DOI QR코드

DOI QR Code

Rice CHD3/Mi-2 chromatin remodeling factor RFS regulates vascular development and root formation by modulating the transcription of auxin-related genes NAL1 and OsPIN1

  • Hyeryung Yoon (Department of Agriculture, Forestry and Bioresources, Plant Genomics and Breeding Institute, Research Institute of Agriculture and Life Sciences, Seoul National University) ;
  • Chaemyeong Lim (Department of Agriculture, Forestry and Bioresources, Plant Genomics and Breeding Institute, Research Institute of Agriculture and Life Sciences, Seoul National University) ;
  • Bo Lyu (Division of Plant Science and Technology, University of Missouri) ;
  • Qisheng Song (Division of Plant Science and Technology, University of Missouri) ;
  • So-Yon Park (Division of Plant Science and Technology, University of Missouri) ;
  • Kiyoon Kang (Division of Life Sciences, Incheon National University) ;
  • Sung-Hwan Cho (Department of Agriculture, Forestry and Bioresources, Plant Genomics and Breeding Institute, Research Institute of Agriculture and Life Sciences, Seoul National University) ;
  • Nam-Chon Paek (Department of Agriculture, Forestry and Bioresources, Plant Genomics and Breeding Institute, Research Institute of Agriculture and Life Sciences, Seoul National University)
  • Received : 2024.01.13
  • Accepted : 2024.02.23
  • Published : 2024.10.31

Abstract

The vascular system in plants facilitates long-distance transportation of water and nutrients through the xylem and phloem, while also providing mechanical support for vertical growth. Although many genes that regulate vascular development in rice have been identified, the mechanism by which epigenetic regulators control vascular development remains unclear. This study found that Rolled Fine Striped (RFS), a Chromodomain Helicase DNA-binding 3 (CHD3)/Mi-2 subfamily protein, regulates vascular development in rice by affecting the initiation and development of primordia. The rfs mutant was found to affect auxin-related genes, as revealed by RNA sequencing and reverse transcription-quantitative PCR analysis. The transcript levels of OsPIN1 and NAL1 genes were downregulated in rfs mutant, compared to the wild-type plant. The chromatin immunoprecipitation assays showed lower levels of H3K4me3 in the OsPIN1a and NAL1 genes in rfs mutant. Furthermore, exogenous auxin treatment partially rescued the reduced adventitious root vascular development in rfs mutant. Subsequently, exogenous treatments with auxin or an auxin-transport inhibitor revealed that the expression of OsPIN1a and NAL1 is mainly affected by auxin. These results provide strong evidence that RFS plays an important role in vascular development and root formation through the auxin signaling pathway in rice.

Keywords

Acknowledgement

This research was supported by the Basic Science Research Program through the NRF of Korea grant funded by the Korean Government (NRF-2010-355-F00003), the Brain Pool program funded by the Ministry of Science and ICT through the National Research Foundation of Korea (2022H1D3A2A01096185), and the Basic Science Research Program through the NRF of Korea grant funded by the Korean Government (RS-2023-00247376).

References

  1. Sack L and Scoffoni C (2013) Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future. New Phytol 198, 983-1000
  2. Scarpella E, Marcos D, Friml J and Berleth T (2006) Control of leaf vascular patterning by polar auxin transport. Genes Dev 20, 1015-1027
  3. Benkova E, Michniewicz M, Sauer M et al (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115, 591-602
  4. Fabregas N, Formosa-Jordan P, Confraria A et al (2015) Auxin influx carriers control vascular patterning and xylem differentiation in Arabidopsis thaliana. PLoS Genet 11, e1005183
  5. Petrasek J, Mravec J, Bouchard R et al (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312, 914-918
  6. Wisniewska J, Xu J, Seifertova D et al (2006) Polar PIN localization directs auxin flow in plants. Science 312, 883
  7. Petrasek J and Friml J (2009) Auxin transport routes in plant development. Development 136, 2675-2688
  8. Weijers D and Jurgens G (2005) Auxin and embryo axis formation: the ends in sight? Curr Opin Plant Biol 8, 32-37
  9. Wang JR, Hu H, Wang GH et al (2009) Expression of PIN genes in rice (Oryza sativa L.): tissue specificity and regulation by hormones. Mol Plant 2, 823-831
  10. Xu M, Zhu L, Shou H and Wu P (2005) A PIN1 family gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in rice. Plant Cell Physiol 46, 1674-1681
  11. Lu G, Coneva V, Casaretto JA et al (2015) OsPIN5b modulates rice (Oryza sativa) plant architecture and yield by changing auxin homeostasis, transport and distribution. Plant J 83, 913-925
  12. Qi J, Qian Q, Bu Q et al (2008) Mutation of the rice Narrow leaf1 gene, which encodes a novel protein, affects vein patterning and polar auxin transport. Plant Physiol 147, 1947-1959
  13. Cho SH, Yoo SC, Zhang H et al (2014) Rice NARROW LEAF1 regulates leaf and adventitious root development. Plant Mol Biol Rep 32, 270-281
  14. Cho SH, Yoo SC, Zhang H et al (2013) The rice narrow leaf2 and narrow leaf3 loci encode WUSCHEL-related homeobox 3A (OsWOX3A) and function in leaf, spikelet, tiller and lateral root development. New Phytol 198, 1071-1084
  15. Yoo SC, Cho SH and Paek NC (2013) Rice WUSCHEL-related homeobox 3A (OsWOX3A) modulates auxin-transport gene expression in lateral root and root hair development. Plant Signal Behav 8, e25929
  16. Cho SH and Paek NC (2016) Regulatory role of the OsWOX3A transcription factor in rice root development. Plant Signal Behav 11, e1184807
  17. Cho SH, Lee CH, Gi E et al (2018) The rice rolled fine striped (RFS) CHD3/Mi-2 chromatin remodeling factor epigenetically regulates genes involved in oxidative stress responses during leaf development. Front Plant Sci 9, 364
  18. Guo M, Zhao H, He Z et al (2022) Comparative expression profiling of Snf2 family genes during reproductive development and stress responses in rice. Front Plant Sci 13, 910663
  19. Ogas J, Cheng JC, Sung ZR and Somerville C (1997) Cellular differentiation regulated by gibberellin in the Arabidopsis thaliana pickle mutant. Science 277, 91-94
  20. Aichinger E, Villar CB, Di Mambro R et al (2011) The CHD3 chromatin remodeler PICKLE and polycomb group proteins antagonistically regulate meristem activity in the Arabidopsis root. Plant Cell 23, 1047-1060
  21. Zha P, Jing Y, Xu G and Lin R (2017) PICKLE chromatin-remodeling factor controls thermosensory hypocotyl growth of Arabidopsis. Plant Cell Environ 40, 2426-2436
  22. Hu Y, Liu D, Zhong X et al (2012) CHD3 protein recognizes and regulates methylated histone H3 lysines 4 and 27 over a subset of targets in the rice genome. Proc Natl Acad Sci U S A 109, 5773-5778
  23. Wang Y, Wang D, Gan T et al (2016) CRL6, a member of the CHD protein family, is required for crown root development in rice. Plant Physiol Biochem 105, 185-194
  24. Xu J, Wang L, Zhou M et al (2017) Narrow albino leaf 1 is allelic to CHR729, regulates leaf morphogenesis and development by affecting auxin metabolism in rice. Plant Growth Regulation 82, 175-186
  25. Muro-Villanueva F, Mao X and Chapple C (2019) Linking phenylpropanoid metabolism, lignin deposition, and plant growth inhibition. Curr Opin Biotechnol 56, 202-208
  26. Fujino K, Matsuda Y, Ozawa K et al (2008) NARROW LEAF 7 controls leaf shape mediated by auxin in rice. Mol Genet Genomics 279, 499-507
  27. Zhuang X, Jiang J, Li J et al (2006) Over-expression of OsAGAP, an ARF-GAP, interferes with auxin influx, vesicle trafficking and root development. Plant J 48, 581-591
  28. Friml J and Palme K (2002) Polar auxin transport-old questions and new concepts? Plant Mol Biol 49, 273-284
  29. Wang H, Ouyang Q, Yang C et al (2022) Mutation of OsPIN1b by CRISPR/Cas9 reveals a role for auxin transport in modulating rice architecture and root Gravitropism. Int J Mol Sci 23, 8965
  30. Ma X, Ma J, Zhai H et al (2015) CHR729 is a CHD3 protein that controls seedling development in rice. PLoS One 10, e0138934
  31. Guo T, Wang D, Fang J et al (2019) Mutations in the rice OsCHR4 gene, encoding a CHD3 family chromatin remodeler, induce narrow and rolled leaves with increased cuticular wax. Int J Mol Sci 20, 2567
  32. Eshed Y, Baum SF and Bowman JL (1999) Distinct mechanisms promote polarity establishment in carpels of arabidopsis. Cell 99, 199-209
  33. Xu M, Hu T, Smith MR and Poethig RS (2016) Epigenetic regulation of vegetative phase change in arabidopsis. The Plant Cell 28, 28-41
  34. Fukaki H, Taniguchi N and Tasaka M (2006) PICKLE is required for SOLITARY-ROOT/IAA14-mediated repression of ARF7 and ARF19 activity during Arabidopsis lateral root initiation. Plant J 48, 380-389
  35. Ghelli R, Brunetti P, Napoli N et al (2018) A newly identified flower-specific splice variant of AUXIN RESPONSE FACTOR8 regulates stamen elongation and endothecium lignification in arabidopsis. Plant Cell 30, 620-637
  36. Wang W, Li Y, Cai C and Zhu Q (2023) Auxin response factors fine-tune lignin biosynthesis in response to mechanical bending in bamboo. New Phytol 241, 1161-1176
  37. Rogers LA and Campbell MM (2004) The genetic control of lignin deposition during plant growth and development. New Phytol 164, 17-30
  38. Li Y, Zhu J, Wu L et al (2019) Functional divergence of PIN1 paralogous genes in rice. Plant Cell Physiol 60, 2720-2732
  39. Li W, Yan J, Zhang Y et al (2023) Serine protease NAL1 exerts pleiotropic functions through degradation of TOPLESS-related corepressor in rice. Nat Plants 9, 1130-1142