Abstract
Ovate Family Proteins (OFPs) belong to a plant-specific transcription factor family. They have been found to have significant roles in growth and development in Arabidopsis and tomato; however, little is known regarding their role in banana. Thus, a genome-wide study of OFP genes in banana was conducted for the first time in the present study. The results demonstrated that 49 OFP family members are unequally distributed across 11 chromosomes. Phylogenetic analysis grouped these genes into two subfamilies and eight subgroups, which was confirmed by the conserved motif and gene structure analysis. Furthermore, MaOFPs genes duplicates were found to have originated from whole-genome duplication (WGD). The expression patterns of the genes in the various tissues and at different fruit development and ripening stages in the BaXi Jiao (BX) and Feng Jiao (FJ), banana cultivars were elucidated using transcriptome analysis. Using co-expression network analysis, MaOFP1 was found to interact not only with MaMADS36 but also with hormone response proteins. These findings improve our understanding of the functions of MaOFPs genes in the control of plant hormone signal transduction pathways during banana growth and ripening, which should inform the genetic improvement of important agricultural characters.
Similar content being viewed by others
Data Availability
The identified OFP gene sequences of the DH-Pahang genome can be obtained from the banana genome database (https://banana-genome.cirad.fr/) (The accession numbers were listed in Supplementary Table S1).
References
Azzi L, Deluche C, Gévaudant F, Frangne N, Delmas F, Hernould M, Chevalier C (2015) Fruit growth-related genes in tomato. J Exp Bot 66(4):1075–1086. https://doi.org/10.1093/jxb/eru527
Chen L, Zhong HY, Kuang JF, Li JG, Lu WJ, Chen JY (2011) Validation of reference genes for RT-qPCR studies of gene expression in banana fruit under different experimental conditions. Planta 234(2):377–390. https://doi.org/10.1007/s00425-011-1410-3
D’Hont A, Denoeud F, Aury JM, Baurens FC, Carreel F, Garsmeur O et al (2012) The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488(7410):213–217. https://doi.org/10.1038/nature11241
Dale J, James A, Paul JY, Khanna H, Smith M, Peraza-Echeverria S, Garcia-Bastidas F, Kema G, Waterhouse P, Mengersen K, Harding R (2017) Transgenic Cavendish bananas with resistance to Fusarium wilt tropical race 4. Nat Commun 8(1):1496. https://doi.org/10.1038/s41467-017-01670-6
Davey MW, Gudimella R, Harikrishna JA, Sin LW, Khalid N, Keulemans J (2013) A draft Musa balbisiana genome sequence for molecular genetics in polyploid, inter- and intra-specific Musa hybrids. BMC Genomics 14:683. https://doi.org/10.1186/1471-2164-14-683
Eddy SR (2011) Accelerated profile HMM searches. PLoS Comp Biol 7(10):e1002195. https://doi.org/10.1371/journal.pcbi.1002195
Hackbusch J, Richter K, Müller J, Salamini F, Uhrig JF (2005) A central role of Arabidopsis thaliana ovate family proteins in networking and subcellular localization of 3-aa loop extension homeodomain proteins. Proc Natl Acad Sci USA 102(13):4908–4912. https://doi.org/10.1073/pnas.0501181102
Ku HM, Liu J, Doganlar S, Tanksley SD (2001) Exploitation of Arabidopsis-tomato synteny to construct a high-resolution map of the ovate-containing region in tomato chromosome 2. Genome 44(3):470–475
Li E, Wang S, Liu Y, Chen JG, Douglas CJ (2011) OVATE FAMILY PROTEIN4 (OFP4) interaction with KNAT7 regulates secondary cell wall formation in Arabidopsis thaliana. Plant J 67(2):328–341. https://doi.org/10.1111/j.1365-313X.2011.04595.x
Liu J, van Eck J, Cong B, Tanksley SD (2002) A new class of regulatory genes underlying the cause of pear-shaped tomato fruit. Proc Natl Acad Sci USA 99(20):13302–13306. https://doi.org/10.1073/pnas.162485999
Liu D, Sun W, Yuan Y, Zhang N, Hayward A, Liu Y, Wang Y (2014) Phylogenetic analyses provide the first insights into the evolution of OVATE family proteins in land plants. Ann Bot 113(7):1219–1233. https://doi.org/10.1093/aob/mcu061
Liu J, Zhang J, Miao H, Jia C, Wang J, Xu B, Jin Z (2017) Elucidating the mechanisms of the tomato ovate mutation in regulating fruit quality using proteomics analysis. J Agric Food Chem 65(46):10048–10057. https://doi.org/10.1021/acs.jafc.7b03656
Liu JH, Zhang J, Wang JY, Zhang JB, Miao HX, Jia CH, Wang Z, Xu BY, Jin ZQ (2018) MuMADS1 and MaOFP1 regulate fruit quality in a tomato ovate mutant. Plant Biotechnol J 16(5):989–1001. https://doi.org/10.1111/pbi.12843
Liu J, Zhang J, Hu W, Miao H, Zhang J, Jia C, Wang Z, Xu B, Jin Z (2015) Banana Ovate family protein MaOFP1 and MADS-box protein MuMADS1 antagonistically regulated banana fruit ripening. PLoS ONE 10(4):e0123870. https://doi.org/10.1371/journal.pone.0123870
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−△△CT method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Mohapatra D, Mishra S, Sutar N (2010) Banana and its by-product utilization: an overview. J Sci Ind Res 69:323–329
Monforte AJ, Diaz A, Caño-Delgado A, van der Knaap E (2014) The genetic basis of fruit morphology in horticultural crops: lessons from tomato and melon. J Exp Bot 65(16):4625–4637. https://doi.org/10.1093/jxb/eru017
Nuruzzaman M, Manimekalai R, Sharoni AM, Satoh A, Kondoh H, Ooka H, Kikuchi S (2010) Genome-wide analysis of NAC transcription factor family in rice. Gene 465(1–2):30–44. https://doi.org/10.1016/j.gene.2010.06.008
Pagnussat GC, Yu HJ, Sundaresan V (2007) Cell-fate switch of synergid to egg cell in Arabidopsis eostre mutant embryo sacs arises from misexpression of the BEL1-like homeodomain gene BLH1. Plant Cell 19(11):3578–3592. https://doi.org/10.1105/tpc.107.054890
Pillay M, Tenkouano A (2011) Banana breeding: progress and challenges. Taylor and Francis Group LLC., CRC Press, Boca Raton
Schmitz AJ, Begcy K, Sarat GH, Walia H (2015) Rice Ovate Family Protein 2 (OFP2) alters hormonal homeostasis and vasculature development. Plant Sci 241:177–188. https://doi.org/10.1016/j.plantsci.2015.10.011
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13(11):2498–2504. https://doi.org/10.1101/gr.1239303
Shu Y, Yu D, Wang D, Guo D, Guo C (2013) Genome-wide survey and expression analysis of the MADS-box gene family in soybean. Mol Biol Rep 40(6):3901–3911. https://doi.org/10.1007/s11033-012-2438-6
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. Mol Biol Evol 28(10):2731–2739. https://doi.org/10.1093/molbev/msr121
Thangavel G, Nayar S (2018) A survey of MIKC type MADS-box genes in non-seed plants: algae, bryophytes, lycophytes and ferns. Fron Plant Sci 9:510. https://doi.org/10.3389/fpls.2018.00510
Theißen G, Rümpler F, Gramzow L (2018) Array of MADS-box genes: facilitator for rapid adaptation? Trends Plant Sci 23(7):563–576. https://doi.org/10.1016/j.tplants.2018.04.008
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
Tsaballa A, Athanasiadis C, Pasentsis K, Ganopoulos I, Nianiou-Obeidat I, Tasftaris A (2013) Molecular studies of inheritable grafting induced changes in pepper (Capsicum annuum) fruit shape. Sci Hortic 149:2–8
van der Knaap E, Tanksley SD (2001) Identification and characterization of a novel locus controlling early fruit development in tomato. Theor Appl Genet 103:353–358
Wang S, Chang Y, Guo J, Chen JG (2007) Arabidopsis Ovate Family Protein 1 is a transcriptional repressor that suppresses cell elongation. Plant J 50(5):858–872. https://doi.org/10.1111/j.1365-313X.2007.03096.x
Wang L, Feng Z, Wang X, Wang X, Zhang X (2010a) DEGseq: an R package for identifying differentially expressed genes from RNAseq data. Bioinformatics 26:136–138
Wang S, Chang Y, Guo J, Zeng Q, Ellis BE, Chen JG (2011) Arabidopsis Ovate Family Proteins, a novel transcriptional repressor family, control multiple aspects of plant growth and development. PLoS ONE 6(8):e23896. https://doi.org/10.1371/journal.pone.0023896
Wang L, Li J, Zhao J, He C (2015) Evolutionary developmental genetics of fruit morphological variation within the Solanaceae. Front Plant Sci 6:248. https://doi.org/10.3389/fpls.2015.00248
Wang S, Chang Y, Ellis B (2016) Overview of OVATE FAMILY PROTEINS, a novel class of plant-specific growth regulators. Front Plant Sci 7:417. https://doi.org/10.3389/fpls.2016.00417
Wang YK, Chang WC, Liu PF, Hsiao MK, Lin CT, Lin SM, Rong-Long Pan RL (2010b) Ovate family protein1 as a plant Ku70 interacting protein involving in DNA double-strand break repair. Plant Mol Biol 74(4–5):453–466. https://doi.org/10.1007/s11103-010-9685-5
Wu S, Clevenger JP, Sun L, Visa S, Kamiya Y, Jikumaru Y, Blakeslee J, van der Knaap E (2015) The control of tomato fruit elongation orchestrated by sun, ovate and fs8.1 in a wild relative of tomato. Pant Sci 238:95–104. https://doi.org/10.1016/j.plantsci.2015.05.019
Xu BY, Su W, Liu JH, Wang JB, Jin ZQ (2007) Differentially expressed cDNAs at the early stage of banana ripening identified by suppression subtractive hybridization and cDNA microarray. Planta 226(2):529–539. https://doi.org/10.1007/s00425-007-0502-6
Acknowledgements
This work was financially supported by the National Natural Science Foundation of China (NNSFC) (31872161), the National Natural Science Foundation of Hainan Province (2019CXTD412), the Central Public-interest Scientific Institution Basal Research Fund for Innovative Research Team Program of CATAS (1630052017018; 1630052019024) and the earmarked fund for Modern Agro-industry Technology Research System (CARS-31).
Author information
Authors and Affiliations
Contributions
JHL, ZQJ and BYXu conceived the study. JYW, CHJ and JBZ performed the experiments and carried out the analysis. JZ, HXM and BYXie designed the experiments and wrote the manuscript. All authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors claim no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zhang, J., Miao, H., Xie, B. et al. Genomic and Transcriptional Analysis of Banana Ovate Family Proteins Reveals Their Relationship with Fruit Development and Ripening. Biochem Genet 58, 412–429 (2020). https://doi.org/10.1007/s10528-020-09951-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10528-020-09951-4