BMB Reports 2020; 53(3): 160-165  https://doi.org/10.5483/BMBRep.2020.53.3.286
Overexpression of three related root-cap outermost-cell-specific C2H2-type zinc-finger protein genes suppresses the growth of Arabidopsis in an EAR-motif-dependent manner
Sang-Kee Song1,#,*, Hyeon-Ung Jang1,#, Yo Han Kim1,#, Bang Heon Lee1 & Myeong Min Lee2,*
1Department of Biology, Chosun University, Gwangju 61452, 2Department of Systems Biology, Yonsei University, Seoul 03722, Korea
Correspondence to: Myeong Min Lee, Tel: +82-2-2123-2654; Fax: +82-2-312-5657; E-mail: mmlee@yonsei.ac.kr; Sang-Kee Song, Tel: +82-62-230-6655; Fax +82-62-230-6650; E-mail: sangkeesong@chosun.ac.kr
#These authors contributed equally to this work.
Received: November 15, 2019; Revised: December 24, 2019; Accepted: January 1, 2020; Published online: March 31, 2020.
© Korean Society for Biochemistry and Molecular Biology. All rights reserved.

Abstract
The root meristem of Arabidopsis thaliana is protected by the root cap, the size of which is tightly regulated by the balance between the formative cell divisions and the dispersal of the outermost cells. We isolated an enhancer-tagged dominant mutant displaying the short and twisted root by the overexpression of ZINC-FINGER OF ARABIDOPSIS THALIANA1 (ZAT1) encoding an EAR motif-containing zinc-finger protein. The growth inhibition by ZAT1 was shared by ZAT4 and ZAT9, the ZAT1 homologues. The ZAT1 promoter was specifically active in the outermost cells of the root cap, in which ZAT1-GFP was localized when expressed by the ZAT1 promoter. The outermost cell-specific expression pattern of ZAT1 was not altered in the sombrero (smb) or smb bearskin1 (brn1) brn2 accumulating additional root-cap layers. In contrast, ZAT4-GFP and ZAT9- GFP fusion proteins were distributed to the inner root-cap cells in addition to the outermost cells where ZAT4 and ZAT9 promoters were active. Overexpression of ZAT1 induced the ectopic expression of PUTATIVE ASPARTIC PROTEASE3 involved in the programmed cell death. The EAR motif was essential for the growth inhibition by ZAT1. These results suggest that the three related ZATs might regulate the maturation of the outermost cells of the root cap.
Keywords: Arabidopsis thaliana, EAR motif, Growth inhibition, Root cap, ZINC-FINGER OF ARABIDOPSIS THALIANA
INTRODUCTION

Plants as sessile organisms rely on their root systems to anchor themselves in the soil and to deliver water and nutrients to aerial organs. The primary root of Arabidopsis (Arabidopsis thaliana) consists of discrete concentric tissues, such as the root cap, epidermis, cortex, endodermis, and stele, from outside to inside. These tissues arise continuously from the specially organized group of cells named the root apical meristem (RAM) residing at the root tip. The quiescent center (QC) composed of around four slowly dividing cells resides at the very center of RAM and is supposed to emit signals suppressing the differentiation of the surrounding stem cells, such as the columella, epidermis/lateral root cap (EPI/LRC), cortex/endodermis, and stele initials (1, 2).

The root caps of plants are required for the protection of the RAM, the perception of the environmental cues, and the interaction with the rhizosphere. Root caps originate in two separate ways, one from the columella initial and the other from the EPI/LRC initials, which provide LRC and epidermis by periclinal division and anticlinal division, respectively (3). WUS RELATED HOMEBOX 5 (WOX5) is essential for the maintenance of columella stem cells (CSCs), as shown by the loss-of-function and the gain-of-function studies (4). WOX5 is mobile and suppresses the expression of CYCLING DOF FACTOR 4 which in turn increases the root-cap differentiation (5). CLV3/ENDOSPERM SURROUNDING REGION (CLE) 40 encoding a polypeptide hormone increases the differentiation of CSC, because cle40 develops an additional layer of CSCs (6). The treatment CLE40 peptide induces the consumption of CSCs, whereas the loss-of-function in ARABIDOPSIS CRINKLY4 and CLAVATA1 suppresses this effect of CLE40 (7).

Several related NAM ATAF and CUC (NAC) domain transcription factors are required for the maintenance of the proper number of root-cap cell layers. FEZ promotes the formative cell divisions in the columella and the EPI/LRC initials, whereas SOMBRERO (SMB) increases the differentiation of the root cap. FEZ positively regulates SMB expression in the differentiating daughter cells, whereas SMB negatively regulates the FEZ expression, preventing additional formative cell divisions (8). In addition, BEARSKIN1 (BRN1) and BRN2 are involved in the cell sloughing-off in the root cap by regulating the expression of cell-wall degradation enzyme genes, such as the CELLULASE5 (9) and ROOT CAP POLYGALACTURONASE (RCPG) genes (10, 11).

Recently, it was reported that INFLORESCENCE DEFICIENT IN ABSCISSION-LIKE1, a polypeptide hormone, and HAESA-LIKE2, a receptor kinase, signaling is required for the proper detachment of root-cap cells, possibly by regulating the expression of RCPG and BIFUNCTIONAL NUCLEASE1 (BFN1), a gene related to developmental programmed cell death (dPCD) in the root cap (12). For the matured root-cap cell layers to be detached, the dPCD occurs at the LRC following the expression of BFN1 and PUTATIVE ASPARTIC PROTEASE3 (PASPA3) encoding an aspartic protease under the regulation of SMB and then triggers the detachment of the columella cells (13).

C2H2-type (C2H2) zinc-finger protein genes are involved in transcription regulation for the responses to abiotic stresses and developmental regulations (14). Some zinc-finger protein contains a transcriptional repressor domain known as the ethylene-responsive element binding factor-αssociated amphiphilic repression (EAR) motifs that regulate the gene expression negatively by the interaction with corepressor TOPLESS (TPL) and TPL-related proteins (TPRs) recruiting the histone deacetylase complex (15-17). Among the three-fingered C2H2 zinc-finger proteins, the function of DUO1-ACTIVATED ZINC FINGER1 (DAZ1) and DAZ2 are best characterized. They are required for the male germ cell divisions and can interact with corepressor TPL/TPR for the transcriptional suppression (18). However, the roles of other three-fingered zinc-finger protein genes have been poorly characterized (19, 20).

To screen for genes regulating the root development of Arabidopsis, we introduced 5x UAS activation tags into a Q2610 enhancer trap line, of which the root tip expresses GAL4-VP16 transcription factor abundantly (21), and then isolated a dominant mutant displaying a short and twisted root overexpressing a zinc-finger protein gene. Here, we report the functions and expression patterns of the three closely related three-fingered C2H2 zinc-finger protein genes (14).

RESULTS AND DISCUSSION

Isolation and characterization of drd2-D displaying short and twisted root phenotypes

We isolated a dominant mutant developing short and twisted roots named defective root development 2-D (drd2-D) by introducing the 5x UAS tag into a Q2610 enhancer trap line (Fig. 1B). The drd2-D displayed the compromised root epidermal patterning as shown by the non-hair cell markers (Supplementary Fig. S1). By thermal asymmetric interlaced polymerase chain reaction (TAIL-PCR) analysis, we found the insertion site of the UAS tag at the 132 base pairs (bps) upstream of the start codon of a C2H2-type zinc-finger protein gene, ZINC-FINGER OF ARABIDOPSIS THALIANA (ZAT1, At1g02030) (Fig. 1C) that was only partially characterized previously (22). The transcripts of ZAT1 increased in drd2-D compared with the WT control, as shown by the reverse transcription (RT)-PCR analysis (Fig. 1D), and the transgenic expression of UASp: ZAT1 under the control of Q2610 (Q2610>>ZAT1) induced severe growth inhibition in the root of transgenic seedlings (Fig. 1E). When UASp:ZAT1 was expressed during the embryogenesis by a J1721 enhancer mimicking the expression of MONOPTEROS (MP) (23-25), the transgenic seedlings exhibited rudimentary roots reminiscent of the mp phenotype (Fig. 1F). The organization of RAM of the Q2610>>ZAT1 seedling was compromised, as shown by the diffusively extended expression pattern of WOX5p:GUS, a QC marker (Supplementary Fig. S2A, B). In addition, the cell division was suppressed in the RAM of Q0990>>ZAT1, displaying defective growth and a reduced meristematic zone (Supplementary Fig. S2C, D), as shown by the reduced expression of CYCB1;1p:GUS (Supplementary Fig. S2E, F). These results indicate that ZAT1 can inhibit the growth of Arabidopsis, leading to the complete loss of specific organs where it is highly expressed.

In the Arabidopsis genome, there are two ZAT1-related genes, ZAT4 and ZAT9. ZAT1 possesses 43.4% and 43.8% amino-acid (a.a.) sequence identity with ZAT4 and ZAT9, respectively, and ZAT4 and ZAT9 exhibit 60.4% identity with each other (Supplementary Fig. S3). They share a conserved EAR motif at the C-terminal ends together with three conserved C2H2 zinc-finger motifs. Both ZAT4 and ZAT9 likely shared the function of ZAT1 as Q2610>>ZAT4 and Q2610>>ZAT9 exhibited severe growth inhibition in the primary root (Fig. 1G, H) comparable to Q2610>>ZAT1 (Fig. 1E). These results suggest that the three related ZATs might function redundantly to suppress the growth of Arabidopsis in the specific tissues.

To find out whether ZAT1 can affect the growth of aerial organs as well, we compared the organ size and the ZAT1 transcription level in a weak transgenic line, J0571>>ZAT1, that can complete the whole life cycle by developing reproductive organs. The growth inhibition in the roots (Fig. 1I, J) and siliques (Fig. 1K, L) was well correlated with the transcription level of ZAT1 (Fig. 1M).

The outmost cell-specific expression patterns of ZAT1, ZAT4, and ZAT9

To examine the overall expression patterns of the ZATs in various organs, we did RT-PCR analysis with gene-specific primers. The transcripts of ZATs accumulated in the various tissues at the various developmental stages (Supplementary Fig. S4). To visualize the tissue-specific expression patterns of ZATs, a β-glucuronidase (GUS) reporter was driven by each ZAT promoter in the transgenic plants. The three ZATs commonly expressed in the outermost layer of the root cap (Fig. 2A, H, O). To identify the earliest developmental stage when ZATs begin to express, we examined the GUS activity in the transgenic embryos. ZATs did not express at the torpedo (Fig 2B, I, P) and bent cotyledon (Fig 2C, J, Q) stages when the three discrete root-cap layers are present.

The ZAT1p:GUS and ZAT4p:GUS began to express around 24 h after germination (Fig. 2D, K), whereas ZAT9p:GUS did around 36 h after germination (Fig. 2S). In addition to the root cap, the ZAT1-specific GUS expression was observed in the stele and endodermis in the root (Supplementary Fig. S5A-B) and hydathode (Fig. 2F). The ZAT4-specific expression was found in the guard cells (Fig. 2M) and pollen grains (Fig 2N), where the ZAT9p:GUS was active as well (Fig. 2U). These results indicate that the promoters of ZATs are inactive during the embryogenesis and then are activated post-embryonically after the root tips are exposed to growth media.

The expression pattern of ZAT1p:GUS was not apparently altered in drd2-D, where ZAT1 is highly expressed (Supplementary Fig. S5C) and in the Q2610>>SMB line, in which the root-cap layers increased (Supplementary Fig. S5D). In contrast, the number of root-cap layers expressing ZAT1p:GUS increased in tyrosylprotein sulfotransferase (tpst)-1 developing an array of partially detached root-cap layers attached at the columella cells (26) (Supplementary Fig. S5E, F). These results suggest that ZAT1 expression is not under the regulation of ZAT1 and is activated when the root-cap cells are exposed to growth media. It was reported that the expression of ZAT1 is responsive to nitrate (20, 27); however, this interaction might be indirect, because nitrate affects the development of lateral roots and thereby the ‘ZAT1-expressing’ root caps as well (28).

The outermost layer-specific expression of ZAT1 is not altered in the background-accumulating additional root-cap layers

To more precisely examine the ZAT1-expressing cell layers in the root cap, the GFP5-ER reporter and ZAT1-GFP were driven by the ZAT1 promoter in the transgenic plants. Both ZAT1p: GFP5-ER and ZAT1p:ZAT1-GFP expression was specifically localized in the outermost cell layer of the root caps of wild-type seedlings (Fig. 3A, B, H-K). This layer-specific expression was not altered even in the background of smb-3 and smb-3 brn1-1 brn2-1 triple mutant, where additional root-cap layers accumulated (Fig. 3C-G, 3L, M). Interestingly, the underlying cells began to express the ZAT1 as they were exposed to growth media, even though the ex-outermost cells was not completely detached (Fig. 3F). In addition to the root cap, ZAT1-GFP was localized in the nuclei of the endodermal cells (Fig. 3J, K). These results suggest that ZAT1 promoter might not be gradually activated as the root-cap cells move away from the initial position, but are rather abruptly activated by the exposure to the growth media. Furthermore, ZAT1 expression is likely regulated independently of SMB, BRN1 and BRN2.

Both ZAT4p:GFP5-ER and ZAT9p:GFP5-ER were specifically expressed in the outermost layers of the root cap as well (Fig. 3N-O, 3R-S). Unlike ZAT1-GFP, ZAT4-GFP and ZAT9-GFP were broadly distributed to the inner root-cap cells even close to the CSCs (Fig. 3P, Q, 3T, U) together with the outermost cells. These results suggest that ZAT4 and ZAT9 proteins or ZAT4 and ZAT9 transcripts might be mobile, unlike ZAT1 or ZAT1. The discrepancy between the expression sites and the location of ZAT4-GFP and ZAT9-GFP fusion proteins implies that these proteins could transfer the growth inhibition signals from the outermost cells that can directly sense the environmental cues.

The expression of PASPA3 was induced by the ectopic expression of ZAT1

To examine whether ZAT1 regulates the expression of the root-cap-specific genes such as SMB, CEL5, and PASPA3, each GUS reporter driven by the respective promoter was introduced into the Q2610>>ZAT1 background. The expression of SMBp:GUS and CEL5p:GUS was maintained at the root tip but reduced, probably because of the growth inhibition by ZAT1 (Fig. 4A, B, 4G, H). In contrast, the expression of PASPA3p: GUS in the Q2610>>ZAT1 seedlings was increased in the root-hypocotyl transition zone, where Q2610 is actively expressed (Fig. 4C-F, 4I-L). These results suggest that SMB and CEL5 are not under the regulation of ZAT1, whereas ZAT1 might be involved in the regulation of the PASPA3 expression triggering dPCD.

The growth inhibition by ZAT1 is dependent on the EAR motif

EAR motif is known to mediate the interaction between transcription repressors and TPL/TPR co-repressors to recruit histone deacetylase complexes (15). ZAT1 possesses two conserved EAR motifs, motif 1 (LSLML) present in the 130-134th a.a. and motif 2 (DLNLPA) in the 250-255th a.a. (16). Because motif 2 is well conserved among ZAT1, ZAT4, and ZAT9 (Supplementary Fig. S3), we introduced the single or double mutation into motif 2 by site-directed mutagenesis to investigate whether the EAR motif 2 is required for the growth inhibition (Fig. 4M).

Overexpression of the UASp:ZAT1-L251A or UASp:ZAT1-L253A single mutant driven by Q2610 induced the growth inhibition of transgenic seedlings comparable to that of Q2610>>ZAT1 (Fig. 4N-P). However, the overexpression of UASp:ZAT1-mEAR2 (L251; 253A) failed to inhibit the growth when we examined 30 independent transgenic lines (Fig. 4Q). These results indicate that the conserved EAR motif 2 is required for the growth inhibition by ZAT1.

It was reported that transgenic plants overexpressing ZAT7, a C2H2 zinc-finger protein gene with an EAR motif, displayed salinity resistance together with growth-inhibition phenotypes. The EAR motif of ZAT7 was essential for the salinity resistance but not for the growth inhibition by ZAT7 (29). In contrast, the growth inhibition by ZAT1 in this study is dependent on the EAR motif of ZAT1, suggesting that the function of an EAR-motif differs for each zinc-finger protein.

Considering the growth inhibition activities, the roles of ZAT1 in the outmost cells might be to prevent them from further growth and to induce cell maturation after the exposure to the media. Indeed, the ZAT1 overexpression induced the ectopic expression of PASPA3, a marker for dPCD (30), in the hypocotyl-root transition zone, although it is not clear whether this interaction is direct or not. Because the endogenous expression patterns of ZAT1 and PASPA3 partially overlap in the columella and bottom of LRC, ZAT1 might regulate the PASPA expression in the corresponding tissues (13).

The shared functions of ZATs might not be essential for normal growth, because a zat1 zat4 zat9 triple mutant did not display any discernible phenotypes (Supplementary Fig. S6). However, in a specific environmental condition that we have not yet investigated, ZATs might be required for the proper growth of Arabidopsis.

MATERIALS AND METHODS

Plant materials and growth condition

The T-DNA insertion site of drd2-D was identified as described previously (31). The T-DNA insertion lines SAIL_142_F08 (zat1-1), Wisceq_DsLox477-480D18 (zat9-1), smb-3 (SALK_143526) (8), brn1-1 (SALK_151986), and brn2-1 (SALK_151604) (10) were obtained from Arabidopsis Biological Resource Center (ABRC), and GABIseq_181A01 (zat4-1) was obtained from Nottingham Arabidopsis Stock Centre. GL2p:GUS (32), CYCB1;1p:GUS (33), WOX5p:GUS (4), and CPCp:GUS (34) were described previously (35, 36). Plants were grown as described in the supplementary materials.

Gene expression analyses

GUS activity was defined histochemically by staining four-day-old seedlings as described (37). To investigate ZATs transcripts expression level, we extracted total RNA from various tissues and used it for the templates for cDNA synthesis. We used ELONGATION FACTOR1 (EF1) to normalize the relative levels of each transcript. Primers used in this study are given in Supplementary Table 1.

Confocal Microscopy

To detect GFP signals, we stained seedlings with 5 μg/mL propidium iodide (PI) and used a Zeiss LSM 880 confocal microscope (38). The GFP signals were detected with excitation at 488 nm and detected with a 493 to 544 nm band-path filter, PI signal was detected with a 604 to 718 nm long-path filter.

Preparation of gene constructs

Gene constructs were prepared as described in the supplementary materials and methods.

Supplemental Materials
BMB-53-160_Supple.pdf
ACKNOWLEDGEMENTS

This work was supported by the National Research Foundation of Korea (grant No. NRF-2014R1A2A1A11051172 to MML), the National Research Foundation of Korea (grant no. NRF-2015R1D1A1A01059797 to S.S.), research fund from Chosun University 2015 (K206888002) to S.S.

CONFLICTS OF INTEREST

The authors have no conflicting interests.

Figures
Fig. 1. Overexpression of ZAT1 inhibits growth of various organs in transgenic plants including drd2-D mutant. (A, B) A drd2-D seedling exhibiting the short and twisted root phenotypes as compared with WT. (C) The T-DNA insertion site inducing drd2-D phenotype identified by the TAIL-PCR analysis. T-DNA is located at 144 bp upstream from the start codon of ZAT1 (At1g02030). (D) An RT-PCR analysis showing the increased transcripts of ZAT1 gene in the drd2-D. (E-H) The root-defective phenotypes of seedlings of Q2610>>ZAT1 (E), J1721>>ZAT1 (F), Q2610>>ZAT4 (G), and Q2610>>ZAT9 (H). (I-M) J0571>>ZAT1 exhibits reduced root growth (I, J) and siliques length (K, L), which correlated with the ZAT1 expression in transgenic lines identified by RT-PCR analysis (M). Bars = 200 μm in (A-I) and 1 mm in (K). ***P < 0.01, one-way-ANOVA (Tukey HSD), root n = 16; silique n = 13.
Fig. 2. Expression patterns of ZAT1p:GUS, ZAT4p:GUS, and ZAT9p: GUS reporter genes. ZAT1p:GUS (A-G), ZAT4p:GUS (H-N), and ZAT9p:GUS (O-U) expression in the root tips (A, H, O), torpedo-stage embryos (B, I, P), bent-cotyledon stage embryos (C, J, Q), seedlings 24 h after germination (D, K, R), 36 h after germination (E, L, S), cotyledons 5 d after germination (F), and open flowers (G, N, U). Inset in M is an enlarged view of the cotyledon. Bars = 50 μm in (A-E, H-L, O-S, inset in M), 200 μm in (F-G, M-N, T-U).
Fig. 3. The expression patterns of GFP5-ER and ZAT1/4/9-GFP fusion proteins driven by the respective ZAT1/4/9 promoters in the transgenic roots. (A-G) ZAT1p:GFP5-ER expression in WT (A, B), smb-3 (C, D), and smb-3 brn1-1 brn2-1 (E-G). A black closed arrowhead in (F) indicates a newly exposed outermost cell. (H-M) ZAT1p:ZAT1-GFP expression in WT (H-K) and smb-3 (L-M). (N-U) Reporter gene expression in transgenic roots expressing ZAT4p: GFP5-ER (N, O), ZAT4p:ZAT4-GFP (P, Q), ZAT9p:GFP5-ER (R, S), and ZAT9p:ZAT9-GFP (T, U). White arrowheads indicate nuclei expressing ZAT1-GFP (J), ZAT4-GFP (Q), and ZAT9-GFP (T). Asterisks indicate QCs. Bars = 50 μm.
Fig. 4. The ectopic expression of ZAT1 induced the mis-expression of PASPA3 and the requirement of the EAR motif for the ZAT1 activity for growth inhibition. (A-L) The expression patterns of root-cap reporters in the Q2610>>ZAT1 background (G-L) as compared with control (A-F). SMBp:GUS (A, G), CEL5p:GUS (B, H), PASPA3p:GUS (C-F, I-L). Bars = 50 μm. (M) A diagram indicating the amino-acid sequences of EAR motif 2 of WT and EAR motif mutants of ZAT1. (N-Q) The phenotypes of 4-d-old transgenic seedlings of Q2610>>ZAT1 (N), Q2610>>ZAT1-L251A (O), Q2610>>ZAT1-L253A (P), and Q2610>>ZAT1-mEAR2 (Q). Inset in Q is a reduced view of the seedling. Bars = 200 μm in (N-Q) and = 1 mm in inset.
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