Abstract
Growth-regulating factor (GRF) proteins are vital in regulating plant growth, development, and abiotic stress response. However, little information is known about the GRF gene family in the sweet cherry. This study identified nine PavGRFs from the sweet cherry genome and classified into three clades by phylogenetic, conserved motif, and gene structure analyses. Sequence analysis indicated that genes in the same clade had similar gene structures and all members contained QLQ (Gln-Leu-Gln) and WRC(Trp-Arg-Cys) domains. In addition, evolutionary analyses revealed that soybean and sweet cherry had the highest number of co-linear gene pairs, and among Rosaceae, peach and pear had a pattern of co-linear gene pairs that was largely similar to that of sweet cherry. Furthermore, the promoters of PavGRFs were found to contain many MYB-MYC elements and elements related to abiotic stress responses such as low-temperature response elements (LTRs) and damage-inducible elements (WRE3, W box), and the predicted protein-interaction network of PavGRFs discovered that most PavGRFs could interact with AtGIF1.Tissue-specific expression of the PavGRFs was analyzed using qRT-PCR, and it was found that the expression of the PavGRFs was higher during the dormant period of the flower buds and throughout fruit development. The expression patterns of PavGRFs under cold stress were investigated and four PavGRFs were found to be significantly up-regulated in expression levels under cold treatment. In conclusion, this study systematically analyzed the bioinformatics and expression patterns of PavGRFs and provided a basis for further understanding of the role of the PavGRF family in the response of the sweet cherry to cold stress and growth and development.
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References
Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:202–208. https://doi.org/10.1093/nar/gkp335
Baucher M, Moussawi J, Vandeputte OM, Monteyne D, Mol A, Pérez-Morga D, El Jaziri M (2013) A role for the miR396/GRF network in specification of organ type during flower development, as supported by ectopic expression of Populus trichocarpa miR396c in transgenic tobacco. Plant Biol 15:892–898. https://doi.org/10.1111/j.1438-8677.2012.00696.x
Bodenhofer U, Bonatesta E, Horejs-Kainrath C, Hochreiter S (2015) msa: an R package for multiple sequence alignment. Bioinformatics 31:3997–3999. https://doi.org/10.1093/bioinformatics/btv494
Brown AP, Dunn MA, Goddard NJ, Hughes MA (2001) Identification of a novel low-temperature-response element in the promoter of the barley (Hordeum vulgare L.) gene blt101.1. Planta 213:770–780. https://doi.org/10.1007/s004250100549
Cai X, Zhang L, Xiao L, Wen Z, Hou Q, Yang K (2022) Genome-wide identification of GRF gene family and their contribution to abiotic stress response in pitaya (Hylocereus polyrhizus). Int J Biol Macromol 223:618–635. https://doi.org/10.1016/j.ijbiomac.2022.10.284
Cao Y, Hang Y, Jin Q, Lin Y, Cai Y (2016) Comparative Genomic analysis of the GRF genes in Chinese pear (Pyrus bretschneideri Rehd), poplar (Populous), grape (Vitis vinifera), Arabidopsis and Rice (Oryza sativa). Front Plant Sci 7:1750. https://doi.org/10.3389/fpls.2016.01750
Cao JF, Huang JQ, Liu X, Huang CC, Zheng ZS, Zhang XF, Shangguan XX, Wang LJ, Zhang YG, Wendel JF, Grover CE, Chen ZW (2020) Genome-wide characterization of the GRF family and their roles in response to salt stress in Gossypium. BMC Genom 21:1–16. https://doi.org/10.1186/s12864-020-06986-0
Chen F, Yang Y, Luo X, Zhou W, Dai Y, Zheng C, Liu W, Yang W, Shu K (2019) Genome-wide identification of GRF transcription factors in soybean and expression analysis of GmGRF family under shade stress. Bmc Plant Biol 19:1–13. https://doi.org/10.1186/s12870-019-1861-4
Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202. https://doi.org/10.1016/j.molp.2020.06.009
Chen GZ, Huang J, Zhou XQ, Hao Y, Chen JL, Zhou YZ, Ahmad S, Lan S, Liu ZJ, Peng DH (2022) Comprehensive analysis for GRF transcription factors in sacred lotus (Nelumbo nucifera). Int J Mol Sci 23:6673. https://doi.org/10.3390/ijms23126673
Cheng Z, Wen S, Wu Y, Shang L, Wu L, Lyu D, Yu H, Wang J, Jian H (2023) Comparatively evolution and expression analysis of GRF transcription factor genes in seven plant species. Plants 12:2790
Chou KC, Shen HB (2010) A new method for predicting the subcellular localization of eukaryotic proteins with both single and multiple sites: Euk-mPLoc 2.0. PLoS ONE 5:e9931. https://doi.org/10.1371/journal.pone.0009931
Cittadini ED, de Ridder N, Peri PL, van Keulen H (2006) A method for assessing frost damage risk in sweet cherry orchards of South Patagonia. Agr Forest Meteorol 141:235–243. https://doi.org/10.1016/j.agrformet.2006.10.011
Debernardi JM, Mecchia MA, Vercruyssen L, Smaczniak C, Kaufmann K, Inze D, Rodriguez RE, Palatnik JF (2014) Post-transcriptional control of GRF transcription factors by microRNA miR396 and GIF co-activator affects leaf size and longevity. Plant J 79:413–426. https://doi.org/10.1111/tpj.12567
Dunn MA, White AJ, Vural S, Hughes MA (1998) Identification of promoter elements in a low-temperature-responsive gene (blt4.9) from barley (Hordeum vulgare L.). Plant Mol Biol 38:551–564. https://doi.org/10.1023/a:1006098132352
Duvaud S, Gabella C, Lisacek F, Stockinger H, Ioannidis V, Durinx C (2021) Expasy, the swiss bioinformatics resource portal, as designed by its users. Nucleic Acids Res 49:216–227. https://doi.org/10.1093/nar/gkab225
Fonini LS, Lazzarotto F, Barros PM, Cabreira-Cagliari C, Begossi Martins MA, Saibo NJM, Turchetto-Zolet AC, Margis-Pinheiro M (2020) Molecular evolution and diversification of the GRF transcription factor family. Genet Mol Biol. https://doi.org/10.1590/1678-4685-gmb-2020-0080
He Z, Zhang H, Gao S, Lercher MJ, Chen WH, Hu S (2016) Evolview v2: an online visualization and management tool for customized and annotated phylogenetic trees. Nucleic Acids Res 44:236–241. https://doi.org/10.1093/nar/gkw370
Heidel AJ, Clarke JD, Antonovics J, Dong X (2004) Fitness costs of mutations affecting the systemic acquired resistance pathway in Arabidopsis thaliana. Genetics 168:2197–2206. https://doi.org/10.1534/genetics.104.032193
Hernandez-Garcia CM, Finer JJ (2014) Identification and validation of promoters and cis-acting regulatory elements. Plant Sci 217:109–119. https://doi.org/10.1016/j.plantsci.2013.12.007
Hong JK, Suh EJ, Lee SB, Yoon HJ, Lee YH (2018) Effects of overexpression of Brassica rapa GROWTH-REGULATING FACTORgenes on B. napus organ size. Korean J Breed Sci 50:378–386. https://doi.org/10.9787/kjbs.2018.50.4.378
Horiguchi G, Kim GT, Tsukaya H (2005) The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana. Plant J 43:68–78. https://doi.org/10.1111/j.1365-313X.2005.02429
Hou QD, Hong Y, Wen Z, Shuang CQ, Li ZC, Cai XW, Qiao G, Wen XP (2023) Molecular characterization of the SAUR gene family in sweet cherry and functional analysis of PavSAUR55 in the process of abscission. J Integr Agr 22:1720–1739. https://doi.org/10.1016/j.jia.2023.04.031
Jing S, Malladi A (2022) Identification of potential regulators of cell production and early fruit growth in apple (Malus x domestica Borkh.). Sci Hortic 297:110939. https://doi.org/10.1016/j.scienta.2022.110939
Jung S, Lee T, Cheng CH, Buble K, Zheng P, Yu J, Humann J, Ficklin SP, Gasic K, Scott K, Frank M, Ru S, Hough H, Evans K, Peace C, Olmstead M, DeVetter LW, McFerson J, Coe M, Wegrzyn JL, Staton ME, Abbott AG, Main D (2019) 15 years of GDR: new data and functionality in the genome database for rosaceae. Nucleic Acids Res 47:1137–1145. https://doi.org/10.1093/nar/gky1000
Kim JH (2019) Biological roles and an evolutionary sketch of the GRF-GIF transcriptional complex in plants. BMB Rep 52:227–238. https://doi.org/10.5483/BMBRep.2019.52.4.051
Kim JH, Tsukaya H (2015) Regulation of plant growth and development by the GROWTH-REGULATING FACTOR and GRF-INTERACTING FACTOR duo. J Exp Bot 66:6093–6107. https://doi.org/10.1093/jxb/erv349
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Lantzouni O, Alkofer A, Falter-Braun P, Schwechheimer C (2020) GROWTH-REGULATING FACTORS Interact with DELLAs and regulate growth in cold stress. Plant Cell 32:1018–1034. https://doi.org/10.1105/tpc.19.00784
Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouze P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327. https://doi.org/10.1093/nar/30.1.325
Levine M, Tjian R (2003) Transcription regulation and animal diversity. Nature 424:147–151. https://doi.org/10.1038/nature01763
Li S, Gao F, Xie K, Zeng X, Cao Y, Zeng J, He Z, Ren Y, Li W, Deng Q, Wang S, Zheng A, Zhu J, Liu H, Wang L, Li P (2016) The OsmiR396c-OsGRF4-OsGIF1 regulatory module determines grain size and yield in rice. Plant Biotechnol J 14:2134–2146. https://doi.org/10.1111/pbi.12569
Li Z, Xie Q, Yan J, Chen J, Chen Q (2021) Genome-wide identification and characterization of the abiotic-stress-responsive GRF gene family in diploid woodland strawberry (Fragaria vesca). Plants-Basel 10:1916. https://doi.org/10.3390/plants10091916
Li H, Qiu T, Zhou Z, Kang L, Chen R, Zeng L, Yu H, Wang Y, Song J (2023) Genome-wide analysis of the growth-regulating factor family in Medicago truncatula. J Plant Growth Regul 42:2305–2316. https://doi.org/10.1007/s00344-022-10704-3
Li X (2011) Infiltration of Nicotiana benthamiana protocol for transient expression via agrobacterium. Bio-protocol e95-e95.
Liebsch D, Palatnik JF (2020) MicroRNA miR396, GRF transcription factors and GIF co-regulators: a conserved plant growth regulatory module with potential for breeding and biotechnology. Curr Opin Plant Biol 53:31–42. https://doi.org/10.1016/j.pbi.2019.09.008
Liu X, Guo LX, Jin LF, Liu YZ, Liu T, Fan YH, Peng SA (2016) Identification and transcript profiles of citrus growth-regulating factor genes involved in the regulation of leaf and fruit development. Mol Biol Rep 43:1059–1067. https://doi.org/10.1007/s11033-016-4048-1
Liu L, Li XJ, Li B, Sun MY, Li SX (2022) Genome-wide analysis of the GRF gene family their expression profiling in peach (Prunus persica). J Plant Interact 17:437–449. https://doi.org/10.1080/17429145.2022.2045370
Liu Y, Guo P, Wang J, Xu ZY (2023) Growth-regulating factors: conserved and divergent roles in plant growth and development and potential value for crop improvement. Plant J 113:1122–1145. https://doi.org/10.1111/tpj.16090
Marchler-Bauer A, Zheng C, Chitsaz F, Derbyshire MK, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lanczycki J, Lu F, Lu S, Marchler GH, Song JS, Thanki N, Yamashita RA, Zhang D, Bryant SH (2013) CDD: conserved domains and protein three-dimensional structure. Nucleic Acids Res 41:348–352. https://doi.org/10.1093/nar/gks1243
Mascarenhas D, Mettler IJ, Pierce DA, Lowe HW (1990) Intron-mediated enhancement of heterologous gene expression in maize. Plant Mol Biol 15:913–920. https://doi.org/10.1007/BF00039430
Mistry J, Finn RD, Eddy SR, Bateman A, Punta M (2013) Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions. Nucleic Acids Res 41:e121. https://doi.org/10.1093/nar/gkt263
Niu DK, Yang YF (2011) Why eukaryotic cells use introns to enhance gene expression: splicing reduces transcription-associated mutagenesis by inhibiting topoisomerase I cutting activity. Biol Direct 6:1–10. https://doi.org/10.1186/1745-6150-6-24
Okada M, Lanzatella C, Saha MC, Bouton J, Wu R, Tobias CM (2010) complete switchgrass genetic maps reveal subgenome collinearity, preferential pairing and multilocus interactions. Genetics 185:745–760. https://doi.org/10.1534/genetics.110.113910
Omidbakhshfard MA, Proost S, Fujikura U, Mueller-Roeber B (2015) Growth-regulating factors (GRFs): a small transcription factor family with important functions in plant biology. Mol Plant 8:998–1010. https://doi.org/10.1016/j.molp.2015.01.013
Pajoro A, Madrigal P, Muiño JM, Matus JT, Jin J, Mecchia MA, Debernardi JM, Palatnik JF, Balazadeh S, Arif M, Ó’Maoiléidigh DS, Wellmer F, Krajewski P, Riechmann JL, Angenent GC, Kaufmann K (2014) Dynamics of chromatin accessibility and gene regulation by MADS-domain transcription factors in flower development. Genome Biol 15:1–19. https://doi.org/10.1186/gb-2014-15-3-r41
Peng X, Wu Q, Teng L, Tang F, Pi Z, Shen S (2015) Transcriptional regulation of the paper mulberry under cold stress as revealed by a comprehensive analysis of transcription factors. BMC Plant Bio 15:1–14. https://doi.org/10.1186/s12870-015-0489-2
Qin L, Chen H, Wu Q, Wang X (2022) Identification and exploration of the GRF and GIF families in maize and foxtail millet. Physiol Mol Biol Pla 28:1717–1735. https://doi.org/10.1007/s12298-022-01234-z
Rose AB, Carter A, Korf I, Kojima N (2016) Intron sequences that stimulate gene expression in Arabidopsis. Plant Mol Biol 92:337–346. https://doi.org/10.1007/s11103-016-0516-1
Roy SW, Gilbert W (2006) The evolution of spliceosomal introns: patterns, puzzles and progress, nature reviews. Genetics 7:211–221. https://doi.org/10.1038/nrg1807
Shahan R (2020) The cold never bothered me anyway: DELLA-interacting GROWTH REGULATING FACTORS mediate plant growth in cold stress. Plant Cell 32:797–798. https://doi.org/10.1105/tpc.20.00079
Szklarczyk D, Kirsch R, Koutrouli M, Nastou K, Mehryary F, Hachilif R, Gable AL, Fang T, Doncheva NT, Pyysalo S, Bork P, Jensen LJ, von Mering C (2023) The STRING database in 2023: protein-protein association networks and functional enrichment analyses for any sequenced genome of interest. Nucleic Acids Res 51:638–646. https://doi.org/10.1093/nar/gkac1000
van der Knaap E, Kim JH, Kende H (2000) A novel gibberellin-induced gene from rice and its potential regulatory role in stem growth. Plant Physiol 122:695–704. https://doi.org/10.1104/pp.122.3.695
Wang Y, Tang H, DeBarry JD, Tan X, Li J, Wang X, Lee Th, Jin H, Marler B, Guo H, Kissinger JC, Paterson AH (2012) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40:e49–e49. https://doi.org/10.1093/nar/gkr1293
Wang P, Xiao Y, Yan M, Yan Y, Lei X, Di P, Wang Y (2023) Whole-genome identification and expression profiling of growth-regulating factor (GRF) and GRF-interacting factor (GIF) gene families in Panax ginseng. BMC Genom 24:1–15. https://doi.org/10.1186/s12864-023-09435-w
Wu ZJ, Wang WL, Zhuang J (2017) Developmental processes and responses to hormonal stimuli in tea plant (Camellia sinensis) leaves are controlled by GRF and GIF gene families. Funct Integr Genom 17:503–512. https://doi.org/10.1007/s10142-017-0553-0
Xu H, Wang N, Wang Y, Jiang S, Fang H, Zhang J, Su M, Zuo W, Xu L, Zhang Z, Chen X (2018) Overexpression of the transcription factor MdbHLH33 increases cold tolerance of transgenic apple callus. Plant Cell Tiss Org 134:131–140. https://doi.org/10.1007/s11240-018-1406-9
Yang M, Derbyshire MK, Yamashita RA, Marchler-Bauer A (2020) NCBI’s conserved domain database and tools for protein domain analysis. Curr Protoc Bioinform 69:e90–e90. https://doi.org/10.1002/cpbi.90
Yi W, Luan A, Liu C, Wu J, Zhang W, Zhong Z, Wang Z, Yang M, Chen C, He Y (2023) Genome-wide identification, phylogeny, and expression analysis of GRF transcription factors in pineapple (Ananas comosus). Front Plant Sci 14:1159223. https://doi.org/10.3389/fpls.2023.1159223
Zafar I, Rubab A, Aslam M, Ahmad SU, Liyaqat I, Malik A, Alam M, Wani TA, Khan AA (2022) Genome-wide identification and analysis of GRF (growth-regulating factor) gene family in Camila sativa through in silico approaches. J King Saud Univ Sci 34:102038. https://doi.org/10.1016/j.jksus.2022.102038
Zan T, Zhang L, Xie T, Li L (2020) Genome-wide identification and analysis of the growth-regulating factor (GRF) gene family and GRF-interacting factor family in triticum aestivum L. Biochem Genet 58:705–724. https://doi.org/10.1007/s10528-020-09969-8
Zhang DF, Li B, Jia GQ, Zhang TF, Dai JR, Li JS, Wang SC (2008) Isolation and characterization of genes encoding GRF transcription factors and GIF transcriptional coactivators in Maize (Zea mays L.). Plant Sci 175:809–817. https://doi.org/10.1016/j.plantsci.2008.08.002
Zhang J, Li Z, Jin J, Xie X, Zhang H, Chen Q, Luo Z, Yang J (2018) Genome-wide identification and analysis of the growth-regulating factor family in tobacco (Nicotiana tabacum). Gene 639:117–127. https://doi.org/10.1016/j.gene.2017.09.070
Zheng L, Ma J, Song C, Zhang L, Gao C, Zhang D, An N, Mao J, Han M (2018) Genome-wide identification and expression analysis of GRF genes regulating apple tree architecture. Tree Genet Genom 14:1–17. https://doi.org/10.1007/s11295-018-1267-8
Zhu R, Cao B, Sun M, Wu J, Li J (2023) Genome-wide identification and evolution of the GRF gene family and functional characterization of PbGRF18 in Pear. Int J Mol Sci 24:14690. https://doi.org/10.3390/ijms241914690
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This research was supported by the National Natural Science Foundation of China (Grant No. 32160700) the Guizhou Provincial Science and Technology Projects of China (Grant No. YQK [2023]008), as well as the National Guidance Foundation for Local Science and Technology Development of China (Grant No. [2023]009).
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Deng, H., Wen, Z., Hou, Q. et al. Genome-wide identification and analysis of the growth-regulating factor (GRF) family in sweet cherry. Genet Resour Crop Evol (2024). https://doi.org/10.1007/s10722-024-01886-8
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DOI: https://doi.org/10.1007/s10722-024-01886-8