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Short title：mTERF8 Function in Arabidopsis 1 Corresponding author: Prof. Zhong-Nan Yang 2

College of Life Sciences, 3 Shanghai Normal University, Shanghai, 200234, China 4

Tel: +86-21-64324650 5 Fax: +86-21-64324190 6 E-mail: [email protected] 7

8 mTERF8, a Member of the Mitochondrial Transcription Termination Factor Family, is 9 Involved in the Transcription Termination of Chloroplast Gene psbJ1 10 11 12 Hai-Bo Xiong, Jing Wang, Chao Huang, Jean-David Rochaix, Fei-Min Lin, Jia-Xing Zhang, 13 Lin-Shan Ye, Xiao-He Shi, Qing-Bo Yu*, and Zhong-Nan Yang* 14 15 Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai 16 Normal University, Shanghai, 200234, China (H.B.X., J.W., C.H., F.M.L., J.X.Z., L.S.Y., X.H.S., 17 Q.B.Y., Z.N.Y.) 18 Departments of Molecular Biology and Plant Biology, University of Geneva, Geneva, Switzerland 19 (J.-D.R.) 20 Hunan Provincial Key Laboratory of Phytohormones and Growth Development, Hunan 21 Agricultural University, Changsha 410128, China (C.H.) 22 23 *To whom correspondence should be addressed. E-mail: [email protected], and 24 [email protected]; fax:+86-21-64324190 25 26 Author Contributions: H.B.X performed most of the experiments; and J.W., C.H., F.M.L., J.X.Z., 27 L.S.Y., X.H.S. provided technical assistance; J.D.R contributed to data analysis and discussion; 28 Q.B.Y., and Z.N.Y designed and supervised the study, and wrote the manuscript. 29 30 One-sentence Summary: mTERF8 functions as a transcription terminator of chloroplast gene 31 psbJ in Arabidopsis. 32 33 Footnotes: 34 1This work was supported by the National Natural Scientific Foundation of China (grant no. 35 31570232 and 31370271), and the Shanghai Science and Technology Committee (18DZ2260500, 36 17DZ2252700). The author responsible for distribution of materials integral to the findings 37 presented in this article in accordance with the policy described in the Instructions for Authors is: Dr. 38

Plant Physiology Preview. Published on November 4, 2019, as DOI:10.1104/pp.19.00906

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Qing-Bo Yu ([email protected]). 39 40 ABSTRACT 41 Members of the mitochondrial transcription terminator factor (mTERF) family, originally identified 42 in vertebrate mitochondria, are involved in the termination of organellular transcription. In plants, 43 mTERF proteins are mainly localized in chloroplasts and mitochondria. In Arabidopsis thaliana, 44 mTERF8/pTAC15 was identified in the plastid-encoded RNA polymerase (PEP) complex, the 45 major RNA polymerase of chloroplasts. In this work, we demonstrate that mTERF8 is associated 46 with the PEP complex. An mTERF8 knockout line displayed a wild type-like phenotype under 47 standard growth conditions, but showed impaired efficiency of photosystem II electron flow. 48 Transcription of most chloroplast genes was not substantially affected in the mterf8 mutant; 49 however, the level of the psbJ transcript from the psbEFLJ polycistron was increased. RNA blot 50 analysis showed that a larger transcript accumulates in mterf8 than in the wild type. Thus, 51 abnormal transcription and/or RNA processing occur for the psbEFLJ polycistron. Circular 52 reverse transcription polymerase chain reaction and sequence analysis showed that the psbJ 53 transcript terminates 95 nucleotides downstream of the translation stop codon in the wild type, 54 whereas its termination is aberrant in mterf8. Both electrophoresis mobility shift assays and 55 chloroplast chromatin immunoprecipitation analysis showed that mTERF8 specifically binds to 56 the 3′ terminal region of psbJ. Transcription analysis using the in vitro T7 RNA polymerase 57 system showed that mTERF8 terminates psbJ transcription. Together, these results suggest that 58 mTERF8 is specifically involved in the transcription termination of the chloroplast gene psbJ. 59

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INTRDUCTION 61 Plastids in plant cells originated from a single endosymbiotic event, in which the ancestor of the 62 plant lineage engulfed a green photosynthetic cyanobacterium more than one billion years ago. This 63 progenitor retained a small-scale genome during plant evolution (Raven and Allen, 2003; Timmis 64 et al., 2004; Yagi and Shiina, 2012). Although plastid genomes of land plants contain only 120–65 135 genes (López-Juez, 2007; http://megasun.bch.umontreal.ca/ogmp), their products are essential 66 for chloroplast development and plant survival. Transcription of plastid genomes is mediated by at 67 least two different types of RNA polymerases: a multi-subunit Plastid-Encoded RNA Polymerase 68 (PEP) and a single subunit Nucleus-Encoded RNA Polymerase (NEP) (Lerbs-Mache, 2011; Börner 69 et al., 2015). PEP is the major RNA polymerase in chloroplasts. It consists of the plastid-encoded 70 core subunits and of numerous nucleus-encoded accessory proteins (Hajdukiewicz et al., 1997, 71 Lopez-Juez and Pyke 2005; Schweer et al., 2010). The core components of the transcriptional 72 machinery share common features with those of prokaryotic organisms (Liere et al., 2011). 73 Numerous nucleus-encoded accessory proteins have been identified from the PEP RNA polymerase 74 complex in plants (Pfannschmidt and Link, 1994; Pfalz et al., 2006; Schweer et al., 2010; Pfalz and 75 Pfannschmidt, 2013; Yu et al., 2014). Thus, the chloroplast transcriptional machinery is a unique 76 hybrid transcription system, which is composed of the remnant prokaryotic subunits as well as of 77 nucleus-encoded eukaryotic components, and is therefore much more complex in plants than in 78 bacteria. 79 80 The mitochondrial transcription terminator factor (mTERF) family is characterized by tandem 81 repetition of a 30-amino acid motif called ‘mTERF’. So far, four sub-families have been identified 82 in vertebrates (Linder et al., 2005). Structure analysis suggested that mTERF proteins have evolved 83 to bind nucleic acids (Byrnes and Garcia-Diaz, 2011). Human mTERF1 was the first identified 84 member of this protein family. It was proposed to promote transcription termination of human 85 mitochondrial genes (Kruse et al, 1989), which gave rise to the mTERF nomenclature. Recent 86 investigations suggest that human mTERF1 is also involved in the termination of antisense 87 transcripts which would prevent light-strand transcripts from proceeding around the mitochondrial 88 DNA (mtDNA) circle and avoid transcriptional interference at the light-strand promoter (Terzioglu 89 et al., 2013). MOC1, an mTERF-like protein in Chlamydomonas reinhardtii, binds specifically to a 90 sequence within the mitochondrial rRNA-coding module S3 to terminate the antisense transcript as 91 observed for human mTERF1 in vivo (Wobbe and Nixon, 2013). The mTERF family has been 92 characterized in terrestrial plants, but it is absent in fungi and prokaryotes. In Arabidopsis thaliana, 93 35 genes encode mTERF members, 12 of which are localized in chloroplasts (Linder et al., 2005; 94 Babiychuk et al., 2011). Arabidopsis mutants defective in the mTERF proteins SOLDAT10 95 (SINGLET OXYGEN-LINKED DEATH ACTIVATOR10)/mTERF1 (Meskauskiene et al., 2009) 96 and BELAYA SMERT (BSM)/RUGOSA2 (RUG2)/mTERF4 (Babiychuk et al., 2011; Quesada et 97 al., 2011; Sun et al., 2016) display arrested development of the embryo, and the knock-out of 98



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mTERF6 (Romani et al., 2015; Zhang et al., 2018) has serious defects in chloroplast development. 99 mTERFs are also involved in responses to abiotic stress (Meskauskiene et al., 2009; Kim et al., 100 2012; Quesada, 2016; Xu et al., 2017). However, the molecular functions of mTERFs in plants 101 remains poorly understood. In maize (Zea mays), Zm-mTERF4 is involved in group-II intron 102 splicing, and this function in chloroplast RNA splicing might be conserved in its putative ortholog 103 BSM/RUG2 in Arabidopsis (Hammani and Barkan, 2014). Similar to the role of mTERF4 in 104 splicing in chloroplasts, mTERF15 was shown to be involved in the processing of nad2 pre-RNA 105 in Arabidopsis mitochondria (Hsu et al., 2014). mTERF6 interacts specifically with a sequence 106 within the chloroplast isoleucine transfer RNA gene (trnI.2) located in the rRNA operon, and is 107 required for the maturation of this RNA. In vitro, recombinant mTERF6 binds to its plastid DNA 108 target site and can terminate transcription (Romani et al., 2015). mTERF6 was also shown to be 109 involved in the transcription termination of rpoA encoding one core subunit of PEP (Zhang et al., 110 2018). mTERF5 was recently characterized as a transcriptional pausing factor to positively 111 regulate transcription of chloroplast psbEFLJ (Ding et al., 2019). The molecular functions of the 112 other mTERFs in plants remain to be elucidated. 113 114 Transcription termination includes arrest of RNA biosynthesis, release of the transcript, and 115 dissociation of the RNA polymerase from the DNA template. Proper transcription termination may 116 assist in avoiding interference with transcription of downstream genes and preventing formation of 117 antisense RNAs that can interfere with normal pre-RNA production. Also, it ensures that a pool of 118 RNA polymerases is available for recycling (Greger et al., 2000; Richard and Manley, 2009). 119 Several regulatory mechanisms for transcription termination have been elucidated in bacteria and 120 eukaryotes. In prokaryotes, two different processes exist, namely Rho-independent and 121 Rho-dependent transcription termination. In the former, the termination signal is mainly located on 122 the mRNA that forms a GC-rich stem loop followed by a string of Us, whereas the latter relies on 123 both mRNA elements and trans-acting factors (Richardson, 2003). In eukaryotes, the mechanisms 124 for terminating transcription are very complex. RNA polymerase II transcription termination is 125 associated with 3′-end processing of the pre-mRNA (Birse et al., 1998; Hirose and Manley 2000; 126 Yonaha and Proudfoot, 2000; Proudfoot, 2004; Buratowski, 2005), and an intact polyadenylation 127 signal is required for transcription termination of protein-coding genes in human and yeast cells 128 (Whitelaw and Proudfoot, 1986; Logan et al. 1987; Connelly and Manley, 1988). By comparison, 129 termination with RNA polymerases III and I is simpler. RNA polymerase III terminates 130 transcription at T-rich sequences located near the mature RNA 3′-end together with a few auxiliary 131 factors (Arimbasseri et al., 2013), whereas RNA polymerase I latter terminates at a major 132 terminator located downstream from the rRNA precursor sequence and requires terminator 133 recognition by specific factors (Kuhn and Grummt, 1989; Lang and Reeder, 1995). 134 135 Plastids are specific organelles in plant cells, and the mechanisms of their transcription 136



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termination remain obscure. In earlier studies, biochemical assays showed that termination of 137 chloroplast transcription occurs at intrinsic bacterial-like terminators in vitro (Chen and Orozco, 138 1988). Plastid RNA polymerase is likely to recognize bacterial terminator sequences with specific 139 features under in vivo conditions. Chi et al. (2014) found that a RNA binding protein RHON1 140 participates in transcriptional termination of rbcL (encoding the large subunit of 141 ribulose-1,5-bisphosphate carboxylase/oxygenase) in Arabidopsis thaliana. RHON1 can bind to 142 the mRNA as well as to single-stranded DNA of rbcL, displays RNA-dependent ATPase activity, 143 and terminates transcription of rbcL in vitro (Chi et al., 2014). RHON1 terminates rbcL 144 transcription through an ATP-driven mechanism similar to that of Rho of Escherichia coli. 145 146 pTAC15 is one component of the plastid transcriptionally active complex (Pfalz et al., 2006). It 147 was characterized as a member of mTERF family, named mTERF8 (Babiychuk et al., 2011) in 148 Arabidopsis thaliana. Our results show that mTERF8 is localized in chloroplast nucleoids, and 149 co-fractionates with the core RNA polymerase subunit RpoB. An mterf8 knockout line is affected 150 in plastid gene expression, and displays impaired efficiency of photosystem II electron flow. 151 mTERF8 binds to the DNA of psbJ. The recombinant protein MBP:mTERF8 displays 152 transcription termination activity for psbJ. These data suggest that mTERF8 is involved in 153 transcription termination by specifically binding to the 3′-terminal end of the chloroplast gene 154 psbJ in Arabidopsis. 155 156 157



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RESULTS 158 mTERF8 is Associated with the PEP complex in Chloroplasts 159 pTAC15 was initially identified in the chloroplast PEP RNA polymerase complex of plants (Pfalz 160 et al., 2006). This protein contains a putative transit peptide of 59 residues at its N-terminus and 161 eight mTERF motifs (PPDB, http://ppdb.tc.cornell.edu/). pTAC15 was, thus, also named mTERF8 162 (Babiychuk et al., 2011). Alignment analysis of the amino acid sequences of the mTERF motifs in 163 mTERF8 with those of other mTERFs revealed the conservation of a proline residue at the 8th 164 position of the motifs (Figure 1A). Basic Local Alignment Search Tool (BLAST) searching 165 revealed that putative ortholog of mTERF8 exist in angiosperms, gymnosperms, and 166 photosynthetic bacteria (Supplementary Figure S1). Available putative ortholog of mTERF8 167 from different species which represent different plant families, including Brassicaceae 168 (XP_013689181.1), Malvaceae (XP_016726590.1, XP_017612337.1), Euphorbiaceae 169 (XP_002515871.2, OAY51230.1), Rosaceae (XP_010482826.1, XP_006347515.1, 170 XP_009361283.1, XP_020412334.1), Leguminosae (XP_003602380.1, KRH64303.1), and 171 Solanaceae (XP_004235022.1), were used to construct a phylogenetic tree. This tree revealed that 172 the proteins in the same family form distinct sub-clades (Figure 1B), which is consistent with 173 their evolutionary relationship. 174 175 Babiychuk et al. (2011) have determined that mTERF8 is targeted to chloroplasts through analysis 176 of GFP fluorescence patterns resulting from mTERF8:GFP expression. In this study, we produced 177 a construct consisting of the full-length mTERF8 coding sequence fused to GFP, and transiently 178 expressed this fusion in tobacco leaf mesophyll cells. Fluorescence microscopy revealed that the 179 fluorescence signal from mTERF8:eGFP co-localized with chlorophyll autofluorescence (Figure 180 1C), which confirms its chloroplast localization. GFP fluorescence displayed a punctate pattern in 181 chloroplasts (Figure 1C). We further produced genomic complementation mTERF8:MYC 182 transgenic plants (see Material and Methods) to investigate mTERF8 sub-cellular localization 183 (Figure 1D). Featured proteins of each compartment, such as the light-harvesting complex of PSII 184 (Lhcb5) in the thylakoid and the Rubisco large subunit (RbcL) in the stroma, were examined by 185 immunoblotting. As shown in Figure 1D, as expected, Lhcb5 was mainly present in the thylakoids, 186 whereas RbcL was mainly present in the chloroplast stroma. Immunoblot analysis was performed 187 using an anti-MYC antibody on chloroplast fractions isolated from the transgenic plants. The 188 mTERF8:MYC fusion protein was mainly detected in the thylakoid membrane fraction. mTERF8 189 was originally identified in the plastid transcription activation complex in Arabidopsis thaliana 190 (Pfalz et al., 2006). However, it was not included in the twelve PEP-associated proteins (PAPs) 191 that are tightly associated with the PEP complex (Steiner et al., 2011; Pfalz and Pfannschmidt, 192 2013). To further examine the association of mTERF8 with the PEP complex, thylakoid membrane 193 proteins from 3-week-old mTERF8:MYC transgenic seedlings were first fractionated by blue 194 native (BN) gel electrophoresis followed by SDS-PAGE in the second dimension. Immunoblotting 195



7revealed that mTERF8:MYC co-migrates with RpoB, a core component of PEP, in a ~670 kDa 196



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complex. To confirm that mTERF8 is specifically associated with the PEP complex, we used ATP 197 synthase as a negative control. Immunoblotting with an antibody against AtpA, a subunit of ATP 198 synthase, showed that this complex migrates at 440 kDa where there is no signal corresponding to 199 mTERF8:MYC (Figure 1E). Taken together these data indicate that mTERF8 is associated with 200 the PEP complex. 201 202 Electron Transfer Rate is Slightly Impaired in the Knockout Mutant of mTERF8 203 To investigate the function of the mTERF8 gene, we obtained one homozygous T-DNA insertion 204 line (SALK_021988) from the Arabidopsis Bioresource Center (ABRC, 205 http://www.arabidopsis.org). The T-DNA is inserted in the first exon (position 17964170 in 206 chromosome 5) in the SALK_021988 line (Figure 2A). The homozygous plants displayed a 207 wild-type phenotype under standard growth conditions (Figure 2B). RT-PCR analysis showed that 208 mTERF8 transcripts are not present in the homozygous lines, but are present in the wild type 209 (Figure 2C). Thus, the mTERF8 gene in the T-DNA homozygous line is not expressed, and this 210 line was named mterf8. To test whether the loss of mTERF8 affects photosynthetic activity, we 211 investigated chlorophyll a fluorescence transients under growth light conditions (90 μmol 212 photons·m−2·s−1). The ratio (Fv/Fm) of variable fluorescence (Fv = Fm - Fo; where Fv is variable 213 fluorescence, Fm is maximum fluorescence, and Fo is minimal fluorescence) to maximum 214 fluorescence in the mterf8 mutant (Fv/Fm =0.777± 0.016) was similar to that in wild type (Fv/Fm 215 =0.779 ± 0.007). This indicated the presence of an active PSII in the mterf8 mutant. We also 216 measured the light intensity dependence of three chlorophyll fluorescence parameters: 217 light-response curves of non-photochemical quenching (NPQ), PSII quantum yield, photochemical 218 quenching, and electron transport rate. Non-photochemical quenching (NPQ), PSII quantum yield, 219 photochemical quenching, and electron transport rate were slightly lower in the mterf8 mutants 220 than in the wild type (Figure 2D). These data indicate a slightly decreased efficiency of 221 photosynthetic electron flow in the mterf8 mutant. We then investigated whether the absence of 222 mTERF8 affects the accumulation of photosynthetic complexes. Thylakoid membranes were 223 solubilized with 2% DM and membrane protein complexes were separated by BN-PAGE. Our 224 results show that the amount of PSII super-complexes is slightly decreased in the mterf8 mutant, 225 compared with wild type (Supplemental Figure S2 A and B). Accumulation of the PSII proteins 226 PsbA and PsbB was slightly reduced (Supplemental Figure S2C). The other photosynthetic 227 proteins PsaA, PsaD, AtpA, AtpC, CytF, and NdhO accumulated to a similar level as in wild type. 228 229 To further confirm that the loss of mTERF8 causes the observed mterf8 phenotype, the AT5G54180 230 genomic sequence, including its 1500-bp upstream and 232-bp downstream regions, was introduced 231 into homozygous mterf8 plants by Agrobacterium tumefaciens-mediated transformation (Clough 232 and Bent, 1998). Five out of 41 independent T1 transgenic plants were identified as complemented 233 lines (Figure 2B). RT-PCR analysis showed that the transcripts of mTERF8 are present in the 234



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complemented lines (Figure 2B). Furthermore, analysis of induction of NPQ and chlorophyll 235 fluorescence kinetics showed that the complemented lines exhibit similar responses as the wild 236



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type (Supplemental Figure S3). Taken together, these results show that the loss of mTERF8 237 slightly affects the electron transfer rate under normal growth conditions. 238 239 Chloroplast Gene Expression Profile in the mterf8 Mutant 240 Since mTERF8 is associated with the PEP complex, we analyzed whether the loss of mTERF8 241 affects the expression profile of plastid genes through reverse transcription quantitative PCR 242 (RT-qPCR) analysis. Our results show that the expression profile of some plastid genes is aberrant 243 in the mterf8 mutant (Figure 3A and Supplemental Figure S4). The expression levels of typical 244 PEP-transcribed genes, except rbcL, are reduced. For example, the amounts of the transcripts of 245 two PEP-transcribed genes psbA and psbB, were approximately 80% of the wild-type level, 246 whereas the transcript abundance of another PEP-transcribed gene rbcL, was approximately 1.1 247 fold compared to wild type (Figure 3A). The abundance of transcripts of NEP-dependent plastid 248 genes, for example, accD and rpoA, was slightly increased (Figure 3A).The expression of genes 249 transcribed by both NEP and PEP including atpB, atpE, and 16S rRNA, were approximately 60–80% 250 of the wild-type level (Supplemental Figure S4). Among these plastid transcripts, the most 251 pronounced change was observed for psbJ in the mutant with a 2.4-fold increase compared to wild 252 type (Figure 3A). In Arabidopsis chloroplasts, the psbE, psbF, psbL, and psbJ genes are part of a 253 large polycistron (Figure 3B). RT-qPCR analysis showed that the transcripts of psbE, psbF, psbL, 254 and psbJ were increased 1.1-, 1.4-, 1.4-, and 2.4-fold compared to wild type, respectively (Figure 255 3B and Supplemental Figure S4). We also checked the transcript of the psbEFLJ polycistron by 256 RNA blot analysis with a probe spanning the three transcripts. A specific transcript could be 257 observed in the wild type as previously reported (Jin et al., 2018). However, an extra larger 258 transcript was observed in the mterf8 mutant. These data suggest that read-through transcription of 259 the psbJ gene cluster and/or changes in RNA processing occur in the mterf8 mutant (Figure 3C). 260 It is not clear whether transcription of these genes is performed by PEP polymerase. 261 Spectinomycin is an inhibitor of plastid protein synthesis (Moazed and Noller, 1987). Since the 262 core subunits of PEP are synthesized on plastid ribosomes, growth of Arabidopsis on 263 spectinomycin-containing medium should lead to PEP-deficiency (Zubko and Day, 1998; 264 Swiatecka-Hagenbruch et al., 2007; Chi et al., 2014). Accordingly, we analyzed the transcripts of 265 psbE and psbJ in wild-type plants after spectinomycin treatment and found that their levels were 266 about 20% of those in plants without treatment (Figure 3D). These results indicate that the 267 psbEFLJ polycistron is transcribed by PEP polymerase. Taken together, our data show that 268 aberrant expression of plastid genes occurs in the mterf8 mutant, especially for the psbJ gene. 269 270 psbJ Transcription Termination is Defective in the mterf8 Mutant 271 mTERF8 shows structural similarity with human mTERF1 that acts as a transcription termination 272 factor (Supplemental Figure S5, Zhang et al., 2008; Byrnes and Garcia-Diaz, 2011). We analyzed 273 the potential transcription read-through in the mutant with specific primers as described (Zhang et 274



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al., 2018). Transcripts from the spacer regions of the ycf9, rbcL, psbA, rps14, ycf5, and psbJ genes 275 were only slightly changed for five of these genes (ycf9, psbA, rpoA, ycf5, and rbcL) in mterf8 276 relative to the wild type (Figure 4A). By contrast, the transcripts from the spacer regions of the 277



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psbJ gene in the mterf8 mutant were much higher than that in wild type (Figure 4A). This 278 suggests a potential transcription read-through for the psbJ gene in mterf8. Because the exact 279 transcription termination site of psbJ gene is unknown, we designed five pairs of primers for 280 different regions of psbJ (Figure 4B) to analyze its transcription termination. Our results showed 281 that the relative levels of the detected transcripts in the mterf8 mutant are close to those of the wild 282 type when three primer sets (primers 1–3) located inside the coding region or within the 3′ 283 termination region were used (Figure 4C). However, transcript levels of psbJ in the mterf8 mutant 284 were about 30–50-fold higher than in wild type when the two primer sets (primers 4 and primers 5) 285 located downstream of the psbJ gene were used (Figure 4B). These data indicate that transcription 286 of the psbJ polycistron terminates in the region between the primer set 3 and 4, and its 287



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transcription termination is defective in the mterf8 mutant. 288 289 We further identified the termination site of the psbJ gene through a circular RT-PCR (cRT-PCR) 290 analysis. cRT-PCR has been applied to identify the 5′ and 3′ extremities of organelle transcripts 291 (Perrin et al., 2004; Barkan, 2011). Total RNA or polyadenylated RNA are circularized with T4 292 RNA ligase and reverse transcribed with gene-specific primers. We used cRT-PCR to analyze 293 transcription termination of psbA in wild type and the mterf8 mutant to test the reliability of the 294 method for transcription termination analysis. Transcription termination of psbA was not changed 295 in mterf8 (Supplemental Figure S6A). Further sequence analysis showed that the psbA transcripts 296 from wild type and the mterf8 mutant terminated at residue 90 or 91 downstream of the psbA stop 297 codon (Supplemental Figure S6B and C). This indicated that cRT-PCR can reliably determine 298 transcription termination sites. Subsequently, we analyzed the psbJ termination site in both wild 299 type and the mterf8 mutant through cRT-PCR with the corresponding primers (Figure 4E). Our 300 results showed the 5′–3′-end ligation products were different between wild-type and mterf8 plants 301 (Figure 4B). We further determined the termination sites of psbJ through sequence analysis. In the 302 15 sequenced clones containing the psbJ cRT-PCR product from wild type, the termination site of 303 the psbJ transcript is located at residue 94 or 96 downstream of its stop codon (Figure 4C and D). 304 By contrast, among the 16 sequenced clones containing the corresponding product from mterf8, 7 305 clones contain psbJ transcripts with the same ends as in wild type (Figure 4C and D). The 306 remaining clones were variants, with psbJ transcript termination sites at nucleotides 3, 56, 59, 137, 307 229, 237, or 510 downstream of its stop codon (Figure 4D). These results indicate that termination 308 of psbJ transcripts is altered in the mterf8 mutant. 309 310 mTERF8 Binds to the Chloroplast psbJ Gene 311 mTERF8 is structurally analogous to human mTERF1 that binds to specific organelle DNA 312 sequences (Terzioglu et al., 2013). Thus, we analyzed whether the mTERF8 protein binds 313 specifically to the psbJ gene. The purified recombinant MBP:mTERF8 protein was incubated with 314 a double stranded (ds) DNA fragment containing the 3′ terminal region of psbJ to perform 315 electrophoretic mobility-shift assays (EMSA). A shifted band that migrated slower than the free 316 DNA probe was detected. The signal of the retarded band became weaker upon addition of 317 increasing amounts of the corresponding unlabeled competitor probe. By contrast, MBP alone did 318 not bind the DNA probe (probe 2 in Figure 5A). To further examine the specificity of binding of 319 mTERF8 to the abovementioned probe, we also test the terminal region of another chloroplast gene, 320 psbA, as a competitor in the EMSA (Figure 5A). This psbA probe did not compete with the psbJ 321 terminal region indicating that the recombinant MBP:mTERF8 protein binds specifically to the 322 psbJ probe. Subsequently, we further determined which region of the psbJ 3′-end is bound by the 323 recombinant MBP:mTERF8 protein by testing probes that cover different parts of this region. Our 324 EMSA results show that MBP:mTERF8 binds to the 100-bp fragment downstream of the stop 325



14codon of psbJ (probe 2 in Figure 5A), but not to the 100-bp fragment that is further downstream 326



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(probe 3 in Figure 5A). In the rice (Oryza sativa) plastid genome, the psbE, psbF, psbL, and psbJ 327 genes are also arranged in a large polycistron, similar to that of Arabidopsis. We checked whether 328 mTERF8 is able to bind to the corresponding region of the rice psbJ terminal region. Our results 329 indicated that this is not the case (Supplemental Figure S7). Sequence alignments showed that 330 the psbJ terminal region of maize and rice is conserved, but it is different in Arabidopsis 331 (Supplemental Figure S9). To further determine the binding motif of mTERF8, we split the 332 fragment (probe 2 in Figure 5A) into two fragments, a 55-bp fragment (probe 4) and a 39-bp 333 fragment (probe 5) to perform an EMSA (Figure 5A). MBP:mTERF8 is able to bind to the 39-bp 334 fragment but not to the 55-bp fragment (Figure 5A). Based on the above data, we focused on the 335 divergent nucleotides in the 39-bp fragment among Arabidopsis, maize, and rice and prepared the 336 probe 6 with the double tandem non-conserved sequence “TGtcTgattCGagggGG” (lowercase 337 letters represent the non-conserved nucleotides) (Supplemental Figure S9). EMSA shows that 338 MBP:mTERF8 is able to bind to this probe. This data suggest that mTERF8 binds the psbJ 3′ 339 terminal region through this motif. We further tested whether mTERF8 binds to other regions of 340 the polycistron. Three probes corresponding to the coding region of psbJ, psbL, and the intergenic 341 region of psbJ-psbL were designed (Supplemental Figure S7). EMSA showed that the mTERF8 342 protein did not bind to any of these probes. This confirms that mTERF8 binds preferentially to the 343 psbJ 3′ terminal region. We further examined whether MBP:mTERF8 binds to the terminal region 344 of another plastid gene, psbA. The psbA probe corresponding to its 3′ terminal region was 345 incubated with the MBP:mTERF8. However, no binding was detected (Supplemental Figure S7), 346 which is in agreement with the inability of psbA to compete with the binding of MBP-mTERF8 to 347 psbJ (Figure 5A). Taken together, these data indicate that MBP:mTERF8 binds to the psbJ gene 348 within the 39-bp dsDNA fragment of the psbJ terminal region. 349 350 To confirm the binding of mTERF8 to the terminal region of psbJ, we further performed a 351 co-immunoprecipitation ChIP analysis with anti-MYC antibody using extracts from the 352 mTERF8:MYC complemented plants. The immunoprecipitated DNA was analyzed by RT-qPCR. 353 Chloroplast genes whose expression is PEP-dependent such as psbA, rbcL, and psbJ were enriched 354 in these assays but not rpoA that is not transcribed by PEP (Figure 5B). The enrichment in these 355 PEP-dependent genes is probably due to the association of mTERF8 with the PEP complex 356 (Figure 2E). Among these PEP-dependent enriched genes, the highest enrichment was found for 357 the coding region of psbJ (Figure 5B). We also examined the distribution of mTERF8 along the 358 psbEFLJ polycistron. Here also, the association with mTERF8 with psbJ was the highest (Figure 359 5C). Additionally, we used four pairs of primers spanning different regions of psbJ (Figure 5D). 360 As expected, mTERF8 was enriched with each of the four different segments, and the peak 361 association occurred with fragments of the 3′ terminal part of psbJ (Figure 5E). Taken together, 362 these data show that mTERF8 binds preferentially near the psbJ termination site. 363 364



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mTERF8 can Terminate Transcription of the psbJ Gene in vitro 365 We further investigated whether mTERF8 has transcription termination activity. For this purpose, 366 an assay for transcription termination activity was performed (Supplemental Figure S8) 367 following previous reports (Prieto-Martín et al., 2004; Romani et al., 2015). We cloned the 100-bp 368 genomic psbJ fragment containing the binding site of mTERF8 into the pGEM vector. After 369 linearization of the plasmid, the construct was transcribed with T7 RNA polymerase in the 370 presence of recombinant MBP:mTERF8. A run-off long transcript (Full-length) was generated 371 with the T7 RNA polymerase. When recombinant MBP:mTERF8 was added to the reaction, an 372 additional shorter transcript corresponding to the psbJ transcript was generated (Figure 6A). The 373 abundance of this transcript increased gradually with increasing amounts of MBP:mTERF8 in the 374 reaction (Figure 6A). We also analyzed whether the recombinant MBP:mTERF8 has termination 375 activity for other chloroplast genes. We cloned five chloroplast genes (psbA, rbcL, psaJ, petD, and 376 petA) including their down-stream sequences into the pGEM plasmid. They were linearized as 377 indicated above, and transcribed with T7 RNA polymerase in the presence of MBP:mTERF8 as 378 described above. Only a longer run-off transcript was observed for each gene (Figure 6B-F). 379 These data suggest that mTERF8 acts specifically on the 3′ terminal region of psbJ. 380 381 382



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DISCUSSION 383 mTERF8 is Associated with the PEP Complex and is Able to Terminate Transcription 384 PEP polymerase is a multi-subunit bacterial-type enzyme with plastid-encoded core subunits 385 (α2ββ´β´´) and numerous nucleus-encoded accessory proteins (Schweer et al., 2010). Similar to 386 the case of bacterial RNA polymerase, the nucleus-encoded sigma factors confer promoter 387 specificity on PEP, whereas the PEP core enzyme is responsible for transcription elongation. The 388 accessory proteins include the elongation factor EF-Tu, ribosomal proteins, proteins with 389 DNA/RNA binding domains, such as the PPR, SMR, SAP, OB fold, S1, KOW, NGN, mTERF, or 390 with single-stranded DNA (ssDNA) binding motifs (Pfalz et al., 2006; Yu et al., 2014). These 391 proteins are involved in transcription and post-transcriptional processes (Yu et al., 2014). Recent 392 studies on plant mTERF genes have revealed that they are involved in organelle gene expression 393 (Hammani and Barkan, 2014; Hsu et al., 2014; Romani et al., 2015). mTERF8, a member of the 394 mTERF family, was initially named pTAC15 because it was first isolated from the chloroplast PEP 395 RNA polymerase complex in plants (Pfalz et al., 2006). Our results confirm that mTERF8 is 396 localized in chloroplasts (Figure 1B), consistent with previous proteomics data (Pfalz et al., 2006) 397 and fluorescence microscopy observations (Babiychuk et al., 2011). The fluorescence of the 398 mTERF8:eGFP displayed a punctate pattern (Figure 1B), as found for PEP-associated proteins 399



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such as pTAC3 (Steiner et al., 2011; Yagi et al., 2012), FLN1 (Arsova et al., 2010; Steiner et al., 400 2011), and FSD3 (Myouga et al., 2008; Steiner et al., 2011). The plastid transcriptional apparatus 401 in chloroplast nucleoids has been proposed to be associated with the thylakoid membranes in 402 mature chloroplasts (Sato, 2001; Sato et al., 2003; Karcher et al., 2009; Schweer et al., 2010; 403 Jeong et al., 2003). Our chloroplast fractionation analysis indicating that most of mTERF8 is 404 associated with thylakoids is in agreement with this proposal (Figure 2). Our two-dimensional 405 BN-SDS-PAGE electrophoresis and immunoblotting analysis also shows that mTERF8:MYC is 406 present in a super-molecular complex with a molecular mass of 670 kDa, which co-migrates with 407 RpoB(Zhong et al., 2013), one core subunit of the PEP complex (Figure 2). Combined, these data 408 indicate that mTERF8/pTAC15 is a component of the PEP complex, which is associated with 409 thylakoids. 410 411 Transcription termination is the final step in RNA synthesis, wherein the nascent transcript is 412 released from RNA polymerase. Efficient and timely transcription termination ensures proper gene 413 expression. In human mitochondria, mTERF1, a founder of the mTERF family, is able to bind the 414 organelle genome and is involved in promoting termination of mitochondrial light-strand antisense 415 transcription (Terzioglu et al., 2013). In the unicellular green alga Chlamydomonas reinhardtii, the 416 mTERF protein MOC1 was reported to terminate mitochondrial DNA transcription like human 417 mTERF1. MOC1 binds specifically to an octanucleotide sequence within the mitochondrial rRNA 418 coding module S3, and loss of MOC1 increases read-through transcription at the S3-binding site, 419 thereby causing elevated amounts of antisense RNA in the mutant stm6 (Wobbe and Nixon, 2013). 420 In plants, there are over 30 members of the mTERF family, which are mainly localized in 421 chloroplasts and mitochondria (Babiychuk et al., 2011; Robles et al., 2012; Zhao et al., 2014). The 422 available evidence shows that plant mTERF proteins are involved in post-transcriptional processes, 423 such as organelle RNA splicing (Hammani and Barkan, 2014; Hsu et al., 2014) and chloroplast 424 isoleucine transfer RNA maturation (Romani et al., 2015). In vitro assays show that recombinant 425 mTERF6 displays transcription termination activity (Romani et al., 2015). In agreement with this 426 finding, mTERF6 was recently suggested be involved in transcription termination of rpoA (Zhang 427 et al., 2018). In this study, we report that mTERF8 shares structural features with human mTERF1 428 (Supplemental Figure S6). Genetic analysis demonstrates that mTERF8 is involved in 429 transcription termination of psbJ (Figure 3 and 5). Additionally, recombinant mTERF8 was able 430 to terminate psbJ transcription in vitro (Figure 6). Taken together, these results indicate that 431 mTERF8, a homologue of human mitochondrial mTERF1, is likely to be involved in transcription 432 termination of psbJ. Although we cannot fully rule out that the loss of mTERF8 promotes 433 initiation of transcription within the terminal region of psbJ, this possibility seems unlikely. 434 435 The psbEFLJ operon encodes low-molecular-weight proteins of photosystem II. In tobacco, ΔpsbJ 436 plants grew photoautotrophically, and displayed impaired PSII activity in young leaves. 437



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Photosynthetic electron flow was decreased in the absence of PsbJ protein (Regel et al., 2001; 438 Ohad et al., 2004) suggesting a role of PsbJ protein for optimal electron flow. The mterf8 mutant 439 displayed aberrant transcription termination of psbJ (Figure 3 and 4). Nevertheless, this mutant 440 grows photoautotrophically similar to wild type (Figure 2). Measurements of several 441 photosynthetic parameters indicates that photosynthetic electron flow is only slightly impaired in 442 mterf8 (Figure 2). Consistent with these observations, accumulation of the PSII complexes is only 443 weakly reduced in the mutant (Supplemental Figure S5). 444 445 mTERF8 Mediates Preferential Transcription Termination of the Chloroplast Gene psbJ in 446 Arabidopsis 447 The chloroplast transcription machinery is a unique chimeric system with remnant prokaryotic 448 components and nucleus-encoded eukaryotic components (Yagi et al., 2012). As for the bacterial 449 RNA polymerase, the PEP complex in plants recognizes chloroplast promoters through sigma 450 factors. The association of PEP with sigma factors is enriched at promoter-proximal regions, and 451 declines gradually along the transcribed region, similar to the distribution patterns in bacteria. This 452 suggests that PEP-dependent transcription initiation, elongation and termination steps are 453 regulated by mechanisms similar to those of bacteria (Yagi et al., 2011, 2012). A Rho-like factor, 454 Rhon1, is involved in transcription termination of rbcL in Arabidopsis chloroplasts through an 455 ATP-driven mechanism similar to E. coli Rho factor (Chi et al., 2014). In this work, we found that 456 the eukaryotic-type plastid nucleoid protein mTERF8, which is a component of the PEP complex, 457 can directly bind to the termination region of the psbJ gene as a termination factor (Figure 5). 458 This region is GC rich and is able to form a stem-loop structure, similar to the terminators of 459 Rho-independent transcription termination in E. coli. Thus, it is likely that mTERF8-mediated 460 transcription termination of psbJ is similar to Rho-independent transcription termination in E. coli. 461 462 PEP is the major RNA polymerase responsible for most plastid gene transcription. The psbA gene 463 is transcribed only by the PEP RNA polymerase in Arabidopsis. Knockout of core members of the 464 PEP complex substantially reduced the abundance of psbA transcripts (Pfalz et al., 2006, 2015; 465 Garcia et al., 2008; Myouga et al., 2008; Arsova et al., 2010; Gao et al., 2011; Yagi et al., 2012; Yu 466 et al., 2013, 2018). Although mTERF8 is associated with the PEP complex (Figure 1) transcription 467 termination of psbA is not affected, although psbA transcript abundance is slightly decreased in 468 mterf8 (Figure 6 and Supplemental Figure S5). These data suggest that mTERF8 is not 469 responsible for psbA transcription termination. Similarly, MBP:mTERF8 does not terminate 470 transcription of other PEP-dependent genes including rbcL, psaJ, petD, and petA (Figure 6). 471 Combined, these data suggest that mTERF8 is not a general terminator for PEP-transcribed plastid 472 genes in Arabidopsis. In a similar way, RHON1 only terminates transcription of rbcL but not of 473 other PEP-dependent genes. As in Arabidopsis, the psbE, psbF, psbL, and psbJ genes are also 474 arranged in a large polycistron in the rice plastid genome. However, the sequences of the psbJ 475



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terminal regions differ between Arabidopsis and rice (Supplemental Figure S8). We found that 476 mTERF8 is not able to bind the rice terminal region of the OspsbJ gene (Supplemental Figure 477 S7), and in vitro analysis showed that the MBP:mTERF8 is not able to terminate OspsbJ 478 transcription. Further analysis revealed that mTERF8 binds to a non-conserved segment of the 479 psbJ terminal sequence region. These data suggest that transcription termination mechanisms, at 480 least in the case of psbJ, have diverged in dicotyledons and monocotyledons. The picture which is 481 emerging from all these studies is that termination of PEP-transcription in chloroplasts is mediated 482 by nucleus-encoded factors that act in a gene-specific manner, at least in the case of psbJ and rbcL. 483 It is noteworthy that several post-transcriptional steps of chloroplast gene expression including 484 RNA turn-over and processing and translation are also modulated by gene-specific factors. Taken 485 together, these results reveal a surprisingly large number of accessory factors involved both in 486 chloroplast transcriptional and post-transcriptional processes. 487 488 Molecular Functions of mTERF Proteins in Plants 489 In mammals, the mTERF family plays important roles in organelle gene expression (Kruse et al., 490 1989; Park et al., 2007; Cámara et al., 2011; Spåhr et al., 2012). However these mTERF proteins 491 do not actually terminate transcription, as their designation suggests, but appear to function in 492 antisense transcription termination and ribosome biogenesis (Kleine, 2012; Kleine and Leister, 493 2015). In Chlamydomonas reinhardtii, MOC1, an mTERF-like protein, can bind to the 494 mitochondrial DNA specifically like human mTERF1 in vivo for the regulation of transcription of 495 the mitochondrial genome (Wobbe and Nixon, 2013). The conserved function shared by mTERF 496 genes in Chlamydomonas reinhardtii and humans probably underlies similar mechanisms for 497 mitochondrial transcription regulation (Wobbe and Nixon, 2013). In land plants, the mTERF 498 family has expanded to about 30 members. The additional mTERF members in plants may 499 account for the complicated regulation of the mitochondrial and chloroplast genomes. Plant 500 mTERF proteins share a conserved mTERF motif and a similar 3D structure with human mTERF 501 proteins (Zhao et al., 2014). So far, molecular functions of only a few mTERF proteins in 502 flowering plants have been examined including organellular splicing (Hammani and Barkan, 2014; 503 Hsu et al., 2014), chloroplast isoleucine tRNA maturation (Romani et al., 2015), and 504 transcriptional pausing (Ding et al., 2019). These mTERF proteins in plants display DNA-binding 505 activity (Romani et al., 2015) and are also able to bind RNA (Hsu et al., 2014). It remains to be 506 seen whether mTERF proteins in plants have similar roles as human mTERFs and MOC1 in 507 Chlamydomonas. The mTERF6 protein shares 25%/46% identity/similarity over a stretch of 194 508 amino acids with human mTERF1 (Romani et al., 2015), whereas the predicted structure of 509 mTERF8 shares similarity with the human mTERF1 (Supplemental Figure S6). Both mTERF8 510 and mTERF6 (Zhang et al., 2018) are involved in transcription termination of chloroplast genes. 511 Consistent with their functions, recombinant mTERF8 (Figure 6) and mTERF6 mediate 512 transcription termination in vitro (Romani et al., 2015). It is possible that plant mTERF proteins 513



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have an evolutionarily conserved function in transcription termination as in mammals. 514 515 MATERIALS AND METHODS 516 Plant Material and Growth Conditions 517 Arabidopsis (Arabidopsis thaliana; ecotype Columbia) plants were grown in soil in a greenhouse 518 under a 16-h/8-h light/dark cycle with a light intensity of 120 µmol photons m-2s-1 at 22°C. The 519 mterf8 mutant (SALK_021988) was obtained from the Arabidopsis Biological Resource Center 520 and identified by PCR using genomic DNA and T-DNA specific primers in combination with 521 gene-specific primers (Alonso et al., 2003). The T-DNA insertion site was determined by 522 sequencing of PCR products. 523 524 Nucleic Acid Isolation, cDNA Synthesis, Reverse Transcription Quantitative PCR (RT-qPCR) 525 Analysis, and RNA Hybridization 526 For DNA extraction, leaf tissue was homogenized in lysis buffer containing 200 mM Tris-HCl, pH 527 7.5, 25 mM NaCl, 25 mM EDTA, and 0.5% (w/v) SDS. After centrifugation, DNA was 528 precipitated from the supernatant with cold isopropyl alcohol. After washing with 70% (v/v) 529 ethanol, the DNA was dissolved in distilled water. For total RNA isolation, frozen tissue was 530 ground in liquid nitrogen, then total RNA isolation was performed with Trizol reagent (Invitrogen, 531 https://www.thermofisher.com/) according to the manufacturer’s instructions. Purification of RNA 532 was performed with QIAGEN RNeasy Mini kit after DNAse I treatment. cDNA synthesis, 533 RT-qPCR analysis, and RNA hybridization were performed as described previously (Yu et al., 534 2013). All qPCR analysis reactions were performed in triplicate on at least two biological 535 replicates (for oligonucleotide information, see Supplemental Table S1 and S2). 536 537 Genomic Complementation and Subcellular Localization Analysis 538 For mterf8 mutant complementation, the 3,141-bp genomic sequence without the stop codon was 539 amplified by KOD plus polymerase from the Columbia wild-type genome with specific primers 540 (Supplemental Table S1) and cloned into the modified pCAMBIA1300 vector in frame with four 541 tandem MYC coding sequences. The construct was transformed into Agrobacterium tumefaciens 542 strain GV3101, and introduced into mterf8 mutant plants by the floral-dip method (Clough and 543 Bent, 1998). Transgenic plants were selected for hygromycin resistance and analyzed using PCR 544 analysis. For the mTERF8:eGFP fluorescence analysis, the full-length coding sequence of the 545 mTERF8 gene was amplified by KOD plus polymerase (TOYOBO, http://www.toyobo.co.jp) with 546 gene-specific primers (Supplemental Table S1).The coding sequence of the mTERF8 gene was 547 subcloned into the modified vector pRIN101eGFP (TOYOBO, http://www.toyobo.co.jp) and to 548 produce a fusion encoding mTERF8:eGFP. The construct was transformed into Agrobacterium 549 tumefaciens strain GV3101, and introduced into Nicotiana tabacum by injection. The green 550 fluorescent protein (GFP) fluorescence was imaged by laser confocal microscope (Zeiss, 551



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Oberkochen, Germany). 552 553 Chlorophyll Fluorescence Analysis 554 Chlorophyll Fluorescence measurements were performed using an IMAGING-PAM fluorimeter or 555 a MINI-PAM portable chlorophyll fluorimeter (Walz, Effeltrich, Germany) as described in Duan et 556 al. (2016). 557 558 Circular RT-PCR 559 For the determination of the psbJ and the psbA transcript ends, circular RT-PCR was performed as 560 described previously (Perrin et al., 2004). 5 µg total RNA was circularized using T4 RNA ligase 561 (New England Biolabs). cDNA spanning the junction of the 5′ and 3′ ligated ends was synthesized 562 with the corresponding psbJ and psbA reverse gene primers, respectively (Supplemental Table 563 S1), using SuperScript II RNaseH reverse transcriptase (Invitrogen). The region of circularized 564 psbJ and psbA containing the junction between the original 5′ and 3′ ends was then amplified by 565 RT-PCR using specific primers (Supplemental Table S1), cloned into pMD19-T vector 566 (TAKARA), and sequenced. 567 568 MBP:mTERF8 Expression in E. coli and Purification 569 The sequence encoding the putative mature mTERF8 was amplified from wild-type cDNA with 570 gene-specific primers (Supplemental Table S1) and the PCR product was cloned into the 571 pMALc5X vector (NEB, http://www.neb.com). E. coli BL21-CodonPlus (DE3)-RIPL cells 572 harboring the MBP:mTERF8 construct were induced with 1 mM IPTG, incubated in a shaker 573 overnight at 18°C, and harvested at 7,000 g for 10 min. Purification of MBP:mTERF8 was 574 performed following the manufacturer’s instruction (NEB, http://www.neb.com). 575 576 Electrophoretic Mobility Shift Assay 577 The interactions between MBP:mTERF8 and the dsDNA were detected using the LightShift 578 Chemiluminescent EMSA kit (Pierce, http://www.pierce.com). Briefly, the target DNA was 579 amplified with gene-specific primers that were biotin-labeled at the 5′ end (Supplemental Table 580 S1) and then incubated with the purified MBP:mTERF8 in the provided binding reaction system. 581 After incubation for 20 min at 25°C, the samples were resolved on a 6% Tris-borate gel in TBE 582 buffer and transferred to a nylon membrane. The biotin end-labeled DNA was detected using a 583 streptavidin-horseradish peroxidase conjugate and chemiluminescent substrate. The images were 584 caught by TANON-5500 Chemiluminescent Imaging System (TANON, China, 585 http://www.bio-tanon.com.cn). 586 587 Chloroplast Chromatin Immunoprecipitation 588 CpChIP assay was performed following the protocol described in Yagi et al. (2012). One gram of 589



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6-day-old transgenic mTERF8:MYC Arabidopsis seedlings was used for CpChIP assays with 590 MYC antibody (Millipore, http://www.merckmillipore.com/). 591 592 Transcription Termination Assay in vitro 593 The sequences of the intact psbJ, rbcL, psaJ, petD, and petA genes were amplified from the 594 wild-type genome (for oligonucleotide information, see Supplemental Table S1) and cloned 595 individually into the pGEM-T easy vector (Promega, http://www.promega.org). In vitro 596 transcription was performed in 20-µL reactions containing 100 ng of each vector; 1 µM mTERF8; 597 ATP, CTP, UTP, and GTP (0.5 mM each); 20 units of T7 RNA polymerase (Fermentas); 4 µL of 598 5× transcription buffer; and 20 units of RNase Inhibitor (Fermentas). Reactions were incubated for 599 1 h at 25°C, and the transcripts were subjected to 2% agarose gel electrophoresis. 600 601 Chloroplast Subfractionation, Immunoblotting, SDS-PAGE, and BN-PAGE Analyses 602 Two to three-week-old seedlings were homogenized in ice-cold buffer I (0.33 M sorbitol, 0.02 M 603 Tricine/KOH pH 8.4, 5 mM EGTA pH 8.35, 5 mM EDTA pH 8.0, 10 mM NaHCO3). The 604 homogenate was successively filtered through a double layer of Miracloth then 100- and 40-µm 605 sieves. The filtered solution was centrifuged in a swing-out rotor at 2000 g for 5 min at 4℃. Intact 606 chloroplasts were further resuspended in buffer II (0.33 M sorbitol, 5 mM MgCl2, 2.5 M EDTA pH 607 8.0, 20 mM HEPES/KOH pH 7.6). Thylakoid membranes and stromal proteins were prepared 608 from isolated intact chloroplasts. The intact chloroplasts were resuspended in buffer III (5 mM 609 MgCl2-6H2O, 25 M EDTA pH 8.0, 20 mM HEPES/KOH pH 7.6). After centrifugation at 4°C, the 610 supernatant was used as stroma and the sediment as thylakoid fraction. Total protein preparation 611 and immunoblot analyses were performed as described previously (Yu et al., 2013). BN-PAGE 612 analysis was performed as described previously (Peng et al., 2006; Zhang et al., 2018). One gram 613 of 2–3-week-old seedlings was homogenized in ice-cold HMSN buffer (0.4 M Sucrose, 10 mM 614 NaCl, 5 mM MgCl2-6H2O, 10 mM HEPES) and then filtered through multi-layer micro-cloth. The 615 isolated thylakoid pellets were suspended in resuspension buffer (25 mM Bis-Tris-HCl, pH 7.0, 1% 616 n-Dodecyl b-D-maltoside [w/v], and 20% glycerol [w/v]) at 1.0 mg chlorophyll/mL. After 617 incubation at 4°C for 5 min and centrifugation at 12,000 g for 10 min, one-tenth volume of 618 loading buffer (100 mM Bis-Tris-HCl, pH 7.0, 0.5 M 6-amino-n-caproic acid, 5% Serva blue G 619 [w/v], and 30% glycerol [w/v]) was added to the supernatant and applied to 0.75-mm 4–12% 620 acrylamide gradient gels in a Tannon vertical electrophoresis at 4℃. For two-dimensional analysis, 621 excised BN-PAGE lanes were soaked in SDS sample buffer for 30 min and layered onto 1-mm 10% 622 SDS polyacrylamide gels containing 6 M urea. After electrophoresis, the proteins were transferred 623 to nitrocellulose membranes, probed with antibodies against MYC (cwbio, 624 http://www.cwbiotech.com/) and RpoB, and visualized by enhanced chemiluminescence. 625 Polyclonal antibodies against proteins involved in photosynthesis used in this study were obtained 626 from Agrisera (http://www.agrisera.com). 627



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628 Accession Numbers 629 The accession numbers of the genes mentioned in this article are given below and their sequence 630 data can be found in the Arabidopsis Genome Initiative or GenBank/EMBL databases under the 631 following accession numbers: Arabidopsis thaliana (mTERF8/AT5G54180, NP_200229.1), 632 Camelina sativa (XP_010482826.1), Brassica napus (XP_013689181.1), Gossypium hirsutum 633 (XP_016726590.1), Gossypium arboreum (XP_017612337.1), Manihot esculenta (OAY51230.1), 634 Ricinus communis (XP_002515871.2), Prunus persica (XP_020412334.1), Pyrus xbretschneideri 635 (XP_009361283.1), Glycine max (KRH64303.1), Medicago truncatula (XP_003602380.1), 636 Solanum lycopersicum (XP_004235022.1), Solanum tuberosum (XP_006347515.1), psbA 637 (AtCG00020), rbcL(AtCG00490), psaJ(AtCG00630), petD(AtCG00730), petA(AtCG00540), 638 Oryza sativa (OspsbJ, NC_031333), Zea mays (ZmpsbJ, NP_043038.1). 639 640 SUPPLEMENTAL DATA 641 The following supplemental materials are available. 642 Supplemental Figure S1. Sequence alignment of mTERF8 with its putative orthologs. 643 Supplemental Figure S2. Accumulation of photosynthetic complexes and photosynthetic proteins 644 in wild type (WT) and the mterf8 mutant. 645 Supplemental Figure S3. Photosynthetic parameters of wild type (WT), mterf8, and the 646 complemented line (Com). 647 Supplemental Figure S4. Plastid gene expression profile of WT and mterf8. 648 Supplemental Figure S5. Predicted structure of mTERF8 and protein purification. 649 Supplemental Figure S6. Circularized RT-PCR of chloroplast psbA transcripts in wild type and 650 mterf8. 651 Supplemental Figure S7. EMSA with psbA and OspsbJ probes. 652 Supplemental Figure S8. Schematic of transcription termination activity analysis in vitro. 653 Supplemental Figure S9. Sequence alignment of psbJ terminal sequences. 654 Supplemental Table S1. Primers used for mTERF8 functional analysis in this study. 655 Supplemental Table S2. Primers for RT-qPCR analysis of plastid gene expression used in this 656 study. 657 658 ACKNOWLEDGMENTS 659 We thank ABRC Bioresources, which kindly offered the transgenic Arabidopsis lines 660 (SALK_021988). 661 662 Figure Legends 663 Figure 1. Sequence Analysis of mTERF8 and its Subcellular Localization. 664 (A) Scheme of mTERF8 protein, and alignment of eight mTERF motifs. Red boxes represent the 665



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mTERF motifs. Green box represents the transit peptide. (B) A neighbor-joining phylogenetic 666 analysis of the mTERF8 protein and its putative orthologs in different species, including Camelina 667 sativa (XP_010482826.1), Brassica napus (XP_013689181.1), Gossypium hirsutum 668 (XP_016726590.1), Gossypium arboreum (XP_017612337.1), Manihot esculenta 669 (OAY51230.1), Ricinus communis (XP_002515871.2), Prunus persica (XP_020412334.1), Pyrus 670 xbretschneideri (XP_009361283.1), Glycine max (KRH64303.1), Medicago truncatula 671 (XP_003602380.1), Solanum lycopersicum (XP_004235022.1), and Solanum tuberosum 672 (XP_006347515.1). These species represent different plant families, including Brassicaceae, 673 Malvaceae, Euphorbiaceae, Rosaceae, Leguminosae, and Solanaceae. The scale bar below the 674 tree indicates branch length. (C) Localization of eGFP, and mTERF8:eGFP in tobacco mesophyll 675 cells. Green fluorescence shows GFP fluorescence, red fluorescence indicates chlorophyll 676 autofluorescence, and orange/yellow fluorescence (Merge) shows colocalization. Scale bars: 5 μm. 677 (D) mTERF8:MYC is present in both stroma and thylakoids. Proteins of different fractions of 678 chloroplasts from transgenic Arabidopsis seedlings and from wild type were separated by PAGE 679 and immunoblotted with anti-MYC, anti-Lhcb5, and anti-RbcL antibodies. TP, Total protein from 680 the transgenic Arabidopsis seedlings; Tc, Total chloroplast protein; Str, stroma; Thy, thylakoid 681 fraction; WT, total protein from wild type. (E) Immunoblot detection of mTERF8, AtpA and RpoB 682 after two-dimensional gel electrophoresis. AtpA was used as a negative control. Thylakoid 683 membrane proteins from 3-week-old mTERF8:MYC seedlings were fractionated by BN-PAGE in 684 the first dimension and by SDS-PAGE in the second dimension. The approximate molecular masses 685 of the labeled protein complexes are indicated at the top. 686 687 Figure 2. Characterization of the Knockout Line of mTERF8. 688 (A) Schematic illustrating the genomic structure of mTERF8 and the location of the T-DNA 689 insertion. Black boxes and lines indicate exons and introns, respectively. The T-DNA insertion site 690 is indicated by a triangle. Both left border (LB) and right border (RB) are shown. Lba represents 691 the left border primer of the T-DNA insertion. LP and RP represent the left and right genomic 692 primers, respectively. (B) Phenotypes of 21-day-old plants of wild type (WT), mterf8, and the 693 complemented line (Com). Bar represents 1 cm. (C) RT-PCR analysis of mTERF8 expression in 694 wild type (WT), mterf8 and the complemented line (Com). TUBLIN was used as a control. (D) 695 Light-response curves of PSII quantum yield, photochemical quenching (qP), electron transport 696 rate (ETR), and non-photochemical quenching (NPQ) in the wild type (Col), mterf8 mutant, and 697 the complemented line (Com). Measurements were performed at the following light intensities: 0, 698 21, 56, 111, 281, 461, 701, 1076, and 1251 μmol photons m−2 s−1. PPDF, photosynthetic photon 699 flux density. Data were presented as mean±SD. Each data point represents at least 9 independent 700 plants. 701 702 Figure 3. Expression Pattern of the Chloroplast Polycistron psbJ-psbL-psbF-psbE in the 703



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Knockout Line of mTERF8. 704 (A) RT-qPCR analysis of chloroplast gene expression in wild type (WT) and the mterf8 mutant. 705 TUBLIN4 was used as an internal control. Relative expression patterns of plastid-encoded genes, 706 including psbA, rbcL, psbJ, rpoA, rrna16, and accD of WT and mterf8 are shown. (B) Schematic 707 illustration of the chloroplast polycistron psbJ-psbL-psbF-psbE in Arabidopsis, and relative 708 expression levels of the chloroplast genes psbJ, psbI, psbF, and psbE in WT and mterf8. (C) 709 Profile of the psbJ-psbL-psbF-psbE polycistron in WT and mterf8 by RNA blot analysis. The grey 710 values of the transcripts in WT and mterf8 mutant are 135.8 and 146.5, respectively. The values 711 were measured by Image J software. (D) Expression of the chloroplast genes psbJ and psbE in WT 712 treated with spectinomycin or not. The tublin4 gene was used as control. For the RT-qPCR results, 713 the data represent the mean of triplicate experiments for each gene. Bars represent standard 714 deviations calculated by ABI7300 system SDS software. Two independent biological replicates 715 showed similar results. 716 717 Figure 4. Analysis of the Defect in psbJ Transcription Termination in the mterf8 mutant. 718 (A) Comparison of the expression of genes with the selected primer pairs by RT-qPCR in wild type 719 (WT) and the mterf8 mutant. Error bars indicate standard deviations for triplicate replicates. (B) 720 Distribution of the five pairs of primers in the psbJ gene. The names of the five primers are shown 721 on the right. Relative expression level of psbJ transcripts in WT and mterf8, with the different five 722 sets of primers. (C) Schematic illustration of the chloroplast polycistron, and the primers (FW, RV, 723 and RFW) used for circular RT-PCR (cRT-PCR).cRT-PCR of chloroplast polycistron 724 psbJ-psbI-psbF-psbE in both WT and mterf8. The bands of the cRT-PCR products in the mterf8 725 mutant are indicated by black triangles. (D) Schematic illustration of the psbJ genes. Both the 5′- 726 and 3′- end nucleotides of the psbJ transcript are shown. The 3′-end nucleotide sequences 727 (termination sites) of the mature psbJ RNA in both WT and mterf8 are shown. The numbers in the 728 brackets at the right of the sequences represent the number of sequenced clones that contained 729 each of the sequence variant. 730 731 Figure 5. mTERF8 Binds to the Chloroplast Gene psbJ. 732 (A) EMSAs using six DNA probes from psbJ of Arabidopsis. Labeled DNA probes were incubated 733 with recombinant MBP:mTERF8 protein, whereas free biotinylated DNA probes only (Mock) or 734 incubated with empty MBP protein (MBP) served as negative controls. Increasing concentrations of 735 the corresponding competitor probes (competitor 1, 3, 4, 5, 6, and 7) were used, respectively. The 736 terminal region of the psbA gene was used as a competitor probe (competitor 2) in the analysis. 737 The location of the six probes is shown in the schematic of the polycistron.“**”indicates the 738 bands of free probes and “*” indicates the bands of shifted probes. (B) cpCHIP analysis of the 739 relative enrichment of the four representative chloroplast genes including psbA, psbJ, rbcL, rpoA, 740 and rrn16. (C) cpCHIP analysis of the relative enrichment of the four chloroplast genes psbE, 741



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psbF, psbL, and psbJ. (D) Distribution of the four different fragments in the psbJ gene. The names 742 of the four fragments (psbJ-1, psbJ-2, psbJ-3, and psbJ-4) are indicated on the right. (E) cpCHIP 743 analysis of the relative enrichment of the four different fragments of the psbJ gene. Bars represent 744 standard deviations calculated by ABI7300 system SDS software. 745 746 Figure 6. Transcription Termination Activity of MBP:mTERF8 in vitro. 747 (A) Transcription termination activity of MBP:mTERF8 in vitro. MBP:mTERF8 was added to the 748 T7 RNA polymerase transcription system in vitro with the Arabidopsis psbJ gene as a template. 749 (B)-(F) Transcription termination activity of MBP:mTERF8 in vitro. MBP:mTERF8 was added to 750 the T7 RNA polymerase transcription system in vitro with the Arabidopsis psbA, rbcL, psaJ, petD, 751 and petA genes as a template. All the above transcripts were separated by electrophoresis on a 2% 752 agarose gel, then stained with ethidium bromide. 753 754 755 756



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https://www.ncbi.nlm.nih.gov/pubmed?term=Alonso JM%2C Stepanova AN%2C Leisse TJ%2C Kim CJ%2C Chen HM%2C Shinn P%2C Stevenson DK%2C Zimmerman J%2C Barajas P%2C Cheuk R%2C et al%2E%2C %282013%29 Genome%2DWide Insertional Mutagenesis of Arabidopsis thaliana%2E Science&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Kuhn A%2C Grummt I %281989%29 3%27%2Dend formation of mouse pre%2DrRNA involves both transcription termination and a specific processing reaction%2E Genes Dev&dopt=abstract

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https://scholar.google.com/scholar?as_q=3'-end formation of mouse pre-rRNA involves both transcription termination and a specific processing reaction&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kuhn&as_ylo=1989&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Lang WH%2C Reeder RH %281995%29 Transcription termination of RNA polymerase I due to a T%2Drich element interacting with Reb1p%2E Proc Natl Acad Sci USA&dopt=abstract

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https://scholar.google.com/scholar?as_q=Transcription termination of RNA polymerase I due to a T-rich element interacting with Reb1p&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=Transcription termination of RNA polymerase I due to a T-rich element interacting with Reb1p&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lang&as_ylo=1995&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Lerbs%2DMache S %282011%29 Function of plastid sigma factors in higher plants%3A regulation of gene expression or just preservation of constitutive transcription%3F Plant Mol Biol&dopt=abstract

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https://scholar.google.com/scholar?as_q=Function of plastid sigma factors in higher plants: regulation of gene expression or just preservation of constitutive transcription&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lerbs-Mache&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Liere K%2C Weihe A%2C B�rner T %282011%29 The transcription machineries of plant mitochondria and chloroplasts%3A composition%2C function%2C and regulation%2E J Plant Physiol 168%3A 1345%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Linder T%2C Park CB%2C Asin%2DCayuela J%2C Pellegrini M%2C Larsson NG%2C Falkenberg M%2C Samuelsson T%2C Gustafsson CM %282005%29 A family of putative transcription termination factors shared amongst metazoans and plants%2E Curr Genet 48%3A 265%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Logan J%2C Falck%2DPedersen E%2C Darnell JE Jr%2C Shenk T %281987%29 A poly%28A%29 addition site and a downstream termination region are required for efficient cessation of transcription by RNA polymerase II in the mouse beta maj%2Dglobin gene%2E Proc Natl Acad Sci USA&dopt=abstract

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https://scholar.google.com/scholar?as_q=A poly(A) addition site and a downstream termination region are required for efficient cessation of transcription by RNA polymerase II in the mouse beta maj-globin gene&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Logan&as_ylo=1987&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Lopez%2DJuez E%2C Pyke KA %282005%29 Plastids unleashed%3A their development and their integration in plant development%2E Int J Dev Biol&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=L�pez%2DJuez E %282007%29 Plastid biogenesis%2C between light and shadows%2E J Exp Bot&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Pfalz J%2C Holtzegel U%2C Barkan A%2C Weisheit W%2C Mittag M%2C Pfannschmidt T %282015%29 ZmpTAC12 binds single%2Dstranded nucleic acids and is essential for accumulation of the plastid%2Dencoded polymerase complex in maize%2E New Phytologist&dopt=abstract


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https://www.ncbi.nlm.nih.gov/pubmed?term=Pfalz J%2C Pfannschmidt T %282013%29 Essential nucleoid proteins in early chloroplast development%2E Trends in Plant Science&dopt=abstract


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https://www.ncbi.nlm.nih.gov/pubmed?term=Pfannschmidt T%2C Link G %281994%29 Separation of two classes of plastid DNA%2Ddependent RNA polymerases that are differentially expressed in mustard %28Sinapis alba L%2E%29 seedlings%2E Plant Mol Biol&dopt=abstract

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https://scholar.google.com/scholar?as_q=Phosphorylation of rat mitochondrial transcription termination factor (mTERF) is required for transcription termination but not for binding to DNA&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Prieto-Martín&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Proudfoot N %282004%29 New perspectives on connecting messenger RNA 3%27 end formation to transcription%2E Curr Opin Cell Biol&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Quesada V %282016%29 The roles of mitochondrial transcription termination factors %28MTERFs%29 in plants%2E Physiol Plant&dopt=abstract

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https://scholar.google.com/scholar?as_q=The roles of mitochondrial transcription termination factors (MTERFs) in plants&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

https://scholar.google.com/scholar?as_q=The roles of mitochondrial transcription termination factors (MTERFs) in plants&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Quesada&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

https://www.ncbi.nlm.nih.gov/pubmed?term=Quesada V%2C Sarmiento%2DMa��s R%2C Gonz�lez%2DBay�n R%2C Hricov� A%2C P�rez%2DMarcos R%2C Graci�%2DMart�nez E%2C Medina%2DRuiz L%2C Leyva%2DD�az E%2C Ponce MR%2C Micol JL %282011%29 Arabidopsis RUGOSA2 encodes an mTERF family member required for mitochondrion%2C chloroplast and leaf development%2E Plant J 68%3A 738%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Regel RE%2C Ivleva NB%2C Zer H%2C Meurer J%2C Shestakov SV%2C Herrmann RG%2C Pakrasi HB%2C Ohad I%2E %282001%29 Deregulation of electron flow within photosystem II in the absence of the PsbJ protein%2E J Biol Chem&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Romani I%2C Manavski N%2C Morosetti A%2C Tadini L%2C Maier S%2C K�hn K%2C Ruwe H%2C Schmitz%2DLinneweber C%2C Wanner G%2C Leister D%2C Kleine T %282015%29 A Member of the Arabidopsis Mitochondrial Transcription Termination Factor Family Is Required for Maturation of Chloroplast Transfer RNAIle%28GAU%29%2E Plant Physiol&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Sato N %282001%29 Was the evolution of plastid genetic machinery discontinuous%3F Trends Plant Sci&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Sato N%2C Terasawa K%2C Miyajima K%2C Kabeya Y %282003%29 Organization%2C developmental dynamics%2C and evolution of plastid nucleoids%2E Int Rev Cytol 232%3A 217%26%23x&dopt=abstract

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https://www.ncbi.nlm.nih.gov/pubmed?term=Schweer J%2C T�rkeri H%2C Kolpack A%2C Link G %282010%29 Role and regulation of plastid sigma factors and their functional interactors during chloroplast transcription %2D recent lessons from Arabidopsis thaliana%2E Eur J Cell Biol&dopt=abstract

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https://scholar.google.com/scholar?as_q=Role and regulation of plastid sigma factors and their functional interactors during chloroplast transcription - recent lessons from Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Schweer&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

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mterf8, a member of the mitochondrial transcription … · transcription analysis using the in...

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