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Tree Genetics & Genomes

, 15:10 | Cite as

Phosphoproteomic changes in root cells of Poncirus trifoliata (L.) Raf. induced by Rhizophagus intraradices inoculation

  • Fuxi Bai
  • Fang Song
  • Zijun Zheng
  • Huimin Yu
  • Xiuxin Deng
  • Shunyuan Xiao
  • Zhiyong PanEmail author
Original Article
  • 12 Downloads
Part of the following topical collections:
  1. Disease Resistance

Abstract

Arbuscular mycorrhiza (AM) is a widespread endosymbiosis between terrestrial plants and AM fungi belonging to sub-phylum Glomeromycotina (Mycologia 108: 1028–1046, 2016). To date, many plant genes involved in establishing the AM symbiosis have been identified. Yet, the precise mechanisms governing the early signaling process are still not well understood. In this study, we employed the isotope tags for relative and absolute quantification (iTRAQ) and LC–MS/MS analysis to investigate the phosphoproteomic changes in the root cells of Poncirus trifoliata (L.) Raf. (a common citrus rootstock) during the establishment of the AM symbiosis. A total of 1920 unique phosphopeptides derived from 1016 phosphoproteins were identified, which collectively contained 2308 phosphorylation sites. Motif-X analysis of all the detected phosphopeptides showed that 25 phosphoserine motifs and 4 phosphothreonine motifs were overrepresented in phosphorylation processes. Among the phosphoserine motifs, [SDXE] and [PXSP] showed the highest fold increase upon colonization by Rhizophagus intraradices, suggesting that they may play potential roles in AM symbiosis. At 1 week post-inoculation of R. intraradices, the phosphorylation levels of 65 phosphopeptides were significantly changed (p value < 0.05 and fold change > 1.35), with 39 upregulated and 26 downregulated, implying that at least some of the 65 phosphoproteins may be involved in the signal transduction during early events of the AM symbiosis. This study provides a comprehensive phosphoproteomic analysis in a citrus rootstock and the phosphoproteomic changes should shed light onto the signaling mechanisms involved in the establishment of AM symbiosis.

Keywords

Phosphoproteome Arbuscular mycorrhizal symbiosis Rhizophagus intraradices Poncirus 

Notes

Acknowledgements

We would like to thank Yunliu Zeng (Huazhong Agricultural University) for critical discussion and suggestions and Chengquan Yang (North West Agriculture and Forestry University) for his technical assistance with bioinformatic analysis and manuscript revision.

Author contributions

ZY. P., XX. D., and SY. X. conceived and designed the experiments. FX. B., F. S., ZJ. Z., and HM. Y. prepared the materials and performed the experiments, FX. B. and HM. Y. collected, analyzed, and deposited the data. FX. B. proofread the final draft and revised the manuscript. All authors have read and approved the manuscript.

Funding

This work was funded by the National Key Research and Development Program of China (Grant Number 2017YFD0202001), National Natural Science Foundation of China (No. 31521092), and the Fundamental Research Funds for the Central Universities (Grant Number 2662018JC039).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Data archiving statement

The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium (Deutsch et al. 2017) via the PRIDE (Vizcaino et al. 2016) partner repository with the dataset identifier PXD007840.

Supplementary material

11295_2019_1317_MOESM1_ESM.xlsx (380 kb)
Table S1 List of identified phosphorylation sites and changes in their phosphorylation levels upon Rhizophagus intraradices inoculation in Poncirus. a Complete list of total identified phosphorylation sites and changes in their phosphorylation levels upon R. intraradices inoculation in Poncirus. b Phosphopeptides identified in this experiment with p value < 0.05. (XLSX 380 kb)
11295_2019_1317_MOESM2_ESM.xlsx (276 kb)
Table S2 Mercator functional annotation of phosphoprotein sequence data. a Mercator functional annotation of total phosphoprotein sequence data. b Mercator functional annotation of significant changed phosphoprotein sequence data. (XLSX 275 kb)
11295_2019_1317_MOESM3_ESM.xlsx (119 kb)
Table S3 The blast result of total phosphoproteins searching for the P3DB database. a The blast result of total phosphoproteins searching for the P3DB database. b Novel phosphoproteins identified in this experiment. (XLSX 119 kb)
11295_2019_1317_MOESM4_ESM.xlsx (43 kb)
Table S4 The blast results of the Poncirus phosphoproteins (p value < 0.05) against the Medicago and soybean genome. The proteins that labeled with green were significantly changed in Medicago or soybean phosphoproteome and they were the best hit or the e-value was zero. The proteins that labeled with gray were significantly changed in Medicago or soybean phosphoproteome, but they were not the best hit and the e-value was not zero. (XLSX 43 kb)
11295_2019_1317_MOESM5_ESM.xlsx (13 kb)
Table S5 The pathway enrichment analysis of the significantly changed phosphoproteins by using KOBAS3.0 (XLSX 12 kb)
11295_2019_1317_MOESM6_ESM.pdf (7.5 mb)
Fig. S1 Ink stained roots of Poncirus at different time point post-Rhizophagus intraradices inoculation. a Ink-stained roots of AM group after 1 weeks. b Ink-stained root of AM group 2 weeks post-inoculation. c Ink-stained root of AM group 8 weeks post-inoculation. Arbuscular(ab), vesicle(ve), and hyphae(hp) were shown. Scale bars, 200 μm. (PDF 7711 kb)
11295_2019_1317_Fig3_ESM.png (1.5 mb)
Fig. S2

Phosphorylation motif logos that enriched in Rhizophagus intraradices responsive phosphoproteome. Motif-X analysis was performed with a 15 amino acid window, an occurrence of 20, a significance of 10–5, and the C. sinensis protein database was used as the background database to normalize the score against a random distribution of amino acids (PNG 1488 kb)

11295_2019_1317_MOESM7_ESM.eps (4.3 mb)
High resolution image (EPS 4426 kb)

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Key Laboratory of Horticultural Plant Biology (Ministry of Education), Key Laboratory of Horticultural Crop Biology and Genetic Improvement (Central Region, Ministry of Agriculture), College of Horticulture and Forestry SciencesHuazhong Agricultural UniversityWuhan CityPeople’s Republic of China
  2. 2.Institute for Bioscience and Biotechnology Research & Department of Plant Sciences and Landscape ArchitectureUniversity of Maryland, College ParkRockvilleUSA

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