Abstract
Plant 14–3-3 proteins play key roles in regulating growth, development, and stress responses. However, little is known about this gene family in papaya (Carica papaya L.). We characterized eight 14–3-3 genes from the papaya genome and designed them as CpGRF1–8. Based on phylogenetic, conserved motif, and gene structure analyses, papaya CpGRFs were divided into ε and non-ε groups. Expression analysis showed differential and class-specific transcription patterns in different organs. Quantitative real-time polymerase chain reaction analysis showed that most CpGRFs had large changes in expression during fruit development and ripening. This indicated that the CpGRFs were involved in regulating fruit development and ripening. Significant expression changes occurred after cold, salt, and drought treatments in papaya seedlings, indicating that CpGRFs were also involved in signaling responses to abiotic stress. These results provide a transcription profile of 14–3-3 genes in organs, during fruit development and ripening and in response to stress. Some highly expressed, fruit-specific, and stress-responsive candidate CpGRFs will be identified for further genetic improvement of papayas.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
The identified 14–3-3 gene sequences can be obtained from the Carica papaya ASGPBv0.4 genome database (https://phytozome.jgi.doe.gov/pz/portal.html/) (accession numbers are listed in Table S1).
References
Bian S, Li R, Xia S, Liu Y, Jin D, Xie X, Dhaubhadel S, Zhai L, Wang J, Li X (2018) Soybean CCA1-like MYB transcription factor GmMYB133 modulates isoflavonoid biosynthesis. Biochem Biophys Res Commun 507(1–4):324–329. https://doi.org/10.1016/j.bbrc.2018.11.033
Camoni L, Visconti S, Aducci P, Marra M (2018) Proteins in plant hormone signaling: doing several things at once. Front Plant Sci 9:297. https://doi.org/10.3389/fpls.2018.00297
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. Front Plant Sci 7:1099. https://doi.org/10.3389/fpls.2016.01099
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. Front Plant Sci 7:12. https://doi.org/10.3389/fpls.2016.00012
Chen T, Chen JH, Zhang W, Yang G, Yu LJ, Li DM, Li B, Sheng HM, Zhang H, An LZ (2019) BYPASS1-LIKE, A DUF793 family protein, participates in freezing tolerance via the CBF pathway in Arabidopsis. Front Plant Sci 10:807. https://doi.org/10.3389/fpls.2019.00807
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(1):579. https://doi.org/10.1186/s12864-018-4955-8
Chevalier D, Morris ER, Walker JC (2009) 14–3–3 and FHA domains mediate phosphoprotein interactions. Annu Rev Plant Biol 60:67–91. https://doi.org/10.1146/annurev.arplant.59.025607.092844
Collani S, Neumann M, Yant L, Schmid M (2019) FT modulates genome-wide DNA-binding of the bZIP transcription factor FD. Plant Physiol 180(1):367–380. https://doi.org/10.1104/pp.18.01505
Cotelle V, Leonhardt N (2016) 14–3–3 Proteins in guard cell signaling. Front Plant Sci 6:1210. https://doi.org/10.3389/fpls.2015.01210
de Boer AH, van Kleeff PJ, Gao J (2013) Plant 14–3–3 proteins as spiders in a web of phosphorylation. Protoplasma 250:425–440. https://doi.org/10.1007/s00709-012-0437-z
Ghorbel M, Zaidi I, Ebel C, Hanin M (2019) Differential regulation of the durum wheat MAPK phosphatase 1 by calmodulin, bivalent cations and possibly mitogen activated protein kinase 3. Plant Physiol Biochem 135:242–252. https://doi.org/10.1016/j.plaphy.2018.12.016
Guo J, Dai S, Li H, Liu A, Liu C, Cheng D, Cao X, Chu X, Zhai S, Liu J, Zhao Z, Song J (2018) Identification and expression analysis of wheat TaGF14 Genes. Front Genet 9:12. https://doi.org/10.3389/fgene.2018.00012
Hernández-Domínguez EE, Vargas-Ortiz E, Bojórquez-Velázquez E, Barrera-Pacheco A, Santos-Díaz MS, Camarena-Rangel NG, Barba de la Rosa AP (2019) Molecular characterization and in vitro interaction analysis of Op14–3–3 μ protein from Opuntia ficus-indica: identification of a new client protein from shikimate pathway. J Proteomics 198:151–162. https://doi.org/10.1016/j.jprot.2019.01.013
Huang X, Zhang Q, Jiang Y, Yang C, Wang Q, Li L (2018) Shade-induced nuclear localization of PIF7 is regulated by phosphorylation and 14–3–3 proteins in Arabidopsis. Elife 7:31636. https://doi.org/10.7554/eLife.31636
Huang Y, Cao H, Yang L, Chen C, Shabala L, Xiong M, Niu M, Liu J, Zheng Z, Zhou L, Peng Z, Bie Z, Shabala S (2019) Tissue-specific respiratory burst oxidase homologue -dependent H2O2 signaling to the plasma membrane H+-ATPase confers potassium uptake and salinity tolerance in Cucurbitaceae. J Exp Bot. https://doi.org/10.1093/jxb/erz328
Laughner B, Lawrence SD, Ferl RJ (1995) Two cDNA clones encoding 14–3–3 homologs from tomato fruit. Biochim Biophys Acta 1263(1):67–70. https://doi.org/10.1016/0167-4781(95)00092-u
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. Front Plant Sci 9:105. https://doi.org/10.3389/fpls.2018.00105
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. Front Plant Sci 7:1442. https://doi.org/10.3389/fpls.2016.01442
Li MY, Xu BY, Liu JH, Yang XL, Zhang JB, Jia CH, Ren LC, Jin ZQ (2012) Identification and expression analysis of four 14–3–3 genes during fruit ripening in banana (Musa acuminata L AAA group, cv Brazilian). Plant Cell Rep 31(2):369–378. https://doi.org/10.1007/s00299-011-1172-1
Li R, Jiang X, Jin D, Dhaubhadel S, Bian S, Li X (2015) Identification of 14–3–3 family in common bean and their response to abiotic stress. PLoS ONE 10(11):0143280. https://doi.org/10.1371/journal.pone.0143280
Liu K, Yuan C, Li H, Lin W, Yang Y, Shen C, Zheng X (2015) Genome-wide identification and characterization of auxin response factor (ARF) family genes related to flower and fruit development in papaya (Carica papaya L.). BMC Genomics 16:901. https://doi.org/10.1186/s12864-015-2182-0
Lu Y, Yasuda S, Li X, Fukao Y, Tohge T, Fernie AR, Matsukura C, Ezura H, Sato T, Yamaguchi J (2016) Characterization of ubiquitin ligase SlATL31 and proteomic analysis of 14–3–3 targets in tomato fruit tissue (Solanum lycopersicum L.). J Proteomics 143:254–264. https://doi.org/10.1016/j.jprot.2016.04.016
Minami A, Takahashi K, Inoue SI, Tada Y, Kinoshita T (2019) Brassinosteroid induces phosphorylation of the plasma membrane H+-ATPase during hypocotyl elongation in Arabidopsis thaliana. Plant Cell Physiol 60(5):935–944. https://doi.org/10.1093/pcp/pcz005
Ming R, Hou S, Feng Y, Yu Q, Dionne-Laporte A, Saw JH, Senin P, Wang W, Ly BV, Lewis KL, Salzberg SL, Feng L, Jones MR, Skelton RL, Murray JE, Chen C, Qian W, Shen J, Du P, Eustice M, Tong E, Tang H, Lyons E, Paull RE, Michael TP, Wall K, Rice DW, Albert H, Wang ML, Zhu YJ, Schatz M, Nagarajan N, Acob RA, Guan P, Blas A, Wai CM, Ackerman CM, Ren Y, Liu C, Wang J, Wang J, Na JK, Shakirov EV, Haas B, Thimmapuram J, Nelson D, Wang X, Bowers JE, Gschwend AR, Delcher AL, Singh R, Suzuki JY, Tripathi S, Neupane K, Wei H, Irikura B, Paidi M, Jiang N, Zhang W, Presting G, Windsor A, Navajas-Pérez R, Torres MJ, Feltus FA, Porter B, Li Y, Burroughs AM, Luo MC, Liu L, Christopher DA, Mount SM, Moore PH, Sugimura T, Jiang J, Schuler MA, Friedman V, Mitchell-Olds T, Shippen DE, dePamphilis CW, Palmer JD, Freeling M, Paterson AH, Gonsalves D, Wang L, Alam M (2008) The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452(7190):991–996. https://doi.org/10.1038/nature06856
Pandit SS, Kulkarni RS, Giri AP, Köllner TG, Degenhardt J, Gershenzon J, Gupta VS (2010) Expression profiling of various genes during the fruit development and ripening of mango. Plant Physiol Biochem 48(6):426–433. https://doi.org/10.1016/j.plaphy.2010.02.012
Paul AL, Denison FC, Schultz ER, Zupanska AK, Ferl RJ (2012) 14–3–3 phosphoprotein interaction networks - does isoform diversity present functional interaction specification? Front Plant Sci 3:190. https://doi.org/10.3389/fpls.2012.00190
Prado K, Cotelle V, Li G, Bellati J, Tang N, Tournaire-Roux C, Martinière A, Santoni V, Maurel C (2019) Oscillating aquaporin phosphorylation and 14–3–3 proteins mediate the circadian regulation of leaf hydraulics. Plant Cell 31(2):417–429. https://doi.org/10.1105/tpc.18.00804
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. Front Plant Sci 7:320. https://doi.org/10.3389/fpls.2016.00320
Shang S, Wu C, Huang C, Tie W, Yan Y, Ding Z, Xia Z, Wang W, Peng M, Tian L, Hu W (2018) Genome-wide analysis of the GRF family reveals their involvement in abiotic stress response in cassava. Genes (basel) 9(2):110. https://doi.org/10.3390/genes9020110
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. J Genet 93(3):747–753
Tian F, Wang T, Xie Y, Zhang J, Hu J (2015) Genome-wide identification, classification, and expression analysis of 14–3–3 gene family in Populus. PLoS ONE 10(4):0123225. https://doi.org/10.1371/journal.pone.0123225
Trapnell C, Roberts A, Goff LA, Pachter L (2012) Differential gene and transcript expression analysis of RNA-Seq experiments with TopHat and Cufflinks. Nat Protoc 7(3):562–578. https://doi.org/10.1038/nprot.2012.016
Vitavska O, Bartölke R, Tabke K, Heinisch JJ, Wieczorek H (2018) Interaction of mammalian and plant H+/sucrose transporters with 14–3–3 proteins. Biochem J 475(20):3239–3254. https://doi.org/10.1042/BCJ20180293
Wen C, Zhao W, Liu W, Yang L, Wang Y, Liu X, Xu Y, Ren H, Guo Y, Li C, Li J, Weng Y, Zhang X (2019) CsTFL1 inhibits determinate growth and terminal flower formation through interaction with CsNOT2a in cucumber. Development 146(14):180166. https://doi.org/10.1242/dev.180166
Xiao G, Li B, Chen H, Chen W, Wang Z, Mao B, Gui R, Guo X (2018) Overexpression of PvCO1, a bamboo CONSTANS-LIKE gene, delays flowering by reducing expression of the FT gene in transgenic Arabidopsis. BMC Plant Biol 18(1):232. https://doi.org/10.1186/s12870-018-1469-0
Yang Z, Wang C, Xue Y, Liu X, Chen S, Song C, Yang Y, Guo Y (2019) Calcium-activated 14–3–3 proteins as a molecular switch in salt stress tolerance. Nat Commun 10(1):1199. https://doi.org/10.1038/s41467-019-09181-2
Yao Y, Du Y, Jiang L, Liu JY (2007) Molecular analysis and expression patterns of the 14-3-3 gene family from Oryza sativa. J Biochem Mol Biol 40(3):349–357
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 Physiol Biochem 117:1–11. https://doi.org/10.1016/j.plaphy.2017.05.013
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.). Plant J 99(2):344–358. https://doi.org/10.1111/tpj.14329
Zhang L, Li G, Li Y, Min J, Kronzucker HJ, Shi W (2018a) Tomato plants ectopically expressing Arabidopsis GRF9 show enhanced resistance to phosphate deficiency and improved fruit production in the field. J Plant Physiol 226:31–39. https://doi.org/10.1016/j.jplph.2018.04.005
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 (2018b) Expression of TaGF14b, a 14–3–3 adaptor protein gene from wheat, enhances drought and salt tolerance in transgenic tobacco. Planta 248(1):117–137. https://doi.org/10.1007/s00425-018-2887-9
Zhu X, Li X, Chen W, Chen J, Lu W, Chen L, Fu D (2012) Evaluation of new reference genes in papaya for accurate transcript normalization under different experimental conditions. PLoS ONE 7(8):44405. https://doi.org/10.1371/journal.pone.0044405
Acknowledgements
This work was supported by the Key Research and Development Project of Hainan Province (ZDYF2017017), Central Public-interest Scientific Institution Basal Research Fund for Chinese Academy of Tropical Agricultural Sciences (No. 1630052017015), and the National Natural Science Foundation of China (31201663). None of these organizations influenced the study design, the data analysis, and the decision to submit manuscript for publication. We thank LetPub (www.letpub.com) for its linguistic assistance during the preparation of this manuscript.
Author information
Authors and Affiliations
Contributions
The study was designed by APG, MYL, and LCR. ZZ, WH, SSX, XLY, ZHD, YY, WWT, and JHY conducted the experiments and analyzed the data. MYL and APG wrote the manuscript. The final manuscript was read and approved by all authors.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflicts of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Li, M., Ren, L., Zou, Z. et al. Identification and Expression Analyses of the Special 14–3-3 Gene Family in Papaya and its Involvement in Fruit Development, Ripening, and Abiotic Stress Responses. Biochem Genet 59, 1599–1616 (2021). https://doi.org/10.1007/s10528-021-10077-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10528-021-10077-4