Characterization of leucine aminopeptidase (LAP) activity in sweet pepper fruits during ripening and its inhibition by nitration and reducing events.
Aminopeptidase
Cyanide
Fruit ripening
Glutathione
Intron/exon
Nitration
Nitric oxide
Pepper
Journal
Plant cell reports
ISSN: 1432-203X
Titre abrégé: Plant Cell Rep
Pays: Germany
ID NLM: 9880970
Informations de publication
Date de publication:
11 Mar 2024
11 Mar 2024
Historique:
received:
22
11
2023
accepted:
22
02
2024
medline:
11
3
2024
pubmed:
11
3
2024
entrez:
11
3
2024
Statut:
epublish
Résumé
Pepper fruits contain two leucine aminopeptidase (LAP) genes which are differentially modulated during ripening and by nitric oxide. The LAP activity increases during ripening but is negatively modulated by nitration. Leucine aminopeptidase (LAP) is an essential metalloenzyme that cleaves N-terminal leucine residues from proteins but also metabolizes dipeptides and tripeptides. LAPs play a fundamental role in cell protein turnover and participate in physiological processes such as defense mechanisms against biotic and abiotic stresses, but little is known about their involvement in fruit physiology. This study aims to identify and characterize genes encoding LAP and evaluate their role during the ripening of pepper (Capsicum annuum L.) fruits and under a nitric oxide (NO)-enriched environment. Using a data-mining approach of the pepper plant genome and fruit transcriptome (RNA-seq), two LAP genes, designated CaLAP1 and CaLAP2, were identified. The time course expression analysis of these genes during different fruit ripening stages showed that whereas CaLAP1 decreased, CaLAP2 was upregulated. However, under an exogenous NO treatment of fruits, both genes were downregulated. On the contrary, it was shown that during fruit ripening LAP activity increased by 81%. An in vitro assay of the LAP activity in the presence of different modulating compounds including peroxynitrite (ONOO
Identifiants
pubmed: 38466441
doi: 10.1007/s00299-024-03179-x
pii: 10.1007/s00299-024-03179-x
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
92Subventions
Organisme : Ministerio de Ciencia, Innovación y Universidades
ID : PID2019-103924GB-I00
Informations de copyright
© 2024. The Author(s).
Références
Antonio AS, Wiedemann LSM, Veiga Junior VF (2018) The genus Capsicum: a phytochemical review of bioactive secondary metabolites. RSC Adv 8(45):25767–25784
pubmed: 35539808
pmcid: 9082723
doi: 10.1039/C8RA02067A
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(1):425–431
pubmed: 1555602
doi: 10.1111/j.1432-1033.1992.tb16796.x
Cappiello M, Lazzarotti A, Buono F, Scaloni A, D’ambrosio C, Amodeo P, Méndez BL, Pelosi P, Del Corso A, Mura U (2004) New role for leucyl aminopeptidase in glutathione turnover. Biochem J 378:35–44
pubmed: 14583094
pmcid: 1223929
doi: 10.1042/bj20031336
Casano LM, Desimone M, Trippi VS (1989) Proteolytic activity at alkaline pH in oat leaves, isolation of an aminopeptidase. Plant Physiol 91(4):1414–1418
pubmed: 16667194
pmcid: 1062199
doi: 10.1104/pp.91.4.1414
Chaki M, Álvarez de Morales P, Ruiz C, Begara-Morales JC, Barroso JB, Corpas FJ, Palma JM (2015) Ripening of pepper (Capsicum annuum) fruit is characterized by an enhancement of protein tyrosine nitration. Ann Bot 116(4):637–647
pubmed: 25814060
pmcid: 4577987
doi: 10.1093/aob/mcv016
Chang N, Sun Q, Hu J, An C, Gao AH (2017) Large introns of 5 to 10 kilo base pairs can be spliced out in Arabidopsis. Genes 8:200
pubmed: 28800125
pmcid: 5575664
doi: 10.3390/genes8080200
Chao WS, Gu YQ, Pautot VV, Bray EA, Walling LL (1999) Leucine aminopeptidase RNAs, proteins, and activities increase in response to water deficit, salinity, and the wound signals systemin, methyl jasmonate, and abscisic acid. Plant Physiol 120(4):979–992
pubmed: 10444081
pmcid: 59357
doi: 10.1104/pp.120.4.979
Chao WS, Pautot V, Holzer FM, Walling LL (2000) Leucine aminopeptidases: the ubiquity of LAP-N and the specificity of LAP-A. Planta 210(4):563–573
pubmed: 10787049
doi: 10.1007/s004250050045
Chao J, Li Z, Sun Y, Aluko OO, Wu X, Wang Q, Liu G (2021) MG2C: a user-friendly online tool for drawing genetic maps. Mol Hortic 1(1):16
pubmed: 37789491
pmcid: 10514940
doi: 10.1186/s43897-021-00020-x
Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202
pubmed: 32585190
doi: 10.1016/j.molp.2020.06.009
Chiaiese P, Corrado G, Minutolo M, Barone A, Errico A (2019) Transcriptional regulation of ascorbic acid during fruit ripening in pepper (Capsicum annuum) varieties with low and high antioxidants content. Plants (basel) 8(7):206
pubmed: 31277433
doi: 10.3390/plants8070206
Chu L, Lai Y, Xu X, Eddy S, Yang S, Song L, Kolodrubetz D (2008) A 52-kDa leucyl aminopeptidase from Treponema denticola is a cysteinylglycinase that mediates the second step of glutathione metabolism. J Biol Chem 283:19351–19358
pubmed: 18482986
pmcid: 2443665
doi: 10.1074/jbc.M801034200
Corpas FJ, Palma JM, del Río LA (1993) Evidence for the presence of proteolytic activity in peroxisomes. Eur J Cell Biol 61(1):81–85
pubmed: 8223710
Corpas FJ, Barroso JB, Carreras A, Quirós M, León AM, Romero-Puertas MC, Esteban FJ, Valderrama R, Palma JM, Sandalio LM, Gómez M, del Río LA (2004) Cellular and subcellular localization of endogenous nitric oxide in young and senescent pea plants. Plant Physiol 136(1):2722–2733
pubmed: 15347796
pmcid: 523336
doi: 10.1104/pp.104.042812
Corpas FJ, Freschi L, Rodríguez-Ruiz M, Mioto PT, González-Gordo S, Palma JM (2018) Nitro-oxidative metabolism during fruit ripening. J Exp Bot 69(14):3449–3463
pubmed: 29304200
doi: 10.1093/jxb/erx453
Corpas FJ, González-Gordo S, Palma JM (2022a) NO source in higher plants: present and future of an unresolved question. Trends Plant Sci 27(2):116–119
pubmed: 34893427
doi: 10.1016/j.tplants.2021.11.016
Corpas FJ, González-Gordo S, Rodríguez-Ruiz M, Muñoz-Vargas MA, Palma JM (2022b) Thiol-based oxidative posttranslational modifications (oxiPTMs) of plant proteins. Plant Cell Physiol 63(7):889–900
pubmed: 35323963
pmcid: 9282725
doi: 10.1093/pcp/pcac036
Del Corso A, Vilardo PG, Cappiello M, Cecconi I, Dal Monte M, Barsacchi D, Mura U (2002) Physiological thiols as promoters of glutathione oxidation and modifying agents in protein S-thiolation. Arch Biochem Biophys 397:392–398
pubmed: 11795899
doi: 10.1006/abbi.2001.2678
Del Giúdice LZ, Falquetto-Gomes P, de Almeida Costa PM, Martins AO, Omena-Garcia RP, Araújo WL, Zsögön A, Picoli EAT, Nunes-Nesi A (2023) Dynamic shifts in primary metabolism across fruit development stages in Capsicum chinense (cv. Habanero). J Plant Physiol 291:154121
pubmed: 37924627
doi: 10.1016/j.jplph.2023.154121
Drinkwater N, Malcolm TR, McGowan S (2019) M17 aminopeptidases diversify function by moderating their macromolecular assemblies and active site environment. Biochimie 166:38–51
pubmed: 30654132
doi: 10.1016/j.biochi.2019.01.007
Dubey M, Jaiswal V, Rawoof A, Kumar A, Nitin M, Chhapekar SS, Kumar N, Ahmad I, Islam K, Brahma V, Ramchiary N (2019) Identification of genes involved in fruit development/ripening in Capsicum and development of functional markers. Genomics 111(6):1913–1922
pubmed: 30615924
doi: 10.1016/j.ygeno.2019.01.002
Duprez K, Scranton MA, Walling LL, Fan L (2014) Structure of tomato wound-induced leucine aminopeptidase sheds light on substrate specificity. Acta Crystallogr D Biol Crystallogr 70:1649–1658
pubmed: 24914976
doi: 10.1107/S1399004714006245
Duprez KT, Scranton MA, Walling LL, Fan L (2016) Structural insights into chaperone-activity enhancement by a K354E mutation in tomato acidic leucine aminopeptidase. Acta Cryst D72:694–702
Dyachenko EA, Filyushin MA, Efremov GI, Dzhos EA, Shchennikova AV, Kochieva EZ (2020) Structural and functional features of phytoene synthase isoforms PSY1 and PSY2 in pepper Capsicum annuum L. cultivars. Vavilovskii Zhurnal Genet Selektsii 24(7):687–696
pubmed: 33738386
pmcid: 7960444
Elleman TC (1974) Aminopeptides of pea. Biochem J 141(1):113–118
pubmed: 4455194
pmcid: 1168055
doi: 10.1042/bj1410113
Esposito S, Aiese Cigliano R, Cardi T, Tripodi P (2022) Whole-genome resequencing reveals genomic footprints of Italian sweet and hot pepper heirlooms giving insight into genes underlying key agronomic and qualitative traits. BMC Genom Data 23(1):21
pubmed: 35337259
pmcid: 8957157
doi: 10.1186/s12863-022-01039-9
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
pubmed: 28561359
doi: 10.2307/2408678
Florencio-Ortiz V, Sellés-Marchart S, Casas JL (2021) Proteome changes in pepper (Capsicum annuum L.) leaves induced by the green peach aphid (Myzus persicae Sulzer). BMC Plant Biol 21(1):12
pubmed: 33407137
pmcid: 7788789
doi: 10.1186/s12870-020-02749-x
Fowler JH, Narváez-Vásquez J, Aromdee DN, Pautot V, Holzer FM, Walling LL (2009) Leucine aminopeptidase regulates defense and wound signaling in tomato downstream of jasmonic acid. Plant Cell 21(4):1239–1251
pubmed: 19376935
pmcid: 2685619
doi: 10.1105/tpc.108.065029
García I, Arenas-Alfonseca L, Moreno I, Gotor C, Romero LC (2019) HCN regulates cellular processes through posttranslational modification of proteins by S-cyanylation. Plant Physiol 179(1):107–123
pubmed: 30377236
doi: 10.1104/pp.18.01083
Gayte IG, Moreno RB, Zonjic PS, Claros MG (2017) DEgenes Hunter—a flexible R pipeline for automated RNA-seq studies in organisms without reference genome. Genomics Computat Biol 3:31
doi: 10.18547/gcb.2017.vol3.iss3.e31
Ghifari AS, Teixeira PF, Kmiec B, Pružinská A, Glaser E, Murcha MW (2020) A mitochondrial prolyl aminopeptidase PAP2 releases N-terminal proline and regulates proline homeostasis during stress response. Plant J 104(5):1182–1194
pubmed: 32920905
doi: 10.1111/tpj.14987
Ghifari AS, Teixeira PF, Kmiec B, Singh N, Glaser E, Murcha MW (2022) The dual-targeted prolyl aminopeptidase PAP1 is involved in proline accumulation in response to stress and during pollen development. J Exp Bot 73(1):78–93
pubmed: 34460901
doi: 10.1093/jxb/erab397
González-Gordo S, Bautista R, Claros MG, Cañas A, Palma JM, Corpas FJ (2019) Nitric oxide-dependent regulation of sweet pepper fruit ripening. J Exp Bot 70:4557–4570
pubmed: 31046097
pmcid: 6736391
doi: 10.1093/jxb/erz136
González-Gordo S, Rodríguez-Ruiz M, López-Jaramillo J, Muñoz-Vargas MA, Palma JM, Corpas FJ (2022) Nitric oxide (NO) differentially modulates the ascorbate peroxidase (APX) isozymes of sweet pepper (Capsicum annuum L.) fruits. Antioxidants (basel) 11(4):765
pubmed: 35453450
doi: 10.3390/antiox11040765
González-Gordo S, Muñoz-Vargas MA, Palma JM, Corpas FJ (2023) Class III peroxidases (POD) in pepper (Capsicum annuum L.): genome-wide identification and regulation during nitric oxide (NO)-influenced fruit ripening. Antioxidants (basel) 12(5):1013
pubmed: 37237879
doi: 10.3390/antiox12051013
Gu YQ, Walling LL (2000) Specificity of the wound-induced leucine aminopeptidase LAP-A) of tomato: activity on dipeptide and tripeptide substrates. Eur J Biochem 267:1178–1187
pubmed: 10672029
doi: 10.1046/j.1432-1327.2000.01116.x
Gu Y-Q, Chao WS, Walling LL (1996) Localization and post-translational processing of the wound-induced leucine aminopeptidase proteins of tomato. J Biol Chem 271(42):25880–25887
pubmed: 8824220
doi: 10.1074/jbc.271.42.25880
Guijarro-Real C, Adalid-Martínez AM, Pires CK, Ribes-Moya AM, Fita A, Rodríguez-Burruezo A (2023) The effect of the varietal type, ripening stage, and growing conditions on the content and profile of sugars and capsaicinoids in Capsicum peppers. Plants (basel) 12(2):231
pubmed: 36678946
doi: 10.3390/plants12020231
Gupta VK, Pawar VS (1974) Leucine aminopeptidase activity in tall and dwarf cultivars of rice at successive stages of development. Ann Bot 38(1):205–208
doi: 10.1093/oxfordjournals.aob.a084794
Herbers K, Prat S, Willmitzer L (1994) Functional analysis of a leucine aminopeptidase from Solanum tuberosum L. Planta 194(2):230–240
pubmed: 7765119
doi: 10.1007/BF01101682
Horton P, Park K-J, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585–W587
pubmed: 17517783
pmcid: 1933216
doi: 10.1093/nar/gkm259
Hulse-Kemp AM, Maheshwari S, Stoffel K, Hill TA, Jaffe D, Williams SR, Weisenfeld N, Ramakrishnan S, Kumar V, Shah P, Schatz MC, Church DM, Van Deynze A (2018) Reference quality assembly of the 3.5-Gb genome of Capsicum annuum from a single linked-read library. Hortic Res 5:4
Islam K, Rawoof A, Kumar A, Momo J, Ahmed I, Dubey M, Ramchiary N (2023) Genetic regulation, environmental cues, and extraction methods for higher yield of secondary metabolites in Capsicum. J Agric Food Chem 71(24):9213–9242
pubmed: 37289974
doi: 10.1021/acs.jafc.3c01901
Ito T, Ohkama-Ohtsu N (2023) Degradation of glutathione and glutathione conjugates in plants. J Exp Bot 74(11):3313–3327
pubmed: 36651789
doi: 10.1093/jxb/erad018
Jang S, Kim GW, Han K, Kim YM, Jo J, Lee SY, Kwon JK, Kang BC (2022) Investigation of genetic factors regulating chlorophyll and carotenoid biosynthesis in red pepper fruit. Front Plant Sci 13:922963
pubmed: 36186014
pmcid: 9521427
doi: 10.3389/fpls.2022.922963
Jaouani K, Karmous I, Ostrowski M, Ferjani EE, Jakubowska A, Chaoui A (2018) Cadmium effects on embryo growth of pea seeds during germination: investigation of the mechanisms of interference of the heavy metal with protein mobilization-related factors. J Plant Physiol 226:64–76
pubmed: 29704645
doi: 10.1016/j.jplph.2018.02.009
Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282
pubmed: 1633570
Jumper J, Evans R, Pritzel A, Green T, Figurnov M, Ronneberger O, Tunyasuvunakool K, Bates R, Žídek A, Potapenko A, Bridgland A, Meyer C, Kohl SA, Ballard AJ, Cowie A, Romera-Paredes B, Nikolov S, Jain R, Adler J et al (2021) Highly accurate protein structure prediction with AlphaFold. Nature 596(7873):583–589
pubmed: 34265844
pmcid: 8371605
doi: 10.1038/s41586-021-03819-2
Kang H-C, Hahn T-R, Chung I-S, Park J-C (1999) Characterization of an aminopeptidase from grapes. Int J Plant Sci 160(2):299–306
doi: 10.1086/314132
Kania J, Krawczyk T, Gillner DM (2021) Oilseed rape (Brassica napus): the importance of aminopeptidases in germination under normal and heavy metals stress conditions. J Sci Food Agric 101(15):6533–6541
pubmed: 34010498
doi: 10.1002/jsfa.11325
Kirmizi S, Güleryüz G (2006) Protein mobilization and proteolytic enzyme activities during seed germination of broad bean (Vicia faba L.). Z Naturforsch C J Biosci 61(3–4):222–226
pubmed: 16729580
doi: 10.1515/znc-2006-3-411
Kmiec B, Branca RMM, Berkowitz O, Li L, Wang Y, Murcha MW, Whelan J, Lehtiö J, Glaser E, Teixeira PF (2018) Accumulation of endogenous peptides triggers a pathogen stress response in Arabidopsis thaliana. Plant J 96(4):705–715
pubmed: 30242930
doi: 10.1111/tpj.14100
Kolbert Z, Barroso JB, Brouquisse R, Corpas FJ, Gupta KJ, Lindermayr C, Loake GJ, Palma JM, Petřivalský M, Wendehenne D, Hancock JT (2019) A forty year journey: the generation and roles of NO in plants. Nitric Oxide 93:53–70
pubmed: 31541734
doi: 10.1016/j.niox.2019.09.006
Kolehmainen L, Mikola J (1971) Partial purification and enzymatic properties of an aminopeptidase from barley. Arch Biochem Biophys 145(2):633–642
pubmed: 5001478
doi: 10.1016/S0003-9861(71)80023-1
Kovács Z, Bedő J, Pápai B, Tóth-Lencsés AK, Csilléry G, Szőke A, Bányai-Stefanovits É, Kiss E, Veres A (2022) Ripening-induced changes in the nutraceutical compounds of differently coloured pepper (Capsicum annuum L.) breeding lines. Antioxidants (basel) 11(4):637
pubmed: 35453324
doi: 10.3390/antiox11040637
Kumar S, Kaur A, Chattopadhyay B, Bachhawat AK (2015) Defining the cytosolic pathway of glutathione degradation in Arabidopsis thaliana: role of the ChaC/GCG family of γ-glutamyl cyclotransferases as glutathione-degrading enzymes and AtLAP1 as the Cys-Gly peptidase. Biochem J 468(1):73–85
pubmed: 25716890
doi: 10.1042/BJ20141154
Lahbib K, Bnejdi F, Pandino G, Lombardo S, El-Gazzah M, El-Bok S, Dabbou S (2023) Changes in yield-related traits, phytochemical composition, and antioxidant activity of pepper (Capsicum annuum) depending on its variety, fruit position, and ripening stage. Foods 12(21):3948
pubmed: 37959067
pmcid: 10648119
doi: 10.3390/foods12213948
Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE.; a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327
pubmed: 11752327
pmcid: 99092
doi: 10.1093/nar/30.1.325
Leterrier M, Airaki M, Palma JM, Chaki M, Barroso JB, Corpas FJ (2012) Arsenic triggers the nitric oxide (NO) and S-nitrosoglutathione (GSNO) metabolism in Arabidopsis. Environ Pollut 166:136–143
pubmed: 22504427
doi: 10.1016/j.envpol.2012.03.012
Letunic I, Bork P (2006) Interactive tree of life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23(1):127–128
pubmed: 17050570
doi: 10.1093/bioinformatics/btl529
Ling Q, Sadali NM, Soufi Z, Zhou Y, Huang B, Zeng Y, Rodriguez-Concepcion M, Jarvis RP (2021) The chloroplast-associated protein degradation pathway controls chromoplast development and fruit ripening in tomato. Nat Plants 7(5):655–666
pubmed: 34007040
doi: 10.1038/s41477-021-00916-y
Liu Z, Cao J, Ma Q, Gao X, Ren J, Xue Y (2011) GPS-YNO2: computational prediction of tyrosine nitration sites in proteins. Mol Biosyst 7(4):1197–1204
pubmed: 21258675
doi: 10.1039/c0mb00279h
Liu Y, Zhou J, Yi C, Chen F, Liu Y, Liao Y, Zhang Z, Liu W, Lv J (2023) Integrative analysis of non-targeted metabolome and transcriptome reveals the mechanism of volatile formation in pepper fruit. Front Genet 10(14):1290492
doi: 10.3389/fgene.2023.1290492
Lopez-Ortiz C, Peña-Garcia Y, Bhandari M, Abburi VL, Natarajan P, Stommel J, Nimmakayala P, Reddy UK (2021) Identification of miRNAs and their targets involved in flower and fruit development across domesticated and wild capsicum species. Int J Mol Sci 22(9):4866
pubmed: 34064462
pmcid: 8125703
doi: 10.3390/ijms22094866
Mahagamasekera MGP, Leung DWM (2001) Development of leucine aminopeptidase activity during daylily flower growth and senescence. Acta Physiol Plant 23(2):181–186
doi: 10.1007/s11738-001-0006-0
Matsui M, Fowler JH, Walling LL (2006) Leucine aminopeptidases: diversity in structure and function. Biol Chem 387(12):1535–1544
pubmed: 17132098
doi: 10.1515/BC.2006.191
Mohn MA, Thaqi B, Fischer-Schrader K (2019) Isoform-specific NO synthesis by Arabidopsis thaliana nitrate reductase. Plants (basel) 8(3):67
pubmed: 30884848
doi: 10.3390/plants8030067
Momo J, Kumar A, Islam K, Ahmad I, Rawoof A, Ramchiary N (2022) A comprehensive update on Capsicum proteomics: advances and future prospects. J Proteomics 261:104578
pubmed: 35398364
doi: 10.1016/j.jprot.2022.104578
Muñoz-Vargas MA, González-Gordo S, Cañas A, López-Jaramillo J, Palma JM, Corpas FJ (2018) Endogenous hydrogen sulfide (H
pubmed: 30326260
doi: 10.1016/j.niox.2018.10.002
Muñoz-Vargas MA, González-Gordo S, Taboada J, Palma JM, Corpas FJ (2023a) In silico RNAseq and biochemical analyses of glucose-6-phosphate dehydrogenase (G6PDH) from sweet pepper fruits: involvement of nitric oxide (NO) in ripening and modulation. Plants (basel) 12(19):3408
pubmed: 37836149
pmcid: 10574341
doi: 10.3390/plants12193408
Muñoz-Vargas MA, López-Jaramillo J, González-Gordo S, Paradela A, Palma JM, Corpas FJ (2023b) H
pubmed: 36950799
pmcid: 10585658
doi: 10.1089/ars.2022.0222
Murphy A, Peer W, Taiz L (2000) Regulation of auxin transport by aminopeptidases and endogenous flavonoids. Planta 211:315–324
pubmed: 10987549
doi: 10.1007/s004250000300
Narváez-Vásquez J, Tu CJ, Park SY, Walling LL (2008) Targeting and localization of wound-inducible leucine aminopeptidase A in tomato leaves. Planta 227(2):341–351
pubmed: 17896114
doi: 10.1007/s00425-007-0621-0
Nimmakayala P, Abburi VL, Saminathan T, Almeida A, Davenport B, Davidson J, Reddy CV, Hankins G, Ebert A, Choi D, Stommel J, Reddy UK (2016) Genome-wide divergence and linkage disequilibrium analyses for Capsicum baccatum revealed by genome-anchored single nucleotide polymorphisms. Front Plant Sci 7:1646
pubmed: 27857720
pmcid: 5093146
doi: 10.3389/fpls.2016.01646
Niu L, Yu J, Liao W, Xie J, Yu J, Lv J, Xiao X, Hu L, Wu Y (2019) Proteomic investigation of S-nitrosylated proteins during NO-induced adventitious rooting of cucumber. Int J Mol Sci 20(21):5363
pubmed: 31661878
pmcid: 6862188
doi: 10.3390/ijms20215363
Oszywa B, Makowski M, Pawełczak M (2013) Purification and partial characterization of aminopeptidase from barley (Hordeum vulgare L.) seeds. Plant Physiol Biochem 65:75–80
pubmed: 23434924
doi: 10.1016/j.plaphy.2013.01.014
Pallavicini C, Peruffo ADB, Santoro M (1981) Isolation and partial characterization of grape aminopeptidase. J Agric Food Chem 29(1981):1216–1220
doi: 10.1021/jf00108a029
Panpetch P, Sirikantaramas S (2021) Fruit ripening-associated leucylaminopeptidase with cysteinylglycine dipeptidase activity from durian suggests its involvement in glutathione recycling. BMC Plant Biol 211:69
doi: 10.1186/s12870-021-02845-6
Park SY, Scranton MA, Stajich JE, Yee A, Walling LL (2017) Chlorophyte aspartyl aminopeptidases: ancient origins, expanded families, new locations, and secondary functions. PLoS ONE 12(10):e0185492
pubmed: 29023459
pmcid: 5638241
doi: 10.1371/journal.pone.0185492
Parveen N, Kandhol N, Sharma S, Singh VP, Chauhan DK, Ludwig-Müller J, Corpas FJ, Tripathi DK (2023) Auxin crosstalk with reactive oxygen and nitrogen species in plant development and abiotic stress. Plant Cell Physiol 63(12):1814–1825
pubmed: 36208156
doi: 10.1093/pcp/pcac138
Pautot V, Holzer FM, Chaufaux J, Walling LL (2001) The induction of tomato leucine aminopeptidase genes LapA after Pseudomonas syringae pv. tomato infection is primarily a wound response triggered by coronatine. Mol Plant Microbe Interact 14:214–224
pubmed: 11204785
doi: 10.1094/MPMI.2001.14.2.214
Peer WA (2011) The role of multifunctional M1 metallopeptidases in cell cycle progression. Ann Bot 107(7):1171–1181
pubmed: 21258033
pmcid: 3091800
doi: 10.1093/aob/mcq265
Polge C, Jaquinod M, Holzer F, Bourguignon J, Walling L, Brouquisse R (2009) Evidence for the existence in Arabidopsis thaliana of the proteasome proteolytic pathway. J Biol Chem 284(51):35412–35424
pubmed: 19822524
pmcid: 2790970
doi: 10.1074/jbc.M109.035394
Potato Genome Sequencing Consortium; Xu X, Pan S, Cheng S, Zhang B, Mu D, Ni P, Zhang G, Yang S, Li R, Wang J, Orjeda G, Guzman F, Torres M, Lozano R, Ponce O, Martinez D, De la Cruz G, Chakrabarti SK, Patil VU, Skryabin KG, Kuznetsov BB, Ravin NV, Kolganova TV, Beletsky AV, Mardanov AV, Di Genova A, Bolser DM, Martin DM, Li G, Yang Y, Kuang H, Hu Q, Xiong X, Bishop GJ, Sagredo B, Mejía N, Zagorski W, Gromadka R, Gawor J, Szczesny P, Huang S, Zhang Z, Liang C, He J, Li Y, He Y, Xu J, Zhang Y, Xie B, Du Y, Qu D, Bonierbale M, Ghislain M, Herrera Mdel R, Giuliano G, Pietrella M, Perrotta G, Facella P, O’Brien K, Feingold SE, Barreiro LE, Massa GA, Diambra L, Whitty BR, Vaillancourt B, Lin H, Massa AN, Geoffroy M, Lundback S, DellaPenna D, Buell CR, Sharma SK, Marshall DF, Waugh R, Bryan GJ, Destefanis M, Nagy I, Milbourne D, Thomson SJ, Fiers M, Jacobs JM, Nielsen KL, Sønderkær M, Iovene M, Torres GA, Jiang J, Veilleux RE, Bachem CW, de Boer J, Borm T, Kloosterman B, van Eck H, Datema E, Hekkert Bt, Goverse A, van Ham RC, Visser RG (2011) Genome sequence and analysis of the tuber crop potato. Nature 475(7355):189–195
Razo-Mendivil FG, Hernandez-Godínez F, Hayano-Kanashiro C, Martínez O (2021) Transcriptomic analysis of a wild and a cultivated varieties of Capsicum annuum over fruit development and ripening. PLoS ONE 16(8):e0256319
pubmed: 34428253
pmcid: 8384167
doi: 10.1371/journal.pone.0256319
Ribes-Moya AM, Adalid AM, Raigón MD, Hellín P, Fita A, Rodríguez-Burruezo A (2020) Variation in flavonoids in a collection of peppers (Capsicum sp.) under organic and conventional cultivation: effect of the genotype, ripening stage, and growing system. J Sci Food Agric 100(5):2208–2223
pubmed: 31909478
doi: 10.1002/jsfa.10245
Rödiger A, Agne B, Dobritzsch D, Helm S, Müller F, Pötzsch N, Baginsky S (2021) Chromoplast differentiation in bell pepper (Capsicum annuum) fruits. Plant J 105(5):1431–1442
pubmed: 33258209
doi: 10.1111/tpj.15104
Rodriguez-Concepcion M, D’Andrea L, Pulido P (2019) Control of plastidial metabolism by the Clp protease complex. J Exp Bot 70:2049–2058
pubmed: 30576524
doi: 10.1093/jxb/ery441
Rodríguez-Ruiz M, Mateos RM, Codesido V, Corpas FJ, Palma JM (2017) Characterization of the galactono-1,4-lactone dehydrogenase from pepper fruits and its modulation in the ascorbate biosynthesis. Role of nitric oxide. Redox Biol 12:171–181
pubmed: 28242561
pmcid: 5328913
doi: 10.1016/j.redox.2017.02.009
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(22):18408–18417
pubmed: 22493451
pmcid: 3365729
doi: 10.1074/jbc.M111.309500
Seoane P, Espigares M, Carmona R et al (2018) TransFlow: a modular framework for assembling and assessing accurate de novo transcriptomes in non-model organisms. BMC Bioinformatics 19:416
pubmed: 30453874
pmcid: 6245506
doi: 10.1186/s12859-018-2384-y
Song S, Song SY, Nian P, Lv D, Jing Y, Lu S, Wang Q, Zhou F (2022) Transcriptomic analysis suggests a coordinated regulation of carotenoid metabolism in ripening chili pepper (Capsicum annuum var. conoides) fruits. Antioxidants (basel) 11(11):2245
pubmed: 36421431
doi: 10.3390/antiox11112245
Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38:3022–3027
pubmed: 33892491
pmcid: 8233496
doi: 10.1093/molbev/msab120
Teixeira PF, Glaser E (2013) Processing peptidases in mitochondria and chloroplasts. Biochim Biophys Acta 1833(2):360–370
pubmed: 22495024
doi: 10.1016/j.bbamcr.2012.03.012
Tu C-J, Park S-Y, Walling LL (2003) Isolation and characterization of the neutral leucine aminopeptidase (LapN) of tomato. Plant Physiol 132:243–255
pubmed: 12746529
pmcid: 166969
doi: 10.1104/pp.102.013854
Tuppy H, Wiesbauer U, Wintersberger E (1962) Amino acid-p-nitroanilide as a substrate for aminopeptidases and other proteolytic enzymes. Hoppe Seylers Z Physiol Chem 329:278–288
pubmed: 13994792
doi: 10.1515/bchm2.1962.329.1.278
Vázquez-Espinosa M, Fayos O, González-de-Peredo AV, Espada-Bellido E, Ferreiro-González M, Palma M, Garcés-Claver A, Barbero GF (2020) Content of capsaicinoids and capsiate in “filius” pepper varieties as affected by ripening. Plants (basel) 9(9):1222
pubmed: 32957596
doi: 10.3390/plants9091222
Villa-Rivera MG, Martínez O, Ochoa-Alejo N (2022) Putative transcription factor genes associated with regulation of carotenoid biosynthesis in chili pepper fruits revealed by RNA-Seq coexpression analysis. Int J Mol Sci 23(19):11774
pubmed: 36233073
pmcid: 9569626
doi: 10.3390/ijms231911774
Vinogradov AE (1999) Intron-genome size relationship on a large evolutionary scale. J Mol Evol 49:376–384
pubmed: 10473779
doi: 10.1007/PL00006561
Waditee-Sirisattha R, Shibato J, Rakwal R, Sirisattha S, Hattori A, Nakano T, Takabe T, Tsujimoto M (2011) The Arabidopsis aminopeptidase LAP2 regulates plant growth, leaf longevity and stress response. New Phytol 191(4):958–969
pubmed: 21569035
doi: 10.1111/j.1469-8137.2011.03758.x
Wang T, Long C, Chang M, Wu Y, Su S, Wei J, Jiang S, Wang X, He J, Xing D, He Y, Ran Y, Li W (2024) Genome-wide identification of the B3 transcription factor family in pepper (Capsicum annuum) and expression patterns during fruit ripening. Sci Rep 14(1):2226
pubmed: 38278802
pmcid: 10817905
doi: 10.1038/s41598-023-51080-6
Wendel JF, Cronn RC, Alvarez I, Liu B, Small RL, Senchina DS (2002) Intron size and genome size in plants. Mol Biol Evol 19(12):2346–2352
pubmed: 12446829
doi: 10.1093/oxfordjournals.molbev.a004062
Wu J, Xiao J, Wang L, Zhong J, Yin H, Wu S, Zhang Z, Yu J (2013) Systematic analysis of intron size and abundance parameters in diverse lineages. Sci China Life Sci 56(10):968–974
pubmed: 24022126
doi: 10.1007/s11427-013-4540-y
Yamasaki H, Sakihama Y (2000) Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NR-dependent formation of active nitrogen species. FEBS Lett 468(1):89–92
pubmed: 10683447
doi: 10.1016/S0014-5793(00)01203-5
Zdunek-Zastocka E, Grabowska A, Branicki T, Michniewska B (2017) Biochemical characterization of the triticale TsPAP1, a new type of plant prolyl aminopeptidase, and its impact on proline content and flowering time in transgenic Arabidopsis plants. Plant Physiol Biochem 116:18–26
pubmed: 28482331
doi: 10.1016/j.plaphy.2017.04.026
Zhang Z, Yang J, Wu Y (2015) Transcriptional regulation of zein gene expression in maize through the additive and synergistic action of opaque2, prolamine-box binding factor, and O
pubmed: 25901087
pmcid: 4558697
doi: 10.1105/tpc.15.00035
Zuo J, Wang Y, Zhu B, Luo Y, Wang Q, Gao L (2019) Network analysis of noncoding RNAs in pepper provides insights into fruit ripening control. Sci Rep 9(1):8734
pubmed: 31217463
pmcid: 6584694
doi: 10.1038/s41598-019-45427-1