Comprehensive analysis of 14-3-3 family genes and their responses to cold and drought stress in cucumber
Mingyuan Xu A # , Zhaoyang Hu A # , Wei Lai B , Shiqiang Liu A , Hao Wu C * and Yong Zhou![https://orcid.org/0000-0002-8432-6678](/media/client/orcid_16x16.png)
A College of Bioscience and Bioengineering, Jiangxi Agricultural University, Nanchang 330045, China.
B College of Agronomy, Jiangxi Agricultural University, Nanchang 330045, China.
C Henry Fok College of Biology and Agriculture, Shaoguan University, Shaoguan 512005, China.
Handling Editor: Manuela Chaves
Functional Plant Biology 48(12) 1264-1276 https://doi.org/10.1071/FP21022
Submitted: 22 January 2021 Accepted: 10 September 2021 Published: 12 October 2021
© 2021 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
The 14-3-3 proteins play essential roles in regulating various biological processes and abiotic stress responses in plants. However, there have been few studies of 14-3-3 family members in cucumber. Here, we identified a total of ten 14-3-3 genes (named as CsGF14a–j) in the cucumber genome. These genes are unevenly distributed across six cucumber chromosomes, and six of them were found to be segmentally duplicated. A phylogenetic analysis of 14-3-3 proteins in cucumber and other plant species showed that they could be divided into two distinct groups (ε and non-ε). Members in the same group tend to have similar exon-intron structure and conserved motif patterns. Several hormone-, stress- and development-related cis-elements associated with transcriptional regulation were found in the promoters of CsGF14 genes. RNA-seq data showed that most CsGF14 genes have broad expression in different tissues, and some had preferential expression in specific tissues and variable expression at certain developmental stages during fruit development. Quantitative real-time PCR (qRT-PCR) results revealed that nearly all tested CsGF14 genes were significantly up-regulated under cold and drought stress at certain time points. These results provide important information about the functions of CsGF14 genes in cucumber.
Keywords: 14-3-3, 14-3-3 protein, cold stress, cucumber, drought stress, expression analysis, gene family, phylogeny.
References
Benzinger A, Popowicz GM, Joy JK, Majumdar S, Holak TA, Hermeking H (2005) The crystal structure of the non-liganded 14-3-3σ protein: insights into determinants of isoform specific ligand binding and dimerization. Cell Research 15, 219–227.| The crystal structure of the non-liganded 14-3-3σ protein: insights into determinants of isoform specific ligand binding and dimerization.Crossref | GoogleScholarGoogle Scholar | 15857576PubMed |
Cao H, Xu Y, Yuan L, Bian Y, Wang L, Zhen S, Hu Y, Yan Y (2016) Molecular characterization of the 14-3-3 gene family in Brachypodium distachyon L. reveals high evolutionary conservation and diverse responses to abiotic stresses. Frontiers in Plant Science 7, 993
| Molecular characterization of the 14-3-3 gene family in Brachypodium distachyon L. reveals high evolutionary conservation and diverse responses to abiotic stresses.Crossref | GoogleScholarGoogle Scholar |
Catalá R, López-Cobollo R, Mar Castellano M, Angosto T, Alonso JM, Ecker JR, Salinas J (2014) The Arabidopsis 14-3-3 protein RARE COLD INDUCIBLE 1A links low-temperature response and ethylene biosynthesis to regulate freezing tolerance and cold acclimation. The Plant Cell 26, 3326–3342.
| The Arabidopsis 14-3-3 protein RARE COLD INDUCIBLE 1A links low-temperature response and ethylene biosynthesis to regulate freezing tolerance and cold acclimation.Crossref | GoogleScholarGoogle Scholar | 25122152PubMed |
Chandna R, Augustine R, Kanchupati P, Kumar R, Kumar P, Arya GC, Bisht NC (2016) Class-specific evolution and transcriptional differentiation of 14-3-3 family members in mesohexaploid Brassica rapa. Frontiers in Plant Science 7, 12
| Class-specific evolution and transcriptional differentiation of 14-3-3 family members in mesohexaploid Brassica rapa.Crossref | GoogleScholarGoogle Scholar | 26858736PubMed |
Chang L, Tong Z, Peng C, Wang D, Kong H, Yang Q, Luo M, Guo A, Xu B (2020) Genome-wide analysis and phosphorylation sites identification of the 14-3-3 gene family and functional characterization of MeGRF3 in cassava. Physiologia Plantarum 169, 244–257.
| Genome-wide analysis and phosphorylation sites identification of the 14-3-3 gene family and functional characterization of MeGRF3 in cassava.Crossref | GoogleScholarGoogle Scholar | 32020618PubMed |
Chen F, Li Q, Sun L, He Z (2006) The rice 14-3-3 gene family and its involvement in responses to biotic and abiotic stress. DNA Research 13, 53–63.
| The rice 14-3-3 gene family and its involvement in responses to biotic and abiotic stress.Crossref | GoogleScholarGoogle Scholar | 16766513PubMed |
Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020a) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Molecular Plant 13, 1194–1202.
| TBtools: an integrative toolkit developed for interactive analyses of big biological data.Crossref | GoogleScholarGoogle Scholar | 32585190PubMed |
Chen L, Zhou Y, Lai W, Hu L, Jiang L, Liu S (2020b) In silico identification and expression analysis of nuclear factor Y (NF-Y) transcription factors in cucumber. Agronomy-Basel 10, 236
| In silico identification and expression analysis of nuclear factor Y (NF-Y) transcription factors in cucumber.Crossref | GoogleScholarGoogle Scholar |
Cheng C, Wang Y, Chai F, Li S, Xin H, Liang Z (2018) Genome-wide identification and characterization of the 14-3-3 family in Vitis vinifera L. during berry development and cold- and heat-stress response. BMC Genomics 19, 617
| Genome-wide identification and characterization of the 14-3-3 family in Vitis vinifera L. during berry development and cold- and heat-stress response.Crossref | GoogleScholarGoogle Scholar |
DeLille JM, Sehnke PC, Ferl RJ (2001) The Arabidopsis 14-3-3 family of signaling regulators. Plant Physiology 126, 35–38.
| The Arabidopsis 14-3-3 family of signaling regulators.Crossref | GoogleScholarGoogle Scholar | 11351068PubMed |
Denison FC, Paul A-L, Zupanska AK, Ferl RJ (2011) 14-3-3 proteins in plant physiology. Seminars in Cell & Developmental Biology 22, 720–727.
| 14-3-3 proteins in plant physiology.Crossref | GoogleScholarGoogle Scholar |
Eddy SR, Pearson WR (2011) Accelerated profile HMM searches. PLoS Computational Biology 7, e1002195
| Accelerated profile HMM searches.Crossref | GoogleScholarGoogle Scholar | 22039361PubMed |
He Y, Zhang Y, Chen L, Wu C, Luo Q, Zhang F, Wei Q, Li K, Chang J, Yang G, He G (2017) A member of the 14-3-3 gene family in Brachypodium distachyon BdGF14d, confers salt tolerance in transgenic tobacco plants. Frontiers in Plant Science 8, 340
| A member of the 14-3-3 gene family in Brachypodium distachyon BdGF14d, confers salt tolerance in transgenic tobacco plants.Crossref | GoogleScholarGoogle Scholar | 28348575PubMed |
Huang W, Hu B, Liu J, Zhou Y, Liu S (2020) Identification and characterization of tonoplast sugar transporter (TST) gene family in cucumber. Horticultural Plant Journal 6, 145–157.
| Identification and characterization of tonoplast sugar transporter (TST) gene family in cucumber.Crossref | GoogleScholarGoogle Scholar |
Kong Q, Ma W (2018) WRINKLED1 as a novel 14-3-3 client: function of 14-3-3 proteins in plant lipid metabolism. Plant Signaling & Behavior 13, e1482176
| WRINKLED1 as a novel 14-3-3 client: function of 14-3-3 proteins in plant lipid metabolism.Crossref | GoogleScholarGoogle Scholar |
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.
| MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets.Crossref | GoogleScholarGoogle Scholar | 27004904PubMed |
Lai W, Zhou Y, Pan R, Liao L, He J, Liu H, Yang Y, Liu S (2020) Identification and expression analysis of stress-associated proteins (SAPs) containing A20/AN1 zinc finger in cucumber. Plants-Basel 9, 400
| Identification and expression analysis of stress-associated proteins (SAPs) containing A20/AN1 zinc finger in cucumber.Crossref | GoogleScholarGoogle Scholar |
Lee JH, Kwak G, Lim YP, Oh MH (2020) 14-3-3 proteins contribute to leaf and root development via brassinosteroid insensitive 1 in Arabidopsis thaliana. Genes & Genomics 42, 347–354.
| 14-3-3 proteins contribute to leaf and root development via brassinosteroid insensitive 1 in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Li Z, Zhang Z, Yan P, Huang S, Fei Z, Lin K (2011) RNA-Seq improves annotation of protein-coding genes in the cucumber genome. BMC Genomics 12, 540
| RNA-Seq improves annotation of protein-coding genes in the cucumber genome.Crossref | GoogleScholarGoogle Scholar | 22047402PubMed |
Li R, Jiang X, Jin D, Dhaubhadel S, Bian S, Li X, Chan Z (2015) Identification of 14-3-3 family in common bean and their response to abiotic stress. PLoS One 10, e0143280
| Identification of 14-3-3 family in common bean and their response to abiotic stress.Crossref | GoogleScholarGoogle Scholar | 26599110PubMed |
Li M, Ren L, Xu B, Yang X, Xia Q, He P, Xiao S, Guo A, Hu W, Jin Z (2016) Genome-wide identification, phylogeny, and expression analyses of the 14-3-3 family reveal their involvement in the development, ripening, and abiotic stress response in banana. Frontiers in Plant Science 7, 1442
| Genome-wide identification, phylogeny, and expression analyses of the 14-3-3 family reveal their involvement in the development, ripening, and abiotic stress response in banana.Crossref | GoogleScholarGoogle Scholar | 27713761PubMed |
Li B, Xiao G, Luo K, Wang Z, Mao B, Lin X, Guo X (2018) Overexpression of PvGF14c from Phyllostachys violascens delays flowering time in transgenic Arabidopsis. Frontiers in Plant Science 9, 105
| Overexpression of PvGF14c from Phyllostachys violascens delays flowering time in transgenic Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 29491870PubMed |
Liu D, Bienkowska J, Petosa C, Collier RJ, Fu H, Liddington R (1995) Crystal structure of the zeta isoform of the 14-3-3 protein. Nature 376, 191–194.
| Crystal structure of the zeta isoform of the 14-3-3 protein.Crossref | GoogleScholarGoogle Scholar | 7603574PubMed |
Liu J, Sun X, Liao W, Zhang J, Liang J, Xu W (2019) Involvement of OsGF14b adaptation in the drought resistance of rice plants. Rice (N Y) 12, 82
| Involvement of OsGF14b adaptation in the drought resistance of rice plants.Crossref | GoogleScholarGoogle Scholar |
Liu J, Jiang C, Kang L, Zhang H, Song Y, Zou Z, Zheng W (2020) Over-expression of a 14-3-3 protein from foxtail millet improves plant tolerance to salinity stress in Arabidopsis thaliana. Frontiers in Plant Science 11, 449
| Over-expression of a 14-3-3 protein from foxtail millet improves plant tolerance to salinity stress in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 32351536PubMed |
Macdonald N, Welburn JPI, Noble MEM, Nguyen A, Yaffe MB, Clynes D, Moggs JG, Orphanides G, Thomson S, Edmunds JW, Clayton AL, Endicott JA, Mahadevan LC (2005) Molecular basis for the recognition of phosphorylated and phosphoacetylated histone h3 by 14-3-3. Molecular Cell 20, 199–211.
| Molecular basis for the recognition of phosphorylated and phosphoacetylated histone h3 by 14-3-3.Crossref | GoogleScholarGoogle Scholar | 16246723PubMed |
Qin C, Cheng L, Shen J, Zhang Y, Cao H, Lu D, Shen C (2016) Genome-wide identification and expression analysis of the 14-3-3 family genes in Medicago truncatula. Frontiers in Plant Science 7, 320
| Genome-wide identification and expression analysis of the 14-3-3 family genes in Medicago truncatula.Crossref | GoogleScholarGoogle Scholar | 27047505PubMed |
Ren YR, Yang YY, Zhang R, You CX, Zhao Q, Hao YJ (2019) MdGRF11, an apple 14-3-3 protein, acts as a positive regulator of drought and salt tolerance. Plant Science 288, 110219
| MdGRF11, an apple 14-3-3 protein, acts as a positive regulator of drought and salt tolerance.Crossref | GoogleScholarGoogle Scholar | 31521216PubMed |
Roberts MR (2003) 14-3-3 proteins find new partners in plant cell signalling. Trends in Plant Science 8, 218–223.
| 14-3-3 proteins find new partners in plant cell signalling.Crossref | GoogleScholarGoogle Scholar | 12758039PubMed |
Roberts MR, Salinas J, Collinge DB (2002) 14-3-3 proteins and the response to abiotic and biotic stress. Plant Molecular Biology 50, 1031–1039.
| 14-3-3 proteins and the response to abiotic and biotic stress.Crossref | GoogleScholarGoogle Scholar | 12516870PubMed |
Sehnke PC, Chung H-J, Wu K, Ferl RJ (2001) Regulation of starch accumulation by granule-associated plant 14-3-3 proteins. Proceedings of the National Academy of Sciences of the United States of America 98, 765–770.
| Regulation of starch accumulation by granule-associated plant 14-3-3 proteins.Crossref | GoogleScholarGoogle Scholar | 11149942PubMed |
Shen C, Yuan J (2021) Genome-wide investigation and expression analysis of K+-transport-related gene families in Chinese cabbage (Brassica rapa ssp. pekinensis. Biochemical Genetics 59, 256–282.
| Genome-wide investigation and expression analysis of K+-transport-related gene families in Chinese cabbage (Brassica rapa ssp. pekinensis.Crossref | GoogleScholarGoogle Scholar | 32990910PubMed |
Shi H, Zhang Y (2014) Pear 14-3-3a gene (Pp14-3-3a) is regulated during fruit ripening and senescense, and involved in response to salicylic acid and ethylene signalling. Journal of Genetics 93, 747–753.
| Pear 14-3-3a gene (Pp14-3-3a) is regulated during fruit ripening and senescense, and involved in response to salicylic acid and ethylene signalling.Crossref | GoogleScholarGoogle Scholar | 25572233PubMed |
Sun X, Luo X, Sun M, Chen C, Ding X, Wang X, Yang S, Yu Q, Jia B, Ji W, Cai H, Zhu Y (2014) A Glycine soja 14-3-3 protein GsGF14o participates in stomatal and root hair development and drought tolerance in Arabidopsis thaliana. Plant and Cell Physiology 55, 99–118.
| A Glycine soja 14-3-3 protein GsGF14o participates in stomatal and root hair development and drought tolerance in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 24272249PubMed |
Tian F, Wang T, Xie Y, Zhang J, Hu J, Pandey GK (2015) Genome-wide identification, classification, and expression analysis of 14-3-3 gene family in Populus. PLoS One 10, e0123225
| Genome-wide identification, classification, and expression analysis of 14-3-3 gene family in Populus.Crossref | GoogleScholarGoogle Scholar | 25867623PubMed |
van Heusden GPH (2005) 14-3-3 proteins: regulators of numerous eukaryote proteins. IUBMB Life 57, 623–629.
| 14-3-3 proteins: regulators of numerous eukaryote proteins.Crossref | GoogleScholarGoogle Scholar |
Visconti S, D’Ambrosio C, Fiorillo A, Arena S, Muzi C, Zottini M, Aducci P, Marra M, Scaloni A, Camoni L (2019) Overexpression of 14-3-3 proteins enhances cold tolerance and increases levels of stress-responsive proteins of Arabidopsis plants. Plant Science 289, 110215
| Overexpression of 14-3-3 proteins enhances cold tolerance and increases levels of stress-responsive proteins of Arabidopsis plants.Crossref | GoogleScholarGoogle Scholar | 31623776PubMed |
Wang Y, Ling L, Jiang Z, Tan W, Liu Z, Wu L, Zhao Y, Xia S, Ma J, Wang G, Li W (2019) Genome-wide identification and expression analysis of the 14-3-3 gene family in soybean (Glycine max. PeerJ 7, e7950
| Genome-wide identification and expression analysis of the 14-3-3 gene family in soybean (Glycine max.Crossref | GoogleScholarGoogle Scholar | 31824753PubMed |
Yang X, Lee WH, Sobott F, Papagrigoriou E, Robinson CV, Grossmann JG, Sundström M, Doyle DA, Elkins JM (2006) Structural basis for protein–protein interactions in the 14-3-3 protein family. Proceedings of the National Academy of Sciences of the United States of America 103, 17237–17242.
| Structural basis for protein–protein interactions in the 14-3-3 protein family.Crossref | GoogleScholarGoogle Scholar | 17085597PubMed |
Yang Z-P, Li H-L, Guo D, Tang X, Peng S-Q (2014) Identification and characterization of the 14-3-3 gene family in Hevea brasiliensis. Plant Physiology and Biochemistry 80, 121–127.
| Identification and characterization of the 14-3-3 gene family in Hevea brasiliensis.Crossref | GoogleScholarGoogle Scholar | 24751399PubMed |
Yang Y, Yu M, Xu F, Yu Y, Liu C, Li J, Wang X (2015) Identification and expression analysis of the 14-3-3 gene family in the mulberry tree. Plant Molecular Biology Reporter 33, 1815–1824.
| Identification and expression analysis of the 14-3-3 gene family in the mulberry tree.Crossref | GoogleScholarGoogle Scholar |
Yang L, You J, Wang Y, Li J, Quan W, Yin M, Wang Q, Chan Z (2017) Systematic analysis of the G-box factor 14-3-3 gene family and functional characterization of GF14a in Brachypodium distachyon. Plant Physiology and Biochemistry 117, 1–11.
| Systematic analysis of the G-box factor 14-3-3 gene family and functional characterization of GF14a in Brachypodium distachyon.Crossref | GoogleScholarGoogle Scholar | 28575641PubMed |
Yashvardhini N, Bhattacharya S, Chaudhuri S, Sengupta DN (2018) Molecular characterization of the 14-3-3 gene family in rice and its expression studies under abiotic stress. Planta 247, 229–253.
| Molecular characterization of the 14-3-3 gene family in rice and its expression studies under abiotic stress.Crossref | GoogleScholarGoogle Scholar | 28956163PubMed |
Zhang Z-T, Zhou Y, Li Y, Shao S-Q, Li B-Y, Shi H-Y, Li X-B (2010) Interactome analysis of the six cotton 14-3-3s that are preferentially expressed in fibres and involved in cell elongation. Journal of Experimental Botany 61, 3331–3344.
| Interactome analysis of the six cotton 14-3-3s that are preferentially expressed in fibres and involved in cell elongation.Crossref | GoogleScholarGoogle Scholar | 20519337PubMed |
Zhang Y, Zhao H, Zhou S, He Y, Luo Q, Zhang F, Qiu D, Feng J, Wei Q, Chen L, Chen M, Chang J, Yang G, He G (2018) Expression of TaGF14b, a 14-3-3 adaptor protein gene from wheat, enhances drought and salt tolerance in transgenic tobacco. Planta 248, 117–137.
| Expression of TaGF14b, a 14-3-3 adaptor protein gene from wheat, enhances drought and salt tolerance in transgenic tobacco.Crossref | GoogleScholarGoogle Scholar | 29616395PubMed |
Zhang Z, Zhao H, Huang F, Long J, Song G, Lin W (2019) The 14-3-3 protein GF14f negatively affects grain filling of inferior spikelets of rice (Oryza sativa L. The Plant Journal 99, 344–358.
| The 14-3-3 protein GF14f negatively affects grain filling of inferior spikelets of rice (Oryza sativa L.Crossref | GoogleScholarGoogle Scholar | 30912217PubMed |
Zhou Y, Ge L, Li G, He P, Yang Y, Liu S (2020) In silico identification and expression analysis of Rare Cold Inducible 2 (RCI2) gene family in cucumber. Journal of Plant Biochemistry and Biotechnology 29, 56–66.
| In silico identification and expression analysis of Rare Cold Inducible 2 (RCI2) gene family in cucumber.Crossref | GoogleScholarGoogle Scholar |
Zuo X, Wang S, Xiang W, Yang H, Tahir MM, Zheng S, An N, Han M, Zhao C, Zhang D (2021) Genome-wide identification of the 14-3-3 gene family and its participation in floral transition by interacting with TFL1/FT in apple. BMC Genomics 22, 41
| Genome-wide identification of the 14-3-3 gene family and its participation in floral transition by interacting with TFL1/FT in apple.Crossref | GoogleScholarGoogle Scholar | 33419402PubMed |