A Large-Scale Proteome Analysis of Proteins Expressed in the Peel of Malus Domestica ‘Hong-Ro’

Jae Ho Kim; Soo Yong Shim; Eun-Sil Chang; Young-Geol Sohn; Yun-Hee Kim; Jin Gook Kim; Jeung Joo Lee

doi:10.7235/HORT.20200072

All Issue

2020 Vol.38, Issue 6 Preview Page Next Page

Research Article

A Large-Scale Proteome Analysis of Proteins Expressed in the Peel of Malus Domestica ‘Hong-Ro’ 사과 ‘홍로’ 과피에서 발현되는 대규모 단백질체 분석

31 December 2020. pp. 795-809

PDF XML

Abstract

The proteome expressed in the peel of the Korean apple cv. 'Hongro' was analyzed using two-dimensional electrophoresis, and it was confirmed that 502 proteins were expressed. As a result of analyzing these proteins with MALDI-TOF/TOF, 408 proteins were identified. The identified proteins were sorted by biological function: the most abundant (87) were in the carbohydrate metabolism category [abundance value (AV) total 120.97, 18.2% of total 665.09 in AV]; followed by protein metabolism, 59 (AV total 72.08, 10.8%); protein folding, 37 (AV total 34.12, 5.1%); defense and stress response, 35 (AV total 56.95, 8.6%); protein degradation, 33 (AV total 28.87, 4.3%); antioxidant enzyme, 29 (AV total 41.58, 6.3%); secondary metabolite metabolism, 16 (AV total 16.4, 2.5%); lipid metabolism, 16 (AV total 8.89, 1.3%); transport, 15 (AV total 8.75, 1.3%); cytoskeleton constitution, 14 (AV total, 12.89, 1.9%); allergen, 12 (AV total 104.55, 15.7%); nucleotide metabolism, 11 (AV total 10.83, 1.6%); and ATP synthesis, 10 (AV total 18.46, 2.8%). Among the expressed protein spots, the 1st AV was spot 451 major allergen Mal d 1 (AV 54.42), 2nd was spot 419 unidentified protein (AV 28.40), 3rd was spot 455 MLP-like protein (AV 24.08), 4th was spot 480 glutathione S-transferase (AV 18.61), 5th was spot 166 glutamine cytosolic isozyme (AV 13.26), 6th was spot 421 L-ascorbate peroxidase (AV 12.67), 7th was spot 163 β-cyanoalanine synthase (AV 10.81), 8th was spot 114 enolase-like (AV 10.48), 9th was spot 36 unidentified (AV 10.16), and 10th was spot 452 major allergen Mal d 1 ( AV 8.80). As described above, only a small number of allergen-related proteins were identified, but the total AV was found to be ranked second among all functional classifications, indicating that allergen-related proteins are expressed in large quantities in the peel. From the results of this experiment, it was possible to conceptualize the proteome expressed in the apple peel, and the results may be used as a coordinate for the study of the proteome related to the physiology and breeding fields of apples in the future.

Keywords

allergy protein

apple peel

carbohydrate metabolism

proteomics

two-dimensional electrophoresis

국내 육성 사과품종인 ‘홍로’의 과피에서 발현되는 단백질체를 이차원 전기영동으로 분석한 결과, 502개의 단백질들이 발현되는 것으로 확인되었으며, 이들 단백질들을 MALDI-TOF/TOF로 분석한 결과, 408개의 단백질들이 동정되었다. 동정된 단백질들을 생물학적 기능별로 정리한 결과, carbohydrate metabolism에 속하는 것들이 87개로 가장 많았으며[abundance value(AV) 합계 120.97, 전체 AV의 합계 665.09의 18.2%], 그 다음은 protein metabolism 59개(AV 합계 72.08, 10.8%), protein folding 37개(AV 합계 34.12, 5.1%), defense 및 stress response 35개(AV 합계 56.95, 8.6%), protein degradation 33개(AV 합계 28.87, 4.3%), antioxidant enzyme 29개(AV 합계 41.58, 6.3%), secondary metabolite metabolism 16개(AV 합계 16.4, 2.5%), lipid metabolism 16개(AV 합계 8.89, 1.3%), transport 15개(AV 합계 8.75, 1.3%), cytoskeleton constitution 14개(AV 합계 12.89, 1.9%), allergy 12개(AV 합계 104.55, 15.7%), nucleotide metabolism 11개(AV 합계 10.83, 1.6%) 및 ATP synthesis 10개(AV 합계 18.46, 2.8%) 등의 순이었다. 발현된 단백질 spot들 가운데 AV 1위는 spot 451번인 major allergen Mal d 1(AV 54.42), 2위는 spot 419번 unidentified protein(AV 28.40), 3위는 spot 455번 MLP-like protein(AV 24.08), 4위는 spot 480번 glutathione S-transferase(AV 18.61), 5위는 spot 166번 glutamine cytosolic isozyme(AV 13.26), 6위는 spot 421번 L-ascorbate peroxidase(AV 는 12.67), 7위는 spot 163번 β-cyanoalanine synthase(AV 10.81), 8위는 spot 114번 enolase-like(AV 10.48), 9위는 spot 36번 unidentified(AV 10.16), 10위는 spot 452번 major allergen Mal d 1(AV 8.80)이었다. 이상에서와 같이, 동정된 단백질들 중 알레르기와 관련된 것들은 소수에 불과하였으나 그 AV의 합계는 전체 기능별 분류 중 2위에 해당하는 것으로 보아, 과피에서는 알레르기 관련 단백질들이 대량으로 발현된다는 것을 알 수 있었다. 본 실험의 결과로부터 사과 과피에서 발현되는 단백질체의 대략적인 전체상을 파악할 수 있었으며, 그 결과는 추후 사과의 재배 및 육종과 관련된 단백질체 연구를 위한 좌표로 이용될 수 있을 것이다.

키워드

사과 과피

알레르기 단백질

이차원 전기영동

탄수화물 대사

프로테오믹스

References

Bartling D, Weiler EW (1992) Leucine aminopeptidase from arabidopsis thaliana molecular evidence for a phylogenetically conserved enzyme of protein turnover in higher plants. Eur J Biochem 205:425-431. doi:10.1111/j.1432-1033.1992.tb16796.x 10.1111/j.1432-1033.1992.tb16796.x1555602

Boyer J, Liu RH (2004) Apple phytochemicals and their health benefits. Nutr J 3:1-15. doi:10.1186/1475-2891-3-5 10.1186/1475-2891-3-515140261PMC442131

Bradford MM (1976) A rapid sensitive methods for the quantization of microgram quantities of protein utilizing the principles of protein-dye binding. Anal Biochem 72:248-255. doi:10.1016/0003-2697(76)90527-3 10.1016/0003-2697(76)90527-3

Brehler R, Theissen U, Mohr C, Luger T (1997) 'Latex-fruit syndrome': frequency of cross-reacting IgE antibodies. Allergy 52:404-10. doi:10.1111/j.1398-9995.1997.tb01019.x 10.1111/j.1398-9995.1997.tb01019.x9188921

Doherty GJ, McMahon HT (2008) Mediation, modulation, and consequences of membrane-cytoskeleton interactions. Annu Rev Biophys 37:65-95. doi:10.1146/annurev.biophys.37.032807.125912 10.1146/annurev.biophys.37.032807.12591218573073

Eastmond PJ (2007) MONODEHYROASCORBATE REDUCTASE4 is required for seed storage oil hydrolysis and postgerminative growth in Arabidopsis. Plant Cell 19:1376-1387. doi:10.1105/tpc.106.043992 10.1105/tpc.106.04399217449810PMC1913749

Eldakak M, Milad SIM, Nawar AI, Rohila JS (2013) Proteomics: a biotechnology tool for crop improvement. Front Plant Sci 4:1-12. doi:10.3389/fpls.2013.00035 10.3389/fpls.2013.0003523450788PMC3584254

Esteve C, D'Amato A, Marina ML, García MC, Righett PG (2013) In-depth proteomic analysis of banana (Musa spp.) fruit with combinatorial peptide ligand libraries. Electrophoresis 34:207-214. doi:10.1002/elps.201200389 10.1002/elps.20120038923161558

Fukamatsu Y, Yabe N, Hasunuma K (2003) Arabidopsis NDK1 is a component of ROS signaling by interacting with three catalases. Plant Cell Physiol 44:982-989. doi:10.1093/pcp/pcg140 10.1093/pcp/pcg14014581623

Gill SS, Anjum NA, Hasanuzzaman M, Gill R, Trivedi DK, Ahmad I, Pereira E, Tuteja N (2013) Glutathione and glutathione reductase: a boon in disguise for plant abiotic stress defense operations. Plant Physiol Biochem 70:204-12. doi:10.1016/j.plaphy.2013.05.032 10.1016/j.plaphy.2013.05.03223792825

Gowri G, Bugos RC, Campbell WH, Maxwell CA, Dixon RA (1991) Stress responses in alfalfa (Medicago sativa L) X Molecular cloning and expression of S-adenosyl-L-methionine: caffeic acid 3-O-methyltransferase, a key enzyme of lignin biosynthesis. Plant Physiol 97:7-14. doi:10.1104/pp.97.1.7 10.1104/pp.97.1.716668418PMC1080956

Guarino C, Arena S, De Simone L, D'Ambrosio C, Santoro S, Rocco M, Scaloni A, Marra M (2007) Proteomic analysis of the major soluble components in Annurca apple flesh. Mol Nutr Food Res 51:255-262. doi:10.1002/mnfr.200600133 10.1002/mnfr.20060013317266180

Han SE, Seo YS, Kim D, Sung SK, Kim WT (2007) concomitantly induced during ripening and implicates MdCASs in the possible role of the cyanide detoxification in Fuji apple (Malus domestica Borkh) fruits. Plant Cell Rep 26:1321-1331. doi:10.1007/s00299-007-0316-9 10.1007/s00299-007-0316-917333023

Hartl FU, Hayer-Hartl M (2009) Converging concepts of protein folding in vitro and in vivo. Nat Struc Mol Biol 16:574-581. doi:10.1038/nsmb.1591 10.1038/nsmb.159119491934

Herndl A, Marzban G, Hahn R, Boscia D, Hemmer W, Maghuly F, Stoyanova E, Katinger, Laimer M (2007) Mapping of Malus domestica allergens by 2-D electrophoresis and IgE-reacivity. Electrophoresis 28:437-438. doi:10.1002/elps.200600342 10.1002/elps.20060034217195260

Hoepflinger MC, Reitsamer J, Geretschlaeger AM, Mehlmer N, Tenhaken R (2013) The effect of translationally controlled tumour protein (TCTP) on programmed cell death in plants. BMC Plant Biol 13:135-135. doi:10.1186/1471-2229-13-135 10.1186/1471-2229-13-13524040826PMC3847524

Hourton-Cabassa C, Ambard-Bretteville F, Moreau F, Davy de Virville J, Remy R, Colas des Francs-Small C (1998) Stress induction of mitochondrial formate dehydrogenase in potato leaves. Plant Physiol 116:627-635. doi:10.1104/pp.116.2.627 10.1104/pp.116.2.6279490763PMC35120

Hurkman WJ, Tanaka CK (1986) Solubilization of plant membrane proteins for analysis by two-dimensional gel glectrophoresis. Plant Physiol 81:802-806. doi:10.1104/pp.81.3.802 10.1104/pp.81.3.80216664906PMC1075430

Ito H, Iwabuchi M, Ogawa K (2003) The sugar-metabolic enzymes aldolase and triose-phosphate isomerase are targets of glutathionylation in Arabidopsis thaliana: detection using biotinylated glutathione. Plant Cell Physiol 44:655-660. doi:10.1093/pcp/pcg098 10.1093/pcp/pcg09812881492

Izumi M, Tsunoda H, Suzuki Y, Makino A, Ishida H (2012) RBCS1A and RBCS3B, two major members within the Arabidopsis RBCS multigene family, function to yield sufficient Rubisco content for leaf photosynthetic capacity. J Exp Bot 63:2159-2170. doi:10.1093/jxb/err434 10.1093/jxb/err43422223809PMC3295403

Janick J, Cummins JV, Brown SK, Hemmat M (1996) Apples. In J Janick, JN Moore, eds, Fruit breeding, vol 1. Tree and tropical fruits. Wiley, New York, USA, pp 1-66

Jin H, Song Z, Nikolau BJ (2012) Reverse genetic characterization of two paralogous acetoacetyl CoA thiolase genes in Arabidopsis reveals their importance in plant growth and development. Plant J 70:1015-1032. doi:10.1111/j.1365-313X.2012.04942.x 10.1111/j.1365-313X.2012.04942.x22332816

Junge W, Nelson N (2015) ATP synthase. Annu Rev Biochem 84:631-57. doi:10.1146/annurev-biochem-060614-034124 10.1146/annurev-biochem-060614-03412425839341

Kajikawa M, Hirai N, Hashimoto T (2009) A PIP-family protein is required for biosynthesis of tobacco alkaloids. Plant Mol Biol 69:287-298. doi:10.1007/s11103-008-9424-3 10.1007/s11103-008-9424-319002761

Kato M, Nagasaki-Takeuchi N, Ide Y, Tomioka R, Maeshima M (2010) PCaPs, possible regulators of PtdInsP signals on plasma membrane. Plant Signal Behav 5:848-850. doi:10.4161/psb.5.7.11825 10.4161/psb.5.7.1182520448467PMC3014536

Kopylov M, Bass HW, Stroupe ME (2015) The maize (Zea mays L.) nucleoside diphosphate kinase1 (ZmNDPK1) gene encodes a human NM23-H2 homologue that binds and stabilizes G-quadruplex DNA. Biochemistry 54:1743-1757. doi:10.1021/bi501284g 10.1021/bi501284g25679041

Kwak KJ, Kim YO, Kang H (2005) Characterization of transgenic Arabidopsis plants overexpressing GR-RBP4 under high salinity, dehydration, or cold stress. J Exp Bot 56:3007-3016. doi:10.1093/jxb/eri298 10.1093/jxb/eri29816207746

Kwon K, Choi D, Hyun JK, Jung HS, Baek K, Park C (2013) Novel glyoxalases from Arabidopsis thaliana. FEBS J 280:3328-3339. doi:10.1111/febs.12321 10.1111/febs.1232123651081

Kwon YS, Lee DY, Rakwal R, Baek SB, Lee JH, Kwak YS, Seo JS, Chung WS, Bae DW, et al. (2016) Proteomic analyses of the interaction between the plant-growth promoting rhizobacterium Paenibacillus polymyxa E681 and Arabidopsis thaliana. Proteom 16:122-135. doi:10.1002/pmic.201500196 10.1002/pmic.20150019626460066

Lamkemeyer P, Laxa M, Collin V, Li W, Finkemeier I, Schoettler MA, Holtkamp V, Tognetti VB, Issakidis-Bourguet E, et al. (2006) Peroxiredoxin Q of Arabidopsis thaliana is attached to the thylakoids and functions in context of photosynthesis. Plant J 45:968-981. doi:10.1111/j.1365-313X.2006.02665.x 10.1111/j.1365-313X.2006.02665.x16507087

Latijnhouwers M, Xu XM, Moeller SG (2010) Arabidopsis stromal 70-kDa heat shock proteins are essential for chloroplast development. Planta 232:567-578. doi:10.1007/s00425-010-1192-z 10.1007/s00425-010-1192-z20506024

Lee JJ, Park KW, Kwak YS, Ahn JY, Jung YH, Lee BH, Jeng JC, Lee HS, Kwak SS (2012) Comparative proteomic study between tuberous roots of light orange- and purple-fleshed sweetpotato cultivars. Plant Sci 193-194:120-129. doi:10.1016/j.plantsci.2012.06.003 10.1016/j.plantsci.2012.06.00322794925

Lee TA, Bailey-Serres J (2019) Integrative analysis from the epigenome to translatome uncovers patterns of dominant nuclear regulation during transient stress. Plant Cell 31:2573-2595. doi:10.1105/tpc.19.00463 10.1105/tpc.19.0046331519798PMC6881120

Li R, Qiu Z, Wang X, Gong P, Xu Q, Yu QB, Guan Y (2019) Pooled CRISPR/Cas9 reveals redundant roles of plastidial phosphoglycerate kinases in carbon fixation and metabolism. Plant J 98:1078-1089. doi:10.1111/tpj.14303 10.1111/tpj.1430330834637

Marondedze C, Thomas LA (2012) Apple hypanthium firmness: New insights from comparative proteomics. Appl Biochem Biotechnol 168:306-326. doi:10.1007/s12010-012-9774-9 10.1007/s12010-012-9774-922733236

Maruta T, Ichikawa Y, Mieda T, Takeda T, Tamoi M, Yabuta Y, Ishikawa T, Shigeoka S (2010) The contribution of Arabidopsis homologs of L-gulono-1,4-lactone oxidase to the biosynthesis of ascorbic acid. Biosci Biotechnol Biochem 74:1494-1497. doi:10.1271/bbb.100157 10.1271/bbb.10015720622436

Maruta T, Noshi M, Tanouchi A, Tamoi M, Yabuta Y, Yoshimura K, Ishikawa T, Shigeoka S (2012) H₂O₂-triggered retrograde signaling from chloroplasts to nucleus plays specific role in response to stress. J Biol Chem 287:11717-11729. doi:10.1074/jbc.M111.292847 10.1074/jbc.M111.29284722334687PMC3320920

Marzban G, Puehringer H, Dey R, Brynda S, Ma Y, Martinelli A, Zaccarini M, van der Weg E, Housley Z, et al. (2005) Localisation and distribution of the major allergens in apple fruits. Plant Sci 169:387-394 10.1016/j.plantsci.2005.03.027

Matsui NM, Smith-Beckerman DM, Epstein LB (1999) Staining of preparative 2-D gels. In AJ Link, ed, 2-D Proteome Analysis Protocols. Humana Press, Totowa, NJ, USA, pp 301-311. doi:10.1016/j.plantsci.2005.03.027 10.1016/j.plantsci.2005.03.027

Meng M, Geisler M, Johansson H, Harholt J, Scheller HV, Mellerowicz EJ, Kleczkowski LA (2009) UDP-glucose pyrophosphorylase is not rate limiting, but is essential in Arabidopsis. Plant Cell Physiol 50:998-1011. doi:10.1093/pcp/pcp052 10.1093/pcp/pcp05219366709

Nagase T, Seki N, Tanaka A, Ishikawa K, Nomura N (1996) Prediction of the coding sequences of unidentified human genes IV the coding sequences of 40 new genes (KIAA0121-KIAA0160) deduced by analysis of cDNA clones from human cell line KG-1. DNA Res 2:167-174. doi:10.1093/dnares/2.4.167 10.1093/dnares/2.4.1678590280

Ngoc LD, Brillard M, Hoebeke J (1993) The alpha- and beta-subunits of the jacalins are cleavage products from a 17-kDa precursor. Biochim Biophys Acta 1156:219-222. doi:10.1016/0304-4165(93)90139-Y 10.1016/0304-4165(93)90139-Y

Nikolovski N, Rubtsov D, Segura MP, Miles GP, Stevens TJ, Dunkley TP, Munro S, Lilley KS, Dupree P (2012) Putative glycosyltransferases and other plant Golgi apparatus proteins are revealed by LOPIT proteomics. Plant Physiol 160:1037-1051. doi:10.1104/pp.112.204263 10.1104/pp.112.20426322923678PMC3461528

Paiva NL, Edwards R, Sun Y, Hrazdina G, Dixon RA (1991) Stress responses in alfalfa (Medicago sativa L.) 11 Molecular cloning and expression of alfalfa isoflavone reductase, a key enzyme of isoflavonoid phytoalexin biosynthesis. Plant Mol Biol 17:653-667. doi:10.1007/BF00037051 10.1007/BF000370511912490

Patron NJ, Rogers MB, Keeling PJ (2004) Gene replacement of fructose-1,6-bisphosphate aldolase supports the hypothesis of a single photosynthetic ancestor of chromalveolates. Eukaryot Cell 3:1169-75. doi:10.1128/EC.3.5.1169-1175.2004 10.1128/EC.3.5.1169-1175.200415470245PMC522617

Peng Y, Lu R (2007) Prediction of apple fruit firmness and soluble solids content using characteristics of multispectral scattering images. J Food Eng 82:142-152. doi:10.1016/j.jfoodeng.2006.12.027 10.1016/j.jfoodeng.2006.12.027

Prabhakar V, Lottgert T, Gigolashvili T, Bell K, Flugge UI, Hausler RE (2009) Molecular and functional characterization of the plastid-localized Phosphoenolpyruvate enolase (ENO1) from Arabidopsis thaliana. FEBS Lett 583:983-991. doi:10.1016/j.febslet.2009.02.017 10.1016/j.febslet.2009.02.01719223001

Qin G, Wang Q, Liu J, Li B, Tian S (2009) Proteomic analysis of changes in mitochondrial protein expression during fruit senescence. Proteomics 9:4241-53. doi:10.1002/pmic.200900133 10.1002/pmic.20090013319688753

Sancho AI, Foxall R, Rigby NM, Browne T, Zuidmeer L, van Ree R, Waldron KW, Mills EN (2006a) Maturity and storage influence on the apple (Malus domestica) allergen Mal d 3, a nonspecific lipid transfer protein. J Agric Food Chem 54, 5098-5104. doi:10.1021/jf0530446 10.1021/jf053044616819922

Sancho AI, Foxall R, Browne T, Dey R, Zuidmeer L, Marzban G, Waldron, K.W, van Ree R, et al. (2006b) Effect of postharvest storage on the expression of the apple allergen Mal d 1. J Agric Food Chem 54:5917-5923. doi:10.1021/jf060880m 10.1021/jf060880m16881695

Schiefner A, Sinz Q, Neumaier I, Schwab W, Skerra A (2013) Structural basis for the enzymatic formation of the key strawberry flavor compound 4-hydroxy-2,5-dimethyl-3(2H)-furanone. J Biol Chem 288:16815-16826. doi:10.1074/jbc.M113.453852 10.1074/jbc.M113.45385223589283PMC3675614

Scranton MA, Yee A, Park SY, Walling LL (2012) Plant leucine aminopeptidases moonlight as molecular chaperones to alleviate stress-induced damage. J Biol Chem 287:18408-18417. doi:10.1074/jbc.M111.309500 10.1074/jbc.M111.30950022493451PMC3365729

Selinski J, Koenig N, Wellmeyer B, Hanke GT, Linke V, Neuhaus HE, Scheibe R (2014) The plastid-localized NAD-dependent malate dehydrogenase is crucial for energy homeostasis in developing Arabidopsis thaliana seeds. Mol Plant 7:170-186. doi:10.1093/mp/sst151 10.1093/mp/sst15124198233

Shin MH, Munner S, Kim YH, Lee JJ, Bae DW, Kwack YB, Kumarihami HMPC, Kim JG (2020) Proteomic analysis reveals dynamic regulation of fruit ripening in response to exogenous ethylene in kiwifruit cultivars. Hortic Environ Biotechnol 61:93-114. doi:10.1007/s13580-019-00209-6 10.1007/s13580-019-00209-6

Sukrong S, Yun KY, Stadler P, Kumar C, Facciuolo T, Moffatt BA, Falcone DL (2012) Improved growth and stress tolerance in the Arabidopsis oxt1 mutant triggered by altered adenine metabolism. Mol Plant 5:1310-1332. doi:10.1093/mp/sss065 10.1093/mp/sss06522859732

Suzuki K, Nakanishi H, Bower J, Yoder DW, Osteryoung KW, Miyagishima SY (2009) Plastidchaperoninproteins Cpn60 alpha and Cpn60 beta are required for plastid division in Arabidopsis thaliana. BMC Plant Biol 9:38-38. doi:10.1186/1471-2229-9-38 10.1186/1471-2229-9-3819344532PMC2670834

Tabuchi M, Sugiyama K, Ishiyama K, Inoue E, Sato T, Takahashi H, Yamaya T (2005) Severe reduction in growth rate and grain filling of rice mutants lacking OsGS1;1, a cytosolic glutamine synthetase1;1. Plant J 42:641-651. doi:10.1111/j.1365-313X.2005.02406.x 10.1111/j.1365-313X.2005.02406.x15918879

Teixeira PF, Glaser E (2013) Processing peptidases in mitochondria and chloroplasts. Biochim Biophys Acta 1833:360-70. doi:10.1016/j.bbamcr.2012.03.012 10.1016/j.bbamcr.2012.03.01222495024

Thornalley PJ, Langborg A, Minhas HS (1999) Formation of glyoxal, methylglyoxal and 3-deoxyglucosone in the glycation of proteins by glucose. Biochem J 344:109-116. doi:10.1042/bj3440109 10.1042/bj3440109PMC1220620

van't Veer P, Jansen MC, Klerk M, Kok FJ (2000) Fruits and vegetables in the prevention of cancer and cardiovascular disease. Public Health Nutr 3:103-107. doi:10.1017/S1368980000000136 10.1017/S136898000000013610786730

Walker JE, Runswick MJ, Neuhaus D, Montgomery MG, Carbajo RJ, Kellas FA (2005) Structure of the F1-binding domain of the stator of bovine F1Fo-ATPase and how it binds an alpha-subunit. J Mol Biol 351:824-838. doi:10.1016/j.jmb.2005.06.012 10.1016/j.jmb.2005.06.01216045926

Wheeler MC, Tronconi MA, Drincovich MF, Andreo CS, Fluegge UI, Maurino VG (2005) A comprehensive analysis of the NADP-malic enzyme gene family of Arabidopsis. Plant Physiol 139:39-51. doi:10.1104/pp.105.065953 10.1104/pp.105.06595316113210PMC1203356

Yahalom A, Kim TH, Roy B, Singer R, von Arnim AG, Chamovitz DA (2008) Arabidopsis eIF3e is regulated by the COP9 signalosome and has an impact on development and protein translation. Plant J 53:300-311. doi:10.1111/j.1365-313X.2007.03347.x 10.1111/j.1365-313X.2007.03347.x18067529

Yamauchi Y, Hasegawa A, Taninaka A, Mizutani M, Sugimoto Y (2011) NADPH-dependent reductases involved in the detoxification of reactive carbonyls in plants. J Biol Chem 286:6999-7009. doi:10.1074/jbc.M110.202226 10.1074/jbc.M110.20222621169366PMC3044956

Yang H, Zhang T, Masuda T, Lv C, Sun L, Qu G, Zhao G (2011) Chitinase III in pomegranate seeds (Punica granatum Linn): a high-capacity calcium-binding protein in amyloplasts. Plant J 68:765-776. doi:10.1111/j.1365-313X.2011.04727.x 10.1111/j.1365-313X.2011.04727.x21790816

Zhao Z, Assmann SM (2011) The glycolytic enzyme, phosphoglycerate mutase, has critical roles in stomatal movement, vegetative growth, and pollen production in Arabidopsis thaliana. J Exp Bot 62:5179-5189 93:276-94. doi:10.1093/jxb/err223 10.1093/jxb/err22321813794PMC3193020

Zheng Q, Song J, Campbell-Palmer L, Thompson K, Li L, Walker B, Cui Y, Li X (2013) A proteomic investigation of apple fruit during ripening and in response to ethylene treatment. J Proteom 93:276-294. doi:10.1016/j.jprot.2013.02.006 10.1016/j.jprot.2013.02.00623435059

Zhi T, Zhou Z, Huang Y, Han C, Liu Y, Zhu Q, Ren C (2016) Sugar suppresses cell death caused by disruption of fumarylacetoacetate hydrolase in Arabidopsis. Planta 244:557-571. doi:10.1007/s00425-016-2530-6 10.1007/s00425-016-2530-627097641

Information

Publisher :KOREAN SOCIETY FOR HORTICULTURAL SCIENCE
Publisher(Ko) :원예과학기술지
Journal Title :Horticultural Science and Technology
Journal Title(Ko) :원예과학기술지
Volume : 38
No :6
Pages :795-809
Received Date : 2020-05-27
Revised Date : 2020-07-03
Accepted Date : 2020-08-21
DOI :https://doi.org/10.7235/HORT.20200072

Horticultural Science and Technology ISSN:1226-8763(Print) 2465-8588(Online) 원예과학기술지

All Issue