A nuclear-encoded chloroplast protein harboring a single CRM domain plays an important role in the Arabidopsis growth and stress response
© Lee et al.; licensee BioMed Central Ltd. 2014
Received: 21 December 2013
Accepted: 11 April 2014
Published: 16 April 2014
Although several chloroplast RNA splicing and ribosome maturation (CRM) domain-containing proteins have been characterized for intron splicing and rRNA processing during chloroplast gene expression, the functional role of a majority of CRM domain proteins in plant growth and development as well as chloroplast RNA metabolism remains largely unknown. Here, we characterized the developmental and stress response roles of a nuclear-encoded chloroplast protein harboring a single CRM domain (At4g39040), designated CFM4, in Arabidopsis thaliana.
Analysis of CFM4-GFP fusion proteins revealed that CFM4 is localized to chloroplasts. The loss-of-function T-DNA insertion mutants for CFM4 (cfm4) displayed retarded growth and delayed senescence, suggesting that CFM4 plays a role in growth and development of plants under normal growth conditions. In addition, cfm4 mutants showed retarded seed germination and seedling growth under stress conditions. No alteration in the splicing patterns of intron-containing chloroplast genes was observed in the mutant plants, but the processing of 16S and 4.5S rRNAs was abnormal in the mutant plants. Importantly, CFM4 was determined to possess RNA chaperone activity.
These results suggest that the chloroplast-targeted CFM4, one of two Arabidopsis genes encoding a single CRM domain-containing protein, harbors RNA chaperone activity and plays a role in the Arabidopsis growth and stress response by affecting rRNA processing in chloroplasts.
KeywordsArabidopsis thaliana Chloroplast CRM domain RNA-binding protein RNA metabolism
Chloroplasts are derived from cyanobacteria through endosymbiosis, and massive gene transfer from the plastid to the nucleus occurred during evolution . Chloroplasts possess approximately 100-150 genes in their own circular genome that encodes messenger RNAs, ribosome RNAs, and transfer RNAs. In addition to its own gene products, functional communication between chloroplasts and nucleus is required, and many nuclear-encoded proteins are targeted to chloroplasts and play fundamental roles in the regulation of chloroplast gene expression. Expression of chloroplast genes is commonly regulated at posttranscriptional level, including mRNA processing, splicing, editing, decay, and translational control [2–5]. A sophisticated regulatory process between chloroplasts and nuclei is required to fine-tune chloroplast gene expression, and many nuclear-encoded RNA-binding proteins (RBPs) have been recently regarded as the primary elements that modulate posttranscriptional steps in chloroplasts [2, 4, 6, 7]. Although chloroplasts share some features of RNA metabolism with their bacterial ancestors, chloroplasts require a more complicated mechanism of RNA metabolism compared to their ancestor, which have both prokaryotic and eukaryotic characteristics [8, 9]. One particular example is the splicing of group I and group II introns. In contrast to self-splicing of prokaryotic introns, chloroplasts have lost their capacity to self-splice, and the splicing of group I and group II introns in chloroplasts requires many nuclear-encoded proteins that form protein complexes similar to spliceosomal complexes found in eukaryotes [10–14]. Therefore, involvement of nuclear-encoded RBPs is indispensible for posttranscriptional regulation of RNA metabolism and gene expression in chloroplasts.
CRM (chloroplast RNA splicing and ribosome maturation) domain-containing proteins were first found in archaea and bacteria. Based on their structural data and predicted domain structures, CRM domain proteins were suggested to have RNA-binding activity . Prokaryotes contain proteins harboring only a single CRM domain, whereas land plants contain proteins harboring multiple CRM domains. Splicing of group I and group II introns and tRNAs and processing of rRNAs in chloroplasts require different complexes of CRSs (for chloroplast RNA splicing), CAFs (for CRS2-associated factors), and CFMs (for CRM family members) that harbor multiple CRM domains [12, 13, 15–19]. It has also been demonstrated that mutation in CRM domain-containing protein genes results in pale-green phenotypes, delayed development, and aborted seed production in plants, indicating the important roles of CRM domain proteins in plant growth and development [11, 12, 17, 20, 21].
Despite an increased understanding of the roles of CRM domain-containing proteins in chloroplast RNA metabolism and plant growth and development, the functional roles of most of the CRM domain-containing proteins have not been demonstrated experimentally. The Arabidopsis (Arabidopsis thaliana) and rice (Oryza sativa) genomes harbor the genes encoding 16 and 14 CRM domain-containing proteins, respectively . Among the 16 Arabidopsis CRM domain-containing protein genes, two genes (At4g39040 and At2g21350) encode the smallest proteins harboring a single CRM domain . However, the role of single CRM domain-containing proteins has not been demonstrated in plants. Here, we determined the developmental and stress response roles of a single CRM domain-containing protein (At4g39040). Because this protein belongs to subfamily group 4 among CRM domain proteins , we designated it as CRM family member subfamily4 (CFM4). We show that CFM4 possesses RNA chaperone activity and is involved in rRNA processing, which is important for normal growth, development, and the stress response in plants.
Structural features and characterization of CFM4 in Arabidopsis
The CRM proteins in Arabidopsis and rice have been predicted to be targeted mainly to chloroplasts or mitochondria. To determine the subcellular localization of CFM4, the cDNA encoding CFM4 was ligated in front of the green fluorescence protein (GFP) gene, and expression of the CFM4-GFP fusion protein was investigated in transgenic Arabidopsis plants. Strong GFP signals were observed in chloroplasts (Figure 1B). To examine whether CFM4 is also localized to mitochondria, Arabidopsis mitochondria were stained with Mito-tracker that is a red-fluorescent dye and stains mitochondria in live cells, and the signals from plastids in roots and chloroplasts in leaves were examined. The results showed that the signals from mitochondria did not overlap with the signals from chloroplasts, and GFP signals were observed exclusively in chloroplasts (Figure 1C and 1D). These results clearly indicate that CFM4 is localized to chloroplasts.
CFM4 plays a role in Arabidopsisgrowth and senescence
CFM4 is involved in Arabidopsisresponse to abiotic stresses
CFM4 affects rRNA processing in chloroplasts
CFM4 possesses RNA chaperone activity
To further confirm whether CFM4 possesses RNA chaperone activity, the in vitro and in vivo nucleic acid-melting abilities of CFM4 were assessed via DNA-melting and transcription anti-termination assays. For the analysis of in vitro DNA-melting ability of CFM4, the recombinant GST-CFM4 fusion proteins were purified from E. coli (Additional file 8) and GST-CFM4 fusion protein was tested for its ability to destabilize base pairs in the synthetic DNA molecules labeled with a fluorophore (tetramethyl rhodamine) and quencher (dabcyl). Fluorescence of the molecular beacon increased after adding the GST-CFM4 proteins or the GST-CspA fusion proteins (positive control), confirming the DNA-melting activity of CFM4 (Figure 6B). By contrast, adding GST alone (negative control) did not increase fluorescence (Figure 6B). To determine whether CFM4 has the ability to destabilize base pairs in RNA, the in vivo RNA-melting ability of CFM4 was assessed via transcription anti-termination assays using E. coli RL211 cells that harbor a chloramphenicol resistance gene downstream from a trpL terminator with stem-loop structure . When the RL211 cells were grown in the MS medium containing chloramphenicol, the cells expressing CFM4 or CspA grew well, suggesting that CFM4 and CspA destabilize the stem-loop structures present in the transcription termination signal. By contrast, the cells harboring the pINIII vector did not grow in chloramphenicol-containing MS medium (Figure 6C). Taken together, these results indicate that CFM4 possesses RNA chaperone activity.
The results presented here demonstrate that CFM4, one of two Arabidopsis genes encoding single CRM domain-containing protein, plays a role in the Arabidopsis growth and stress response by affecting rRNA processing in chloroplasts. Analysis of the T-DNA knockout lines indicated that CFM4 exhibits important function during plant growth and senescence (Figures 2 and 3), which is in agreement with its postulated roles in chloroplast RNA metabolism. Our current results point to the important roles of CRM domain-containing proteins in plant growth and development. It has been demonstrated that mutation in the genes encoding multiple CRM domain-containing proteins causes pale-green phenotypes, delayed development, and aborted seed production in plants [11, 12, 17, 20, 21]. In addition to its roles in the growth and senescence of Arabidopsis under normal growth conditions, CFM4 also affected the plant response to abiotic stresses. Seed germination and seedling growth of cfm4 mutants were retarded compared with those of the wild-type plants under salt or cold stress conditions (Figure 4), suggesting that CFM4 plays a positive role in seed germination and seedling growth of Arabidopsis under salt or cold stress conditions. Interestingly, the effect of CFM4 on seed germination and seedling growth of plants was confined to salt or cold stress, as no differences in seed germination and seedling growth were observed between the wild type and cfm4 mutants under dehydration stress conditions. Notably, the genes encoding single CRM domain-containing proteins as well as the genes encoding multiple CRM domain-containing proteins play important roles in plant growth, development, and stress response.
All multiple CRM domain-containing proteins whose functions have been characterized in plants are involved in the splicing of chloroplast group II and I introns . CAF1, CAF2, and CRS1, the three maize proteins harboring multiple copies of the domain, are required for the splicing of group II introns in chloroplasts [15, 28]. In addition, it has been demonstrated that CFM2 and CFM3 together with CRS2/CAF complexes promote the splicing of chloroplast introns [12, 17]. In contrast to the well-characterized roles of multiple CRM domain-containing proteins in the splicing of chloroplast introns, CFM4 plays no role in the splicing of chloroplast introns (Figure 5A and Additional file 7). However, our current analysis shows that CFM4 is involved in the processing and maturation of 16S and 4.5S rRNAs (Figure 5B). This observation is in line with previous findings that prokaryotic proteins harboring a single CRM domain participate in ribosome maturation . The YhbY, the CRM domain protein in Escherichia coli, is a small protein with molecular mass of ~10 kDa and is associated with pre-50S ribosomal subunits, which function in ribosome assembly . Among the 16 CRM domain proteins found in Arabidopsis, CRM4 is the most homologous to YhbY in that it harbors little else except a single CRM domain (Additional file 1). We propose that the delayed growth of cfm4 mutants is due to, at least in part, improper processing of 16S and 4.5S rRNAs in chloroplasts. Interestingly, improper rRNA processing in cfm4 mutants resulted in impaired ABA biosynthesis (Figure 2), which supports a notion that proper chloroplast function is required not only for active photosynthesis but also for ABA biosynthesis, both of which are required for normal plant growth .
The proposed mechanistic role of CFM4 as an RNA chaperone in chloroplast rRNA metabolism is intriguing. RNA processing as well as intron splicing requires proper folding of RNA substrates, and many RBPs play an important role in RNA-RNA and RNA-protein interactions during RNA metabolism [23, 29–31]. RNA chaperones are nonspecific RBPs that bind diverse RNA substrates and help RNAs fold by inducing structural rearrangement of misfolded RNAs [25, 32, 33]. It has recently been demonstrated that one of the minor spliceosomal proteins U11/U12-31 K possesses RNA chaperone activity and is indispensible for correct intron splicing and normal growth and development in Arabidopsis and rice [23, 34], which emphasizes the important role of RNA chaperones in maintaining RNA substrates in splicing-competent structures for correct processing to occur. Involvement of RNA chaperone activity in the splicing of group I and group II introns has been demonstrated in yeast mitochondria. The yeast DEAD-box protein MSS116 promotes the splicing of both group I and group II introns in mitochondria via functioning as an RNA chaperone [35–38]. Our current analysis clearly indicates that CFM4 harbors RNA chaperone activity (Figure 6). It is likely that RNA chaperone activity of CFM4 is needed to maintain precursor-rRNA in processing-competent structures for subsequence rRNA processing. Although it is not clear at present how CFM4 affects processing of only two (16S and 4.5S) rRNAs out of the four rRNAs in the chloroplast, it is possible that CFM4 recognizes specific sequence or structural elements in 16S and 4.5S rRNAs and the RNA chaperone activity of CFM4 is involved in the formation of processing-competent structures of these rRNAs.
The present study shows that CFM4 harboring RNA chaperone activity is involved in rRNA processing in chloroplasts, which is important for growth and the stress response of plants. Although much progress has been made in the characterization of the roles of CRM domain-containing proteins in intron splicing and rRNA processing during chloroplast gene expression, the roles of many CRM proteins in plant growth and development as well as chloroplast RNA metabolism remain largely unknown. In particular, understanding the biological function of single CRM domain-containing proteins is far behind compared with that of multiple CRM domain-containing proteins. Exploring the importance of the number of CRM domains and involvement of each CRM domain in substrate recognition during intron splicing and rRNA processing should provide a much deeper insight into the mechanistic role of CRM family members in chloroplast RNA metabolism.
Plant materials and growth conditions
The Arabidopsis thaliana used in this study was Col-0 ecotype. The plants were grown either in a mixture of vermiculite, peat moss, and perlite or on half-strength Murasige & Skoog (MS) medium containing 1% sucrose at 23 ± 2°C under long-day conditions (16 h light/8 h dark cycle). To construct overexpressing transgenic plants and complementation lines, the CFM4 cDNA coding sequence was cloned into the NcoI/BstEII of pCambia1301 vector containing the cauliflower mosaic virus 35S promoter. The Arabidopsis transformation was carried out via vacuum infiltration  using Agrobacteruim tumefaciens GV3101. The T3 transgenic lines were selected and subsequently utilized for the phenotype investigation. Expression of CFM4 in each transgenic plant was analyzed by RT-PCR using the gene-specific primers listed in Additional file 9. Arabidopsis mutant seeds with T-DNA inserted into the CFM4 gene (SALK_076439 and SALK_126978) were obtained from The Arabidopsis Biological Resource Center (Columbus, OH, USA). The absence of CFM4 expression in the mutant lines was confirmed by RT-PCR using the gene-specific primers listed in Additional file 9.
Analysis of cellular localization of CFM4 in Arabidopsis
To determine the cellular localization of CFM4, the cDNA corresponding to the full-length CFM4 was ligated using the XbaI/BamHI site in front of the GFP gene, and CFM4-GFP fusion proteins were expressed under the control of the CaMV 35S promoter in Arabidopsis. The GFP signals in the leaves and roots of the plants were observed using a Zeiss LSM510 laser scanning confocal microscope (Carl Zeiss Inc. Thornwoold, NY, USA). The excitation and emission wavelengths were 488 and 545 nm, respectively. Mitochondria in the leaves and roots of the plants were stained with MitoTracker® Red CMXRos (Invitrogen).
RNA extraction and RT-PCR
Total RNAs were extracted from frozen tissues using the Plant RNeasy Extraction kit (Qiagen, Valencia, CA, USA), and the concentration of RNAs was quantified by spectrophotomety. RT-PCR was performed using the primers spanning the T-DNA insertion site to confirm whether the T-DNA tagged mutant seeds from ABRC were knockout mutants. To examine splicing patterns of intron-containing genes, total RNAs were extracted from 4-week-old plants, and 100 ng RNA was used for RT-PCR with the gene-specific primers listed in Additional file 9. To examine the expression levels of ABA biosynthesis-related genes, total RNAs were extracted from 26-day-old plants, and 100 ng RNA was used for quantitative real-time RT-PCR with the gene-specific primers listed in Additional file 9.
Measurement of ABA content
Ten grams of plant tissues at 26 DAG were ground in liquid nitrogen, mixed with an extraction solution (80% methanol, 2% acetic acid), and incubated overnight at 4°C. After centrifugation at 2000 × g for 10 min, the pellet was dissolved in 10% methanol and TBS (50 mM Tris, 0.1 mM MgCl2, and 0.15 M NaCl, pH 7.8). ABA concentration was determined using Phytodetek® ABA Test kit (Agdia Inc., Elkhart, Indiana, USA) according to the manufacturer’s instructions.
Northern blot analysis of rRNA transcripts in chloroplasts
Total RNA was extracted from 4-week-old wild-type and cfm4 mutant plants for chloroplast rRNA processing analysis. Five or ten micrograms of total RNA was electrophoresed on an 1.2% agarose or 16.5% formaldehyde (w/v) gel, blotted to a Hybond-N+ nylon membrane (Amersham Biosciences, Parsippany, NJ, USA), and then cross-linked under UV. Hybridization with 32P-labeled probes was performed in 0.15% SDS, 5 × SSC, 5 × Denhardt’s solution, salmon sperm DNA (10 mg/ml) and 50% formamide at 42°C overnight. The membrane was washed 2-3 times in 2 × SSC and 0.1% SDS at room temperature and once in 0.1 × SSC and 0.1% SDS at 42°C. The genes encoding chloroplast rRNAs were cloned into the pGEM-T Easy vector using the Arabidopsis chloroplast sequence information (GenBank accession no. AP00023), and the hybridization probes were amplified by PCR from the chloroplast rDNA-cloned vector. The probes contained rDNA sequences of the following region: rrn16S (position 101,500-102,482), rrn23S-5′ (position 104,691-106,691), rrn23S-3′ (position 106,692-107,500), rrn4.5S (position 107,599-107,701), and rrn5S (130,580-130,700). The probes were labeled with 32P-dCTP using the Random Primer DNA Labeling Kit (TaKaRa Bio., Shiga, Japan) according to the manufacturer’s instructions.
RNA chaperone assay
For the cold shock and transcription anti-termination assays in E. coli, the pINIII vector expressing CFM4 was constructed essentially as described previously . In the cold shock assay, the vector was introduced into E. coli BX04 mutant cells  that lack four cold shock proteins and thus are highly sensitive to cold stress. The BX04 mutant cells harboring either pINIII-CFM4, pINIII-CspA (positive control), or pINIII (negative control) were grown in Luria-Bertani (LB) medium containing ampicillin and kanamycin, and the serial-diluted cultures (from 10-1 to 10-5) of BX04 cells were spotted on LB medium and incubated at low temperature (20°C). In the transcription anti-termination assay, E. coli RL211 cells  transformed with each construct were grown in liquid LB medium and spotted on LB-carbenicillin plates with or without chloramphenicol. Growth of the cells was inspected on a daily basis.
For in vitro DNA-melting assay, the DNA molecules labeled with a fluorophore (tetramethyl rhodamine) and quencher (dabcyl) were synthesized as previously described [40, 41] For the expression and purification of recombinant GST-CFM4 fusion proteins in E. coli, the coding region of CFM4 was cloned into pGEX-5X-2 vector (Amersham Pharmacia Biosciences). The recombinant GST-CFM4 fusion proteins were expressed in BL21 DE3 competent cells (Promega) and purified using glutathione Sepharose 4B resin. The fluorescence emitted from the reaction between the GST-CFM4 fusion proteins and the DNA molecules was measured using a Spectra Max GeminiXS spectrofluorometer (Molecular Devices, Sunnyvale, CA, USA) with excitation and emission wavelengths of 555 nm and 575 nm, respectively.
Chloroplast RNA splicing and ribosome maturation
CRM family member subfamily 4
Day after germination
We thank Drs. M. Inouye and S. Phadtare for the BX04 mutant cells and the pINIII vector and Dr. R. Landick for the E. coli RL211 cells. This study was supported by grants from the Mid-career Researcher Program through a National Research Foundation of Korea grant funded by the Ministry of Education, Science and Technology (2011-0017357) and from the Next-Generation BioGreen21 Program (PJ00949102), Rural Development Administration, Republic of Korea.
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