Abstract
Key message
The first in-depth characterization of a subfamily III Snakin/GASA member was performed providing experimental evidence on promoter activity and subcellular localization and unveiling a role of potato Snakin-3 in defense
Abstract
Snakin/GASA proteins share 12 cysteines in conserved positions in the C-terminal region. Most of them were involved in different aspects of plant growth and development, while a small number of these peptides were reported to have antimicrobial activity or participate in abiotic stress tolerance. In potato, 18 Snakin/GASA genes were identified and classified into three groups based on phylogenetic analysis. Snakin-1 and Snakin-2 are members of subfamilies I and II, respectively, and were reported to be implicated not only in defense against pathogens but also in plant development. In this work, we present the first in-depth characterization of Snakin-3, a member of the subfamily III within the Snakin/GASA gene family of potato. Transient co-expression of Snakin-3 fused to the green fluorescent protein and organelle markers revealed that it is located in the endoplasmic reticulum. Furthermore, expression analyses via pSnakin-3::GUS transgenic plants showed GUS staining mainly in roots and vascular tissues of the stem. Moreover, GUS expression levels were increased after inoculation with Pseudomonas syringae pv. tabaci or Pectobacterium carotovorum subsp. carotovorum and also after auxin treatment mainly in roots and stems. To gain further insights into the function of Snakin-3 in planta, potato overexpressing lines were challenged against P. carotovorum subsp. carotovorum showing enhanced tolerance to this bacterial pathogen. In sum, here we report the first functional characterization of a Snakin/GASA gene from subfamily III in Solanaceae. Our findings provide experimental evidence on promoter activity and subcellular localization and reveal a role of potato Snakin-3 in plant defense.
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Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Abdullah C, Faraji S, Mehmood F et al (2021) The gasa gene family in cacao (Theobroma cacao, malvaceae): genome wide identification and expression analysis. Agronomy. https://doi.org/10.3390/agronomy11071425
Allen A, Snyder AK, Preuss M et al (2008) Plant defensins and virally encoded fungal toxin KP4 inhibit plant root growth. Planta 227:331–339. https://doi.org/10.1007/s00425-007-0620-1
Almagro Armenteros JJ, Sønderby CK, Sønderby SK et al (2017) DeepLoc: prediction of protein subcellular localization using deep learning. Bioinformatics 33:3387–3395. https://doi.org/10.1093/bioinformatics/btx431
Almasia NI, Bazzini AA, Hopp HE, Vazquez-Rovere C (2008) Overexpression of snakin-1 gene enhances resistance to Rhizoctonia solani and Erwinia carotovora in transgenic potato plants. Mol Plant Pathol 9:329–338. https://doi.org/10.1111/j.1364-3703.2008.00469.x
Almasia NI, Narhirñak V, Hopp Esteban H, Vazquez-Rovere C (2010) Isolation and characterization of the tissue and development-specific potato snakin-1 promoter inducible by temperature and wounding. Electron J Biotechnol 13:1–21. https://doi.org/10.2225/vol13-issue5-fulltext-12
Almasia NI, Nahirñak V, Hopp HE, Vazquez-Rovere C (2020) Potato Snakin-1: an antimicrobial player of the trade-off between host defense and development. Plant Cell Rep 39:839–849. https://doi.org/10.1007/s00299-020-02557-5
Alonso-Ramírez A, Rodríguez D, Reyes D et al (2009) Evidence for a role of gibberellins in salicylic acid-modulated early plant responses to abiotic stress in Arabidopsis seeds. Plant Physiol 150:1335–1344. https://doi.org/10.1104/pp.109.139352
Aubert D, Chevillard M, Dorne AM et al (1998) Expression patterns of GASA genes in Arabidopsis thaliana: The GASA4 gene is up-regulated by gibberellins in meristematic regions. Plant Mol Biol 36:871–883. https://doi.org/10.1023/A:1005938624418
Babicki S, Arndt D, Marcu A et al (2016) Heatmapper: web-enabled heat map** for all. Nucleic Acids Res 44:W147–W153. https://doi.org/10.1093/nar/gkw419
Balaji V, Smart CD (2012) Over-expression of snakin-2 and extensin-like protein genes restricts pathogen invasiveness and enhances tolerance to Clavibacter michiganensis subsp. michiganensis in transgenic tomato (Solanum lycopersicum). Transgenic Res 21:23–37. https://doi.org/10.1007/s11248-011-9506-x
Ben-Nissan G, Weiss D (1996) The petunia homologue of tomato gast1: Transcript accumulation coincides with gibberellin-induced corolla cell elongation. Plant Mol Biol 32:1067–1074. https://doi.org/10.1007/BF00041390
Ben-Nissan G, Lee JY, Borohov A, Weiss D (2004) GIP, a Petunia hybrida GA-induced cysteine-rich protein: a possible role in shoot elongation and transition to flowering. Plant J 37:229–238. https://doi.org/10.1046/j.1365-313X.2003.01950.x
Berrocal-Lobo M, Segura A, Moreno M et al (2002) Snakin-2, an antimicrobial peptide from potato whose gene is locally induced by wounding and responds to pathogen infection. Plant Physiol 128:951–961. https://doi.org/10.1104/pp.010685
Blum T, Briesemeister S, Kohlbacher O (2009) MultiLoc2: integrating phylogeny and Gene Ontology terms improves subcellular protein localization prediction. BMC Bioinform 10:274. https://doi.org/10.1186/1471-2105-10-274
Bologna G, Yvon C, Duvaud S, Veuthey A-L (2004) N-Terminal myristoylation predictions by ensembles of neural networks. Proteomics 4:1626–1632. https://doi.org/10.1002/pmic.200300783
Boonpa K, Tantong S, Weerawanich K et al (2018) Heterologous expression and antimicrobial activity of OsGASR3 from rice (Oryza sativa L.). J Plant Physiol 224–225:95–102. https://doi.org/10.1016/j.jplph.2018.03.013
Bouteraa MT, Ben Romdhane W, Baazaoui N et al (2023a) GASA proteins: review of their functions in plant environmental stress tolerance. Plants. https://doi.org/10.3390/plants12102045
Bouteraa MT, Ben Romdhane W, Ben Hsouna A et al (2023b) Genome-wide characterization and expression profiling of GASA gene family in Triticum turgidum ssp. durum (desf.) husn (Durum wheat) unveils its involvement in environmental stress responses. Phytochemistry 206:113544. https://doi.org/10.1016/j.phytochem.2022.113544
Briesemeister S, Rahnenfïhrer J, Kohlbacher O (2010) YLoc—an interpretable web server for predicting subcellular localization. Nucleic Acids Res 38:W497–W502. https://doi.org/10.1093/nar/gkq477
Chen K, Liu W, Li X, Li H (2021) Overexpression of GmGASA32 promoted soybean height by interacting with GmCDC25. Plant Signal Behav. https://doi.org/10.1080/15592324.2020.1855017
Cheong J-J, Lee G-H, Kwon H-B (1999) Expression and regulation of theRSI-1 gene during lateral root initiation. J Plant Biol 42:259–265. https://doi.org/10.1007/bf03030338
Chou K-C, Shen H-B (2010) A new method for predicting the subcellular localization of eukaryotic proteins with both single and multiple sites: Euk-mPLoc 2.0. PLoS ONE 5:e9931. https://doi.org/10.1371/journal.pone.0009931
Darqui FS, Radonic LM, Trotz PM et al (2018) Potato snakin-1 gene enhances tolerance to Rhizoctonia solani and Sclerotinia sclerotiorum in transgenic lettuce plants. J Biotechnol 283:62–69. https://doi.org/10.1016/j.jbiotec.2018.07.017
Das K, Datta K, Sarkar SN, Datta SK (2021) Expression of antimicrobial peptide snakin-1 confers effective protection in rice against sheath blight pathogen, Rhizoctonia solani. Plant Biotechnol Rep 15:39–54. https://doi.org/10.1007/s11816-020-00652-3
De La Fuente JI, Amaya I, Castillejo C et al (2006) The strawberry gene FaGAST affects plant growth through inhibition of cell elongation. J Exp Bot 57:2401–2411. https://doi.org/10.1093/jxb/erj213
Deng M, Peng J, Zhang J et al (2021) The cysteine-rich peptide snakin-2 negatively regulates tubers sprouting through modulating lignin biosynthesis and h2o2 accumulation in potato. Int J Mol Sci 22:1–16. https://doi.org/10.3390/ijms22052287
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small amounts of fresh leaf tissue.
Elmayan T, Tepfer M (1995) Evaluation in tobacco of the organ specificity and strength of therolD promoter, domain A of the 35S promoter and the 35S2 promoter. Transgenic Res 4:388–396. https://doi.org/10.1007/BF01973757
Faccio P, Vazquez-Rovere C, Hopp E et al (2011) Increased tolerance to wheat powdery mildew by heterologous constitutive expression of the Solanum chacoense snakin-1 gene. Czech J Genet Plant Breed 47:135–141. https://doi.org/10.17221/3268-cjgpb
Fan S, Zhang D, Zhang L et al (2017) Comprehensive analysis of GASA family members in the Malus domestica genome: Identification, characterization, and their expressions in response to apple flower induction. BMC Genom 18:1–19. https://doi.org/10.1186/s12864-017-4213-5
Fehlberg V, Vieweg MF, Dohmann EMN et al (2005) The promoter of the leghaemoglobin gene VfLb29: functional analysis and identification of modules necessary for its activation in the infected cells of root nodules and in the arbuscule-containing cells of mycorrhizal roots. J Exp Bot 56:799–806. https://doi.org/10.1093/jxb/eri074
Furukawa T, Sakaguchi N, Shimada H (2006) Two OsGASR genes, rice GAST homologue genes that are abundant in proliferating tissues, show different expression patterns in develo** panicles. Genes Genet Syst 81:171–180. https://doi.org/10.1266/ggs.81.171
Gianola D, Norton HW (1981) Scaling threshold characters. Genetics 99:357–364. https://doi.org/10.1093/genetics/99.2.357
Goldberg T, Hecht M, Hamp T et al (2014) LocTree3 prediction of localization. Nucleic Acids Res 42:W350–W355. https://doi.org/10.1093/nar/gku396
Goyal RK, Mattoo AK (2014) Multitasking antimicrobial peptides in plant development and host defense against biotic/abiotic stress. Plant Sci 228:135–149. https://doi.org/10.1016/j.plantsci.2014.05.012
Harris PWR, Yang SH, Molina A et al (2014) Plant antimicrobial peptides snakin-1 and snakin-2: Chemical synthesis and insights into the disulfide connectivity. Chem - A Eur J 20:5102–5110. https://doi.org/10.1002/chem.201303207
Hemsley PA (2015) The importance of lipid modified proteins in plants. New Phytol 205:476–489. https://doi.org/10.1111/nph.13085
Hemsley PA, Grierson CS (2008) Multiple roles for protein palmitoylation in plants. Trends Plant Sci 13:295–302. https://doi.org/10.1016/j.tplants.2008.04.006
Herbel V, Wink M (2016) Mode of action and membrane specificity of the antimicrobial peptide snakin-2. PeerJ 4:e1987. https://doi.org/10.7717/peerj.1987
Herbel V, Schäfer H, Wink M (2015) Recombinant production of snakin-2 (an antimicrobial peptide from tomato) in E. Coli and analysis of its bioactivity. Molecules 20:14889–14901. https://doi.org/10.3390/molecules200814889
Hernández-Martínez MA, Suárez-Rodríguez LM, López-Meza JE et al (2022) Antifungal activity of avocado seed recombinant GASA/snakin PaSn. Antibiotics. https://doi.org/10.3390/antibiotics11111558
Herzog M, Dorne AM, Grellet F (1995) GASA, a gibberellin-regulated gene family from Arabidopsis thaliana related to the tomato GAST1 gene. Plant Mol Biol 27:743–752. https://doi.org/10.1007/BF00020227
Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300. https://doi.org/10.1093/nar/27.1.297
Horton P, Park K-J, Obayashi T et al (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585–W587. https://doi.org/10.1093/nar/gkm259
Jacobs JME, Meiyalaghan S, Mohan S et al (2023) A potato intragene overexpressing GSL1 confers resistance to Pectobacterium atrosepticum. New Zeal J Crop Hortic Sci 51:212–230. https://doi.org/10.1080/01140671.2021.2021954
Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907. https://doi.org/10.1002/j.1460-2075.1987.tb02730.x
Kaleel M, Ellinger L, Lalor C et al (2021) SCLpred-MEM: Subcellular localization prediction of membrane proteins by deep N-to-1 convolutional neural networks. Proteins 89:1233–1239. https://doi.org/10.1002/prot.26144
Karimi M, Inzé D, Depicker A (2002) GATEWAY vectors for Agrobacterium-mediated plant.pdf. Trends Plant Sci 7:193–195
Kaundal R, Saini R, Zhao PX (2010) Combining machine learning and homology-based approaches to accurately predict subcellular localization in Arabidopsis. Plant Physiol 154:36–54. https://doi.org/10.1104/pp.110.156851
Ko CB, Woo YM, Lee DJ et al (2007) Enhanced tolerance to heat stress in transgenic plants expressing the GASA4 gene. Plant Physiol Biochem 45:722–728. https://doi.org/10.1016/j.plaphy.2007.07.010
Kotilainen M, Helariutta Y, Mehto M et al (1999) GEG participates in the regulation of cell and organ shape during corolla and carpel development in Gerbera hybrida. Plant Cell 11:1093–1104. https://doi.org/10.1105/tpc.11.6.1093
Kovalskaya N (2011) Antibacterial and antifungal activity of a snakin-defensin hybrid protein expressed in tobacco and potato plants. Open Plant Sci J 5:29–42. https://doi.org/10.2174/1874294701105010029
Kovalskaya N, Hammond RW (2009) Expression and functional characterization of the plant antimicrobial snakin-1 and defensin recombinant proteins. Protein Expr Purif 63:12–17. https://doi.org/10.1016/j.pep.2008.08.013
Kuddus MR, Rumi F, Tsutsumi M et al (2016) Expression, purification and characterization of the recombinant cysteine-rich antimicrobial peptide snakin-1 in Pichia pastoris. Protein Expr Purif 122:15–22. https://doi.org/10.1016/j.pep.2016.02.002
Kumari B, Kumar R, Kumar M (2014) PalmPred: an SVM based palmitoylation prediction method using sequence profile information. PLoS ONE 9:e89246. https://doi.org/10.1371/journal.pone.0089246
Lescot M, Déhais P, Thijs G et al (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. https://doi.org/10.1093/nar/30.1.325
Li KL, Bai X, Li Y et al (2011) GsGASA1 mediated root growth inhibition in response to chronic cold stress is marked by the accumulation of DELLAs. J Plant Physiol 168:2153–2160. https://doi.org/10.1016/j.jplph.2011.07.006
Li J, Hu S, Jian W et al (2021) Plant antimicrobial peptides: structures, functions, and applications. Bot Stud. https://doi.org/10.1186/s40529-021-00312-x
Li L, Lyu C, Chen J et al (2022a) Snakin-2 interacts with cytosolic glyceraldehyde-3-phosphate dehydrogenase 1 to inhibit sprout growth in potato tubers. Hortic Res 9:1–11. https://doi.org/10.1093/hr/uhab060
Li Z, Gao J, Wang G et al (2022b) Genome-wide identification and characterization of GASA gene family in Nicotiana tabacum. Front Genet 12:1–13. https://doi.org/10.3389/fgene.2021.768942
Li X, Zhang MS, Zhao LQ et al (2023) The study on interacting factors and functions of GASA6 in Jatropha curcas L. BMC Plant Biol 23:1–13. https://doi.org/10.1186/s12870-023-04067-4
Lima AM, Azevedo MIG, Sousa LM et al (2022) Plant antimicrobial peptides: An overview about classification, toxicity and clinical applications. Int J Biol Macromol 214:10–21. https://doi.org/10.1016/j.ijbiomac.2022.06.043
Mao Z, Zheng J, Wang Y et al (2011) The new CaSn gene belonging to the snakin family induces resistance against root-knot nematode infection in pepper. Phytoparasitica 39:151–164. https://doi.org/10.1007/s12600-011-0149-5
Massa AN, Childs KL, Lin H et al (2011) The transcriptome of the reference potato genome solanum tuberosum group Phureja clone DM1–3 516R44. PLoS ONE. https://doi.org/10.1371/journal.pone.0026801
Meiyalaghan S, Thomson SJ, Fiers MWEJ et al (2014) Structure and expression of GSL1 and GSL2 genes encoding gibberellin stimulated-like proteins in diploid and highly heterozygous tetraploid potato reveals their highly conserved and essential status. BMC Genom. https://doi.org/10.1186/1471-2164-15-2
Mohan S, Meiyalaghan S, Latimer JM et al (2014) GSL2 over-expression confers resistance to Pectobacterium atrosepticum in potato. Theor Appl Genet 127:677–689. https://doi.org/10.1007/s00122-013-2250-2
Moyano-Cañete E, Bellido ML, García-Caparrós N et al (2013) FaGAST2, a strawberry ripening-related gene, acts together with fagast1 to determine cell size of the fruit receptacle. Plant Cell Physiol 54:218–236. https://doi.org/10.1093/pcp/pcs167
Nahirñak V, Almasia NI, Fernandez PV et al (2012a) Potato Snakin-1 gene silencing affects cell division, primary metabolism, and cell wall composition. Plant Physiol 158:252–263. https://doi.org/10.1104/pp.111.186544
Nahirñak V, Almasia NI, Hopp HE, Vazquez-Rovere C (2012b) Snakin/GASA proteins: Involvement in hormone crosstalk and redox homeostasis. Plant Signal Behav 7:1–5. https://doi.org/10.4161/psb
Nahirñak V, Rivarola M, de Urreta MG et al (2016) Genome-wide analysis of the Snakin/GASA gene family in Solanum tuberosum cv. Kennebec. Am J Potato Res 93:172–188. https://doi.org/10.1007/s12230-016-9494-8
Nahirñak V, Rivarola M, Almasia NI et al (2019) Snakin-1 affects reactive oxygen species and ascorbic acid levels and hormone balance in potato. PLoS ONE 14:1–18. https://doi.org/10.1371/journal.pone.0214165
Nawrot R, Barylski J, Nowicki G et al (2014) Plant antimicrobial peptides. Folia Microbiol (praha) 59:181–196. https://doi.org/10.1007/s12223-013-0280-4
Nelson BK, Cai X, Nebenführ A (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J 51:1126–1136. https://doi.org/10.1111/j.1365-313X.2007.03212.x
Nicot N, Hausman JF, Hoffmann L, Evers D (2005) Housekee** gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. J Exp Bot 56:2907–2914. https://doi.org/10.1093/jxb/eri285
Oliveira-Lima M, Benko-Iseppon A, Neto J et al (2016) Snakin: structure, roles and applications of a plant antimicrobial peptide. Curr Protein Pept Sci 18:368–374. https://doi.org/10.2174/1389203717666160619183140
Panji A, Ismaili A, Sohrabi SM (2023) Genome-wide identification and expression profiling of snakin/GASA genes under drought stress in barley (Hordeum vulgare L.). 3 Biotech 13(5):126. https://doi.org/10.1007/s13205-023-03545-8
Porto WF, Franco OL (2013) Theoretical structural insights into the snakin/GASA family. Peptides 44:163–167. https://doi.org/10.1016/j.peptides.2013.03.014
Qiao K, Ma C, Lv J et al (2021) Identification, characterization, and expression profiles of the GASA genes in cotton. J Cott Res. https://doi.org/10.1186/s42397-021-00081-9
Qiu B, Zhang Y, Wang Q et al (2020) Panax notoginseng snakin gene increases resistance to Fusarium solani in transgenic tobacco. Ind Crops Prod 157:112902. https://doi.org/10.1016/j.indcrop.2020.112902
Ramakers C, Ruijter JM, Deprez RHL, Moorman AFM (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339:62–66. https://doi.org/10.1016/s0304-3940(02)01423-4
Ren J, Wen L, Gao X et al (2008) CSS-Palm 2.0: an updated software for palmitoylation sites prediction. Protein Eng Des Sel 21:639–644. https://doi.org/10.1093/protein/gzn039
Rodríguez-Decuadro S, Barraco-Vega M, Dans PD et al (2018) Antimicrobial and structural insights of a new snakin-like peptide isolated from Peltophorum dubium (Fabaceae). Amino Acids 50:1245–1259. https://doi.org/10.1007/s00726-018-2598-3
Rong W, Qi L, Wang J et al (2013) Expression of a potato antimicrobial peptide SN1 increases resistance to take-all pathogen Gaeumannomyces graminis var. tritici in transgenic wheat. Funct Integr Genomics 13:403–409. https://doi.org/10.1007/s10142-013-0332-5
Rubinovich L, Weiss D (2010) The Arabidopsis cysteine-rich protein GASA4 promotes GA responses and exhibits redox activity in bacteria and in planta. Plant J 64:1018–1027. https://doi.org/10.1111/j.1365-313X.2010.04390.x
Rubinovich L, Ruthstein S, Weiss D (2014) The arabidopsis cysteine-rich GASA5 is a redox-active metalloprotein that suppresses gibberellin responses. Mol Plant 7:244–247. https://doi.org/10.1093/mp/sst141
Running MP (2014) The role of lipid post-translational modification in plant developmental processes. Front Plant Sci 5:1–9. https://doi.org/10.3389/fpls.2014.00050
Savojardo C, Martelli PL, Fariselli P et al (2018) BUSCA: an integrative web server to predict subcellular localization of proteins. Nucleic Acids Res 46:W459–W466. https://doi.org/10.1093/nar/gky320
Segura A, Moreno M, Madueño F et al (1999) Snakin-1, a peptide from potato that is active against plant pathogens. Mol Plant-Microbe Interact 12:16–23. https://doi.org/10.1094/MPMI.1999.12.1.16
Shang C, Ye T, Zhou Q et al (2023) Genome-wide identification and bioinformatics analyses of host defense peptides snakin/GASA in Mangrove plants. Genes (basel). https://doi.org/10.3390/genes14040923
Shi L, Gast RT, Gopalraj M et al (1992) (1992) Characterization of a shoot-specific, GA3- and ABA-regulated gene from tomato. Plant J 2:153–159
Stotz HU, Spence B, Wang Y (2009) A defensin from tomato with dual function in defense and development. Plant Mol Biol 71:131–143. https://doi.org/10.1007/s11103-009-9512-z
Su T, Han M, Cao D, Xu M (2020) Molecular and biological properties of snakins: The foremost cysteine-rich plant host Defense peptides. J Fungi 6:1–17. https://doi.org/10.3390/jof6040220
Su D, Liu K, Yu Z et al (2023) Genome-wide characterization of the tomato GASA family identifies SlGASA1 as a repressor of fruit ripening. Hortic Res. https://doi.org/10.1093/hr/uhac222
Sun S, Wang H, Yu H et al (2013) GASA14 regulates leaf expansion and abiotic stress resistance by modulating reactive oxygen species accumulation. J Exp Bot 64:1637–1647. https://doi.org/10.1093/jxb/ert021
Taylor BH, Scheuring CF (1994) A molecular marker for lateral root initiation: The RSI-1 gene of tomato (Lycopersicon esculentum Mill) is activated in early lateral root primordia. MGG Mol Gen Genet 243:148–157. https://doi.org/10.1007/BF00280311
Turnbull D, Hemsley PA (2017) Fats and function: protein lipid modifications in plant cell signalling. Curr Opin Plant Biol 40:63–70. https://doi.org/10.1016/j.pbi.2017.07.007
Wang L, Wang Z, Xu Y et al (2009) OsGSR1 is involved in crosstalk between gibberellins and brassinosteroids in rice. Plant J 57:498–510. https://doi.org/10.1111/j.1365-313X.2008.03707.x
Wu T, Cheng C, Zhong Y et al (2020) Molecular characterization of the gibberellin-stimulated transcript of GASA4 in citrus. Plant Growth Regul 91:89–99. https://doi.org/10.1007/s10725-020-00589-1
Wu T, Zhong Y, Chen M et al (2021) Analysis of CcGASA family members in Citrus clementina (Hort. ex Tan.) by a genome-wide approach. BMC Plant Biol 21:1–19. https://doi.org/10.1186/s12870-021-03326-6
Wu K, Qu Y, Rong H et al (2022a) Identification and expression analysis of the Populus trichocarpa GASA-gene family. Int J Mol Sci. https://doi.org/10.3390/ijms23031507
Wu Y, Sun Z, Qi F et al (2022b) Comprehensive analysis of GASA family members in the peanut genome: identification, characterization, and their expressions in response to pod development. Agronomy. https://doi.org/10.3390/agronomy12123067
**e Y, Zheng Y, Li H et al (2016) GPS-Lipid: a robust tool for the prediction of multiple lipid modification sites. Sci Rep 6:28249. https://doi.org/10.1038/srep28249
Xu X, Pan S, Cheng S et al (2011) Genome sequence and analysis of the tuber crop potato. Nature 475:189–195. https://doi.org/10.1038/nature10158
Xue Y, Chen H, ** C et al (2006) NBA-Palm: prediction of palmitoylation site implemented in Naïve Bayes algorithm. BMC Bioinformatics 7:458. https://doi.org/10.1186/1471-2105-7-458
Yang Q, Niu Q, Tang Y et al (2019) PpyGAST1 is potentially involved in bud dormancy release by integrating the GA biosynthesis and ABA signaling in ‘Suli’ pear (Pyrus pyrifolia White Pear Group). Environ Exp Bot 162:302–312. https://doi.org/10.1016/j.envexpbot.2019.03.008
Yeung H, Squire CJ, Yosaatmadja Y et al (2016) Radiation Damage and Racemic Protein Crystallography Reveal the Unique Structure of the GASA/Snakin Protein Superfamily. Angew Chemie - Int Ed 55:7930–7933. https://doi.org/10.1002/anie.201602719
Yu CS, Chen YC, Lu CH et al (2006) Prediction of protein subcellular localization. Proteins 64(3):643–651. https://doi.org/10.1002/prot.21018
Zhang S, Wang X (2017) One new kind of phytohormonal signaling integrator: Up-and-coming GASA family genes. Plant Signal Behav 12:1–6. https://doi.org/10.1080/15592324.2016.1226453
Zhang S, Yang C, Peng J et al (2009) GASA5, a regulator of flowering time and stem growth in Arabidopsis thaliana. Plant Mol Biol 69:745–759. https://doi.org/10.1007/s11103-009-9452-7
Zhang K, Hu Y, Yang D et al (2022a) Genome-wide identification of GASA gene family in ten cucurbitaceae species and expression analysis in cucumber. Agronomy. https://doi.org/10.3390/agronomy12081978
Zhang M, Cheng W, Wang J et al (2022b) Genome-wide identification, evolution, and expression analysis of GASA gene family in Prunus mume. Int J Mol Sci. https://doi.org/10.3390/ijms231810923
Zhang M, Wang Z, Jian S (2022c) Genome-wide identification and functional analysis of the GASA gene family responding to multiple stressors in Canavalia rosea. Genes. https://doi.org/10.3390/genes13111988
Acknowledgements
The authors thank Valeria Beracochea, Florencia Olivari, Laura Ramos, Matías Rodriguez, Ignacio Tevez, and Agustín Montenegro for their excellent technical assistance in the production and maintenance of transgenic potato plants. Microscopic analyses were performed at Laboratorio Integral de Microscopía, CICVyA, INTA.
Funding
This work was supported by PICT-2016-1444 from Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT) and by projects 2019-PD-E6-I116-001 and 2019-PD-E4-I085-001 from Instituto Nacional de Tecnología Agropecuaria (INTA).
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Nahirñak Vanesa participated in the design of the study, carried out the molecular techniques, and drafted the manuscript. Almasia Natalia Ines conducted experiments and helped to draft the manuscript. Lia Veronica Viviana contributed to data interpretation and contribute to writing the manuscript. Hopp Horacio Esteban assisted in the interpretation of the results and contributed to writing the manuscript revising it critically. Vazquez Rovere Cecilia conceived and coordinated the study, contributed to the work by the discussion of the data, and helped draft the manuscript. All authors read and approved the final manuscript.
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Nahirñak, V., Almasia, N.I., Lia, V.V. et al. Unveiling the defensive role of Snakin-3, a member of the subfamily III of Snakin/GASA peptides in potatoes. Plant Cell Rep 43, 47 (2024). https://doi.org/10.1007/s00299-023-03108-4
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DOI: https://doi.org/10.1007/s00299-023-03108-4