Transcriptome analysis of the allotetraploids of the Dilatata group of Paspalum (Poaceae): effects of diploidization on the expression of defensin and Snakin/GASA genes.
Genome rearrangements
Grasses
Plant AMPs
Poliploidy
Journal
Functional & integrative genomics
ISSN: 1438-7948
Titre abrégé: Funct Integr Genomics
Pays: Germany
ID NLM: 100939343
Informations de publication
Date de publication:
16 Oct 2024
16 Oct 2024
Historique:
received:
04
04
2024
accepted:
27
09
2024
revised:
27
09
2024
medline:
16
10
2024
pubmed:
16
10
2024
entrez:
16
10
2024
Statut:
epublish
Résumé
Plant Snakin/GASA and defensin peptides are cysteine-rich molecules with a wide range of biological functions. They are included within the large family of plant antimicrobial peptides (AMPs), characterized by their structural stability, broad spectrum of activity, and diverse mechanisms of action. The Dilatata group of Paspalum includes five allotetraploids that share an equivalent genomic formula IIJJ. From RNA-seq data of seedling tissues, we performed an in silico characterization of the defensin and Snakin/GASA genes in these species and diploids with a II and JJ genome formula and studied the evolutionary consequences of polyploidy on the expression of the two AMPs families. A total of 107 defensins (distributed in eight groups) and 145 Snakin/GASA (grouped in three subfamilies) genes were identified. Deletions, duplications and/or gene silencing seem to have mediated the evolution of these genes in the allotetraploid species. In defensin genes, the IIJJ allopolyploids retained the I subgenome defensin copies in some of the identified groups supporting the closeness of their nuclear genome with the I subgenome species. In both AMPs families, orthologous genes in tetraploids exhibit higher similarity to each other than with diploids. This data supports the theory of a single origin for the allotetraploids. Several copies of both defensin and Snakin/GASA genes were detected in the five polyploids which could have arisen due to duplication events occurring independently during the diploidization processes in the allotetraploid taxa.
Identifiants
pubmed: 39412676
doi: 10.1007/s10142-024-01466-0
pii: 10.1007/s10142-024-01466-0
doi:
Substances chimiques
Defensins
0
Plant Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
190Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Adams KL, Wendel JF (2005) Polyploidy and genome evolution in plants. Curr Opin Plant Biol 8:135–141. https://doi.org/10.1016/j.pbi.2005.01.001
doi: 10.1016/j.pbi.2005.01.001
pubmed: 15752992
Adams KL, Cronn R, Percifield R, Wendel JF (2003) Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. Proc Natl Acad Sci U S A 100:4649–4654. https://doi.org/10.1073/pnas.0630618100
doi: 10.1073/pnas.0630618100
pubmed: 12665616
pmcid: 153610
Apweiler R, Bairoch A, Wu CH, Barker WC, Boeckmann B, Ferro S, Gasteiger E, Huang H, Lopez R, Magrane M, Martin MJ, Natale DA, Donovan CO, Redaschi N, Yeh LL (2004) UniProt: the Universal protein knowledgebase. Nucleic Acids Res 32:D115–D119. https://doi.org/10.1093/nar/gkh131
doi: 10.1093/nar/gkh131
pubmed: 14681372
pmcid: 308865
Bakare OO, Gokul A, Fadaka AO, Wu R, Niekerk LA, Barker AM, Keyster M, Klein A (2022) Plant antimicrobial peptides (PAMPs): features, applications, production, expression and challenges. Molecules 27. https://doi.org/10.3390/molecules27123703
Benko-Iseppon AM, Galdino SL, Calsa T, Kido EA, Tossi A, Belarmino LC, Crovella S (2010) Overview on plant antimicrobial peptides. Curr Protein Pept Sci 11:181–188. https://doi.org/10.2174/138920310791112075
doi: 10.2174/138920310791112075
pubmed: 20088772
Berrocal-Lobo M, Segura A, Moreno M, López G, García-Olmedo F, Molina A (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.010685.1
doi: 10.1104/pp.010685.1
pubmed: 11891250
pmcid: 152207
Bird KA, Pires JC, Vanburen R, Xiong Z, Edger PP (2023) Dosage-sensitivity shapes how genes transcriptionally respond to allopolyploidy and homoeologous exchange in resynthesized Brassica napus. Genetics 225:1–14. https://doi.org/10.1093/genetics/iyad114
doi: 10.1093/genetics/iyad114
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioin 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
doi: 10.1093/bioinformatics/btu170
Bouteraa MT, Ben Romdhane W, Baazaoui N, Alfaifi MY, Chouaibi Y, Ben Akacha B, Ben Hsouna A, Kačániová M, Ćavar Zeljković S, Garzoli S, Ben Saad R (2023) GASA Proteins: review of their functions in Plant Environmental stress tolerance. Plants 12:1–16. https://doi.org/10.3390/plants12102045
doi: 10.3390/plants12102045
Broekaert WF, Terras FR, Cammue BP, Osborn RW (1995) Plant defensins: novel antimicrobial peptides as components of the host defense system. Plant Physiol 108:1353–1358. https://doi.org/10.1104/pp.108.4.1353
doi: 10.1104/pp.108.4.1353
pubmed: 7659744
pmcid: 157512
Burson BL (1983) Phylogenetic investigations of Paspalum dilatatum and related species. In ‘Proceedings of the XIV International GrasslandCongress’. pp. 170–173. (Westview Press: Boulder, CO, USA)
Campos ML, de Souza CM, de Oliveira KBS, Dias SC, Franco OL (2018) The role of antimicrobial peptides in plant immunity. J Exp Bot 69(21):4997–5011.
Carvalho DO, Gomes VM (2009) Peptides Plant defensins—prospects for the biological functions and biotechnological properties. Peptides 30:1007–1020. https://doi.org/10.1016/j.peptides.2009.01.018
doi: 10.1016/j.peptides.2009.01.018
pubmed: 19428780
Chase A (1929) North American species of Paspalum. Contributions from the US National Herbarium. Vol. 28 Part 1
Cheng F, Wu J, Cai X, Liang J, Freeling M, Wang X (2018) Gene retention, fractionation and subgenome differences in polyploid plants. Nat Plants 4(5):258–268
doi: 10.1038/s41477-018-0136-7
pubmed: 29725103
Cornet B, Bonmatin J, Hetru C, Hoffmann JA, Ptak M, Vovelle F (1995) Refined three-dimensional solution structure of insect defensin A. Structure 3:435–448
doi: 10.1016/S0969-2126(01)00177-0
pubmed: 7663941
De Coninck B, Cammue BPA, Thevissen K (2013) Modes of antifungal action and in planta functions of plant defensins and defensin-like peptides. Fungal Biol Rev 26:109–120. https://doi.org/10.1016/j.fbr.2012.10.002
doi: 10.1016/j.fbr.2012.10.002
Denham SS (2005) Revisión sistemática Del subgénero Harpostachys De Paspalum (Poaceae: Panicoideae: Paniceae). Ann Mo Bot Gard 92:463–532
Dong Y, Wang Y, Tang M, Chen W, Chai Y, Wang W (2023) Bioinformatic analysis of wheat defensin gene family and function verification of candidate genes. Front Plant Sci 14:1279502
doi: 10.3389/fpls.2023.1279502
pubmed: 37941661
pmcid: 10628452
Doyle J (1991) DNA protocols for plants-CTAB total DNA isolation. In: Molecular Techniques in Taxonomy. pp 283–293
Espinoza F, Quarin CL (2000) 2n + n hybridization of apomictic Paspalum dilatatum with diploid Paspalum species. IJPS 161:221–225. https://doi.org/10.1086/314250
doi: 10.1086/314250
pubmed: 10777445
Fan S, Zhang D, Zhang L, Gao C, Xin M, Tahir MM, Li Y, Ma J, Han M (2017) Comprehensive analysis of GASA family members in the Malus domestica genome: identification, characterization, and their expressions in response to apple flower induction. BMC Genomics 18:1–19. https://doi.org/10.1186/s12864-017-4213-5
doi: 10.1186/s12864-017-4213-5
Galdeano F, Urbani MH, Sartor ME, Honfi AI, Espinoza F, Quarin CL (2016) Relative DNA content in diploid, polyploid, and multiploid species of Paspalum (Poaceae) with relation to reproductive mode and taxonomy. J Plant Res 129(4):697–710.
Garewal N, Pathania S, Bhatia G, Singh K (2022) Identification of Pseudo-R genes in Vitis vinifera and characterization of their role as immunomodulators in host-pathogen interactions. J Adv Res 42:17–28. https://doi.org/10.1016/j.jare.2022.07.014
doi: 10.1016/j.jare.2022.07.014
pubmed: 35933092
pmcid: 9788958
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, Palma F, Birren BW, Nusbaum C, Lindblad-toh K, Friedman N, Regev A (2013) Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nat Biotechnol 29:644–652. https://doi.org/10.1038/nbt.1883.Trinity
doi: 10.1038/nbt.1883.Trinity
Hall TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Kovaleva V, Bukhteeva I, Kit OY, Nesmelova IV (2020) Plant defensins from a structural perspective. Int J Mol Sci 21:1–23. https://doi.org/10.3390/ijms21155307
doi: 10.3390/ijms21155307
Lay FT, Anderson MA (2005) Defensins-components of the innate immune system in plants. Curr Protein Pept Sci 6:85–101. https://doi.org/10.2174/1389203053027575
doi: 10.2174/1389203053027575
pubmed: 15638771
Lay FT, Poon S, McKenna JA, Connelly AA, Barbeta BL, McGinness BS, Fox JL, Daly NL, Craik DJ, Heath RL, Anderson MA (2014) The C-terminal propeptide of a plant defensin confers cytoprotective and subcellular targeting functions. BMC Plant Biol 14:1–13. https://doi.org/10.1186/1471-2229-14-41
doi: 10.1186/1471-2229-14-41
Li Z, Gao J, Wang G, Wang S, Chen K, Pu W, Wang Y, Xia Q, Fan X (2022) 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
doi: 10.3389/fgene.2021.768942
Nahirñak V, Almasia NI, Hopp HE, Vazquez-Rovere C (2012) Involvement in hormone crosstalk and redox homeostasis Snakin/GASA proteins. Plant Signal Behav 7:1004–1008
doi: 10.4161/psb.20813
pubmed: 22836500
pmcid: 3474668
Nahirñak V, Rivarola M, Gonzalez de Urreta M, Paniego N, Hopp HE, Almasia NI, Vazquez-Rovere C (2016) Genome-wide analysis of the Snakin/GASA gene family in Solanum tuberosum Cv. Kennebec. Am J Potato Res doi. https://doi.org/10.1007/s12230-016-9494-8
doi: 10.1007/s12230-016-9494-8
Nawrot R, Baryiski J, Nowicki G, Justyna B, Buchwald W, Gozdzicka-Jozefiak A (2014) Plant antimicrobial peptides. Folia Microbiol (Praha) 59:181–196. https://doi.org/10.1007/978-3-319-32949-9_5
doi: 10.1007/978-3-319-32949-9_5
pubmed: 24092498
Nielsen H (2017) Predicting secretory proteins with SignalP. In: D. K (ed) Methods in Molecular Biology. New York, pp 59–73
Odintsova T, Egorov T (2012) Plant Antimicrobial Peptides. In: Gehring HRI and C (ed) Plant Signaling peptides. Berlín, pp 107–133
Odintsova TI, Korostyleva TV, Odintsova MS, Pukhalsky VA, Grishin EV, Egorov TA (2008) Analysis of Triticum boeoticum and Triticum urartu seed defensins: to the problem of the origin of polyploid wheat genomes. Biochimie 90(6):939–946
doi: 10.1016/j.biochi.2008.02.023
pubmed: 18358845
Odintsova TI, Slezina MP, Istomina EA, Korostyleva TV, Kasianov AS, Kovtun AS, Kudryavtsev AM (2019) Defensin-like peptides in wheat analyzed by whole-transcriptome sequencing: a focus on structural diversity and role in induced resistance. PeerJ 7:e6125
Odintsova TI, Slezina MP, Istomina EA (2020) Defensins of grasses: a systematic review. Biomolecules 10:1–40. https://doi.org/10.3390/biom10071029
Oliveira-Lima M, Benko-Iseppon AM, Neto JRCF, Rodríguez-Decuadro S, Kido EA, Crovella S, Pandolfi V (2017) Snakin: structure, roles and applications of a plant antimicrobial peptide. Curr Protein Pept Sci 18. https://doi.org/10.2174/1389203717666160619183140
Rodríguez-Decuadro S, da Rosa G, Radío S, Barraco-Vega M, Benko-Iseppon AM, Dans PD, Smircich P, Cecchetto G (2021) Antimicrobial peptides in the seedling transcriptome of the tree legume Peltophorum dubium. Biochimie 180:229–242. https://doi.org/10.1016/j.biochi.2020.11.005
doi: 10.1016/j.biochi.2020.11.005
pubmed: 33197551
Rosso VC, Valls JF, Quarin CL, Speranza PR, Rua GH (2022) New entities of Paspalum and a synopsis of the Dilatata Group. Syst Bot 21:125–139. https://doi.org/10.1600/036364422X16442668423437
doi: 10.1600/036364422X16442668423437
Rua GH, Speranza P, Vaio M, Arakaki M (2010) A phylogenetic analysis of the genus Paspalum (Poaceae) based on cpDNA and morphology. Pl Syst Evol 288:227–243. https://doi.org/10.1007/s00606-010-0327-9
doi: 10.1007/s00606-010-0327-9
Segura A, Moreno M, Madueño F, Molina A, García-Olmedo F (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
Shafee TMA, Lay FT, Phan TK, Anderson MA, Hulett MD (2017) Convergent evolution of defensin sequence, structure and function. Cell Mol Life Sci 74:663–682. https://doi.org/10.1007/s00018-016-2344-5
doi: 10.1007/s00018-016-2344-5
pubmed: 27557668
Shenton MR, Ohyanagi H, Wang ZX, Toyoda A, Fujiyama A, Nagata T, Feng Q, Han B, Kurata N (2015) Rapid turnover of antimicrobial-type cysteine-rich protein genes in closely related Oryza genomes. Mol Genet Genomics 290:1753–1770. https://doi.org/10.1007/s00438-015-1028-4
doi: 10.1007/s00438-015-1028-4
pubmed: 25842177
Silverstein Ka, T, Graham M, a, Paape TD, VandenBosch Ka (2005) Genome organization of more than 300 defensin-like genes in Arabidopsis. Plant Physiol 138:600–610. https://doi.org/10.1104/pp.105.060079
doi: 10.1104/pp.105.060079
pubmed: 15955924
pmcid: 1150381
Slavokhotova AA, Shelenkov AA, Korostyleva TV, Rogozhin EA, Melnikova NV, Kudryavtseva AV, Odintsova TI (2017) Defense peptide repertoire of Stellaria media predicted by high throughput next generation sequencing. Biochimie 135:15–27. https://doi.org/10.1016/j.biochi.2016.12.017
doi: 10.1016/j.biochi.2016.12.017
pubmed: 28038935
Soltis DE, Visger CJ, Blaine Marchant D, Soltis PS (2016) Polyploidy: pitfalls and paths to a paradigm. Am J Bot 103:1146–1166. https://doi.org/10.3732/ajb.1500501
doi: 10.3732/ajb.1500501
pubmed: 27234228
Speranza PR (2009) Evolutionary patterns in the Dilatata group (Paspalum. Poaceae) Syst Bot 282:43–56. https://doi.org/10.1007/s00606-009-0205-5
doi: 10.1007/s00606-009-0205-5
Su D, Liu K, Yu Z, Li Y, Zhang Y, Zhu Y, Wu Y, He H, Zeng X, Chen H, Grierson D, Deng H, Liu M (2023) Genome-wide characterization of the tomato GASA family identifies SlGASA1 as a repressor of fruit ripening. Hortic Res 10. https://doi.org/10.1093/hr/uhac222
Sun J, Lu F, Luo Y, Bie L, Xu L, Wang Y (2023) OrthoVenn3: an integrated platform for exploring and visualizing orthologous data across genomes. Nucleic Acids Res 51(W1):W397–W403. https://doi.org/10.1093/nar/gkad313
doi: 10.1093/nar/gkad313
pubmed: 37114999
pmcid: 10320085
Sun B, Zhao X, Gao J, Li J, Xin Y, Zhao Y, Liu Z, Feng H, Tan C (2023a) Genome-wide identification and expression analysis of the GASA gene family in Chinese cabbage (Brassica rapa L. ssp. pekinensis). BMC Genomics 24:1–15. https://doi.org/10.1186/s12864-023-09773-9
doi: 10.1186/s12864-023-09773-9
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony methods Research resource. Mol Biol Evol 28:2731–2739. https://doi.org/10.1093/molbev/msr121
doi: 10.1093/molbev/msr121
pubmed: 21546353
pmcid: 3203626
Thomma BPHJ, Cammue BPA, Thevissen K (2002) Plant defensins. Planta 216:193–202. https://doi.org/10.1007/s00425-002-0902-6
doi: 10.1007/s00425-002-0902-6
pubmed: 12447532
Vaio M, Mazzella C, Porro V, Speranza P, López-Carro B, Estramil E, Folle GA (2007) Nuclear DNA content in allopolyploid species and synthetic hybrids in the grass genus Paspalum. Plant Syst Evol 265:109–121. https://doi.org/10.1007/s00606-006-0506-x
doi: 10.1007/s00606-006-0506-x
Vaio M, Mazzella C, Guerra M, Speranza P (2019) Effects of the diploidisation process upon the 5S and 35S rDNA sequences in the allopolyploid species of the Dilatata group of Paspalum (Poaceae, Paniceae). Aust J Bot 67:521–530. https://doi.org/10.1071/BT18236
Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ (2009) Jalview Version 2 — a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189–1191. https://doi.org/10.1093/bioinformatics/btp033
doi: 10.1093/bioinformatics/btp033
pubmed: 19151095
pmcid: 2672624
Wei Y, Li G, Zhang S, Zhang S, Zhang H, Sun R, Zhang R, Li F (2021) Analysis of transcriptional changes in different Brassica napus synthetic allopolyploids. Genes (Basel) 12:1–15. https://doi.org/10.3390/genes12010082
doi: 10.3390/genes12010082
Wu J, Jin X, Zhao Y, Dong Q, Jiang H, Ma Q (2016) Evolution of the defensin-like gene family in grass genomes. J Genet 95:53–62. https://doi.org/10.1007/s12041-015-0601-2
doi: 10.1007/s12041-015-0601-2
pubmed: 27019432
Yoo MJ, Liu X, Pires JC, Soltis PS, Soltis DE (2014) Nonadditive gene expression in polyploids. Annu Rev Genet 48:485–517. https://doi.org/10.1146/annurev-genet-120213-092159
doi: 10.1146/annurev-genet-120213-092159
pubmed: 25421600
Yount NY, Yeaman MR (2004) Multidimensional signatures in antimicrobial peptides. Proc Natl Acad Sci 101:7363–7368. https://doi.org/10.1073/pnas.0401567101
doi: 10.1073/pnas.0401567101
pubmed: 15118082
pmcid: 409924
Zhang D, Wnag B, Dong L, Wang D, Zhao J, Zhao X, Mao L, Li A (2015) Divergence in homoeolog expression of the grain length-associated gene GASR7 during wheat allohexaploidization. Crop J 3:1–9. https://doi.org/10.1016/j.cj.2014.08.005
doi: 10.1016/j.cj.2014.08.005
Zou C, Lehti-shiu MD, Prakash T (2009) Evolutionary and expression signatures of Pseudogenes. Plant Physiol 151:3–15. https://doi.org/10.1104/pp.109.140632
doi: 10.1104/pp.109.140632
pubmed: 19641029
pmcid: 2736005
Zuloaga F, Morrone O (2005) Revisión De las especies de Paspalum para América Del Sur Austral (Argentina, Bolivia, sur del Brasil, Chile, Paraguay y Uruguay). Monogr Syst Bot Miss Bot Gard 102:1–297