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Qualitative analysis of N-linked glycoproteome in senescent flag leaf of rice

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Abstract

N-Glycosylation is one of the most ubiquitous protein modifications. However, the qualitative analysis of N-glycoproteome during leaf senescence has not been studied yet. In this study, N-glycoproteins were identified in senescent flag leaf of rice through hydrophilic interaction chromatography enrichment and liquid chromatography–tandem mass spectrometry strategy. A total of 381 N-glycoproteins and 479 N-glycosylated sites were identified. In which, 40% of glycoproteins contained signal peptide and 40% had transmembrane domain. Meanwhile, α helix and coil/loop accounted for 1.5% and 98.5% of all N-glycosylated sites. Motif-X analysis suggested that [NxT], [NxS] and [NS] were significantly conserved and enriched. During leaf senescence, proteolysis-related proteins were predominately N-glycosylated by gene ontology analysis. Meanwhile, most identified glycoproteins were enriched in photosynthesis and N-glycan biosynthesis pathways by Kyoto Encyclopedia of Genes and Genomes analysis. Protein–protein interaction analysis showed that N-glycoproteins formed interaction networks to function in the metabolism process of energy substances (carbohydrates, lipids and amino acids), the proteolysis process, and the protein glycosylation process. Among 381 N-glycoproteins, 183 proteins were involved in various and famous senescence-related biological processes including energy substance metabolism (70), proteolysis (44), photosynthesis (17), protein glycosylation (24), reactive oxygen species scavenging (14), transcriptional regulation (6), senescence-associated genes (2) and hormone response (6), suggesting the important role of protein N-glycosylation in leaf senescence. Additionally, ten glycoproteins were found to have been well-studied in senescent process of rice. The results provided a novel insight into the significant involvement of protein N-glycosylation in leaf senescence.

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Abbreviations

ABA:

Abscisic acid

APX:

Ascorbate peroxidase

CAT:

Catalase

FDR:

False discovery rate

GO:

Gene ontology

HILIC:

Hydrophilic interaction chromatography

KEGG:

Kyoto Encyclopedia of Genes and Genomes

LC–MS/MS:

Liquid chromatography–tandem mass spectrometry

Rubisco:

Ribulose 1,5-bisphosphate carboxylase/oxygenase

ROS:

Reactive oxygen species

SAG:

Senescence-associated gene

SOD:

Superoxide dismutase

SP:

Signal peptide

TF:

Transcription factor

References

  • Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53(372):1331–1341

    Article  CAS  PubMed  Google Scholar 

  • Amith SR, Jayanth P, Franchuk S, Siddiqui S, Seyrantepe V, Gee K, Basta S, Beyaert R, Pshezhetsky AV, Szewczuk MR (2009) Dependence of pathogen molecule-induced Toll-like receptor activation and cell function on Neu1 sialidase. Glycoconj J 26(9):1197–1212

    Article  CAS  PubMed  Google Scholar 

  • Ansari MI, Lee R, Chen SG (2005) A novel senescence-associated gene encoding gamma-aminobutyric acid (GABA): pyruvate transaminase is upregulated during rice leaf senescence. Physiol Plant 123:1–8

    Article  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Baum LG, Garner OB, Schaefer K, Lee B (2014) Microbe-host interactions are positively and negatively regulated by galectin–glycan interactions. Front Immunol 5:284

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bu T, Shen J, Chao Q, Shen Z, Yan Z, Zheng H, Wang B (2017) Dynamic N-glycoproteome analysis of maize seedling leaves during de-etiolation using Concanavalin A lectin affinity chromatography and a nano-LC–MS/MS based iTRAQ approach. Plant Cell Rep 36(12):1943–1958

    Article  CAS  PubMed  Google Scholar 

  • Dedvisitsakul P, Jacobsen S, Svensson B, Bunkenborg J, Finnie C, Hägglund P (2014) Glycopeptide enrichment using a combination of ZIC-HILIC and cotton wool for exploring the glycoproteome of wheat flour albumins. J Proteome Res 13(5):2696–2703

    Article  CAS  PubMed  Google Scholar 

  • Deng L, Li L, Zhang S, Shen J, Li S, Hu S, Peng Q, Xiao J, Wu C (2017) Suppressor of rid1 (SID1) shares common targets with RID1 on florigen genes to initiate floral transition in rice. PLoS Genet 13(5):2696–2703

    Google Scholar 

  • Diaz-Mendoza M, Velasco-Arroyo B, Santamaria ME, González-Melendi P, Martinez M, Diaz I (2016) Plant senescence and proteolysis: two processes with one destiny. Genet Mol Biol 39(3):329–338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fanata WID, Lee KH, Son BH, Yoo JY, Harmoko R, Ko KS, Ramasamy NK, Kim KH, Oh D, Jung HS, Kim J, Lee SY, Lee KO (2013) N-Glycan maturation is crucial for cytokinin-mediated development and cellulose synthesis in Oryza sativa. Plant J 73(6):966–979

    Article  CAS  PubMed  Google Scholar 

  • Gao H, Zheng XM, Fei GL, Chen J, Jin MN, Ren YL, Wu WX, Zhou KN, Sheng PK, Zhou F, Jiang L, Wang J, Zhang X, Guo XP, Wang JL, Cheng ZJ, Wu CY, Wang HY, Wan JM (2013) Ehd4 encodes a novel and oryza-genus-specificregulator of photoperiodic flowering in rice. PLoS Genet 9(2):e1003281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48(12):909–930

    Article  CAS  PubMed  Google Scholar 

  • Halim A, Carlsson MC, Madsen CB, Brand S, Møller SR, Olsen CE, Vakhrushev SY, Brimnes J, Wurtzen PA, Ipsen H, Petersen BL, Wandall HH (2015) Glycoproteomic analysis of seven major allergenic proteins reveals novel post-translational modifications. Mol Cell Proteomics 14(1):191–204

    Article  CAS  PubMed  Google Scholar 

  • He Y, Zhang H, Sun Z, Li J, Hong G, Zhu Q, Zhou X, MacFarlane S, Yan F, Chen J (2017) Jasmonic acid-mediated defense suppresses brassinosteroid-mediated susceptibility to rice black streaked dwarf virus infection in rice. New Phytol 214(1):388–399

    Article  CAS  PubMed  Google Scholar 

  • He Y, Li L, Zhang Z, Wu J (2018) Identification and comparative analysis of premature senescence leaf mutants in rice (Oryza sativa L.). Int J Mol Sci 19 (1): 140

  • Hebert DN, Lamriben L, Powers ET, Kelly JW (2014) The intrinsic and extrinsic effects of N-linked glycans on glycoproteostasis. Nat Chem Biol 10(11):902–910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hurkman WJ, Tanaka CK (1986) Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis. Plant Physiol 81(3):802–806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Izumi M, Ishida H (2011) The changes of leaf carbohydrate contents as a regulator of autophagic degradation of chloroplasts via Rubisco-containing bodies during leaf senescence. Plant Signal Behav 6(5):685–687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jan A, Maruyama K, Todaka D, Kidokoro S, Abo M, Yoshimura E, Shinozaki K, Nakashima K, Yamaguchi-Shinozaki K (2013) OsTZF1, a CCCH-tandem zinc finger protein, confers delayed senescence and stress tolerance in rice by regulating stress-related genes. Plant Physiol 161(3):1202–1216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang L, Liu X, Xiong G, Liu H, Chen F, Wang L, Meng X, Liu G, Yu H, Yuan Y, Yi W, Zhao L, Ma H, He Y, Wu Z, Melcher K, Qian Q, Xu HE, Wang Y, Li J (2013) Dwarf 53 acts as a repressor of strigolactone signalling in rice. Nature 504(7480):401–405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang G, Yin D, Zhao J, Chen H, Guo L, Zhu L, Zhai W (2016) The rice thylakoid membrane-bound ascorbate peroxidase OsAPX8 functions in tolerance to bacterial blight. Sci Rep 6(1):26104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiao B, Wang J, Zhu X, Zeng L, Li Q, He Z (2012) A novel protein RLS1 with NB–ARM domains is involved in chloroplast degradation during leaf senescence in rice. Mol Plant 5(1):205–217

    Article  CAS  PubMed  Google Scholar 

  • Kato Y, Murakami S, Yamamoto Y, Chatani H, Kondo Y, Nakano T, Yokota A, Sato F (2004) The DNA-binding protease, CND41, and the degradation of ribulose-1,5-bisphosphate carboxylase/oxygenase in senescent leaves of tobacco. Planta 220(1):97–104

    Article  CAS  PubMed  Google Scholar 

  • Kelleher DJ, Gilmore R (2006) An evolving view of the eukaryotic oligosaccharyltransferase. Glycobiology 16(4):47–62

    Article  CAS  Google Scholar 

  • Koiwa H (2003) The STT3a subunit isoform of the Arabidopsis oligosaccharyltransferase controls adaptive responses to salt/osmotic stress. Plant Cell 15(10):2273–2284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kong Z, Li M, Yang W, Xu W, Xue Y (2006) A novel nuclear-localized CCCH-type zinc finger protein, OsDOS, is involved in delaying leaf senescence in rice. Plant Physiol 141(4):1376–1388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Kumar K, Pandey P, Rajamani V, Padmalatha KV, Dhandapani G, Kanakachari M, Leelavathi S, Kumar PA, Reddy VS (2013) Glycoproteome of elongating cotton fiber cells. Mol Cell Proteomics 12(12):3677–3689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lairson LL, Henrissat B, Davies GJ, Withers SG (2008) Glycosyltransferases: structures, functions, and mechanisms. Annu Rev Biochem 77:521–555

    Article  CAS  PubMed  Google Scholar 

  • Lee RH, Wang CH, Huang LT, Grace-Chen SC (2001) Leaf senescence in rice plants: cloning and characterization of senescence up-regulated genes. J Exp Bot 52(358):1117–1121

    Article  CAS  PubMed  Google Scholar 

  • Leney AC, Atmioui E, Wu W, Ovaa H, Heck AJR (2017) Elucidating crosstalk mechanisms between phosphorylation and O-GlcNAcylation. Proc Natl Acad Sci USA 114(35):E7255–E7261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lerouxel O, Mouille G, Andème-Onzighi C, Bruyant M, Séveno M, Loutelier-Bourhis C, Driouich A, Höfte H, Lerouge P (2005) Mutants in defective glycosylation, an Arabidopsis homolog of an oligosaccharyltransferase complex subunit, show protein underglycosylation and defects in cell differentiation and growth. Plant J 42(4):455–468

    Article  CAS  PubMed  Google Scholar 

  • Lin A, Wang YQ, Tang JY, Xue P, Li CL, Liu LC, Hu B, Yang FQ, Loake GJ, Chu CC (2012) Nitric oxide and protein S-nitrosylation are integral to hydrogen peroxide-induced leaf cell death in rice. Plant Physiol 158(1):451–464

    Article  CAS  PubMed  Google Scholar 

  • Liu L, Zhou Y, Zhou G, Ye R, Zhao L, Li X, Lin Y (2008) Identification of early senescence-associated genes in rice flag leaves. Plant Mol Biol 67(1–2):37–55

    Article  CAS  PubMed  Google Scholar 

  • Mao C, Lu S, Lv B, Zhang B, Shen J, He J, Luo L, Xi D, Chen X, Ming F (2017) A rice NAC transcription factor promotes leaf senescence via ABA biosynthesis. Plant Physiol 174(3):1747–1763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mohorko E, Glockshuber R, Aebi M (2011) Oligosaccharyltransferase: the central enzyme of N-linked protein glycosylation. J Inherit Metab Dis 34(4):869–878

    Article  CAS  PubMed  Google Scholar 

  • Moremen KW, Tiemeyer M, Nairn AV (2012) Vertebrate protein glycosylation: diversity, synthesis and function. Nat Rev Mol Cell Biol 13(7):448–462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nie Y, Liu D (2017) N-Glycosylation is required for FDNC5 stabilization and irisin secretion. Biochem J 474(18):3167–3177

    Article  CAS  PubMed  Google Scholar 

  • Park HS, Ryu HY, Kim BH, Kim SY, Yoon IS, Nam KH (2011) A subset of OsSERK genes, including OsBAK1, affects normal growth and leaf development of rice. Mol Cells 32(6):561–569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parrott DL, Martin JM, Fischer AM (2010) Analysis of barley (Hordeum vulgare) leaf senescence and protease gene expression: a family C1A cysteine protease is specifically induced under conditions characterized by high carbohydrate, but low to moderate nitrogen levels. New Phytol 187(2):313–331

    Article  CAS  PubMed  Google Scholar 

  • Pless DD, Lennarz WJ (1977) Enzymatic conversion of proteins to glycoproteins. Proc Natl Acad Sci USA 74(1):134–138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prabakaran S, Lippens G, Steen H, Gunawardena J (2012) Post-translational modification: nature’s escape from genetic imprisonment and the basis for dynamic information encoding. Wiley Interdiscip Rev Syst Biol Med 4(6):565–583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qin C, Li Y, Gan J, Wang W, Zhang H, Liu Y, Wu P (2013) OsDGL1, a homolog of an oligosaccharyltransferase complex subunit, is involved in N-glycosylation and root development in rice. Plant Cell Physiol 54(1):129–137

    Article  CAS  PubMed  Google Scholar 

  • Roberts IN, Caputo C, Kade M, Criado MV, Barneix A (2011) Subtilisin-like serine proteases involved in N remobilization during grain filling in wheat. Acta Physiol Plant 33(5):1997–2001

    Article  CAS  Google Scholar 

  • Robertsa IN, Caputoa C, Criadoa MV, Funkb C (2012) Senescence-associated proteases in plants. Physiol Plant 145(1):130–139

    Article  CAS  Google Scholar 

  • Ruiz-May E, Hucko S, Howe KJ, Zhang S, Sherwood RW, Thannhauser TW, Rose JKC (2014) A comparative study of lectin affinity based plant N-glycoproteome profiling using tomato fruit as a model. Mol Cell Proteomics 13(2):566

    Article  CAS  PubMed  Google Scholar 

  • Ruyter-Spira C, Al-Babili S, van der Krol S, Bouwmeester H (2013) The biology of strigolactones. Trends Plant Sci 18(2):72–83

    Article  CAS  PubMed  Google Scholar 

  • Sakuraba Y, Piao W, Lim J, Han S, Kim Y, An G, Paek N (2015) Rice ONAC106 inhibits leaf senescence and increases salt tolerance and tiller angle. Plant Cell Physiol 56(12):2325–2339

    Article  CAS  PubMed  Google Scholar 

  • Schumann U, Prestele J, O’Geen H, Brueggeman R, Wanner G, Gietl C (2007) Requirement of the C2H2 zinc ring finger of the Arabidopsis PEX10 for photorespiration and leaf peroxisome contact with chloroplasts. Proc Natl Acad Sci USA 104:1069–1074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scott H, Panin VM (2014) The role of protein N-glycosylation in neural transmission. Glycobiology 24(5):407–417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silva-Sanchez C, Chen S, Li J, Chourey PS (2014) A comparative glycoproteome study of developing endosperm in the hexose-deficient miniature1 (mn1) seed mutant and its wild type Mn1 in maize. Front Plant Sci 5:63

    Article  PubMed  PubMed Central  Google Scholar 

  • Suzuki Y, Makino A (2013) Translational downregulation of RBCL is operative in the coordinated expression of Rubisco genes in senescent leaves in rice. J Exp Bot 64(4):1145–1152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki Y, Makino A, Mae T (2001) Changes in the turnover of Rubisco and levels of mRNAs of rbcL and rbcS in rice leaves from emergence to senescence. Plant Cell Environ 24(12):1353–1360

    Article  CAS  Google Scholar 

  • Troncoso-Ponce MA, Cao X, Yang Z, Ohlrogge JB (2013) Lipid turnover during senescence. Plant Sci 205–206:13–19. https://doi.org/10.1016/j.plantsci.2013.01.004

    Article  CAS  PubMed  Google Scholar 

  • Van den Steen P, Rudd PM, Dwek RA, Opdenakker G (1998) Concepts and principles of O-linked glycosylation. Crit Rev Biochem Mol Biol 33(3):151–208

    Article  PubMed  Google Scholar 

  • Veyres N, Danon A, Aono M, Galliot S, Karibasappa YB, Diet A, Grandmottet F, Tamaoki M, Lesur D, Pilard S, Boitel-Conti M, Sangwan-Norreel BS, Sangwan RS (2008) The Arabidopsis sweetie mutant is affected in carbohydrate metabolism and defective in the control of growth, development and senescence. Plant J 55(4):665–686

    Article  CAS  PubMed  Google Scholar 

  • von Saint Paul V, Zhang W, Kanawati B, Geist B, Faus-Keßler T, Schmitt-Kopplin P, Schäffner AR (2012) The Arabidopsis glucosyltransferase UGT76B1 conjugates isoleucic acid and modulates plant defense and senescence. Plant Cell 23(11):4124–4145

    Google Scholar 

  • Wang Z, Wang Y, Hong X, Hu D, Liu C, Yang J, Li Y, Huang Y, Feng Y, Gong H, Li Y, Fang G, Tang H, Li Y (2015) Functional inactivation of UDP-N-acetylglucosamine pyrophosphorylase 1 (UAP1) induces early leaf senescence and defense responses in rice. J Exp Bot 66(3):973–987

    Article  PubMed  CAS  Google Scholar 

  • Wang HM, Li FD, Wang YC, Li Y, Yang HP (2018a) Quantitative analysis of the global proteome in peripheral blood mononuclear cells from patients with new-onset psoriasis. Proteomics 18(19):e1800003

    Article  PubMed  CAS  Google Scholar 

  • Wang M, Zhang T, Peng H, Luo S, Tan J, Jiang K, Heng Y, Zhang X, Guo X, Zheng J, Cheng Z (2018b) Rice premature leaf senescence 2, encoding a glycosyltransferase (GT), is involved in leaf senescence. Front Plant Sci 9:560

    Article  PubMed  PubMed Central  Google Scholar 

  • Watanabe M, Balazadeh S, Tohge T, Erban A, Giavalisco P, Kopka J, Mueller-Roeber B, Fernie AR, Hoefgen R (2013) Comprehensive dissection of spatiotemporal metabolic shifts in primary, secondary, and lipid metabolism during developmental senescence in Arabidopsis. Plant Physiol 162(3):1290–1310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu S, Medzihradszky KF, Wang Z, Burlingame AL, Chalkley RJ (2016) N-Glycopeptide profiling in Arabidopsis inflorescence. Mol Cell Proteomics 15(6):2048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu L, He H, Hu Z, Ma Z (2016) Comprehensive quantification of N-glycoproteome in fusarium graminearum reveals intensive glycosylation changes against fungicide. J Proteomics 142:82–90

    Article  CAS  PubMed  Google Scholar 

  • Zeng D, Qin R, Li M, Alamin M, Jin X, Liu Y, Shi C (2017) The ferredoxin-dependent glutamate synthase (OsFd-GOGAT) participates in leaf senescence and the nitrogen remobilization in rice. Mol Genet Genomics 292(2):385–395

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Ni L, Liu Y, Wang Y, Zhang A, Tan M, Jiang M (2012) The C2H2-type zinc finger protein ZFP182 is involved in abscisic acid-induced antioxidant defense in rice. J Integr Plant Biol 54(7):500–510

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Liu Y, Wen F, Yao D, Wang L, Guo J, Ni L, Zhang A, Tan M, Jiang M (2014) A novel rice C2H2-type zinc finger protein, ZFP36, is a key player involved in abscisic acid-induced antioxidant defense and oxidative stress tolerance in rice. J Exp Bot 65(20):5795–5809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang M, Chen G, Lv D, Li X, Yan Y (2015) N-Linked glycoproteome profiling of seedling leaf in Brachypodium distachyon L. J Proteome Res 14(4):1727–1738

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Wang X, Cui D, Zhu J (2016) Proteomic and N-glycoproteomic quantification reveal aberrant changes in the human saliva of oral ulcer patients. Proteomics 16(24):3173–3182

    Article  CAS  PubMed  Google Scholar 

  • Zhu J, Sun Z, Cheng K, Chen R, Ye M, Xu B, Sun D, Wang L, Liu J, Wang F, Zou H (2014) Comprehensive mapping of protein N-glycosylation in human liver by combining hydrophilic interaction chromatography and hydrazide chemistry. J Proteome Res 13(3):1713–1721

    Article  CAS  PubMed  Google Scholar 

  • Zielinska DF, Gnad F, Schropp K, Wisniewski JR, Mann M (2012) Mapping N-glycosylation sites across seven evolutionarily distant species reveals a divergent substrate proteome despite a common core machinery. Mol Cell 46:542–548

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant Nos. 31760380, 31860359) and the Science and Technology Projects of Jiangxi Province (20181BAB214011).

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  1. Xiaoping Huang and Hongyu Zhang have contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Crop Physiology, Ecology and Genetic Breeding (Jiangxi Agricultural University), Ministry of Education of the P.R. China, Nanchang, 330045, Jiangxi, China

    Xiaoping Huang, Hongyu Zhang, Jianglin Liao, Lingxia Wei, Rong Guo, Wenbo Xiao, Yingjin Huang & Zhaohai Wang

  2. Southern Regional Collaborative Innovation Center for Grain and Oil Crops in China, Changsha, 410128, Hunan, China

    Jianglin Liao, Yingjin Huang & Zhaohai Wang

  3. College of Agronomy, Jiangxi Agricultural University, Nanchang, 330045, Jiangxi, China

    Weigang Kuang

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Contributions

XH and HZ drafted the manuscript; JL provided the bioinformatics analysis; LW and RG performed the paddy field management; WX and WK conducted partial data analysis; YH participated in the experimental design; ZW provided the overall guidance and the manuscript revision. All authors read and approved the manuscript.

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Supplementary Fig. S1 Protein–protein interaction of the identified N-glycoproteins (PDF 244 kb)

10725_2019_509_MOESM2_ESM.xlsx

Supplementary Table S1 The identified N-glycoproteins and glycosylated sites of senescent flag leaf in rice (XLSX 167 kb)

Supplementary Table S2 The COG function classification of the identified N-glycoproteins (XLSX 48 kb)

10725_2019_509_MOESM4_ESM.xlsx

Supplementary Table S3 The subcellular localization, signal peptide, transmembrane domain, and secondary structure of the identified N-glycoproteins (XLSX 74 kb)

Supplementary Table S4 Conserved motifs of the identified N-glycoproteins (XLSX 18 kb)

Supplementary Table S5 N-glycoproteins enriched in proteolysis biological process of GO enrichment (XLSX 16 kb)

Supplementary Table S6 KEGG enrichment pathway of the identified N-glycoproteins (XLSX 31 kb)

Supplementary Table S7 Protein domain enrichment of the identified N-glycoproteins (XLSX 27 kb)

10725_2019_509_MOESM9_ESM.xlsx

Supplementary Table S8 Protein–protein interaction of the identified N-glycoproteins. Glycoproteins relating to the metabolism of carbohydrates, lipids and amino acids were labelled in red (XLSX 27 kb)

10725_2019_509_MOESM10_ESM.xlsx

Supplementary Table S9 N-glycoproteins related to the metabolism of carbohydrates, lipids and amino acids in senescent flag leaf of rice (XLSX 20 kb)

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Huang, X., Zhang, H., Liao, J. et al. Qualitative analysis of N-linked glycoproteome in senescent flag leaf of rice. Plant Growth Regul 88, 309–326 (2019). https://doi.org/10.1007/s10725-019-00509-y

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