Abstract
Leaf growth and development are primarily driven by cell proliferation and expansion. Among a number of genes involved in the regulation of cell proliferation, the GROWTH-REGULATING FACTOR (GRF) transcription factors have been established to act as positive regulators of cell proliferation and leaf growth in angiosperms. While the Arabidopsis thaliana GRF family comprises nine members, not all members of the family have been experimentally confirmed for the positive role, not only due to no or only slight changes in leaf size of corresponding single mutants, but also due to unavailability of multiple mutants to overcome the obstacle. Furthermore, some discrepancies and confusion in their roles have been disclosed in the literature. Here, we systemically prepared a series of such multiple mutants and confirmed that all GRF members, except for GRF8, acted as positive regulators of cell proliferation and leaf growth. We also systematically examined the spatio-temporal distribution patterns of all nine GRF proteins in the leaf organ, and found that their distribution patterns were highly reminiscent of the behavior of the cell cycle arrest front. We therefore propose that GRFs play an important role in shaping the arrest front and growth patterns of leaves.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Autran D, Jonak C, Belcram K, Beemster GTS, Kronenberger J, Grandjean O et al (2002) Cell numbers and leaf development in Arabidopsis: a functional analysis of the STRUWWELPETER gene. EMBO J 21:6036–6049
Beltramino M, Ercoli MF, Debernardi JM, Goldy C, Rojas AML, Nota F et al (2018) Robust increase of leaf size by Arabidopsis thaliana GRF3-like transcription factors under different growth conditions. Sci Rep 8:13447
Beltramino M, Debernardi JM, Ferela A, Palatnik JF (2021) ARF2 represses expression of plant GRF transcription factors in a complementary mechanism to microRNA miR396. Plant Physiol 185:1798–1812
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
Das Gupta M, Nath U (2015) Divergence in patterns of leaf growth polarity is associated with the expression divergence of miR396. Plant Cell 27:2785–2799
Debernardi JM, Mecchia MA, Vercruyssen L, Smaczniak C, Kaufmann K, Inzé D et al (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
Donnelly PM, Bonetta D, Tsukaya H, Dengler RE, Dengler NG (1999) Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev Biol 215:407–419
Duan P, Ni S, Wang J, Zhang B, Xu R, Wang Y et al (2016) Regulation of OsGRF4 by OsmiR396 controls grain size and yield in rice. Nature Plants 2:1
Ferjani A, Yano S, Horiguchi G, Tsukaya H (2007) Analysis of leaf development in fugu mutants of Arabidopsis reveals three compensation modes that modulate cell expansion in determinate organs. Plant Physiol 144:988–999
Fonini LS, Lazzarotto F, Barros PM, Cabreira-Cagliari C, Martins MAB, Saibo NJM et al (2020) Molecular evolution and diversification of the GRF transcription factor family. Genet Mol Biol 43:e20200080
Horiguchi G, Kim G, 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
Kawade K, Tanimoto H, Horiguchi G, Tsukaya H (2017) Spatially different tissue-scale diffusivity shapes ANGUSTIFOLIA3 gradient in growing leaves. Biophysical J 113:1109–1120
Kazama T, Ichihashi Y, Murata S, Tsukaya H (2010) The mechanism of cell cycle arrest front progression explained by a KLUH/CYP78A5-dependent mobile growth factor in developing leaves of Arabidopsis thaliana. Plant Cell Physiol 51:1046–1054
Kim JH (2019) Biological roles and an evolutionary sketch of the GRF–GIF transcriptional complex in plants. BMB Rep 52:227–238
Kim JH, Kende H (2004) A transcriptional coactivator, AtGIF1, is involved in regulating leaf growth and morphology in Arabidopsis. Proc Natl Acad Sci USA 101:13374–13379
Kim JH, Lee BH (2006) GROWTH-REGULATING FACTOR4 of Arabidopsis thaliana is required for development of leaves, cotyledons, and shoot apical meristem. J Plant Biol 49:463–468
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
Kim JH, Choi D, Kende H (2003) The AtGRF family of putative transcription factors is involved in leaf and cotyledon growth in Arabidopsis. Plant J 36:94–104
Kim JS, Mizoi J, Kidokoro S, Maruyama K, Nakajima J, Nakashima K et al (2012) Arabidopsis GROWTH-REGULATING FACTOR7 functions as a transcriptional repressor of abscisic acid- and osmotic stress-responsive genes, including DREB2A. Plant Cell 24:3393–3405
Lee BH, Kim JH (2014) Spatio-temporal distribution patterns of GRF-INTERACTING FACTOR expression and leaf size control. Plant Signal Behav 9:e29697
Lee BH, Ko JH, Lee S, Lee Y, Pak JH, Kim JH (2009) The Arabidopsis GRF-INTERACTING FACTOR gene family performs an overlapping function in determining organ size as well as multiple developmental properties. Plant Physiol 151:655–668
Lee SJ, Lee BH, Jung JH, Park SK, Song JT, Kim JH (2018) GROWTH-REGULATING FACTOR and GRF-INTERACTING FACTOR specify meristematic cells of gynoecia and anthers. Plant Physiol 176:717–729
Liang G, He H, Li Y, Wang F, Yu D (2014) Molecular mechanism of microRNA396 mediating pistil development in Arabidopsis. Plant Physiol 164:249–258
Liebsch D, Palatnik J (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
Liu D, Song Y, Chen Z, Yu D (2009) Ectopic expression of miR396 suppresses GRF target gene expression and alters leaf growth in Arabidopsis. Physiol Plant 136:223–236
Liu H, Guo S, Xu Y, Li C, Zhang Z, Zhang D et al (2014) OsmiR396d-regulated OsGRFs function in floral organogenesis in rice through binding to their targets OsJMJ706 and OsCR4. Plant Physiol 165:160–174
Nelissen H, Gonzalez N, Inze´ D, (2016) Leaf growth in dicots and monocots: So different yet so alike. Curr Opin Plant Biol 33:72–76
Omidbakhshfard MA, Fujikura U, Olas JJ, Xue GP, Balazadeh S, Mueller-Roeber B (2018) GROWTH-REGULATING FACTOR 9 negatively regulates Arabidopsis leaf growth by controlling ORG3 and restricting cell proliferation in leaf primordia. PLoS Genet 14:e1007484
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
Rodrigues-Pousada RA, De Rycke R, Dedonder A, Van Caeneghem W, Engler G, Van Montagu M et al (1993) The Arabidopsis 1-aminocyclopropane-1-carboxylate synthase gene 1 is expressed during early development. Plant Cell 5:897–911
Rodriguez RE, Mecchia MA, Debernardi JM, Schommer C, Weigel D, Palatnik JF (2010) Control of cell proliferation in Arabidopsis thaliana by microRNA miR396. Development 137:103–112
Sarvepalli K, Gupta MD, Challa KR, Nath U (2019) Molecular cartography of leaf development—role of transcription factors. Curr Opin Plant Biol 47:22–31
Tsukaya H (2002) Interpretation of mutants in leaf morphology: genetic evidence for a compensatory system in leaf morphogenesis that provides a new link between cell and organismal theory. Int Rev Cytol 217:1–39
Tsukaya H (2013) Leaf Development the Arabidopsis Book 11:e0163
Tsukaya H (2021) The leaf meristem enigma: the relationship between the plate meristem and the marginal meristem. Plant Cell 33:3194–3206
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
Vercruysse J, Baekelandt A, Gozalez N, Inzé D (2020) Molecular networks regulating cell division during Arabidopsis leaf growth. J Exp Bot 71:2365–2378
Vercruyssen L, Verkest A, Gonzalez N, Heyndrickx KS, Eeckhout D, Han SK et al (2014) ANGUSTIFOLIA3 binds to SWI/SNF chromatin remodeling complexes to regulate transcription during Arabidopsis leaf development. Plant Cell 26:210–229
Zhang D, Sun W, Singh R, Zheng Y, Cao Z, Li M et al (2018) GRF-interacting factor1 regulates shoot architecture and meristem determinacy in maize. Plant Cell 30:360–374
Acknowledgements
This work was supported by the National Research Foundation of Korea (NRF-2018R1D1A1B07050016). We thank Dr. Palatnik for 35S::MIR396b and GRF2pro:: GRF2::GUS seeds; Dr. Celenza for CYCB1;1::GUS seeds; and the Arabidopsis Biological Resource Center for grf mutant seeds.
Author information
Authors and Affiliations
Contributions
BHL and JHK conceived and designed the research plan. BHL, J-HJ, S-JL, and T-TM contributed to the construction of grf multiple mutants and GRF::GUS transgenic lines. G-HL and BHL prepared multiple mutants containing CYCB1;1::GUS lines and performed most of the experiments. BHL and JHK wrote the manuscript.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare no conflict of interest.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Lee, GH., Lee, B.H., Jung, JH. et al. Systematic Assessment of the Positive Role of Arabidopsis thaliana GROWTH-REGULATING FACTORs in Regulation of Cell Proliferation During Leaf Growth. J. Plant Biol. 65, 413–422 (2022). https://doi.org/10.1007/s12374-022-09366-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12374-022-09366-1