蜂王浆高产蜜蜂与意大利蜜蜂哺育蜂唾液腺蛋白质组分析

doi:10.3864/j.issn.0578-1752.2022.13.015

Abstract

Abstract:

【Objective】The objective of this study is to investigate the proteome profile of the postcereberal gland (PGld) and thoracic gland (ThGld) between high royal jelly producing bees (Apis mellifera liguatica, RJBs) and Italian bees (Apis mellifera liguatica, ITBs) with the aim of revealing the molecular basis of salivary gland regulating royal jelly production, and to provide a basis for analyzing the high-yield mechanism of royal jelly.【Method】PGld and ThGld were dissected from nurse bees of RJBs and ITBs. After protein extraction and enzyme digestion, the peptide samples were analyzed by liquid chromatography coupled with tandem mass spectrometry. Furthermore, the mass spectral data were qualified and quantified by MaxQuant software, and the following bioinformatic analysis was conducted using Perseus software, prediction of secretory protein was achieved by SignalP database, biological process and KEGG pathway were enriched by Cluego software.【Result】Totally 2 335 proteins were identified in salivary glands of RJBs and ITBs nurse bees, including 1 823 proteins in PGld and 1 922 proteins in ThGld. The expression profiles of the core proteins in the PGld and ThGld of RJBs and ITBs were similar, mainly involved in RNA metabolism, nucleic acid metabolism, ATP metabolism, protein translation, translation regulation and catabolism. The principal component analysis (PCA) showed that the molecular basis of salivary gland of RJBs and ITBs had exerted varying extent of differentiation during the selective breeding. Quantitatively, the PGld of ITBs and RJBs expressed 254 and 333 up-regulated proteins, respectively, corresponding to the small molecule and carbohydrate metabolism pathway in ITBs, and the organic nitrogen compound synthesis, cell redox homeostasis, amino acid metabolism in RJBs. Those proved that the protein synthesis, amino acid metabolism and energy supply of salivary gland cells in RJBs were more active than ITBs. In the same way, the up-regulated expressions of 412 and 162 proteins were detected in the ThGld of ITBs and RJBs, respectively, which involved in the pathways of oxidative phosphorylation, translation regulation in ITBs, and oxidative phosphorylation, response to toxic substances in RJBs, indicating that the level of resistance of RJBs ThGld cells was increased. A total of 43 secretory proteins were identified in the salivary glands of RJBs and ITBs, in which 15 were detected in royal jelly. Major royal jelly proteins 1, 2, 3, 4, 5 and 7 were detected in PGld and ThGld, indicating that both of the glands were involved in the synthesis of royal jelly main protein. The identification of α-glucosidase related to nectar transformation and odorant binding proteins 3, 13, 17 and 21 involved in the synthesis and release of chemical pheromones in both PGld and ThGld indicated their basic function of nectar transformation and pheromone synthesis. The enhanced expression of major royal jelly proteins 1, 2, 3 and 7, hexamerin 70a and 110, odorant binding proteins 3, 13, 17 and 21, transferrin and apolipophorin-III-like protein in the salivary gland of RJBs demonstrated that the synthesis of pheromone and royal jelly protein was stronger than ITBs.【Conclusion】The core proteome with similar pattern in salivary glands of RJBs and ITBs ensures the synthesis and secretion of royal jelly protein, pheromone and invertase. Molecular variation between the salivary glands of RJBs and ITBs was developed after long-term selective breeding. Relative to ITBs, the salivary glands of RJBs enhance the ability of protein synthesis, amino acid metabolism, cell energy supply and stress resistance, and upregulate the expression of most secretory proteins, which benefits to a better protein synthesis system with promising efficiency and lasting, and contributes to the high producing of royal jelly.

Key words: salivary gland, proteome, high royal jelly producing bee, Italian bee, royal jelly, secretory protein

WANG RongHua,MENG LiFeng,FENG Mao,FANG Yu,WEI QiaoHong,MA BeiBei,ZHONG WeiLai,LI JianKe. Proteome Analysis of the Salivary Gland of Nurse Bee from High Royal Jelly Producing Bees and Italian Bees[J].Scientia Agricultura Sinica, 2022, 55(13): 2667-2684.

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URL: https://www.chinaagrisci.com/EN/10.3864/j.issn.0578-1752.2022.13.015

https://www.chinaagrisci.com/EN/Y2022/V55/I13/2667

Figures/Tables 11

Table 1

Fig. 1

Fig. 2

Fig. 3

Fig. 4

Fig. 5

Fig. 6

Fig. 7

Fig. 8

Table 2

Identification of proteins in royal jelly"

GI登录号 Gl number	UniProt登录号 UniProtKB	蛋白名称 Protein name	S<BOLD>CHMITZOVÁ</BOLD> et al.^{<BOLD> [3</BOLD><BOLD>7</BOLD><BOLD>]</BOLD>}	<BOLD>S</BOLD><BOLD>CH</BOLD><BOLD>Ö</BOLD><BOLD>NLEBEN </BOLD> et al.^{<BOLD>[3</BOLD><BOLD>8</BOLD><BOLD>]</BOLD>}	<BOLD>FURUSAWA</BOLD> et al.^{<BOLD>[</BOLD><BOLD>39</BOLD><BOLD>]</BOLD>}	<BOLD>HAN</BOLD> et al.^{<BOLD>[</BOLD><BOLD>40</BOLD><BOLD>]</BOLD>}	<BOLD>FUJITA</BOLD> et al.^[1]	张兰Z<BOLD>HANG L</BOLD>an^[41]	本研究 This study
gi\|58585144	Q9U8X5	Alpha-amylase				λ		λ	λ
gi\|58585164	Q17058	Alpha-glucosidase		λ	λ	λ	λ	λ	λ
gi\|166795901	B0LUE8	Apolipophorin-III-like protein		λ	λ	λ	λ	λ	λ
gi\|254910938	P17722	Defensin-1		λ		λ	λ	λ	λ
gi\|406117	Q6J4Q1	Hexamerin							λ
gi\|551648	A7XZB1	Hexamerin 110							λ
gi\|409354	A5YV87	Hexamerin 70c							λ
gi\|406142	Q10416	Hymenoptaecin						λ	λ
gi\|60115688	Q5EF78	Icarapin-like			λ	λ	λ	λ	λ
gi\|506614904	R4TRB9	Lys1 (fragment)						λ	λ
gi\|58585098	O18330	Major royal jelly protein 1	λ	λ	λ	λ	λ	λ	λ
gi\|58585108	O77061	Major royal jelly protein 2	λ	λ	λ	λ	λ	λ	λ
gi\|406121	Q17060	Major royal jelly protein 3	λ					λ	λ
gi\|58585170	Q17061	Major royal jelly protein 4	λ	λ	λ	λ	λ	λ	λ
gi\|66547819	O97432	Major royal jelly protein 5	λ		λ			λ	λ
gi\|58585188	Q6W3E3	Major royal jelly protein 6		λ		λ	λ	λ	λ
gi\|62198227	Q6IMJ9	Major royal jelly protein 7			λ	λ	λ	λ	λ
gi\|67010041	Q4ZJX1	Major royal jelly protein 9					λ	λ	λ
gi\|677674	Q1W641	Odorant binding protein 13							λ
gi\|94158822	Q1W640	Odorant binding protein 14			λ		λ	λ
gi\|66524161	—	Ferritin heavy chain			λ			λ
gi\|110772962	—	Glucose dehydrogenase [acceptor]-like, partial				λ	λ	λ
gi\|110764266	—	Hypothetical protein		λ
gi\|48094573	—	Hypothetical protein loc408608		λ	λ	λ	λ	λ
gi\|110748686	—	Hypothetical protein loc726446		λ
gi\|110762641	—	Ferritin 1 heavy chain homologue cg2216-pe, isoform e			λ	λ		λ
gi\|406078	Q86PH6	Transferrin							λ
gi\|410337	B2D0J4	Venom dipeptidyl peptidase 4						λ	λ
gi\|413894	A0EM59	Yellow-e3						λ	λ
gi\|82527239	A0EM58	Yellow-h			λ				λ

Table 2

Table 3

Identification and relative intensity changes of secretory proteins from salivary gland of RJBs and ITBs"

UniProt登录号 UniProtKB	蛋白名称 Protein name	头唾腺PGld			胸唾腺ThGld
UniProt登录号 UniProtKB	蛋白名称 Protein name	意蜂 ITBs	浆蜂 RJBs	浆蜂相对强度变化倍数 RJBs relative strength change	意蜂 ITBs	浆蜂 RJBs	浆蜂相对强度变化倍数 RJBs relative strength change
Q17058	Alpha-glucosidase*	14	8	0.5	—	—	—
B0LUE8	Apolipophorin-III-like protein*	31	67	2.1	145	267	1.8
P17722	Defensin-1*	23	31	1.4	—	—	—
A7XZB1	Hexamerin 110*	1	6	5.6	5	113	21.2
Q10416	Hymenoptaecin*	—	—	—	2	—	—
Q5BLY4	Icarapin-like*	10	16	1.6	34	32	0.9
O18330	Major royal jelly protein 1*	1378	1820	1.3	131	220	1.7
O77061	Major royal jelly protein 2*	366	589	1.6	81	156	1.9
Q17060	Major royal jelly protein 3*	413	641	1.5	96	132	1.4
UniProt登录号 UniProtKB	蛋白名称 Protein name	头唾腺PGld			胸唾腺ThGld
UniProt登录号 UniProtKB	蛋白名称 Protein name	意蜂 ITBs	浆蜂 RJBs	浆蜂相对强度变化倍数 RJBs relative strength change	意蜂 ITBs	浆蜂 RJBs	浆蜂相对强度变化倍数 RJBs relative strength change
Q17061	Major royal jelly protein 4*	69	116	1.7	10	10	1.0
O97432	Major royal jelly protein 5*	106	105	1.0	10	—	—
Q6W3E3	Major royal jelly protein 6*	10	5	0.5	—	—	—
Q6IMJ9	Major royal jelly protein 7*	68	82	1.2	14	21	1.5
Q1W641	Odorant binding protein 13*	9	15	1.6	15	41	2.8
Q86PH6	Transferrin*	47	105	2.2	86	332	3.9
Q25BT7	Alpha-glucosidase	6	13	2.1	8	17	2.0
Q8I6X7	Antennal-specific protein 3c	200	158	0.8	94	105	1.1
D3XL75	APD-3-like protein	13	33	2.5	5	12	2.5
Q76LA5	Carboxylic ester hydrolase	—	—	—	8	17	2.2
Q3LBA7	Chemosensory protein 1	52	34	0.7	—	—	—
D3XL68	C-type lectin domain-containing protein	21	27	1.3	—	—	—
Q0GQQ4	Cys-loop ligand-gated ion channel subunit	—	—	—	43	23	0.5
C7AHQ2	Gram-negative bacteria-binding protein 1-2	4	3	0.7	2	1	0.5
A5YVK7	Hexamerin 70a	9	34	3.7	5	41	8.7
G9F9Z6	IRP30	4	10	2.4	6	38	6.3
A0A088A676	Maxi-like antifreeze protein	61	5	0.1	—	—	—
P01501	Melittin	—	—	—	7	6	0.8
Q1W637	Odorant binding protein 17	2	3	1.5	4	10	2.4
Q1W636	Odorant binding protein 18	3	4	1.3	—	—	—
Q1W633	Odorant binding protein 21	9	10	1.1	14	17	1.2
Q1W647	Odorant binding protein 3	3	12	3.4	6	22	3.4
H9KQJ7	Omega-conotoxin-like protein 1	30	36	1.2	13	35	2.7
A0A222LPT2	Putative cyclin-dependent serine/threonine-protein kinase	—	—	—	10	16	1.6
A0A087ER55	SBP_bac_5 domain-containing protein	4	4	1.0	—	—	—
H9KB88	Secapin-3	3	4	1.7	5	6	1.3
A5A5E4	Structural cuticle protein	589	650	1.1	326	254	0.8
A0A1B1JID1	Superoxide dismutase [Cu-Zn]	—	—	—	12	6	0.5
Q5XUU6	Take-out-like carrier protein JHBP-1	—	—	—	7	20	3.0
A8J4S9	Trehalase	—	—	—	4	2	0.4
I7KJQ1	Troponin C type iiia	2	1	0.5	—	—	—
D3XL69	Uncharacterized protein (Fragment)	7	11	1.6	—	—	—
Q5BLY5	Venom acid phosphatase Acph-1	—	—	—	2	—	—
Q868N5	Vitellogenin	7	78	11.3	3	189	68.0

Table 3

References 55

[1]	FUJITA T, KOZUKA-HATA H, AO-KONDO H, KUNIEDA T, OYAMA M, KUBO T. Proteomic analysis of the royal jelly and characterization of the functions of its derivation glands in the honeybee. Journal of Proteome Research, 2013, 12(1): 404-411. doi: 10.1021/pr300700e
[2]	BUTTSTEDT A, MORITZ R F, ERLER S. Origin and function of the major royal jelly proteins of the honeybee (Apis mellifera) as members of the yellow gene family. Biological Reviews, 2014, 89(2): 255-269. doi: 10.1111/brv.12052
[3]	HUO X, WU B, FENG M, HAN B, FANG Y, HAO Y, MENG L, WUBIE A J, FAN P, HU H, QI Y, LI J K. Proteomic analysis reveals the molecular underpinnings of mandibular gland development and lipid metabolism in two lines of honeybees (Apis mellifera ligustica). Journal of Proteome Research, 2016, 15(9): 3342-3357. doi: 10.1021/acs.jproteome.6b00526
[4]	KAMAKURA M. Royalactin induces queen differentiation in honeybees. Nature, 2011, 473(7348): 478-483. doi: 10.1038/nature10093
[5]	FAN P, HAN B, HU H, WEI Q, ZHANG X, MENG L, NIE J, TANG X, TIAN X, ZHANG L, WANG L, LI J K. Proteome of thymus and spleen reveals that 10-hydroxydec-2-enoic acid could enhance immunity in mice. Expert Opinion on Therapeutic Targets, 2020, 24(3): 267-279. doi: 10.1080/14728222.2020.1733529
[6]	TOKUNAGA K H, YOSHIDA C, SUZUKI K M, MARUYAMA H, FUTAMURA Y, ARAKI Y, MISHIMA S. Antihypertensive effect of peptides from royal jelly in spontaneously hypertensive rats. Biological and Pharmaceutical Bulletin, 2004, 27(2): 189-192. doi: 10.1248/bpb.27.189
[7]	FUJIWARA S, IMAI J, FUJIWARA M, YAESHIMA T, KAWASHIMA T, KOBAYASHI K. A potent antibacterial protein in royal jelly. Purification and determination of the primary structure of royalisin. The Journal of Biological Chemistry, 1990, 265(19): 11333-11337. doi: 10.1016/S0021-9258(19)38596-5
[8]	MORGAN J F, TOLNAI S, TOWNSEND G F. Studies on the in vitro antitumor activity of fatty acids. II. Saturated dicarboxylic acids. Canadian Journal of Biochemistry and Physiology, 1960, 38(6): 597-603. doi: 10.1139/o60-073
[9]	LI J K, WANG A P. Comprehensive technology for maximizing royal jelly production. American Bee Journal, 2005, 145(8): 661-664.
[10]	LI J K, WANG T, ZHANG Z, PAN Y. Proteomic analysis of royal jelly from three strains of western honeybees (Apis mellifera). Journal of Agricultural and Food Chemistry, 2007, 55(21): 8411-8422. doi: 10.1021/jf0717440
[11]	FANG Y, FENG M, LI J K. Royal jelly proteome comparison between A. mellifera ligustica and A. cerana cerana. Journal of Proteome Research, 2010, 9(5): 2207-2215. doi: 10.1021/pr900979h
[12]	WYTRYCHOWSKI M, CHENAVAS S, DANIELE G, CASABIANCA H, BATTEAU M, GUIBERT S, BRION B. Physicochemical characterisation of French royal jelly: Comparison with commercial royal jellies and royal jellies produced through artificial bee-feeding. Journal of Food Composition and Analysis, 2013, 29(2): 126-133. doi: 10.1016/j.jfca.2012.12.002
[13]	KATZAV-GOZANSKY T, SOROKER V, IONESCU A, ROBINSON G E, HEFETZ A. Task-related chemical analysis of labial gland volatile secretion in worker honeybees (Apis mellifera ligustica). Journal of Chemical Ecology, 2001, 27(5): 919-926. doi: 10.1023/A:1010330902388
[14]	黄少康. 蜜蜂生理学. 北京: 中国农业出版社, 2011: 180-182.
	HUANG S K. Honeybee Physiology. Beijing: China Agriculture Press, 2011: 180-182. (in Chinese)
[15]	MARTIN S J, CORREIA-OLIVEIRA M E, SHEMILT S, DRIJFHOUT F P. Is the salivary gland associated with honey bee recognition compounds in worker honey bees (Apis mellifera)? Journal of Chemical Ecology, 2018, 44(7/8): 650-657.
[16]	POIANI S B, CRUZ-LANDIM C D. Comparison and correlation between chemical profiles of cephalic salivary glands and cuticle surface of workers of Apis mellifera (Hymenoptera, Apidae). Canadian Journal of Zoology, 2017, 95(7): 453-461. doi: 10.1139/cjz-2016-0102
[17]	FENG M, FANG Y, HAN B, ZHANG L, LU X, LI J K. Novel aspects of understanding molecular working mechanisms of salivary glands of worker honeybees (Apis mellifera) investigated by proteomics and phosphoproteomics. Journal of Proteomics, 2013, 87: 1-15. doi: 10.1016/j.jprot.2013.05.021
[18]	FUJITA T, KOZUKA-HATA H, UNO Y, NISHIKORI K, MORIOKA M, OYAMA M, KUBO T. Functional analysis of the honeybee (Apis mellifera L.) salivary system using proteomics. Biochemical and Biophysical Research Communications, 2010, 397(4): 740-744. doi: 10.1016/j.bbrc.2010.06.023
[19]	SIMPSON J. The functions of the salivary glands of Apis mellifera. Journal of Insect Physiology, 1960, 4(2): 107-121. doi: 10.1016/0022-1910(60)90073-1
[20]	SVECNJAK L, PRDUN S, ROGINA J, BUBALO D, JERKOVIC I. Characterization of Satsuma mandarin (Citrus unshiu Marc.) nectar- to-honey transformation pathway using FTIR-ATR spectroscopy. Food Chemistry, 2017, 232: 286-294. doi: 10.1016/j.foodchem.2017.03.159
[21]	KUBOTA M, TSUJI M, NISHIMOTO M, WONGCHAWALIT J, OKUYAMA M, MORI H, MATSUI H, SURARIT R, SVASTI J, KIMURA A, CHIBA S. Localization of alpha-glucosidases I, II, and III in organs of European honeybees, Apis mellifera L., and the origin of alpha-glucosidase in honey. Bioscience, Biotechnology, and Biochemistry, 2004, 68(11): 2346-2352. doi: 10.1271/bbb.68.2346
[22]	PONTOH J, LOW N. Purification and characterization of β- glucosidase from honey bees (Apis mellifera). Insect Biochemistry and Molecular Biology, 2002, 32(6): 679-690. doi: 10.1016/S0965-1748(01)00147-3
[23]	AL-SHERIF A A, MAZEED A M, EWIS M A, NAFEA E A, HAGAG E E, KAMEL A A. Activity of salivary glands in secreting honey-elaborating enzymes in two subspecies of honeybee (Apis mellifera L). Physiological Entomology, 2017, 42(4): 397-403. doi: 10.1111/phen.12213
[24]	李建科, 陈盛禄, 钟伯雄, 苏松坤. 西方蜜蜂产浆量的动态遗传研究. 遗传学报, 2003, 30(6): 547-554.
	LI J K, CHEN S L, ZHONG B X, SU S K. Genetic analysis for developmental behavior of honeybee colony’s royal jelly production traits in western honeybees. Acta Genetica Sinica, 2003, 30(6): 547-554. (in Chinese)
[25]	ALTAYE S Z, MENG L, LI J K. Molecular insights into the enhanced performance of royal jelly secretion by a stock of honeybee (Apis mellifera ligustica) selected for increasing royal jelly production. Apidologie, 2019, 50(4): 436-453. doi: 10.1007/s13592-019-00656-1
[26]	李建科, 陈盛禄, 钟伯雄, 苏松坤. 西方蜜蜂咽下腺与繁殖力的发育遗传研究. 中国畜牧杂志, 2003, 39(6): 9-11.
	LI J K, CHEN S L, ZHONG B X, SU S K. Genetic analysis for developmental behavior of reproductive ability and hypopheryngeal gland in western honeybees (Apis mellifera lingistica). Chinese Journal of Animal Science, 2003, 39(6): 9-11. (in Chinese)
[27]	LI J K, FENG M, BEGNA D, FANG Y, ZHENG A. Proteome comparison of hypopharyngeal gland development between Italian and royal jelly producing worker honeybees (Apis mellifera L.). Journal of Proteome Research, 2010, 9(12): 6578-6594. doi: 10.1021/pr100768t
[28]	HU H, BEZABIH G, FENG M, WEI Q, ZHANG X, WU F, MENG L, FANG Y, HAN B, MA C, LI J K. In-depth proteome of the hypopharyngeal glands of honeybee workers reveals highly activated protein and energy metabolism in priming the secretion of royal jelly. Molecular and Cellular Proteomics, 2019, 18(4): 606-621. doi: 10.1074/mcp.RA118.001257
[29]	李爽, 李建科. 蜂王浆高产蜜蜂与意大利蜜蜂工蜂上颚腺磷酸化蛋白质组分析. 中国农业科学, 2017, 50(23): 4656-4670.
	LI S, LI J K. Comparative analysis of phosphoproteome between mandibular glands of high royal jelly producing bees and Italian bees. Scientia Agricultura Sinica, 2017, 50(23): 4656-4670. (in Chinese)
[30]	ARARSO Z, MA C, QI Y, FENG M, HAN B, HU H, MENG L, LI J K. Proteome comparisons between hemolymph of two honeybee strains (Apis mellifera ligustica) reveal divergent molecular basis in driving hemolymph function and high royal jelly secretion. Journal of Proteome Research, 2018, 17(1): 402-419. doi: 10.1021/acs.jproteome.7b00621
[31]	HAN B, FANG Y, FENG M, HU H, HAO Y, MA C, HUO X, MENG L, ZHANG X, WU F, LI J K. Brain membrane proteome and phosphoproteome reveal molecular basis associating with nursing and foraging behaviors of honeybee workers. Journal of Proteome Research, 2017, 16(10): 3646-3663. doi: 10.1021/acs.jproteome.7b00371
[32]	ZHANG X, HU H, HAN B, WEI Q, MENG L, WU F, FANG Y, FENG M, MA C, RUEPPELL O, LI J K. The neuroproteomic basis of enhanced perception and processing of brood signals that trigger increased reproductive investment in honeybee (Apis mellifera) workers. Molecular and Cellular Proteomics, 2020, 19(10): 1632-1648. doi: 10.1074/mcp.RA120.002123
[33]	FENG M, RAMADAN H, HAN B, FANG Y, LI J K. Hemolymph proteome changes during worker brood development match the biological divergences between western honey bees (Apis mellifera) and eastern honey bees (Apis cerana). BMC Genomics, 2014, 15(1): 563. doi: 10.1186/1471-2164-15-563
[34]	BRADFORD M M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein- dye binding. Analytical Biochemistry, 1976, 72(1/2): 248-254. doi: 10.1016/0003-2697(76)90527-3
[35]	BINDEA G, MLECNIK B, HACKL H, CHAROENTONG P, TOSOLINI M, KIRILOVSKY A, FRIDMAN W H, PAGÈS F, TRAJANOSKI Z, GALON J. ClueGO: A cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics, 2009, 25(8): 1091-1093. doi: 10.1093/bioinformatics/btp101
[36]	ARMENTEROS J J A, TSIRIGOS K D, SØNDERBY C K, PETERSEN T N, WINTHER O, BRUNAK S, VON HEIJNE G, NIELSEN H. SignalP 5.0 improves signal peptide predictions using deep neural networks. Nature Biotechnology, 2019, 37(4): 420-423. doi: 10.1038/s41587-019-0036-z
[37]	SCHMITZOVÁ J, KLAUDINY J, ALBERT Š, SCHRÖDER W, SCHRECKENGOST W, HANES J, JÚDOVA J, ŠIMÚTH J. A family of major royal jelly proteins of the honeybee Apis mellifera L. Cellular and Molecular Life Sciences, 1998, 54(9): 1020-1030. doi: 10.1007/s000180050229
[38]	SCHÖNLEBEN S, SICKMANN A, MUELLER M J, REINDERS J. Proteome analysis of Apis mellifera royal jelly. Analytical and Bioanalytical Chemistry, 2007, 389(4): 1087-1093. doi: 10.1007/s00216-007-1498-2
[39]	FURUSAWA T, RAKWAL R, NAM H W, SHIBATO J, AGRAWAL G K, KIM Y S, OGAWA Y, YOSHIDA Y, KOUZUMA Y, MASUO Y, YONEKURA M. Comprehensive royal jelly (RJ) proteomics using one- and two-dimensional proteomics platforms reveals novel RJ proteins and potential phospho/glycoproteins. Journal of Proteome Research, 2008, 7(8): 3194-3229. doi: 10.1021/pr800061j
[40]	HAN B, LI C, ZHANG L, FANG Y, FENG M, LI J K. Novel royal jelly proteins identified by gel-based and gel-free proteomics. Journal of Agricultural and Food Chemistry, 2011, 59(18): 10346-10355. doi: 10.1021/jf202355n
[41]	张兰. 蜂王浆蛋白翻译后修饰及未知蛋白探索[D]. 北京: 中国农业科学院, 2013.
	ZHANG L. Novel aspects of understanding post-translational modifications and proteins in royal jelly[D]. Beijing: Chinese Academy of Agricultural Sciences, 2013. (in Chinese)
[42]	LE CONTE Y, BECARD J M, COSTAGLIOLA G, DE VAUBLANC G, EL MAATAOUI M, CRAUSER D, PLETTNER E, SLESSOR K N. Larval salivary glands are a source of primer and releaser pheromone in honey bee (Apis mellifera L.). Naturwissenschaften, 2006, 93(5): 237-241. doi: 10.1007/s00114-006-0089-y
[43]	AON M A, BERNIER M, MITCHELL S J, DI GERMANIO C, MATTISON J A, EHRLICH M R, COLMAN R J, ANDERSON R M, DE CABO R. Untangling determinants of enhanced health and lifespan through a multi-omics approach in mice. Cell Metabolism, 2020, 32(1): 100-116. e4. doi: 10.1016/j.cmet.2020.04.018
[44]	LAYMAN D K. The role of leucine in weight loss diets and glucose homeostasis. The Journal of Nutrition, 2003, 133(1): 261S-267S.
[45]	谢小利, 王敏奇. 支链氨基酸在动物营养中的研究进展. 中国饲料, 2009(11): 11-14.
	XIE X L, WANG M Q. Research advance of branced-chain amino acids in animal nutrition. China Feed, 2009(11): 11-14. (in Chinese)
[46]	BURMESTER T, SCHELLER K. Common origin of arthropod tyrosinase, arthropod hemocyanin, insect hexamerin, and dipteran arylphorin receptor. Journal of Molecular Evolution, 1996, 42(6): 713-728. doi: 10.1007/BF02338804
[47]	ZHOU J J. Odorant-binding proteins in insects. Vitamins and Hormones 2010, 83: 241-272.
[48]	LEAL W S. Odorant reception in insects: Roles of receptors, binding proteins, and degrading enzymes. Annual Review of Entomology, 2013, 58: 373-391. doi: 10.1146/annurev-ento-120811-153635
[49]	DANI F R, IOVINELLA I, FELICIOLI A, NICCOLINI A, CALVELLO M A, CARUCCI M G, QIAO H, PIERACCINI G, TURILLAZZI S, MONETI G, PELOSI P. Mapping the expression of soluble olfactory proteins in the honeybee. Journal of Proteome Research, 2010, 9(4): 1822-1833. doi: 10.1021/pr900969k
[50]	IOVINELLA I, CAPPA F, CINI A, PETROCELLI I, CERVO R, TURILLAZZI S, DANI F R. Antennal protein profile in honeybees: Caste and task matter more than age. Frontiers in Physiology, 2018, 9: 748. doi: 10.3389/fphys.2018.00748
[51]	LI R, ZHANG L, FANG Y, HAN B, LU X, ZHOU T, FENG M, LI J K. Proteome and phosphoproteome analysis of honeybee (Apis mellifera) venom collected from electrical stimulation and manual extraction of the venom gland. BMC Genomics, 2013, 14: 766. doi: 10.1186/1471-2164-14-766
[52]	TRHLIN M, RAJCHARD J. Chemical communication in the honeybee (Apis mellifera L.): A review. Veterinarni Medicina, 2011, 56(6): 265-273. doi: 10.17221/1543-VETMED
[53]	KUCHARSKI R, MALESZKA R. Transcriptional profiling reveals multifunctional roles for transferrin in the honeybee, Apis mellifera. Journal of Insect Science, 2003, 3: 27.
[54]	ASGARI S, ZHANG G, ZAREIE R, SCHMIDT O. A serine proteinase homolog venom protein from an endoparasitoid wasp inhibits melanization of the host hemolymph. Insect Biochemistry and Molecular Biology, 2003, 33(10): 1017-1024. doi: 10.1016/S0965-1748(03)00116-4
[55]	ZHANG L, FANG Y, LI R, FENG M, HAN B, ZHOU T, LI J K. Towards posttranslational modification proteome of royal jelly. Journal of Proteomics, 2012, 75(17): 5327-5341. doi: 10.1016/j.jprot.2012.06.008

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参数 Parameter	项目Project	设置Set
群组特定参数 Group specific parameter	固定修饰Fixed modification	脲甲基化Carbamidomethylation (C)
	可变修饰Variable modification	乙酰化和氧化Acetylation (Protein N-term) and oxidation (M)
	每个肽段上所具有的最大个数 Maximum number of modifications per peptide	5
	最大漏切数 Maximal missed cleavages	2
全局参数 Global parameter	蛋白相对定量算法Protein relative quantitative algorithm	LFQ
	鉴定蛋白Identification protein	Unique peptide≥1
	最小比率计数Label minimum ratio count	1
	蛋白定量模式Protein quantitative model	Unique and razor peptides
	肽段和蛋白鉴定最大假阳性率 Maximum false peptide and protein discovery rates	0.01
	运行间的匹配Matching between runs	0.7 min
	时间窗口Alignment time window	20 min
	一级母离子First search peptide	20 ppm
	二级碎片离子MS/MS match tolerance	0.5 Da

Proteome Analysis of the Salivary Gland of Nurse Bee from High Royal Jelly Producing Bees and Italian Bees

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