Genome-wide identification and expression analysis of the Eriobotrya japonica TIFY gene family reveals its functional diversity under abiotic stress conditions.
TIFY gene family
Abiotic stress
Evolution
Expression profile
Loquat
Journal
BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258
Informations de publication
Date de publication:
14 May 2024
14 May 2024
Historique:
received:
06
02
2024
accepted:
03
05
2024
medline:
15
5
2024
pubmed:
15
5
2024
entrez:
14
5
2024
Statut:
epublish
Résumé
Plant-specific TIFY proteins are widely found in terrestrial plants and play important roles in plant adversity responses. Although the genome of loquat at the chromosome level has been published, studies on the TIFY family in loquat are lacking. Therefore, the EjTIFY gene family was bioinformatically analyzed by constructing a phylogenetic tree, chromosomal localization, gene structure, and adversity expression profiling in this study. Twenty-six EjTIFY genes were identified and categorized into four subfamilies (ZML, JAZ, PPD, and TIFY) based on their structural domains. Twenty-four EjTIFY genes were irregularly distributed on 11 of the 17 chromosomes, and the remaining two genes were distributed in fragments. We identified 15 covariate TIFY gene pairs in the loquat genome, 13 of which were involved in large-scale interchromosomal segmental duplication events, and two of which were involved in tandem duplication events. Many abiotic stress cis-elements were widely present in the promoter region. Analysis of the Ka/Ks ratio showed that the paralogous homologs of the EjTIFY family were mainly subjected to purifying selection. Analysis of the RNA-seq data revealed that a total of five differentially expressed genes (DEGs) were expressed in the shoots under gibberellin treatment, whereas only one gene was significantly differentially expressed in the leaves; under both low-temperature and high-temperature stresses, there were significantly differentially expressed genes, and the EjJAZ15 gene was significantly upregulated under both low- and high-temperature stress. RNA-seq and qRT-PCR expression analysis under salt stress conditions revealed that EjJAZ2, EjJAZ4, and EjJAZ9 responded to salt stress in loquat plants, which promoted resistance to salt stress through the JA pathway. The response model of the TIFY genes in the jasmonic acid pathway under salt stress in loquat was systematically summarized. These results provide a theoretical basis for exploring the characteristics and functions of additional EjTIFY genes in the future. This study also provides a theoretical basis for further research on breeding for salt stress resistance in loquat. RT-qPCR analysis revealed that the expression of one of the three EjTIFY genes increased and the expression of two decreased under salt stress conditions, suggesting that EjTIFY exhibited different expression patterns under salt stress conditions.
Sections du résumé
BACKGROUND
BACKGROUND
Plant-specific TIFY proteins are widely found in terrestrial plants and play important roles in plant adversity responses. Although the genome of loquat at the chromosome level has been published, studies on the TIFY family in loquat are lacking. Therefore, the EjTIFY gene family was bioinformatically analyzed by constructing a phylogenetic tree, chromosomal localization, gene structure, and adversity expression profiling in this study.
RESULTS
RESULTS
Twenty-six EjTIFY genes were identified and categorized into four subfamilies (ZML, JAZ, PPD, and TIFY) based on their structural domains. Twenty-four EjTIFY genes were irregularly distributed on 11 of the 17 chromosomes, and the remaining two genes were distributed in fragments. We identified 15 covariate TIFY gene pairs in the loquat genome, 13 of which were involved in large-scale interchromosomal segmental duplication events, and two of which were involved in tandem duplication events. Many abiotic stress cis-elements were widely present in the promoter region. Analysis of the Ka/Ks ratio showed that the paralogous homologs of the EjTIFY family were mainly subjected to purifying selection. Analysis of the RNA-seq data revealed that a total of five differentially expressed genes (DEGs) were expressed in the shoots under gibberellin treatment, whereas only one gene was significantly differentially expressed in the leaves; under both low-temperature and high-temperature stresses, there were significantly differentially expressed genes, and the EjJAZ15 gene was significantly upregulated under both low- and high-temperature stress. RNA-seq and qRT-PCR expression analysis under salt stress conditions revealed that EjJAZ2, EjJAZ4, and EjJAZ9 responded to salt stress in loquat plants, which promoted resistance to salt stress through the JA pathway. The response model of the TIFY genes in the jasmonic acid pathway under salt stress in loquat was systematically summarized.
CONCLUSIONS
CONCLUSIONS
These results provide a theoretical basis for exploring the characteristics and functions of additional EjTIFY genes in the future. This study also provides a theoretical basis for further research on breeding for salt stress resistance in loquat. RT-qPCR analysis revealed that the expression of one of the three EjTIFY genes increased and the expression of two decreased under salt stress conditions, suggesting that EjTIFY exhibited different expression patterns under salt stress conditions.
Identifiants
pubmed: 38745142
doi: 10.1186/s12864-024-10375-2
pii: 10.1186/s12864-024-10375-2
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
468Subventions
Organisme : the National Key R & D Program of China
ID : 2022YFD1601806
Organisme : the National Key R & D Program of China
ID : 2022YFD1601806
Organisme : the Yunnan Academician (expert) Workstation Project
ID : 202305AF150020
Informations de copyright
© 2024. The Author(s).
Références
Shikata M, Matsuda Y, Ando K, Nishii A, Takemura M, Yokota A, Kohchi T. Characterization of Arabidopsis ZIM, a member of a novel plant-specific GATA factor gene family. J Exp Bot. 2004;55(397):631–9. https://doi.org/10.1093/jxb/erh078 .
doi: 10.1093/jxb/erh078
pubmed: 14966217
Sheng Y, Yu H, Pan H, Qiu K, Xie Q, Chen H, Fu S, Zhang J, Zhou H. Genome-wide analysis of the gene structure, expression and protein interactions of the peach (Prunus persica) TIFY gene family. Front Plant Sci. 2022;13:792802. https://doi.org/10.3389/fpls.2022.792802 .
doi: 10.3389/fpls.2022.792802
pubmed: 35251076
pmcid: 8891376
Yan Y, Stolz S, Chételat A, Reymond P, Pagni M, Dubugnon L, Farmer EE. A downstream mediator in the growth repression limb of the jasmonate pathway. Plant Cell. 2007;19(8):2470–83. https://doi.org/10.1105/tpc.107.050708 .
doi: 10.1105/tpc.107.050708
pubmed: 17675405
pmcid: 2002611
Vanholme B, Grunewald W, Bateman A, Kohchi T, Gheysen G. The FIFY family previously known as ZIM. Trends Plant Sci. 2007;12(6):239–44. https://doi.org/10.1016/j.tplants.2007.04.004 .
doi: 10.1016/j.tplants.2007.04.004
pubmed: 17499004
Zhang X, Ran W, Zhang J, Ye M, Lin S, Li X, Sultana R, Sun X. Genome-wide identification of the Tify Gene Family and their expression profiles in response to biotic and abiotic stresses in tea plants (Camellia sinensis). Int J Mol Sci. 2020;21(21):8316. https://doi.org/10.3390/ijms21218316 .
doi: 10.3390/ijms21218316
pubmed: 33167605
pmcid: 7664218
Bai Y, Meng Y, Huang D, Qi Y, Chen M. Origin and evolutionary analysis of the plant-specific TIFY transcription factor family. Genomics. 2011;98(2):128–36. https://doi.org/10.1016/j.ygeno.2011.05.002 .
doi: 10.1016/j.ygeno.2011.05.002
pubmed: 21616136
Zhang Y, Gao M, Singer SD, Fei Z, Wang H, Wang X. Genome-wide identification and analysis of the TIFY gene family in grape. Plos One. 2012;7(9):e44465. https://doi.org/10.1371/journal.pone.0044465 .
doi: 10.1371/journal.pone.0044465
pubmed: 22984514
pmcid: 3439424
Thatcher LF, Cevik V, Grant M, Zhai B, Jones JD, Manners JM, Kazan K. Characterization of a JAZ7 activation-tagged Arabidopsis mutant with increased susceptibility to the fungal pathogen Fusarium oxysporum. J Exp Bot. 2016;67(8):2367–86. https://doi.org/10.1093/jxb/erw040 .
doi: 10.1093/jxb/erw040
pubmed: 26896849
pmcid: 4809290
Song S, Qi T, Huang H, Ren Q, Wu D, Chang C, Peng W, Liu Y, Peng J, Xie D. The Jasmonate-ZIM domain proteins interact with the R2R3-MYB transcription factors MYB21 and MYB24 to affect Jasmonate-regulated stamen development in Arabidopsis. Plant Cell. 2011;23(3):1000–13. https://doi.org/10.1105/tpc.111.083089 .
doi: 10.1105/tpc.111.083089
pubmed: 21447791
pmcid: 3082250
Ye H, Du H, Tang N, Li X, Xiong L. Identification and expression profiling analysis of TIFY family genes involved in stress and phytohormone responses in rice. Plant Mol Biol. 2009;71(3):291–305. https://doi.org/10.1007/s11103-009-9524-8 .
doi: 10.1007/s11103-009-9524-8
pubmed: 19618278
Chen H, Shao H, Li K, Zhang D, Fan S, Li Y, Han M. Genome-wide identification, evolution, and expression analysis of GATA transcription factors in apple (Malus×domestica Borkh). Gene. 2017;627:460–72. https://doi.org/10.1016/j.gene.2017.06.049 .
doi: 10.1016/j.gene.2017.06.049
pubmed: 28669931
Wang Y, Pan F, Chen D, Chu W, Liu H, Xiang Y. Genome-wide identification and analysis of the Populus trichocarpa TIFY gene family. Plant Physiol Biochem. 2017;115:360–71. https://doi.org/10.1016/j.plaphy.2017.04.015 .
doi: 10.1016/j.plaphy.2017.04.015
pubmed: 28431355
Ge L, Yu J, Wang H, Luth D, Bai G, Wang K, Chen R. Increasing seed size and quality by manipulating BIG SEEDS1 in legume species. Proc Natl Acad Sci USA. 2016;113(44):12414–9. https://doi.org/10.1073/pnas.1611763113 .
doi: 10.1073/pnas.1611763113
pubmed: 27791139
pmcid: 5098654
Zhu D, Cai H, Luo X, Bai X, Deyholos MK, Chen Q, Chen C, Ji W, Zhu Y. Over-expression of a novel JAZ family gene from Glycine soja, increases salt and alkali stress tolerance. Biochem Biophys Res Commun. 2012;426(2):273–9. https://doi.org/10.1016/j.bbrc.2012.08.086 .
doi: 10.1016/j.bbrc.2012.08.086
pubmed: 22943855
Peethambaran PK, Glenz R, Höninger S, Islam S, Hummel SM, Harter S, Kolukisaoglu K, Meynard Ü, Guiderdoni D, Nick E, Riemann M. Salt-inducible expression of OsJAZ8 improves resilience against salt-stress. BMC Plant Biol. 2018;18(1):311. https://doi.org/10.1186/s12870-018-1521-0 .
doi: 10.1186/s12870-018-1521-0
pubmed: 30497415
pmcid: 6267056
Seo JS, Joo J, Kim MJ, Kim YK, Nahm BH, Song SI, Cheong JJ, Lee JS, Kim JK, Choi YD. OsbHLH148, a basic helix-loop-helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice. Plant J. 2011;65(6):907–21. https://doi.org/10.1111/j.1365-313X.2010.04477.x .
doi: 10.1111/j.1365-313X.2010.04477.x
pubmed: 21332845
Zhu D, Bai X, Chen C, Chen Q, Cai H, Li Y, Ji W, Zhai H, Lv D, Luo X, Zhu Y. GsTIFY10, a novel positive regulator of plant tolerance to bicarbonate stress and a repressor of jasmonate signaling. Plant Mol Biol. 2011;77(3):285–97. https://doi.org/10.1007/s11103-011-9810-0 .
doi: 10.1007/s11103-011-9810-0
pubmed: 21805375
Bailey-Serres J, Fukao T, Gibbs DJ, Holdsworth MJ, Lee SC, Licausi F, Perata P, Voesenek LA, van Dongen JT. Making sense of low oxygen sensing. Trends Plant Sci. 2012;17(3):129–38. https://doi.org/10.1016/j.tplants.2011.12.004 .
doi: 10.1016/j.tplants.2011.12.004
pubmed: 22280796
Ahuja I, de Vos RC, Bones AM, Hall RD. Plant molecular stress responses face climate change. Trends Plant Sci. 2010;15(12):664–74. https://doi.org/10.1016/j.tplants.2010.08.002 .
doi: 10.1016/j.tplants.2010.08.002
pubmed: 20846898
Huang S, Gao Y, Liu J, Peng X, Niu X, Fei Z, Cao S, Liu Y. Genome-wide analysis of WRKY transcription factors in Solanum lycopersicum. Mol Genet Genomics. 2012;287(6):495–513. https://doi.org/10.1007/s00438-012-0696-6 .
doi: 10.1007/s00438-012-0696-6
pubmed: 22570076
Su W, Jing Y, Lin S, Yue Z, Yang X, Xu J, Wu J, Zhang Z, Xia R, Zhu J, An N, Chen H, Hong Y, Yuan Y, Long T, Zhang L, Jiang Y, Liu Z, Zhang H, Gao Y, Liu Y, Lin H, Wang H, Yant L, Lin S, Liu Z. Polyploidy underlies co-option and diversification of biosynthetic triterpene pathways in the apple tribe. Proc Natl Acad Sci USA. 2021;118(20):e2101767118. https://doi.org/10.1073/pnas.2101767118 .
doi: 10.1073/pnas.2101767118
pubmed: 33986115
pmcid: 8157987
Pu Z, Hu R, Xu X, Guo Q, Xia Y, Jing D. Expression characterization and function analysis of the EjAGL6 gene in triploid loquat [J]. Northwest J Bot. 2022;08:1263–72.
Jia K, Yan C, Zhang J, Cheng Y, Li W, Yan H, Gao J. Genome-wide identification and expression analysis of the JAZ gene family in turnip. Sci Rep. 2021;11(1):21330. https://doi.org/10.1038/s41598-021-99593-2 .
doi: 10.1038/s41598-021-99593-2
pubmed: 34716392
pmcid: 8556354
Dai Z, Dong S, Miao H, Liu X, Han J, Li C, Gu X, Zhang S. Genome-wide identification of TIFY genes and their response to various pathogen infections in cucumber (Cucumis sativus L). Sci Hort. 2022;295(110814):0304–4238. https://doi.org/10.1016/j.scienta.2021.110814 .
doi: 10.1016/j.scienta.2021.110814
Tao J, Jia H, Wu M, Zhong W, Jia D, Wang Z, Huang C. Genome-wide identification and characterization of the TIFY gene family in kiwifruit. BMC Genomics. 2022;23(1):179. https://doi.org/10.1186/s12864-022-08398-8 .
doi: 10.1186/s12864-022-08398-8
pubmed: 35247966
pmcid: 8897921
Liu YL, Zheng L, Jin LG, Liu YX, Kong YN, Wang YX, Yu TF, Chen J, Zhou YB, Chen M, Wang FZ, Ma YZ, Xu ZS, Lan JH. Genome-wide analysis of the soybean TIFY family and identification of GmTIFY10e and GmTIFY10g response to salt stress. Front Plant Sci. 2022;13:845314. https://doi.org/10.3389/fpls.2022.845314 .
doi: 10.3389/fpls.2022.845314
pubmed: 35401633
pmcid: 8984480
Zhu D, Li R, Liu X, Sun M, Wu J, Zhang N, Zhu Y. The positive regulatory roles of the TIFY10 proteins in plant responses to alkaline stress. Plos One. 2014;9(11):e111984. https://doi.org/10.1371/journal.pone.0111984 .
doi: 10.1371/journal.pone.0111984
pubmed: 25375909
pmcid: 4222965
Liu X, Yu F, Yang G, Liu X, Peng S. Identification of TIFY gene family in walnut and analysis of its expression under abiotic stresses. BMC Genomics. 2022;23(1):190. https://doi.org/10.1186/s12864-022-08416-9 .
doi: 10.1186/s12864-022-08416-9
pubmed: 35255828
pmcid: 8903722
Ding A, Li P, Wang J, Cheng T, Bao F, Zhang Q. Genome-wide identification and low-temperature expression analysis of bHLH genes in Prunus mume. Front Genet. 2021;12:762135. https://doi.org/10.3389/fgene.2021.762135 .
doi: 10.3389/fgene.2021.762135
pubmed: 34659372
pmcid: 8519403
Liang J, Fang Y, An C, Yao Y, Wang X, Zhang W, Liu R, Wang L, Aslam M, Cheng Y, Qin Y, Zheng P. Genome-wide identification and expression analysis of the bHLH gene family in passion fruit (Passiflora edulis) and its response to abiotic stress. Int J Biol Macromol. 2023;225:389–403. https://doi.org/10.1016/j.ijbiomac.2022.11.076 .
doi: 10.1016/j.ijbiomac.2022.11.076
pubmed: 36400210
Yu J, Xie Q, Li C, Dong Y, Zhu S, Chen J. Comprehensive characterization and gene expression patterns of LBD gene family in Gossypium. Planta. 2020;251(4):81. https://doi.org/10.1007/s00425-020-03364-8 .
doi: 10.1007/s00425-020-03364-8
pubmed: 32185507
Li X, Yin X, Wang H, Li J, Guo C, Gao H, Zheng Y, Fan C, Wang X. Genome-wide identification and analysis of the apple (Malus × Domestica Borkh.) TIFY gene family. Tree Genet Genomes. 2014;11(1):808. https://doi.org/10.1007/s11295-014-0808-z .
doi: 10.1007/s11295-014-0808-z
Yuan T, Liang J, Dai J, Zhou XR, Liao W, Guo M, Aslam M, Li S, Cao G, Cao S. Genome-wide identification of Eucalyptus heat shock transcription factor family and their transcriptional analysis under salt and temperature stresses. Int J Mol Sci. 2022;23(14):8044. https://doi.org/10.3390/ijms23148044 .
doi: 10.3390/ijms23148044
pubmed: 35887387
pmcid: 9318532
Wimalanathan K, Lawrence-Dill CJ. Gene ontology meta annotator for plants (GOMAP). Plant Methods. 2021;17(1):54. https://doi.org/10.1186/s13007-021-00754-1 .
doi: 10.1186/s13007-021-00754-1
pubmed: 34034755
pmcid: 8146647
Ruan J, Zhou Y, Zhou M, Yan J, Khurshid M, Weng W, Cheng J, Zhang K. Jasmonic acid signaling pathway in plants. Int J Mol Sci. 2019;20(10):2479. https://doi.org/10.3390/ijms20102479 .
doi: 10.3390/ijms20102479
pubmed: 31137463
pmcid: 6566436
Melotto M, Mecey C, Niu Y, Chung HS, Katsir L, Yao J, Zeng W, Thines B, Staswick P, Browse J, Howe GA, He SY. A critical role of two positively charged amino acids in the Jas motif of A. Thaliana JAZ proteins in mediating coronatine- and jasmonoyl isoleucine-dependent interactions with the COI1 F-box protein. Plant J: Cell Mol Biol. 2008;55(6):979–88. https://doi.org/10.1111/j.1365-313X.2008.03566.x .
doi: 10.1111/j.1365-313X.2008.03566.x
Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J. JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature. 2007;448(7154):661–5. https://doi.org/10.1038/nature05960 .
doi: 10.1038/nature05960
pubmed: 17637677
Ju L, Jing Y, Shi P, Liu J, Chen J, Yan J, Chu J, Chen KM, Sun J. JAZ proteins modulate seed germination through interaction with ABI5 in bread wheat and Arabidopsis. New Phytol. 2019;223(1):246–60. https://doi.org/10.1111/nph.15757 .
doi: 10.1111/nph.15757
pubmed: 30802963
Yu X, Chen G, Tang B, Zhang J, Zhou S, Hu Z. The jasmonate ZIM-domain protein gene SlJAZ2 regulates plant morphology and accelerates flower initiation in Solanum lycopersicum plants. Plant Science: Int J Experimental Plant Biology. 2018;267:65–73. https://doi.org/10.1016/j.plantsci.2017.11.008 .
doi: 10.1016/j.plantsci.2017.11.008
Zhao G, Song Y, Wang C, Butt HI, Wang Q, Zhang C, Yang Z, Liu Z, Chen E, Zhang X, Li F. Genome-wide identification and functional analysis of the TIFY gene family in response to drought in cotton. Mol Genet Genomics. 2016;291(6):2173–87. https://doi.org/10.1007/s00438-016-1248-2 .
doi: 10.1007/s00438-016-1248-2
pubmed: 27640194
pmcid: 5080297
Zhao C, Pan X, Yu Y, et al. Overexpression of a TIFY family gene, GsJAZ2, exhibits enhanced tolerance to alkaline stress in soybean. Mol Breeding. 2020;40:33. https://doi.org/10.1007/s11032-020-01113-z .
doi: 10.1007/s11032-020-01113-z
Liu S, Zhang P, Li C, Xia G. The moss jasmonate ZIM-domain protein PnJAZ1 confers salinity tolerance via crosstalk with the abscisic acid signalling pathway. Plant Science: Int J Experimental Plant Biology. 2019;280:1–11. https://doi.org/10.1016/j.plantsci.2018.11.004 .
doi: 10.1016/j.plantsci.2018.11.004
Cai Z, Chen Y, Liao J, Wang D. Genome-wide identification and expression analysis of jasmonate ZIM domain gene family in tuber mustard (Brassica juncea var. Tumida). PLoS One. 2020;15(6):e0234738. https://doi.org/10.1371/journal.pone.0234738 .
doi: 10.1371/journal.pone.0234738
pubmed: 32544205
pmcid: 7297370
Kapli P, Yang Z, Telford MJ. Phylogenetic tree building in the genomic age. Nat Rev Genet. 2020;21(7):428–44. https://doi.org/10.1038/s41576-020-0233-0 .
doi: 10.1038/s41576-020-0233-0
pubmed: 32424311
Zheng L, Wan Q, Wang H, Guo C, Niu X, Zhang X, Zhang R, Chen Y, Luo K. Genome-wide identification and expression of TIFY family in cassava (Manihot esculenta Crantz). Front Plant Sci. 2022;13:1017840. https://doi.org/10.3389/fpls.2022.1017840 .
doi: 10.3389/fpls.2022.1017840
pubmed: 36275529
pmcid: 9581314
He X, Kang Y, Li W, Liu W, Xie P, Liao L, Huang L, Yao M, Qian L, Liu Z, Guan C, Guan M, Hua W. Genome-wide identification and functional analysis of the TIFY gene family in the response to multiple stresses in Brassica napus L. BMC Genomics. 2020;21(1):736. https://doi.org/10.1186/s12864-020-07128-2 .
doi: 10.1186/s12864-020-07128-2
pubmed: 33092535
pmcid: 7583176
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. https://doi.org/10.1186/1471-2229-4-10 .
doi: 10.1186/1471-2229-4-10
pubmed: 15171794
pmcid: 446195
Ahmad MZ, Sana A, Jamil A, Nasir JA, Ahmed S, Hameed MU, Abdullah. A genome-wide approach to the comprehensive analysis of GASA gene family in Glycine max. Plant Mol Biol. 2019;100(6):607–20. https://doi.org/10.1007/s11103-019-00883-1 .
doi: 10.1007/s11103-019-00883-1
pubmed: 31123969
Faraji S, Filiz E, Kazemitabar SK, Vannozzi A, Palumbo F, Barcaccia G, Heidari P. The AP2/ERF gene family in Triticum durum: genome-wide identification and expression analysis under drought and salinity stresses. Genes. 2020;11(12):1464. https://doi.org/10.3390/genes11121464 .
doi: 10.3390/genes11121464
pubmed: 33297327
pmcid: 7762271
Xu G, Guo C, Shan H, Kong H. Divergence of duplicate genes in exon-intron structure. Proc Natl Acad Sci USA. 2012;109(4):1187–92. https://doi.org/10.1073/pnas.1109047109 .
doi: 10.1073/pnas.1109047109
pubmed: 22232673
pmcid: 3268293
Abdullah, Faraji S, Mehmood F, Malik HMT, Ahmed I, Heidari P, Poczai P. The GASA gene family in cacao (Theobroma cacao, Malvaceae): genome wide identification and expression analysis. Agronomy. 2021;11(7):1425. https://doi.org/10.3390/agronomy11071425 .
doi: 10.3390/agronomy11071425
Debnath M, Pandey M, Bisen PS. An omics approach to understand the plant abiotic stress. OMICS. 2011;15(11):739–62. https://doi.org/10.1089/omi.2010.0146 .
doi: 10.1089/omi.2010.0146
pubmed: 22122668
An XH, Hao YJ, Li EM, Xu K, Cheng CG. Functional identification of M. Domestica MdJAZ2 in A. Thaliana with reduced JA-sensitivity and increased stress tolerance. Plant Cell Rep. 2017;36(2):255–65. https://doi.org/10.1007/s00299-016-2077-9 .
doi: 10.1007/s00299-016-2077-9
pubmed: 27844101
Heidari P, Faraji S, Ahmadizadeh M, Ahmar S, Mora-Poblete F. New insights into structure and function of TIFY genes in Zea mays and Solanum lycopersicum: a genome-wide comprehensive analysis. Front Genet. 2021;12:657970. https://doi.org/10.3389/fgene.2021.657970 .
doi: 10.3389/fgene.2021.657970
pubmed: 34054921
pmcid: 8155530
Li G, Manzoor MA, Chen R, Zhang Y, Song C. Genome-wide identification and expression analysis of TIFY genes under MeJA, cold and PEG-induced drought stress treatment in Dendrobium huoshanense. Physiol Mol Biol Plants. 2024:1–16. https://doi.org/10.1007/s12298-024-01442-9 .
Madeira F, Park YM, Lee J, Buso N, Gur T, Madhusoodanan N, Basutkar P, Tivey ARN, Potter SC, Finn RD, Lopez R. The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res. 2019;47(W1):W636-641. https://doi.org/10.1093/nar/gkz268 .
doi: 10.1093/nar/gkz268
pubmed: 30976793
pmcid: 6602479
Yin T, Han P, Xi D, Yu W, Zhu L, Du C, Yang N, Liu X, Zhang H. Genome-wide identification, characterization, and expression profile of NBS-LRR gene family in sweet orange (Citrus sinensis). Gene. 2023;854:147117. https://doi.org/10.1016/j.gene.2022.147117 .
doi: 10.1016/j.gene.2022.147117
pubmed: 36526123
Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ, Lu S, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Geer L, Bryant SH. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res. 2017;45(D1):D200-203. https://doi.org/10.1093/nar/gkw1129 .
doi: 10.1093/nar/gkw1129
pubmed: 27899674
Zhu L, Yin T, Zhang M, Yang X, Wu J, Cai H, Yang N, Li X, Wen K, Chen D, Zhang H, Liu X. Genome-wide identification and expression pattern analysis of the kiwifruit GRAS transcription factor family in response to salt stress. BMC Genomics. 2024;25(1):12. https://doi.org/10.1186/s12864-023-09915-z .
doi: 10.1186/s12864-023-09915-z
pubmed: 38166720
pmcid: 10759511
Chen C, Wu Y, Li J, Wang X, Zeng Z, Xu J, Liu Y, Feng J, Chen H, He Y, Xia R. TBtools-II: a one for all, all for one bioinformatics platform for biological big-data mining. Mol Plant. 2023;16(11):1733–42. https://doi.org/10.1016/j.molp.2023.09.010 .
doi: 10.1016/j.molp.2023.09.010
pubmed: 37740491
Bailey TL, Williams N, Misleh C, Li WW. MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res. 2006;34(Web Server issue):W369–73. https://doi.org/10.1093/nar/gkl198 .
doi: 10.1093/nar/gkl198
pubmed: 16845028
pmcid: 1538909
Katoh K, Rozewicki J, Yamada KD. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform. 2019;20(4):1160–6. https://doi.org/10.1093/bib/bbx108 .
doi: 10.1093/bib/bbx108
pubmed: 28968734
Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32(1):268–74. https://doi.org/10.1093/molbev/msu300 .
doi: 10.1093/molbev/msu300
pubmed: 25371430
Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 2002;30(1):325–7. https://doi.org/10.1093/nar/30.1.325 .
doi: 10.1093/nar/30.1.325
pubmed: 11752327
pmcid: 99092
Liu L, Zheng S, Yang D, Zheng J. Genome-wide in silico identification of glutathione S-transferase (GST) gene family members in fig (Ficus carica L) and expression characteristics during fruit color development. PeerJ. 2023;11: e14406. https://doi.org/10.7717/peerj.14406 .
doi: 10.7717/peerj.14406
pubmed: 36718451
pmcid: 9884035
Wang Y, Tang H, Debarry JD, Tan X, Li J, Wang X, Lee TH, Jin H, Marler B, Guo H, Kissinger JC, Paterson AH. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 2012;40(7):e49. https://doi.org/10.1093/nar/gkr1293 .
doi: 10.1093/nar/gkr1293
pubmed: 22217600
pmcid: 3326336
Jiang Y, Liu Y, Gao Y, Peng J, Su W, Yuan Y, Yang X, Zhao C, Wang M, Lin S, Peng Z, Xie F. Gibberellin induced transcriptome profiles reveal gene regulation of E. Japonica flowering. Front Genet. 2021;12:703688. https://doi.org/10.3389/fgene.2021.703688 .
doi: 10.3389/fgene.2021.703688
pubmed: 34567066
pmcid: 8460860
Moon J, Lee H, Kim M, Lee I. Analysis of flowering pathway integrators in Arabidopsis. Plant Cell Physiol. 2005;46(2):292–9. https://doi.org/10.1093/pcp/pci024 .
doi: 10.1093/pcp/pci024
pubmed: 15695467
Chen Y, Li H, Zhang S, Du S, Wang G, Zhang J, Jiang J. Analysis of the antioxidant mechanism of Tamarix ramosissima roots under NaCl stress based on physiology, transcriptomic and metabolomic. Antioxid (Basel Switzerland). 2022;11(12):2362. https://doi.org/10.3390/antiox11122362 .
doi: 10.3390/antiox11122362
Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods. 2015;12(4):357–60. https://doi.org/10.1038/nmeth.3317 .
doi: 10.1038/nmeth.3317
pubmed: 25751142
pmcid: 4655817
Yu W, Kong G, Chao J, Yin T, Tian H, Ya H, He L, Zhang H. Genome-wide identification of the rubber tree superoxide dismutase (SOD) gene family and analysis of its expression under abiotic stress. PeerJ. 2022;10:e14251. https://doi.org/10.7717/peerj.14251 .
doi: 10.7717/peerj.14251
pubmed: 36312747
pmcid: 9610661
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. https://doi.org/10.1186/s13059-014-0550-8 .
doi: 10.1186/s13059-014-0550-8
pubmed: 25516281
pmcid: 4302049
Wimalanathan K, Friedberg I, Andorf CM, Lawrence-Dill CJ. Maize GO annotation-methods, evaluation, and review (maize-GAMER). Plant Direct. 2018;2(4):e00052. https://doi.org/10.1002/pld3.52 .
doi: 10.1002/pld3.52
pubmed: 31245718
pmcid: 6508527
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods (San Diego Calif). 2001;25(4):402–8. https://doi.org/10.1006/meth.2001.1262 .
doi: 10.1006/meth.2001.1262
pubmed: 11846609
Duricki DA, Soleman S, Moon LD. Analysis of longitudinal data from animals with missing values using SPSS. Nat Protoc. 2016;11(6):1112–29. https://doi.org/10.1038/nprot.2016.048 .
doi: 10.1038/nprot.2016.048
pubmed: 27196723
pmcid: 5582138