BMB Reports 2024; 57(10): 441-446  https://doi.org/10.5483/BMBRep.2024-0008
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 Yoon1, Chaemyeong Lim1, Bo Lyu2, Qisheng Song2, So-Yon Park2, Kiyoon Kang3, Sung-Hwan Cho1,* & Nam-Chon Paek1,*
1Department of Agriculture, Forestry and Bioresources, Plant Genomics and Breeding Institute, Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul 08826, Korea, 2Division of Plant Science and Technology, University of Missouri, Columbia, MO 65211, USA, 3Division of Life Sciences, Incheon National University, Incheon 22012, Korea
Correspondence to: Sung-Hwan Cho, Tel: +82-2-880-4553; Fax: +82-2-877-4550; E-mail: choj1010@snu.ac.kr; Nam-Chon Paek, Tel: +82-2-880-4543; Fax: +82-2-877-4550; E-mail: ncpaek@snu.ac.kr
Received: January 13, 2024; Revised: February 14, 2024; Accepted: February 23, 2024; Published online: October 31, 2024.
© Korean Society for Biochemistry and Molecular Biology. All rights reserved.

cc This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
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: Auxin, CHD3/Mi-2 chromatin remodeling factor, NAL1, OsPIN1, Rice, Root formation, Vascular development
INTRODUCTION

Vascular bundles of plants, composed of xylem and phloem tissues, connect all parts of the plant body from leaf to root through their conductive function, providing water and nutrients transport, mechanical support, and overall structural strength (1). Auxin, which is important for vascular establishment and maintenance, is mainly synthesized in the plant cells of actively growing tissues, such as developing leaves and roots, and transported to other tissues to participate in organ primordia formation, apical meristem maintenance, and vascular tissue differentiation through the process of polar auxin transport (2-4).

Auxin flow distribution and gradient establishment are regulated by the specific cellular auxin transport proteins (5). PIN proteins are known to determine the direction and distribution of auxin movement (5, 6). In Arabidopsis, five PINs are predominantly localized in the plasma membrane, and determine the direction of intracellular auxin flux to maintain auxin gradient distribution (7). The Arabidopsis pin mutants show growth defects in shoot and stems, root, inflorescence, and embryo (3, 8). The rice genome contains twelve PIN genes (9). The ospin mutants are reported to be involved in root development, plant height, tiller and panicle branch angle, panicle formation, yield, and tiller growth (10, 11). Several mutants have been reported to affect rice vascular development and root formation by regulating the expression of OsPIN genes. For example, the mutation of NARROW LEAF1 (NAL1) caused defective cell division by affecting polar auxin transport OsPINs, and showed reduction in veins and adventitious root formation (12, 13). The NARROW LEAF2/3 (NAL2/3) plays a key regulatory role in lateral axis outgrowth, vascular development, and root formation, through the regulation of OsPIN genes (14-16).

Several studies have reported the key role of chromodomain helicase DNA-binding (CHD) family proteins as transcriptional regulators in the regulation of developmental processes and stress response (17, 18). In Arabidopsis, PICKLE belongs to typical CHD protein, while the pkl mutant shows pleiotropic defects, such as semi-dwarfism and reduced root meristem activity (19, 20). PICKLE positively regulates the expression of auxin-related genes IAA19 and IAA29 by repressing H3K27me3 deposition (21). In rice, RFS/CHR729 is a member of the CHD family proteins, and is one of the close homologs of PICKLE (22). RFS/CHR729 protein interacts with the promoter regions of histone H3 lysine 4 trimethylation (H3K4me3) and H3K27me3, while chr729 mutant exhibits pleiotropic phenotypes, such as narrow and rolled leaves, reduced stem elongation, and decreased chlorophyll contents (17, 22). Moreover, all other allelic mutants of RFS/CHR729 display clear defects in vascular development (22-24), suggesting that RFS may modulate specific gene expression related to vascular development by activating or repressing epigenetic marks on histones. However, the detailed molecular mechanisms of the CHD family protein RFS in plant vascular development and root formation remain unclear. To clarify the underlying mechanism of RFS in vascular development and root formation, we used RNA-seq, RT-qPCR, and ChIP assays to analyze the expression and histone methylation levels of auxin-related genes in rfs mutant.

RESULTS

Defects in vascular and adventitious root development in rfs mutant

A previous study found that rice rfs mutant has reduced leaf vascular bundles and the number of roots throughout the life span (17). To better understand whether vascular defects occur throughout the tissue, we performed the histological analysis of shoot apical meristem (M) and leaf primordia in 3-day-old seedlings, using paraffin section. The shoot apical meristem and leaf primordia (P1 to P3) in rfs mutant were similar in size to those of WT, whereas the number of provasculatures in rfs mutant was lower than in WT (Fig. 1A-D). We examined the number of large vascular bundles (LVB) in the leaf sheath and basal region of 10-week-old rfs mutant, and found the number of LVB in rfs mutant was less than that in WT (Fig. 1E-H). Additionally, the phloem (P) and xylem (X) sizes in rfs leaf sheath were smaller than those in WT (Fig. 1J, L). Notably, the LVB of stem in rfs mutant showed impaired differentiation, with an unclear distinction between phloem and xylem (Fig. 1I, K). Furthermore, the leaf sheath of rfs mutant exhibited fewer AE or no SVB (Fig. 1E-H). As we previously observed fewer adventitious roots in rfs mutant (17), we investigated root growth initiation in both 3-day-old seedlings and 10-week-old rfs mutants. The results indicated a 63% reduction in the number of adventitious root primordia in rfs mutant (Fig. 1M-P). In addition, rfs mutant displayed shorter root cap and meristematic zone (Supplementary Fig. 1). These results suggest that RFS is necessary for maintaining vascular and root development from the beginning of plant growth.

Comparative analysis of transcriptome profiling between WT and rfs mutant

Given that RFS remodels chromatin structure by the methylation or acetylation of histone proteins and thus regulates gene transcription (22), the mutation of RFS may affect the rice transcriptome, including vascular development-related genes. To obtain deeper insights into the function of RFS, the transcriptomic profiles in WT and rfs were characterized. A total of 2,284 DEGs were identified between WT and rfs, including 1,519 up-regulated and 765 down-regulated DEGs in rfs mutant (Fig. 2A, Supplementary Table 1).

Subsequently, GO was used to classify the functions of DEGs. The results implied that the DEGs annotated with GO terms were mainly related to “nucleolus”, “preribosome”, “small-subunit processome”, and “protein refolding” (Supplementary Fig. 2A).

To uncover potential signaling pathways that regulate the impaired vascular development phenotypes of rfs mutant, we performed a Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis. KEGG analysis for DEGs between WT and rfs mutant revealed that the phenylpropanoid biosynthesis, phenylalanine metabolism, and plant hormone signal transduction pathways significantly correlated with the rfs phenotype (Supplementary Fig. 2B). In particular, both phenylpropanoid and phenylalanine pathways produce lignin, which is a composite for xylem in vascular tissue (25). Interestingly, three DEGs in “Phenylpropanoid biosynthesis (Os02t0626100-02, Os02t0626400-01/03)” and one DEG in “Phenylalanine metabolism (Os05t0137000-01)” were down-regulated (Supplementary Table 1). The down-regulated DEGs in “Plant hormone signal transduction” were Os06t0232300-01 and Os08t0529000-01 (Supplementary Table 1), encoding auxin transport proteins, which are critical genes for vascular tissue development in rice (10).

RFS regulates the expression of vascular development- and auxin-related genes

Narrow leaf phenotype is generally associated with auxin signal (12-14, 26). NAL2/3 and NAL1 could affect vascular development through auxin transport genes, OsPINs (12, 13). In addition, a previous study reported that allelic mutants of rfs showed both altered OsPIN and reduced NAL1 expressions (24). First, we investigated the DEGs in auxin-related genes. Indeed, many auxin-related genes were altered in rfs mutant (Fig. 2B). Notably, the level of OsPIN1a and OsPIN5b were downregulated in rfs mutant (Fig. 2B). The RT-qPCR results were consistent with the RNA-seq results for the levels of some auxin-related genes (Fig. 2C).

The mutation of NAL1 and NAL2/3 has been reported to affect the expression of OsPIN family genes (13, 14, 16). Therefore, we examined the contribution of other OsPINs, NAL1, NAL2/3, and NAL7 genes in seedling plants. Several OsPIN genes showed significantly altered expression levels in rfs mutant, compared to WT plants (Fig. 2D). Although OsPIN1b, OsPIN1c, OsPIN2, and OsPIN9 were reduced in rfs mutant, a result similar to that previously reported in nal1 mutant (13), OsPIN5a expression was up-regulated. No statistical difference in the level of OsPIN10 was observed in rfs mutant plants. Consistent with the OsPIN1s transcript levels, OsPIN1 protein level was reduced in rfs (Fig. 2E). Furthermore, NAL1 expression was reduced in rfs mutant, whereas there was no difference in NAL2/3 and NAL7 expression (Fig. 2D). These results suggest that the rfs phenotype is due to the perturbed expression of auxin-related genes, especially NAL1 and OsPIN family genes, in the shoot basal region, where the shoot and root tissue primordia initiate.

Altered expression of OsPINs, NAL1, and OsAGAP may reduce adventitious root development in rfs mutant

Previous studies have shown that both nal1 and OsPIN1-RNAi mutants are defective in adventitious root development (10, 13). Moreover, overexpression of OsAGAP resulted in a decrease in both the length and number of adventitious roots (27). Based on the findings and the observed changes in the expression levels of OsPINs, NAL1, and OsAGAP in rfs mutant (Fig. 2), we further investigated the root phenotype. As expected, rfs showed fewer and shorter adventitious roots, compared to WT (Fig. 3A, C, D).

PIN family genes have been implicated in polar auxin transport in plant cells (28). Specifically, auxin treatment restored the defects in adventitious root formation in OsPIN1-RNAi and nal1 mutants (10, 13). Thus, we examined adventitious root development in response to exogenous auxin (IAA) in rfs seedlings. While the adventitious root length of rfs seedlings was rescued by exogenous application of IAA, the number of adventitious roots of rfs seedlings was partially restored (Fig. 3B-D).

Auxin has been reported to induce OsPINs expression (29). To confirm whether the restored root phenotype was due to the induction of OsPINs expression, we investigated the expression of OsPINs after exogenous auxin and auxin inhibitor treatments. The expression of OsPIN1b and OsPIN1c was increased by IAA treatment in rfs mutant, consistent with the morphological responses in roots (Fig. 3F, G). However, after exogenous IAA treatment, OsPIN1a and NAL1 were not increased in rfs mutant (Fig. 3E, H). As expected, following treatment with exogenous auxin inhibitor NPA, the expression of all genes was repressed in both WT and rfs mutant (Fig. 3I-L). These results suggest that altered expression of OsPINs and NAL1 genes affects the appropriate distribution of endogenous auxin in rfs, which in turn may affect adventitious root development.

RFS affects histone modifications in genes related to vascular development and auxin

Previous studies have shown that rfs mutant has a decreased level of overall histone methylation, in particular, a global reduction at the activating mark H3K4me3 (17, 22). Interestingly, unlike OsPIN1b and OsPIN1c, there was no increase in the expression of OsPIN1a and NAL1 in rfs mutant after auxin application (Fig. 3E, H). Thus, we performed a chromatin immunoprecipitation (ChIP) assay to investigate whether RFS affects the levels of H3K4me3 on the auxin-related genes, such as NAL1 and OsPIN1a. The levels of H3K4me3 were found to be reduced in the promoter region of NAL1 and OsPIN1a in rfs mutant, compared with WT (Fig. 4A-D). These findings suggest that RFS affects the modification of histone proteins that bind directly to auxin-related genes, which are essential for maintaining vascular and adventitious root development.

DISCUSSION

Given the previous studies on the rice CHD3/Mi-2 chromatin remodeling factor CHR729/RFS (17, 22-24, 30, 31), RFS is necessary to regulate gene expression related to auxin at the histone level, and contributes to the regulation of vascular development and root development in plants. In this study, we identified rfs mutant with defects in vascular development in the regions of leaf and stem, and root formation (Fig. 1, Supplementary Fig. 1). Mutation of the PKL, an Arabidopsis ortholog of RFS, affects the formation of root meristem tissue (32), which is partially similar to the rfs mutant. In addition, pkl mutants exhibit short height and small leaves, compared to WT (33). Furthermore, it was reported that PKL appears to control tissue specification through changes in the histone modifications of auxin-related gene (34). Interestingly, the transcriptome analysis revealed that rfs mutation affects the expression of auxin-related genes similar to the pkl (Fig. 2). This suggests that CHD family proteins may have similar functions in plant development, specifically in vascular development and root formation through the auxin signaling pathway.

Notably, rfs mutant exhibited the reduced expression of ARFs (Fig. 2B, C). Previous studies showed that ARF3, ARF6, and ARF8 are involved in lignin biosynthesis in various biological processes in plants (35, 36). Our transcriptome analysis showed that the phenylalanine pathway, which is involved in lignin biosynthesis, was significantly affected in rfs mutant (Supplementary Fig. 2B). Lignin is a key component for vascular plants, and biopolymer lignin is deposited in the cell walls of vascular cells (37). Moreover, histological analysis revealed that some of the vascular bundles were absent or defective in rfs mutant (Fig. 1E-L). These data suggest that RFS may affect lignin synthesis, which participates in vascular development through the auxin signaling pathway.

OsPIN1 distributes proper concentration of auxin for the development of vascular tissues and root emergence (10, 38). In particular, it was reported that four OsPIN1 showed functional redundancy (38). Among the single mutants, ospin1b had decreased adventitious root formation, panicle length, and grain number, and increased grain yield and tiller number, whereas the other single mutants had no critical phenotypes (10, 29). Only pin1apin1b or pin1cpin1d double mutants exhibited critical phenotypes, such as reduced plant height, root number and root length, and increased tiller number (38). It was reported that the mutation of NAL1 preferentially affects the expression of overall OsPIN genes, resulting in defects in vascular bundle development and root formation (13). Consistent with these reports, most OsPINs were significantly down-regulated in rfs mutant (Fig. 2). Thus, these data indicate that RFS may regulate auxin homeostasis in rice to control vascular development and root formation through the regulation of OsPINs. In addition, rfs mutant showed defects in yield traits similar to nal1 (Supplementary Table 2) (17, 39). Interestingly, unlike rfs mutant, ospin1b CRISPR mutant exhibited increased grain yield and tiller number, compared to WT (29). This is a different phenotype from rfs mutant, suggesting that while RFS directly regulates OsPIN1a, it may also affect most of OsPINs expression, primarily by regulating NAL1. A recent study reported that the NAL1-OsTPR2 module directly regulates PIN1b at the histone level (39). Therefore, while RFS may be involved in this NAL1 complex module as a coactivator or corepressor, the details require further research.

RT-qPCR and ChIP analysis confirmed that RFS directly activates the transcription of auxin-related genes, OsPIN1a and NAL1, which regulate vascular development and root formation (Figs. 3 and 4), indicating that the RFS may directly regulate vascular development and root formation through both OsPIN1a and NAL1. Taken together, RFS may be a higher hierarchical regulator of the auxin signaling pathway cascades in plant vascular development and root formation.

MATERIALS AND METHODS

Materials and methods are available in supplementary information.

ACKNOWLEDGEMENTS

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).

CONFLICTS OF INTEREST

The authors have no conflicting interests.

FIGURES
Fig. 1. Defective organ development in the shoot base, stem, and root base of rfs mutant. (A-D) Transverse sections were taken through the shoot apical meristem regions in 3-day-old seedlings of WT (A, B) and rfs mutant (C, D). Red arrows indicate vascular bundles. (E-P) Transverse sections through the stem regions in 1-month-old plants of WT (E, F, I, J) and rfs mutant (G, H, K, L), as well as through the basal nodes of WT (M, N) and rfs mutant (O, P). Black arrows represent crown root primordia. The sections were visualized using a light microscope at magnifications of (10-100)×. P1, plastochron1; P2, plastochron2; M, meristem; AE, aerenchyma; LVB, large vascular bundle; SVB, small vascular bundle; P, phloem; X, xylem; VB, vascular bundle. Bars represent 200 μμ.
Fig. 2. Transcriptome analysis and altered expression of genes associated with auxin-related and vascular development in rfs mutant. (A) Volcano Plot of all DEGs. Gray dots represent non-DEGs, orange dots represent upregulated DEGs, and blue dots represent downregulated DEGs. (B) Heat map of auxin signal transduction related genes. The red color in this figure denotes a high level of expression, while blue indicates low expression. WT-1 and WT-2 denote the two control biological replicates, while rfs-1 and rfs-2 denote the two biological replicates for the rfs mutant. The expression levels for each gene are shown in the heat maps using Fragments Per Kilobase of transcript per Million fragments mapped (FPKM) with a log2 scale. (C, D) Relative abundance of mRNAs of auxin-related genes in the shoot base of rfs seedlings. Ten-day-old plants grown in the growth chamber were used for RT-qPCR. Mean and standard deviation values were obtained from three independent samples. Asterisks indicate statistically significant differences compared with WT, as determined by Student’s t-test (*P < 0.05, **P < 0.01, ***P < 0.001). (E) Protein abundances of OsPIN1 in 14-day-old WT and rfs seedlings. The membrane was stained with Coomassie Brilliant Blue (CBB) to show equal loading.
Fig. 3. Exogenous IAA treatment rescues defective adventitious roots in rfs mutant, and affects OsPIN1s and OsNAL1 expression. (A) Root development of 10-day-old seedlings of WT and rfs mutant. (B) Root phenotypes of 2-week-old seedlings of WT and rfs mutant grown on the phytoagar plates with 10−7 M IAA. Red and white arrows indicate adventitious roots and primary roots, respectively. (C, D) The number (C) or length (D) of adventitious root of WT and rfs mutant grown in (A, B). The significance of the differences was determined by a one-way ANOVA with Tukey’s multiple comparison test. Different lowercase letters above the bars indicate significant differences (P < 0.01). (E-L) Relative transcript levels of auxin transport-related genes in 7-day-old seedlings of WT and rfs mutant treated with IAA (E-H) or NPA (I-L). Values represent the mean easem of three independent assays. Asterisks indicate statistically significant differences compared with WT, as determined by Student’s t-test (**P < 0.01). Bars: 1 cm (A, B).
Fig. 4. Chromatin immunoprecipitation (ChIP) assays of NAL1 and OsPIN1a loci. ChIP assays were performed on the chromatin regions at NAL1 (A, B) and OsPIN1a (C, D) in WT and rfs mutant, using antibodies against H3K4me3. The mean standard deviation values are shown from three parallel biological replicates. Asterisks indicate statistically significant differences between WT and rfs mutant, as determined by Student’s t-test (*P < 0.01; **P < 0.01). All experiments were repeated three times, with similar results. (E) The proposed working model for the regulation of NAL1 and OsPIN1 expression by RFS. During rice development, RFS binds to H3K4me3-enriched regions within the chromatin of NAL1 and OsPIN1, facilitating the opening of closed chromatin. This process leads to the expression of NAL1 and OsPIN1 transcripts, which play essential roles in regulating vascular development and root formation.
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Funding Information
  • National Research Foundation of Korea
      10.13039/501100003725
      NRF-2010-355-F00003, RS-2023-00247376, 2022H1D3A2A01096185
  • Ministry of Science and ICT, South Korea
      10.13039/501100014188
      2022H1D3A2A01096185

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