Alam MM, Nakamura H, Ichikawa H, Miyao A, Hirochika H, Kobayashi K et al (2014) Response of an aspartic protease gene OsAP77 to fungal, bacterial and viral infections in rice. Rice 7:9. doi:https://doi.org/10.1186/s12284-014-0009-2
Article
PubMed
PubMed Central
Google Scholar
Allègre M, Héloir MC, Trouvelot S, Daire X, Pugin A, Wendehenne D et al (2009) Are grapevine stomata involved in the elicitor-induced protection against downy mildew? Mol Plant Microbe Interact 22:977–986. doi:https://doi.org/10.1094/MPMI-22-8-0977
CAS
Article
PubMed
Google Scholar
Almagro Armenteros JJ, Sønderby CK, Sønderby SK, Nielsen H, Winther O (2017) DeepLoc: prediction of protein subcellular localization using deep learning. Bioinformatics 33:3387–3395. doi:https://doi.org/10.1093/bioinformatics/btx431
CAS
Article
PubMed
Google Scholar
Armijo G, Schlechter R, Agurto M, Muñoz D, Nuñez C, Arce-Johnson P (2016) Grapevine pathogenic microorganisms: understanding infection strategies and host response scenarios. Front Plant Sci 7:1–18. https://doi.org/10.3389/fpls.2016.00382
Article
Google Scholar
Aziz A, Trotel-Aziz P, Dhuicq L, Jeandet P, Couderchet M, Vernet G (2006) Chitosan oligomers and copper sulfate induce grapevine defense reactions and resistance to gray mold and downy mildew. Phytopathology 96:1188–1194. doi:https://doi.org/10.1094/PHYTO-96-1188
CAS
Article
PubMed
Google Scholar
Babicki S, Arndt D, Marcu A, Liang Y, Grant JR, Maciejewski A et al (2016) Heatmapper: web-enabled heat mapping for all. Nucl Acids Res 44:W147–W153. https://doi.org/10.1093/nar/gkw419
CAS
Article
PubMed
PubMed Central
Google Scholar
Balakireva A, Zamyatnin A (2018) Indispensable role of proteases in plant innate immunity. Int J Mol Sci 19:629. https://doi.org/10.3390/ijms19020629
CAS
Article
PubMed Central
Google Scholar
Bellin D, Peressotti E, Merdinoglu D, Wiedemann-Merdinoglu S, Adam-Blondon AF, Cipriani G et al (2009) Resistance to Plasmopara viticola in grapevine “Bianca” is controlled by a major dominant gene causing localised necrosis at the infection site. Theor Appl Genet 120:163–176. doi:https://doi.org/10.1007/s00122-009-1167-2
Article
PubMed
Google Scholar
Blasi P, Blanc S, Wiedemann-Merdinoglu S, Prado E, Rühl EH, Mestre P et al (2011) Construction of a reference linkage map of Vitis amurensis and genetic mapping of Rpv8, a locus conferring resistance to grapevine downy mildew. Theor Appl Genet 123:43–53. doi:https://doi.org/10.1007/s00122-011-1565-0
Article
PubMed
Google Scholar
Blum M, Chang H-Y, Chuguransky S, Grego T, Kandasaamy S, Mitchell A et al (2020) The InterPro protein families and domains database: 20 years on. Nucl Acids Res. https://doi.org/10.1093/nar/gkaa977
Article
PubMed Central
Google Scholar
Breitenbach HH, Wenig M, Wittek F, Jordá L, Maldonado-Alconada AM, Sarioglu H et al (2014) Contrasting roles of the apoplastic aspartyl protease APOPLASTIC, ENHANCED DISEASE SUSCEPTIBILITY1-DEPENDENT1 and LEGUME LECTIN-LIKE PROTEIN1 in Arabidopsis systemic acquired resistance. Plant Physiol 165:791–809. doi:https://doi.org/10.1104/pp.114.239665
CAS
Article
PubMed
PubMed Central
Google Scholar
Briesemeister S, Rahnenführer J, Kohlbacher O (2010) Going from where to why-interpretable prediction of protein subcellular localization. Bioinformatics 26:1232–1238. doi:https://doi.org/10.1093/bioinformatics/btq115
CAS
Article
PubMed
PubMed Central
Google Scholar
Buonassisi D, Colombo M, Migliaro D, Dolzani C, Peressotti E, Mizzotti C et al (2017) Breeding for grapevine downy mildew resistance: a review of “omics” approaches. Euphytica 213:1–21. doi:https://doi.org/10.1007/s10681-017-1882-8
Article
Google Scholar
Burruano S (2000) The life-cycle of Plasmopara viticola, cause of downy mildew of vine. Mycologist 14:179–182. doi:https://doi.org/10.1016/S0269-915X(00)80040-3
Article
Google Scholar
Cao S, Guo M, Wang C, Xu W, Shi T, Tong G et al (2019) Genome-wide characterization of aspartic protease (AP) gene family in Populus trichocarpa and identification of the potential PtAPs involved in wood formation. BMC Plant Biol 19:276. doi:https://doi.org/10.1186/s12870-019-1865-0
CAS
Article
PubMed
PubMed Central
Google Scholar
Chaudhary S, Jabre I, Reddy ASN, Staiger D, Syed NH (2019) Perspective on Alternative Splicing and Proteome Complexity in Plants. Trends Plant Sci 24:496–506. doi:https://doi.org/10.1016/j.tplants.2019.02.006
CAS
Article
PubMed
Google Scholar
Chen J, Ouyang Y, Wang L, Xie W, Zhang Q (2009) Aspartic proteases gene family in rice: gene structure and expression, predicted protein features and phylogenetic relation. Gene 442:108–118. https://doi.org/10.1016/j.gene.2009.04.021
CAS
Article
PubMed
Google Scholar
Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676. doi:https://doi.org/10.1093/bioinformatics/bti610
CAS
Article
PubMed
Google Scholar
Eisenmann B, Czemmel S, Ziegler T, Buchholz G, Kortekamp A, Trapp O et al (2019) Rpv3–1 mediated resistance to grapevine downy mildew is associated with specific host transcriptional responses and the accumulation of stilbenes. BMC Plant Biol 19:343. doi:https://doi.org/10.1186/s12870-019-1935-3
Faro C, Gal S (2005) Aspartic proteinase content of the arabidopsis genome. Curr Protein Pept Sci 6:493–500. https://doi.org/10.2174/138920305774933268
CAS
Article
PubMed
Google Scholar
Feechan A, Jermakow AM, Ivancevic A, Godfrey D, Pak H, Panstruga R et al (2013) Host cell entry of powdery mildew is correlated with endosomal transport of antagonistically acting VvPEN1 and VvMLO to the papilla. Mol Plant-Microbe Interact 26:1138–1150. doi:https://doi.org/10.1094/MPMI-04-13-0091-R
CAS
Article
PubMed
Google Scholar
Fejfarová K, Kádek A, Mrázek H, Hausner J, Tretyachenko V, Koval’ T et al (2016) Crystallization of nepenthesin I using a low-pH crystallization screen. Acta Crystallogr Sect Struct Biol Commun 72:24–28. doi:https://doi.org/10.1107/S2053230X15022323
CAS
Article
Google Scholar
Figueiredo A, Monteiro F, Fortes AM, Bonow-Rex M, Zyprian E, Sousa L et al (2012) Cultivar-specific kinetics of gene induction during downy mildew early infection in grapevine. Funct Integr Genomics 12:379–386. doi:https://doi.org/10.1007/s10142-012-0261-8
CAS
Article
PubMed
Google Scholar
Figueiredo J, Costa GJ, Maia M, Paulo OS, Malhó R, Sousa Silva M et al (2016) Revisiting Vitis vinifera subtilase gene family: a possible role in grapevine resistance against Plasmopara viticola. Front Plant Sci 7:1783. https://doi.org/10.3389/fpls.2016.01783
Article
PubMed
PubMed Central
Google Scholar
Figueiredo L, Santos RB, Figueiredo A (2021) Defense and offense strategies: the role of aspartic proteases in plant–pathogen interactions. Biology 10. https://doi.org/10.3390/biology10020075
Fischer BM, Salakhutdinov I, Akkurt M, Eibach R, Edwards KJ, Töpfer R et al (2004) Quantitative trait locus analysis of fungal disease resistance factors on a molecular map of grapevine. Theor Appl Genet 108:501–515. doi:https://doi.org/10.1007/s00122-003-1445-3
CAS
Article
PubMed
Google Scholar
Frey ME, D’Ippolito S, Pepe A, Daleo GR, Guevara MG (2018) Transgenic expression of plant-specific insert of potato aspartic proteases (StAP-PSI) confers enhanced resistance to Botrytis cinerea in Arabidopsis thaliana. Phytochemistry 149:1–11. doi:https://doi.org/10.1016/j.phytochem.2018.02.004
CAS
Article
PubMed
Google Scholar
Gao H, Li R, Guo Y (2017) Arabidopsis aspartic proteases A36 and A39 play roles in plant reproduction. Plant Signal Behav 12:e1304343. doi:https://doi.org/10.1080/15592324.2017.1304343
CAS
Article
PubMed
PubMed Central
Google Scholar
Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD et al (2005) Protein Identification and Analysis Tools on the ExPASy Server. In: The Proteomics Protocols Handbook. Humana Press, pp 571–607. https://doi.org/10.1385/1-59259-890-0:571
Ge X, Dietrich C, Matsuno M, Li G, Berg H, Xia Y (2005) An Arabidopsis aspartic protease functions as an anti-cell-death component in reproduction and embryogenesis. EMBO Rep 6:282–288. doi:https://doi.org/10.1038/sj.embor.7400357
CAS
Article
PubMed
PubMed Central
Google Scholar
Gessler C, Pertot I, Perazzolli M (2011) Plasmopara viticola: A review of knowledge on downy mildew of grapevine and effective disease management. Phytopathol Mediterr 50:3–44. doi:https://doi.org/10.14601/Phytopathol_Mediterr-9360
Article
Google Scholar
Goldberg T, Hecht M, Hamp T, Karl T, Yachdav G, Ahmed N et al (2014) LocTree3 prediction of localization. Nucl Acids Res 42. doi:https://doi.org/10.1093/nar/gku396
Gong P, Riemann M, Dong D, Stoeffler N, Gross B, Markel A et al (2019) Two grapevine metacaspase genes mediate ETI-like cell death in grapevine defence against infection of Plasmopara viticola. Protoplasma 256:951–969. doi:https://doi.org/10.1007/s00709-019-01353-7
CAS
Article
PubMed
Google Scholar
Guerra-Guimarães L, Pinheiro C, Chaves I, Barros D, Ricardo C (2016) Protein dynamics in the plant extracellular space. Proteomes 4:22. https://doi.org/10.3390/proteomes4030022
CAS
Article
PubMed Central
Google Scholar
Guevara MG, Almeida C, Mendieta JR, Faro CJ, Veríssimo P, Pires EV et al (2005) Molecular cloning of a potato leaf cDNA encoding an aspartic protease (StAsp) and its expression after P. infestans infection. Plant Physiol Biochem 43:882–889. doi:https://doi.org/10.1016/j.plaphy.2005.07.004
CAS
Article
PubMed
Google Scholar
Guo R, Xu X, Carole B, Li X, Gao M, Zheng Y et al (2013) Genome-wide identification, evolutionary and expression analysis of the aspartic protease gene superfamily in grape. BMC Genom 14:554. https://doi.org/10.1186/1471-2164-14-554
CAS
Article
Google Scholar
Guo R, Tu M, Wang XX, Zhao J, Wan R, Li Z et al (2016) Ectopic expression of a grape aspartic protease gene, AP13, in Arabidopsis thaliana improves resistance to powdery mildew but increases susceptibility to Botrytis cinerea. Plant Sci 248:17–27. doi:https://doi.org/10.1016/j.plantsci.2016.04.006
CAS
Article
PubMed
Google Scholar
Harrington B (2004) Inkscape
Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8:R19. doi:https://doi.org/10.1186/gb-2007-8-2-r19
CAS
Article
PubMed
PubMed Central
Google Scholar
Hou S, Jamieson P, He P (2018) The cloak, dagger, and shield: proteases in plant–pathogen interactions. Biochem J 475:2491–2509. doi:https://doi.org/10.1042/BCJ20170781
CAS
Article
PubMed
Google Scholar
Huang J, Zhao X, Cheng K, Jiang Y, Ouyang Y, Xu C et al (2013) OsAP65, a rice aspartic protease, is essential for male fertility and plays a role in pollen germination and pollen tube growth. J Exp Bot 64:3351–3360. doi:https://doi.org/10.1093/jxb/ert173
CAS
Article
PubMed
PubMed Central
Google Scholar
Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329. doi:https://doi.org/10.1038/nature05286
CAS
Article
PubMed
Google Scholar
Kang J, Gong P, Ge M, Sadeghnezhad E, Liu Z, Zhang M et al (2021) The PLCP gene family of grapevine (Vitis vinifera L.): characterization and differential expression in response to Plasmopara Viticola. BMC Plant Biol 21:1–14. https://doi.org/10.1186/S12870-021-03279-W/FIGURES/6
Article
Google Scholar
Kato Y, Murakami S, Yamamoto Y, Chatani H, Kondo Y, Nakano T et al (2004) The DNA-binding protease, CND41, and the degradation of ribulose-1,5-bisphosphate carboxylase/oxygenase in senescent leaves of tobacco. Planta 220:97–104. doi:https://doi.org/10.1007/s00425-004-1328-0
CAS
Article
PubMed
Google Scholar
King BR, Guda C (2007) ngLOC: an n-gram-based Bayesian method for estimating the subcellular proteomes of eukaryotes. Genome Biol 8. https://doi.org/10.1186/gb-2007-8-5-r68
Kortekamp A (2006) Expression analysis of defence-related genes in grapevine leaves after inoculation with a host and a non-host pathogen. Plant Physiol Biochem 44:58–67. doi:https://doi.org/10.1016/j.plaphy.2006.01.008
CAS
Article
PubMed
Google Scholar
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. doi:https://doi.org/10.1093/molbev/msy096
CAS
Article
PubMed
PubMed Central
Google Scholar
Larkin MA, Blackshields G, Brown NP, Chenna R, Mcgettigan PA, McWilliam H et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. doi:https://doi.org/10.1093/bioinformatics/btm404
CAS
Article
PubMed
Google Scholar
Letunic I, Bork P (2018) 20 years of the SMART protein domain annotation resource. Nucl Acids Res 46:D493–D496. https://doi.org/10.1093/nar/gkx922
CAS
Article
PubMed
Google Scholar
Li Y, Kabbage M, Liu W, Dickman MB (2016) Aspartyl protease-mediated cleavage of BAG6 is necessary for autophagy and fungal resistance in plants. Plant Cell 28:233–247. doi:https://doi.org/10.1105/tpc.15.00626
CAS
Article
PubMed
PubMed Central
Google Scholar
Marguerit E, Boury C, Manicki A, Donnart M, Butterlin G, Némorin A et al (2009) Genetic dissection of sex determinism, inflorescence morphology and downy mildew resistance in grapevine. Theor Appl Genet 118:1261–1278. doi:https://doi.org/10.1007/s00122-009-0979-4
Article
PubMed
Google Scholar
Mistry J, Chuguransky S, Williams L, Qureshi M, Salazar GA, Sonnhammer ELL et al (2021) Pfam: the protein families database in 2021. Nucleic Acids Res 49:D412–D419. https://doi.org/10.1093/nar/gkaa913
CAS
Article
PubMed
Google Scholar
Monteiro F, Sebastiana M, Pais MS, Figueiredo A (2013) Reference gene selection and validation for the early responses to downy mildew infection in susceptible and resistant Vitis vinifera cultivars. PLoS One 8:e72998. https://doi.org/10.1371/journal.pone.0072998
CAS
Article
PubMed
PubMed Central
Google Scholar
Muñoz FF, Mendieta JR, Pagano MR, Paggi RA, Daleo GR, Guevara MG (2010) The swaposin-like domain of potato aspartic protease (StAsp-PSI) exerts antimicrobial activity on plant and human pathogens. Peptides 31:777–785. doi:https://doi.org/10.1016/j.peptides.2010.02.001
CAS
Article
PubMed
Google Scholar
Ochssner I, Hausmann L, Töpfer R (2016) Rpvl4, a new genetic source for Plasmopara viticola resistance conferred by Vitis cinerea. Vitis J Grapevine Res 55:79–81. https://doi.org/10.5073/vitis.2016.55.79-81
CAS
Article
Google Scholar
Panchy N, Lehti-Shiu M, Shiu SH (2016) Evolution of gene duplication in plants. Plant Physiol 171:2294–2316. doi:https://doi.org/10.1104/pp.16.00523
CAS
Article
PubMed
PubMed Central
Google Scholar
Potter SC, Luciani A, Eddy SR, Park Y, Lopez R, Finn RD (2018) HMMER web server: 2018 update. Nucl Acids Res 46:W200–W204. https://doi.org/10.1093/nar/gky448
CAS
Article
PubMed
PubMed Central
Google Scholar
Prasad BD, Creissen G, Lamb C, Chattoo BB (2009) Overexpression of Rice (Oryza sativa L.) OsCDR1 leads to constitutive activation of defense responses in rice and Arabidopsis. Mol Plant Microbe Interact 22:1635–1644. https://doi.org/10.1094/MPMI-22-12-1635
CAS
Article
PubMed
Google Scholar
Prasad BD, Creissen G, Lamb C, Chattoo BB (2010) Heterologous expression and characterization of recombinant OsCDR1, a rice aspartic proteinase involved in disease resistance. Protein Exp Purif 72:169–174. doi:https://doi.org/10.1016/j.pep.2010.03.018
CAS
Article
Google Scholar
Riechmann JL, Heard J, Martin G, Reuber L, Jiang CZ, Keddie J et al (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Sci (80-) 290:2105–2110. https://doi.org/10.1126/science.290.5499.2105
CAS
Article
Google Scholar
Sargolzaei M, Maddalena G, Bitsadze N, Maghradze D, Bianco PA, Failla O et al (2020) Rpv29, Rpv30 and Rpv31: three novel genomic loci associated with resistance to Plasmopara viticola in Vitis vinifera. Front Plant Sci 11:1537. https://doi.org/10.3389/FPLS.2020.562432/BIBTEX
Article
Google Scholar
Schwander F, Eibach R, Fechter I, Hausmann L, Zyprian E, Töpfer R (2012) Rpv10: a new locus from the Asian Vitis gene pool for pyramiding downy mildew resistance loci in grapevine. Theor Appl Genet 124:163–176. https://doi.org/10.1007/s00122-011-1695-4
CAS
Article
PubMed
Google Scholar
Simões I, Faro C (2004) Structure and function of plant aspartic proteinases. Eur J Biochem 271:2067–2075. doi:https://doi.org/10.1111/j.1432-1033.2004.04136.x
CAS
Article
PubMed
Google Scholar
Simões I, Faro R, Bur D, Faro C (2007) Characterization of recombinant CDR1, an Arabidopsis aspartic proteinase involved in disease resistance. J Biol Chem 282:31358–31365. doi:https://doi.org/10.1074/jbc.M702477200
CAS
Article
PubMed
Google Scholar
Soares A, Niedermaier S, Faro R, Loos A, Manadas B, Faro C et al (2019a) An atypical aspartic protease modulates lateral root development in Arabidopsis thaliana. J Exp Bot 70:2157–2171. doi:https://doi.org/10.1093/jxb/erz059
CAS
Article
PubMed
Google Scholar
Soares A, Ribeiro Carlton SM, Simões I (2019b) Atypical and nucellin-like aspartic proteases: emerging players in plant developmental processes and stress responses. J Exp Bot 70:2059–2076. doi:https://doi.org/10.1093/jxb/erz034
CAS
Article
PubMed
Google Scholar
Takahashi K, Athauda S, Matsumoto K, Rajapakshe S, Kuribayashi M, Kojima M et al (2005) Nepenthesin, a unique member of a novel subfamily of aspartic proteinases: enzymatic and structural characteristics. Curr Protein Pept Sci 6:513–525. https://doi.org/10.2174/138920305774933259
CAS
Article
PubMed
Google Scholar
Unger S, Büche C, Boso S, Kassemeyer HH (2007) The course of colonization of two different Vitis genotypes by Plasmopara viticola indicates compatible and incompatible host-pathogen interactions. Phytopathology 97:780–786. doi:https://doi.org/10.1094/PHYTO-97-7-0780
Article
PubMed
Google Scholar
Vitulo N, Forcato C, Carpinelli EC, Telatin A, Campagna D, D’Angelo M et al (2014) A deep survey of alternative splicing in grape reveals changes in the splicing machinery related to tissue, stress condition and genotype. BMC Plant Biol 14:99. doi:https://doi.org/10.1186/1471-2229-14-99
CAS
Article
PubMed
PubMed Central
Google Scholar
Welter LJ, Göktürk-Baydar N, Akkurt M, Maul E, Eibach R, Töpfer R et al (2007) Genetic mapping and localization of quantitative trait loci affecting fungal disease resistance and leaf morphology in grapevine (Vitis vinifera L). Mol Breed 20:359–374. doi:https://doi.org/10.1007/s11032-007-9097-7
CAS
Article
Google Scholar
Xia Y (2004) Proteases in pathogenesis and plant defence. Cell Microbiol 6:905–913. doi:https://doi.org/10.1111/j.1462-5822.2004.00438.x
CAS
Article
PubMed
Google Scholar
Xia Y, Suzuki H, Borevitz J, Blount J, Guo Z, Patel K et al (2004) An extracellular aspartic protease functions in Arabidopsis disease resistance signaling. EMBO J 23:980–988. doi:https://doi.org/10.1038/sj.emboj.7600086
CAS
Article
PubMed
PubMed Central
Google Scholar
Yan H, Dai X, Feng K, Ma Q, Yin T (2016) IGDD: a database of intronless genes in dicots. BMC Bioinform 17:289. https://doi.org/10.1186/s12859-016-1148-9
CAS
Article
Google Scholar
Yang Y, Feng D (2020) Genome-wide identification of the aspartic protease gene family and their response under powdery mildew stress in wheat. Mol Biol Rep. doi:https://doi.org/10.1007/s11033-020-05948-9
Article
PubMed
PubMed Central
Google Scholar
Yao X, Xiong W, Ye T, Wu Y (2012) Overexpression of the aspartic protease ASPG1 gene confers drought avoidance in Arabidopsis. J Exp Bot 63:2579–2593. doi:https://doi.org/10.1093/jxb/err433
CAS
Article
PubMed
PubMed Central
Google Scholar