دورية أكاديمية
Genome-wide identification of Ankyrin (ANK) repeat gene families in three Dendrobium species and the expression of ANK genes in D. officinale under gibberellin and abscisic acid treatments.
| العنوان: | Genome-wide identification of Ankyrin (ANK) repeat gene families in three Dendrobium species and the expression of ANK genes in D. officinale under gibberellin and abscisic acid treatments. |
|---|---|
| المؤلفون: | Li L; College of Life Sciences, Nanjing Normal University, Nanjing, 210023, China.; Jiangsu Provincial Engineering Research Center for Technical Industrialization of Dendrobiums, Nanjing, China., Yang J; College of Life Sciences, Nanjing Normal University, Nanjing, 210023, China.; Jiangsu Provincial Engineering Research Center for Technical Industrialization of Dendrobiums, Nanjing, China., Zhang Q; College of Life Sciences, Nanjing Normal University, Nanjing, 210023, China.; Jiangsu Provincial Engineering Research Center for Technical Industrialization of Dendrobiums, Nanjing, China., Xue Q; College of Life Sciences, Nanjing Normal University, Nanjing, 210023, China.; Jiangsu Provincial Engineering Research Center for Technical Industrialization of Dendrobiums, Nanjing, China., Li M; College of Life Sciences, Nanjing Normal University, Nanjing, 210023, China.; Jiangsu Provincial Engineering Research Center for Technical Industrialization of Dendrobiums, Nanjing, China., Xue Q; College of Life Sciences, Nanjing Normal University, Nanjing, 210023, China.; Jiangsu Provincial Engineering Research Center for Technical Industrialization of Dendrobiums, Nanjing, China., Liu W; College of Life Sciences, Nanjing Normal University, Nanjing, 210023, China.; Jiangsu Provincial Engineering Research Center for Technical Industrialization of Dendrobiums, Nanjing, China., Niu Z; College of Life Sciences, Nanjing Normal University, Nanjing, 210023, China.; Jiangsu Provincial Engineering Research Center for Technical Industrialization of Dendrobiums, Nanjing, China., Ding X; College of Life Sciences, Nanjing Normal University, Nanjing, 210023, China. dingxynj@263.net.; Jiangsu Provincial Engineering Research Center for Technical Industrialization of Dendrobiums, Nanjing, China. dingxynj@263.net. |
| المصدر: | BMC plant biology [BMC Plant Biol] 2024 Aug 10; Vol. 24 (1), pp. 762. Date of Electronic Publication: 2024 Aug 10. |
| نوع المنشور: | Journal Article |
| اللغة: | English |
| بيانات الدورية: | Publisher: BioMed Central Country of Publication: England NLM ID: 100967807 Publication Model: Electronic Cited Medium: Internet ISSN: 1471-2229 (Electronic) Linking ISSN: 14712229 NLM ISO Abbreviation: BMC Plant Biol Subsets: MEDLINE |
| أسماء مطبوعة: | Original Publication: London : BioMed Central, [2001- |
| مواضيع طبية MeSH: | Dendrobium*/genetics , Dendrobium*/drug effects , Abscisic Acid*/pharmacology , Abscisic Acid*/metabolism , Phylogeny* , Gibberellins*/pharmacology , Gibberellins*/metabolism , Multigene Family* , Plant Growth Regulators*/pharmacology , Plant Growth Regulators*/metabolism, Ankyrin Repeat/genetics ; Gene Expression Regulation, Plant ; Plant Proteins/genetics ; Plant Proteins/metabolism ; Genes, Plant ; Genome, Plant ; Gene Expression Profiling |
| مستخلص: | Background: Dendrobium Sw. represents one of the most expansive genera within the Orchidaceae family, renowned for its species' high medicinal and ornamental value. In higher plants, the ankyrin (ANK) repeat protein family is characterized by a unique ANK repeat domain, integral to a plethora of biological functions and biochemical activities. The ANK gene family plays a pivotal role in various plant physiological processes, including stress responses, hormone signaling, and growth. Hence, investigating the ANK gene family and identifying disease-resistance genes in Dendrobium is of paramount importance. Results: This research identified 78 ANK genes in Dendrobium officinale Kimura et Migo, 77 in Dendrobium nobile Lindl., and 58 in Dendrobium chrysotoxum Lindl. Subsequently, we conducted comprehensive bioinformatics analyses on these ANK gene families, encompassing gene classification, chromosomal localization, phylogenetic relationships, gene structure and motif characterization, cis-acting regulatory element identification, collinearity assessment, protein-protein interaction network construction, and gene expression profiling. Concurrently, three DoANK genes (DoANK14, DoANK19, and DoANK47) in D. officinale were discerned to indirectly activate the NPR1 transcription factor in the ETI system via SA, thereby modulating the expression of the antibacterial PR gene. Hormonal treatments with GA Conclusion: Our findings provide a robust framework for the taxonomic classification, evolutionary analysis, and functional prediction of Dendrobium ANK genes. The three highlighted ANK genes (DoANK14, DoANK19, and DoANK47) from D. officinale may prove valuable in disease resistance and stress response research. DoANK32 is implicated in the morphogenesis and development of D. officinale through its role in vesicular transport and auxin polarity, with subcellular localization studies confirming its presence in the nucleus and cell membrane. ANK genes displaying significant expression changes in response to hormonal treatments could play a crucial role in the hormonal response of D. officinale, potentially inhibiting its growth and development through the modulation of plant hormones such as GA (© 2024. The Author(s).) |
| References: | Xiang XG, Schuiteman A, Li DZ, Huang WC, Chung SW, Li JW, Zhou HL, Jin WT, Lai YJ, Li ZY, Jin XH. Molecular systematics of Dendrobium (Orchidaceae, Dendrobieae) from mainland Asia based on plastid and nuclear sequences. Mol Phylogenet Evol. 2013;69(3):950–60. (PMID: 2381143510.1016/j.ympev.2013.06.009) Liu JJ, Liu ZP, Zhang XF, Si JP. Effects of various processing methods on the metabolic profile and antioxidant activity of Dendrobium Catenatum Lindley leaves. Metabolites. 2021;11(6):351. (PMID: 34070913822959810.3390/metabo11060351) Sedgwick SG, Smerdon SJ. The ankyrin repeat: a diversity of interactions on a common structural framework. Trends Biochem Sci. 1999;24(8):311–6. (PMID: 1043117510.1016/S0968-0004(99)01426-7) Breeden L, Nasmyth K. Similarity between cell-cycle genes of budding yeast and fission yeast and the notch gene of Drosophila. Nature. 1987;329(6140):651–4. (PMID: 282140810.1038/329651a0) Bae W, Lee YJ, Kim DH, Lee J, Kim S, Sohn EJ, Hwang I. AKR2A-mediated import of chloroplast outer membrane proteins is essential for chloroplast biogenesis. Nat Cell Biol. 2008;10(2):220–7. (PMID: 1819303410.1038/ncb1683) Seong ES, Cho HS, Choi D, Joung YH, Lim CK, Hur JH, Wang MH. Tomato plants overexpressing CaKR1 enhanced tolerance to salt and oxidative stress. Biochem Biophys Res Commun. 2007;363(4):983–8. (PMID: 1792796310.1016/j.bbrc.2007.09.104) Yan J, Wang J, Zhang H. An ankyrin repeat-containing protein plays a role in both disease resistance and antioxidation metabolism. Plant J. 2002;29(2):193–202. (PMID: 1186294810.1046/j.0960-7412.2001.01205.x) Cao H, Glazebrook J, Clarke JD, Volko S, Dong X. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell. 1997;88(1):57–63. (PMID: 901940610.1016/S0092-8674(00)81858-9) Niu Z, Zhu F, Fan Y, Li C, Zhang B, Zhu S, Hou Z, Wang M, Yang J, Xue Q, Liu W, Ding X. The chromosome-level reference genome assembly for Dendrobium officinale and its utility of functional genomics research and molecular breeding study. Acta Pharm Sin B. 2021;11(7):2080–92. (PMID: 34386340834311010.1016/j.apsb.2021.01.019) Xu Q, Niu SC, Li KL, Zheng PJ, Zhang XJ, Jia Y, Liu Y, Niu YX, Yu LH, Chen DF, Zhang GQ. Chromosome-scale assembly of the Dendrobium nobile genome provides insights into the molecular mechanism of the biosynthesis of the medicinal active ingredient of Dendrobium. Front Genet. 2022;13:844622. (PMID: 35299950892153110.3389/fgene.2022.844622) Zhang Y, Zhang GQ, Zhang D, Liu XD, Xu XY, Sun WH, Yu X, Zhu X, Wang ZW, Zhao X, Zhong WY, Chen H, Yin WL, Huang T, Niu SC, Liu ZJ. Chromosome-scale assembly of the Dendrobium chrysotoxum genome enhances the understanding of orchid evolution. Hortic Res. 2021;8(1):183. (PMID: 34465765840824410.1038/s41438-021-00621-z) Koonin EV, Rogozin IB. Getting positive about selection. Genome Biol. 2003;4(8):331. (PMID: 1291465419363810.1186/gb-2003-4-8-331) Zhang H, Scheirer DC, Fowle WH, Goodman HM. Expression of antisense or sense RNA of an ankyrin repeat-containing gene blocks chloroplast differentiation in Arabidopsis. Plant Cell. 1992;4(12):1575–88. (PMID: 1281700160243) Albert S, Després B, Guilleminot J, Bechtold N, Pelletier G, Delseny M, Devic M. The EMB 506 gene encodes a novel ankyrin repeat containing protein that is essential for the normal development of Arabidopsis embryos. Plant J. 1999;17(2):169–79. (PMID: 1007471410.1046/j.1365-313X.1999.00361.x) Hemsley PA, Kemp AC, Grierson CS. The TIP GROWTH DEFECTIVE1 S-acyl transferase regulates plant cell growth in Arabidopsis. Plant Cell. 2005;17(9):2554–63. (PMID: 16100337119743410.1105/tpc.105.031237) Garcion C, Guilleminot J, Kroj T, Parcy F, Giraudat J, Devic M. AKRP and EMB506 are two ankyrin repeat proteins essential for plastid differentiation and plant development in Arabidopsis. Plant J. 2006;48(6):895–906. (PMID: 1709231210.1111/j.1365-313X.2006.02922.x) Huang J, Chen F, Del Casino C, Autino A, Shen M, Yuan S, Peng J, Shi H, Wang C, Cresti M, Li Y. An ankyrin repeat-containing protein, characterized as a ubiquitin ligase, is closely associated with membrane-enclosed organelles and required for pollen germination and pollen tube growth in lily. Plant Physiol. 2006;140(4):1374–83. (PMID: 16461387143581210.1104/pp.105.074922) Lu H, Rate DN, Song JT, Greenberg JT. ACD6, a novel ankyrin protein, is a regulator and an effector of salicylic acid signaling in the Arabidopsis defense response. Plant Cell. 2003;15(10):2408–20. (PMID: 1450799919730510.1105/tpc.015412) Lu H, Liu Y, Greenberg JT. Structure-function analysis of the plasma membrane- localized Arabidopsis defense component ACD6. Plant J. 2005;44(5):798–809. (PMID: 1629707110.1111/j.1365-313X.2005.02567.x) Nodzon LA, Xu WH, Wang Y, Pi LY, Chakrabarty PK, Song WY. The ubiquitin ligase XBAT32 regulates lateral root development in Arabidopsis. Plant J. 2004;40(6):996–1006. (PMID: 1558496310.1111/j.1365-313X.2004.02266.x) Becerra C, Jahrmann T, Puigdomènech P, Vicient CM. Ankyrin repeat-containing proteins in Arabidopsis: characterization of a novel and abundant group of genes coding ankyrin-transmembrane proteins. Gene. 2004;340(1):111–21. (PMID: 1555629910.1016/j.gene.2004.06.006) Huang J, Zhao X, Yu H, Ouyang Y, Wang L, Zhang Q. The ankyrin repeat gene family in rice: genome-wide identification, classification and expression profiling. Plant Mol Biol. 2009;71(3):207–26. (PMID: 1960968510.1007/s11103-009-9518-6) Moore RC, Purugganan MD. The early stages of duplicate gene evolution. Proc Natl Acad Sci USA. 2003;100(26):15682–7. (PMID: 1467132330762810.1073/pnas.2535513100) Cannon SB, Mitra A, Baumgarten A, Young ND, May G. The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol. 2004;4:10. (PMID: 1517179444619510.1186/1471-2229-4-10) Han GZ. Origin and evolution of the plant immune system. New Phytol. 2019;222(1):70–83. (PMID: 3057597210.1111/nph.15596) Spoel SH, Dong X. How do plants achieve immunity? Defence without specialized immune cells. Nat Rev Immunol. 2012;12(2):89–100. (PMID: 2227377110.1038/nri3141) Zipfel C. Plant pattern-recognition receptors. Trends Immunol. 2014;35(7):345–51. (PMID: 2494668610.1016/j.it.2014.05.004) Dangl JL, Horvath DM, Staskawicz BJ. Pivoting the plant immune system from dissection to deployment. Science. 2013;341(6147):746–51. (PMID: 2395053110.1126/science.1236011) Césari S, Kanzaki H, Fujiwara T, Bernoux M, Chalvon V, Kawano Y, Shimamoto K, Dodds P, Terauchi R, Kroj T. The NB-LRR proteins RGA4 and RGA5 interact functionally and physically to confer disease resistance. EMBO J. 2014;33(17):1941–59. (PMID: 25024433419578810.15252/embj.201487923) Luo S, Peng J, Li K, Wang M, Kuang H. Contrasting evolutionary patterns of the Rp1 resistance gene family in different species of Poaceae. Mol Biol Evol. 2011;28(1):313–25. (PMID: 2071346910.1093/molbev/msq216) Song W, Wang B, Li X, Wei J, Chen L, Zhang D, Zhang W, Li R. Identification of immune related LRR-Containing genes in maize (Zea mays L.) by genome-wide sequence analysis. Int J Genomics. 2015;2015:231358. (PMID: 26609518464548810.1155/2015/231358) Yang X, Wang J. Genome-wide analysis of NBS-LRR genes in sorghum genome revealed several events contributing to NBS-LRR gene evolution in grass species. Evol Bioinform Online. 2016;12:9–21. (PMID: 26792976471465210.4137/EBO.S36433) Shao ZQ, Xue JY, Wu P, Zhang YM, Wu Y, Hang YY, Wang B, Chen JQ. Large-scale analyses of angiosperm nucleotide-binding site-leucine-rich repeat genes reveal three anciently diverged classes with distinct evolutionary patterns. Plant Physiol. 2016;170(4):2095–109. (PMID: 26839128482515210.1104/pp.15.01487) Bruggeman Q, Raynaud C, Benhamed M, Delarue M. To die or not to die? Lessons from lesion mimic mutants. Front Plant Sci. 2015;6:24. (PMID: 25688254431161110.3389/fpls.2015.00024) Musetti R, Buxa SV, De Marco F, Loschi A, Polizzotto R, Kogel KH, van Bel AJ. Phytoplasma-triggered ca(2+) influx is involved in sieve-tube blockage. Mol Plant Microbe Interact. 2013;26(4):379–86. (PMID: 2323440510.1094/MPMI-08-12-0207-R) Wang L, Liu S, Gao M, Wang L, Wang L, Wang Y, Dai L, Zhao J, Liu M, Liu Z. The crosstalk of the salicylic acid and jasmonic acid signaling pathways contributed to different resistance to phytoplasma infection between the two genotypes in Chinese jujube. Front Microbiol. 2022;13:800762. (PMID: 35369447897199410.3389/fmicb.2022.800762) Verhage A, van Wees SC, Pieterse CM. Plant immunity: it’s the hormones talking, but what do they say? Plant Physiol. 2010;154(2):536–40. (PMID: 20921180294903910.1104/pp.110.161570) Clarke SM, Mur LA, Wood JE, Scott IM. Salicylic acid dependent signaling promotes basal thermotolerance but is not essential for acquired thermotolerance in Arabidopsis thaliana. Plant J. 2004;38(3):432–47. (PMID: 1508680410.1111/j.1365-313X.2004.02054.x) Olate E, Jiménez-Gómez JM, Holuigue L, Salinas J. NPR1 mediates a novel regulatory pathway in cold acclimation by interacting with HSFA1 factors. Nat Plants. 2018;4(10):811–23. (PMID: 3025028010.1038/s41477-018-0254-2) Zhang FJ, Xie YH, Jiang H, Wang X, Hao YJ, Zhang Z, You CX. The ankyrin repeat-containing protein MdANK2B regulates salt tolerance and ABA sensitivity in Malus domestica. Plant Cell Rep. 2021;40(2):405–19. (PMID: 3333195310.1007/s00299-020-02642-9) Lopez-Ortiz C, Peña-Garcia Y, Natarajan P, Bhandari M, Abburi V, Dutta SK, Yadav L, Stommel J, Nimmakayala P, Reddy UK. The ankyrin repeat gene family in Capsicum spp: genome-wide survey, characterization and gene expression profile. Sci Rep. 2020;10(1):4044. (PMID: 32132613705528710.1038/s41598-020-61057-4) Yuan X, Zhang S, Liu S, Yu M, Su H, Shu H, Li X. Global analysis of ankyrin repeat domain C3HC4-type RING finger gene family in plants. PLoS ONE. 2013;8(3):e58003. (PMID: 23516424359633110.1371/journal.pone.0058003) Stone SL, Williams LA, Farmer LM, Vierstra RD, Callis J. KEEP ON GOING, a RING E3 ligase essential for Arabidopsis growth and development, is involved in abscisic acid signaling. Plant Cell. 2006;18(12):3415–28. (PMID: 17194765178541410.1105/tpc.106.046532) Loreti E, Povero G, Novi G, Solfanelli C, Alpi A, Perata P. Gibberellins, jasmonate and abscisic acid modulate the sucrose-induced expression of anthocyanin biosynthetic genes in Arabidopsis. New Phytol. 2008;179(4):1004–16. (PMID: 1853789010.1111/j.1469-8137.2008.02511.x) Zhang J, Cheng K, Liu X, Dai Z, Zheng L, Wang Y. Exogenous abscisic acid and sodium nitroprusside regulate flavonoid biosynthesis and photosynthesis of Nitraria Tangutorum Bobr in alkali stress. Front Plant Sci. 2023;14:1118984. (PMID: 370085021005712010.3389/fpls.2023.1118984) Sohn SI, Pandian S, Rakkammal K, Largia MJV, Thamilarasan SK, Balaji S, Zoclanclounon YAB, Shilpha J, Ramesh M. Jasmonates in plant growth and development and elicitation of secondary metabolites: an updated overview. Front Plant Sci. 2022;13:942789. (PMID: 36035665940763610.3389/fpls.2022.942789) Berli FJ, Moreno D, Piccoli P, Hespanhol-Viana L, Silva MF, Bressan-Smith R, Cavagnaro JB, Bottini R. Abscisic acid is involved in the response of grape (Vitis vinifera L.) cv. Malbec leaf tissues to ultraviolet-B radiation by enhancing ultraviolet-absorbing compounds, antioxidant enzymes and membrane sterols. Plant Cell Environ. 2010;33(1):1–10. (PMID: 19781012) Du C, Chong K. ARF-GTPase activating protein mediates auxin influx carrier AUX1 early endosome trafficking to regulate auxin dependent plant development. Plant Signal Behav. 2011;6(11):1644–6. (PMID: 22057332332932510.4161/psb.6.11.17755) Zhuang X, Jiang J, Li J, Ma Q, Xu Y, Xue Y, Xu Z, Chong K. Over-expression of OsAGAP, an ARF-GAP, interferes with auxin influx, vesicle trafficking and root development. Plant J. 2006;48(4):581–91. (PMID: 1705940710.1111/j.1365-313X.2006.02898.x) Chong K, Zhuang X. ARF-GTPase as a molecular switch for polar auxin transport mediated by vesicle trafficking in root development. Plant Signal Behav. 2007;2(2):101–2. (PMID: 19704748263390710.4161/psb.2.2.3615) Naramoto S, Kyozuka J. ARF GTPase machinery at the plasma membrane regulates auxin transport-mediated plant growth. Plant Biotechnol (Tokyo). 2018;35(2):155–9. (PMID: 3181971710.5511/plantbiotechnology.18.0312a) Koizumi K, Naramoto S, Sawa S, Yahara N, Ueda T, Nakano A, Sugiyama M, Fukuda H. VAN3 ARF-GAP-mediated vesicle transport is involved in leaf vascular network formation. Development. 2005;132(7):1699–711. (PMID: 1574387810.1242/dev.01716) Song XF, Yang CY, Liu J, Yang WC. RPA, a class II ARFGAP protein, activates ARF1 and U5 and plays a role in root hair development in Arabidopsis. Plant Physiol. 2006;141(3):966–76. (PMID: 16731582148991710.1104/pp.106.077818) Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Williams KL, Appel RD, Hochstrasser DF. Protein identification and analysis tools in the ExPASy server. Methods Mol Biol. 1999;112:531–52. (PMID: 10027275) Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant. 2020;13(8):1194–202. (PMID: 3258519010.1016/j.molp.2020.06.009) Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. Clustal W and Clustal X version 2.0. Bioinformatics. 2007;23(21):2947–8. (PMID: 1784603610.1093/bioinformatics/btm404) Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35(6):1547–9. (PMID: 29722887596755310.1093/molbev/msy096) Wang D, Zhang Y, Zhang Z, Zhu J, Yu J. KaKs_Calculator 2.0: a toolkit incorporating gamma-series methods and sliding window strategies. Genomics Proteom Bioinf. 2010;8(1):77–80. (PMID: 10.1016/S1672-0229(10)60008-3) Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13(11):2498–504. (PMID: 1459765840376910.1101/gr.1239303) Love MI, Huber W, Anders S. Moderated estimation of Fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15(12):550. (PMID: 25516281430204910.1186/s13059-014-0550-8) Varet H, Brillet-Guéguen L, Coppée JY, Dillies MA, SARTools:. A DESeq2- and EdgeR-based R pipeline for comprehensive differential analysis of RNA-seq data. PLoS ONE. 2016;11(6):e0157022. (PMID: 27280887490064510.1371/journal.pone.0157022) Yu G, Wang LG, Han Y, He QY. clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS. 2012;16(5):284–7. (PMID: 22455463333937910.1089/omi.2011.0118) Chen Z, Yuan Y, Fu D, Shen C, Yang Y. Identification and expression profiling of the auxin response factors in Dendrobium officinale under abiotic stresses. Int J Mol Sci. 2017;18(5):927. (PMID: 28471373545484010.3390/ijms18050927) Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25(4):402–8. (PMID: 1184660910.1006/meth.2001.1262) Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics. 2008;9:559. (PMID: 19114008263148810.1186/1471-2105-9-559) |
| معلومات مُعتمدة: | 32070353 National Natural Science Foundation of China; LYKJ[2021]12 Forestry Science and Technology Innovation and Promotion Project of Jiangsu Province; CX(22)3147 Agricultural Science and Technology Independent Innovation Fund Project of Jiangsu Province |
| فهرسة مساهمة: | Keywords: Dendrobium; Ankyrin repeat gene family; Function genes screening; Genome-wide analysis |
| المشرفين على المادة: | 72S9A8J5GW (Abscisic Acid) 0 (Gibberellins) 0 (Plant Growth Regulators) 0 (Plant Proteins) |
| تواريخ الأحداث: | Date Created: 20240809 Date Completed: 20240809 Latest Revision: 20240809 |
| رمز التحديث: | 20240812 |
| DOI: | 10.1186/s12870-024-05461-2 |
| PMID: | 39123107 |
| قاعدة البيانات: | MEDLINE |
Find this article in full text from Springer Verlag. 
Full Text Finder | تدمد: | 1471-2229 |
|---|---|
| DOI: | 10.1186/s12870-024-05461-2 |