal	May 2015
Convergent Evolution of Effector Protease Recognition by Arabidopsis and Barley Carter, Morgan E.; Helm, Matthew; Chapman, Antony V. E. Molecular Plant-Microbe Interactions®, Vol. 32, Issue 5 https://doi.org/10.1094/MPMI-07-18-0202-FI	journal	May 2019
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks Shannon, P. Genome Research, Vol. 13, Issue 11 https://doi.org/10.1101/gr.1239303	journal	November 2003
The Arabidopsis Unannotated Secreted Peptide Database, a Resource for Plant Peptidomics Lease, Kevin A.; Walker, John C. Plant Physiology, Vol. 142, Issue 3 https://doi.org/10.1104/pp.106.086041	journal	September 2006
Genome-Wide Identification of Medicago Peptides Involved in Macronutrient Responses and Nodulation de Bang, Thomas C.; Lundquist, Peter K.; Dai, Xinbin Plant Physiology, Vol. 175, Issue 4 https://doi.org/10.1104/pp.17.01096	journal	October 2017
CIRCADIAN CLOCK-ASSOCIATED1 Controls Resistance to Aphids by Altering Indole Glucosinolate Production Lei, Jiaxin; Jayaprakasha, Guddadarangavvanahally K.; Singh, Jashbir Plant Physiology, Vol. 181, Issue 3 https://doi.org/10.1104/pp.19.00676	journal	September 2019
The Plant Peptidome: An Expanding Repertoire of Structural Features and Biological Functions Tavormina, Patrizia; De Coninck, Barbara; Nikonorova, Natalia The Plant Cell, Vol. 27, Issue 8 https://doi.org/10.1105/tpc.15.00440	journal	August 2015
Plant Signaling and Metabolic Pathways Enabling Arbuscular Mycorrhizal Symbiosis MacLean, Allyson M.; Bravo, Armando; Harrison, Maria J. The Plant Cell, Vol. 29, Issue 10 https://doi.org/10.1105/tpc.17.00555	journal	August 2017
The interaction between arbuscular mycorrhizal fungi and soil phosphorus availability influences plant community productivity and ecosystem stability Yang, Gaowen; Liu, Nan; Lu, Wenjie Journal of Ecology, Vol. 102, Issue 4 https://doi.org/10.1111/1365-2745.12249	journal	April 2014
Laccaria bicolor MiSSP8 is a small‐secreted protein decisive for the establishment of the ectomycorrhizal symbiosis Pellegrin, Clément; Daguerre, Yohann; Ruytinx, Joske Environmental Microbiology, Vol. 21, Issue 10 https://doi.org/10.1111/1462-2920.14727	journal	July 2019
Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles: Phosphate transport in the AM symbiosis Javot, HÉLÈNe; Pumplin, Nathan; Harrison, Maria J. Plant, Cell & Environment, Vol. 30, Issue 3 https://doi.org/10.1111/j.1365-3040.2006.01617.x	journal	December 2006
mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes Thimm, Oliver; Bläsing, Oliver; Gibon, Yves The Plant Journal, Vol. 37, Issue 6, p. 914-939 https://doi.org/10.1111/j.1365-313X.2004.02016.x	journal	March 2004
Comparative phylogenomics of symbiotic associations Delaux, Pierre-Marc New Phytologist, Vol. 213, Issue 1 https://doi.org/10.1111/nph.14161	journal	September 2016
ApoplastP : prediction of effectors and plant proteins in the apoplast using machine learning Sperschneider, Jana; Dodds, Peter N.; Singh, Karam B. New Phytologist, Vol. 217, Issue 4 https://doi.org/10.1111/nph.14946	journal	December 2017
Partner communication and role of nutrients in the arbuscular mycorrhizal symbiosis Lanfranco, Luisa; Fiorilli, Valentina; Gutjahr, Caroline New Phytologist, Vol. 220, Issue 4 https://doi.org/10.1111/nph.15230	journal	May 2018
Why farmers should manage the arbuscular mycorrhizal symbiosis Rillig, Matthias C.; Aguilar‐Trigueros, Carlos A.; Camenzind, Tessa New Phytologist, Vol. 222, Issue 3 https://doi.org/10.1111/nph.15602	journal	January 2019
The role of peptides cleaved from protein precursors in eliciting plant stress reactions Chen, Ying‐Lan; Fan, Kai‐Ting; Hung, Sheng‐Chi New Phytologist, Vol. 225, Issue 6 https://doi.org/10.1111/nph.16241	journal	November 2019
Rapid evolution in plant–microbe interactions – an evolutionary genomics perspective Vries, Sophie; Stukenbrock, Eva H.; Rose, Laura E. New Phytologist, Vol. 226, Issue 5 https://doi.org/10.1111/nph.16458	journal	March 2020
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
Pattern recognition receptors and signaling in plant-microbe interactions Saijo, Yusuke; Loo, Eliza Po-iian; Yasuda, Shigetaka The Plant Journal, Vol. 93, Issue 4 https://doi.org/10.1111/tpj.13808	journal	February 2018
Tissue-based map of the human proteome Uhlen, M.; Fagerberg, L.; Hallstrom, B. M. Science, Vol. 347, Issue 6220 https://doi.org/10.1126/science.1260419	journal	January 2015
Detecting pore-lining regions in transmembrane protein sequences Nugent, Timothy; Jones, David T. BMC Bioinformatics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2105-13-169	journal	July 2012
Detecting small plant peptides using SPADA (Small Peptide Alignment Discovery Application) Zhou, Peng; Silverstein, Kevin AT; Gao, Liangliang BMC Bioinformatics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2105-14-335	journal	January 2013
MiPepid: MicroPeptide identification tool using machine learning Zhu, Mengmeng; Gribskov, Michael BMC Bioinformatics, Vol. 20, Issue 1 https://doi.org/10.1186/s12859-019-3033-9	journal	November 2019
OrthoFinder: phylogenetic orthology inference for comparative genomics Emms, David M.; Kelly, Steven Genome Biology, Vol. 20, Issue 1 https://doi.org/10.1186/s13059-019-1832-y	journal	November 2019
Thematic Review Series: Glycosylphosphatidylinositol (GPI) Anchors: Biochemistry and Cell Biology Biosynthesis of GPI-anchored proteins: special emphasis on GPI lipid remodeling Kinoshita, Taroh; Fujita, Morihisa Journal of Lipid Research, Vol. 57, Issue 1 https://doi.org/10.1194/jlr.R063313	journal	January 2016
Identification of Populus Small RNAs Responsive to Mutualistic Interactions With Mycorrhizal Fungi, Laccaria bicolor and Rhizophagus irregularis Mewalal, Ritesh; Yin, Hengfu; Hu, Rongbin Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00515	journal	March 2019
Maturation processes and structures of small secreted peptides in plants Tabata, Ryo; Sawa, Shinichiro Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00311	journal	July 2014
Genetic and Molecular Mechanisms Underlying Symbiotic Specificity in Legume-Rhizobium Interactions Wang, Qi; Liu, Jinge; Zhu, Hongyan Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00313	journal	March 2018
Glycosylphosphatidylinositol-Anchored Proteins in Arabidopsis and One of Their Common Roles in Signaling Transduction Zhou, Ke Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.01022	journal	August 2019
Evolutionary Divergence of Duplicated Hsf Genes in Populus Liu, Bobin; Hu, Jianjun; Zhang, Jin Cells, Vol. 8, Issue 5 https://doi.org/10.3390/cells8050438	journal	May 2019
Plant Biosystems Design Research Roadmap 1.0 Yang, Xiaohan; Medford, June I.; Markel, Kasey BioDesign Research, Vol. 2020 https://doi.org/10.34133/2020/8051764	journal	December 2020

Similar Records

The Kalanchoe genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism

Journal Article · Fri Dec 01 00:00:00 UTC 2017 · Nature Communications · OSTI ID:1413629

Yang, Xiaohan; Hu, Rongbin; Yin, Hengfu; +46 more

Genome-wide identification of lineage-specific genes in Arabidopsis, Oryza and Populus

Journal Article · Thu Jan 01 04:00:00 UTC 2009 · Genomics · OSTI ID:953655

Yang, Xiaohan; Jawdy, Sara; Tschaplinski, Timothy J; +1 more

A glycan receptor kinase facilitates intracellular accommodation of arbuscular mycorrhiza and symbiotic rhizobia in the legume Lotus japonicus

Journal Article · Thu May 18 00:00:00 UTC 2023 · PLoS Biology (Online) · OSTI ID:1975906

Kelly, Simon; Hansen, Simon B.; Rübsam, Henriette; +20 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: Diversity and conservation of plant small secreted proteins associated with arbuscular mycorrhizal symbiosis

Citation Formats

References (68)

Similar Records

Related Subjects