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Plastid Gene Expression and Plant Development Require a Plastidic Protein of the Mitochondrial Transcription Termination Factor Family

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Plastid Gene Expression and Plant Development Require a Plastidic Protein of the Mitochondrial Transcription Termination Factor Family Plastid gene expression and plant development require a plastidic protein of the mitochondrial transcription termination factor family Elena Babiychuka,b, Klaas Vandepoelea,b, Josef Wissingc, Miguel Garcia-Diazd, Riet De Ryckea,b, Hana Akbarie, Jérôme Joubèsf, Tom Beeckmana,b, Lothar Jänschc, Margrit Frentzene, Marc C. E. Van Montagub,1, and Sergei Kushnira,b,1 aDepartment of Plant Systems Biology, VIB, 9052 Ghent, Belgium; bDepartment of Plant Biotechnology and Genetics, Ghent University, 9052 Ghent, Belgium; cAbteilung Zellbiologie, Helmholtz-Zentrum für Infektionsforschung GmbH, 38124 Braunschweig, Germany; dPharmacological Sciences, Stony Brook University, Stony Brook, NY 11794-8651; eInstitut für Biologie I, Spezielle Botanik, Rheinisch-Westfälische Technische Hochschule Aachen, 52056 Aachen, Germany; and fUniversité Victor Ségalen Bordeaux 2, Laboratoire de Biogenèse Membranaire, Centre National de la Recherche Scientifique, 33076 Bordeaux Cedex, France Contributed by Marc C. E. Van Montagu, March 3, 2011 (sent for review December 6, 2010) Plastids are DNA-containing organelles unique to plant cells. In fluence transcription (8). mTERF3 acts as a specific repressor of Arabidopsis, one-third of the genes required for embryo devel- mammalian mtDNA transcription initiation in vivo (9). opment encode plastid-localized proteins. To help understand the Here, we show that 11 of 35 annotated Arabidopsis mTERFs role of plastids in embryogenesis and postembryonic develop- are targeted to plastids. Genetic complementation indicated that ment, we characterized proteins of the mitochondrial transcrip- early embryo arrest is a characteristic phenotype of mutation in tion termination factor (mTERF) family, which in animal models, mTERF/At4g02990, whereas in vitro cell culture and analysis of comprises DNA-binding regulators of mitochondrial transcription. genetic mosaics revealed a postembryonic phenotype of a growth- Of 35 Arabidopsis mTERF proteins, 11 are plastid-localized. Ge- compromised albino, which suggested the gene name BELAYA netic complementation shows that at least one plastidic mTERF, SMERT’ (BSM) or white death in Russian. Exogenously supplied BELAYA SMERT’ (BSM), is required for embryogenesis. The main phytohormones and plastidic homomeric acetyl-CoA carboxylase bsm postembryonic phenotypes of genetic mosaics with the mu- (ACC2) promoted the survival of bsm mutant cells, suggesting PLANT BIOLOGY tation are severe abnormalities in leaf development. Mutant bsm that biosynthesis of growth factors and malonyl-CoA underpin cells are albino, are compromised in growth, and suffer defects in the nonautonomous and autonomous cell functions of plastids global plastidic gene expression. The bsm phenotype could be in Arabidopsis development. phenocopied by inhibition of plastid translation with spectinomy- cin. Plastid translation is essential for cell viability in dicotyledon- Results ous species such as tobacco but not in monocotyledonous maize. Arabidopsis Has at Least 11 Plastid-Localized mTERF Proteins. Flow- BSM Here, genetic interactions between and the gene encoding ering plants have the highest number of mTERF genes among plastid homomeric acetyl-CoA carboxylase ACC2 suggest that eukaryotes (Table S1). GFP fusions of all members of the Arabi- there is a functional redundancy in malonyl-CoA biosynthesis dopsis mTERF family showed that 11 mTERF proteins were tar- bsm Arabidopsis that permits cell survival in . Overall, our results geted to chloroplasts and 17 were mitochondrial, whereas one indicate that biosynthesis of malonyl-CoA and plastid-derived fusion was distributed equally between the nuclei and the cyto- systemic growth-promoting compounds are the processes that plasm (Fig. S1). Six gene fusions showed no GFP expression. The link plant development and plastid gene expression. detection of conserved protein motifs revealed the presence of two motifs specificforArabidopsis mTERF proteins targeted to the organellar gene expression | splicing | ClpPR protease | myrosinase | digitonin mitochondria (Fig. S2 and Table S2). Integration of genome or- ganization information (10) indicated species-specific gene family lastids are DNA-containing organelles of endosymbiotic ori- expansion through tandem duplication both in rice and Arabidopsis Pgin that define plant cells (1). Plastid homeostasis is continually (with 45% and 25% of mTERF homologs in tandem, respectively) monitored, and gene expression is regulated by tetrapyrrole bio- (Fig. S3). In contrast, plastid-targeted mTERFs belong to a single synthesis and the monitoring plastid gene expression machinery, subtype, probably representing the ancestral family composition. the abundance of reactive oxygen species, plastidic redox status, To determine the involvement of plastid mTERFs in embryo and the ATP/ADP balance of organelles (2). Consequently, this development, we surveyed transferred DNA (T-DNA) insertion so-called retrograde signaling also affects the progression of de- mutant alleles. Plants with mutations in four genes developed velopmental programs (3). Among 339 nonredundant Arabidopsis seeds with arrested embryos (Table S3). The bsm mutant has fi fi fi genes required for proper embryo formation, 108 encode plastid- been rst identi ed and rst characterized in detail. targeted proteins (4). To study the role of plastid gene expression bsm Cells Are Albino and Dependent on Exogenous Phytohormones. in embryogenesis and postembryonic development, we have In a progeny of BSM/bsm plants, 25% of the seeds had embryos characterized proteins of the mitochondrial transcription termi- arrested at the late globular stage of development (Fig. 1A). nation factor (mTERF) family, a group of proteins named after the human mTERF1. These proteins have a modular architecture based on repetitions of a 30-aa mTERF motif (5). Studies of the Author contributions: E.B., K.V., L.J., M.F., and S.K. designed research; E.B., K.V., J.W., crystal structure of mTERF1 have revealed that these mTERF M.G.-D., R.D.R., H.A., J.J., and T.B. performed research; E.B., K.V., J.W., M.G.-D., L.J., motifs associate to create a helical structure apparently involved in M.F., and S.K. analyzed data; and E.B., K.V., M.G.-D., M.F., M.C.E.V.M., and S.K. wrote the paper. nucleic acid binding (6). Vertebrates have four mTERF paralogs. The authors declare no conflict of interest. In humans, mTERF1 is a sequence-specific DNA-binding protein 1To whom correspondence may be addressed. E-mail: [email protected] or responsible for mitochondrial transcription termination at a site [email protected]. adjacent to the mitochondrial rRNA genes (6). mTERF2 can bind This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. to mitochondrial DNA (7) and, at least in mouse, seems to in- 1073/pnas.1103442108/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1103442108 PNAS Early Edition | 1of6 Downloaded by guest on September 27, 2021 BSM Gene Deficiency Affects Processing and Steady-State Levels of Plastid Transcripts. Plastids possess two types of DNA-dependent RNA polymerases, a nuclear-encoded bacteriophage-type RNA polymerase (NEP) and a bacterium-type multisubunit RNA polymerase (PEP). The PEP catalytic core requires products of the plastid genes rpoA, rpoB, rpoC1, and rpoC2 (11). Plastid- encoded class I genes such as rbcL are transcribed predominantly by PEP. Class II genes are transcribed by both PEP and NEP, whereas a few class III genes rpoB and accD, are thought to be transcribed exclusively by NEP (12). In Arabidopsis, rRNA genes belong to class II, but PEP is responsible for most transcriptional activity of rrn16S and rrn23S genes (12). Mature 16S rRNA and 23S rRNA were not detectable in bsm cells (Fig. 1E). The PEP-dependent expression of the pro- tein coding genes rbcL and atpA was similarly affected, whereas clpP transcripts levels increased (Fig. 1E). A similar response characterized albino tobacco plants mutated in PEP RNA poly- merase (13). To understand the changes in clpP transcript size, we analyzed its splicing by RT-PCR. In Arabidopsis, the coding region of clpP is disrupted by two introns that belong to group IIb and group IIa classes. In albino shoots, RT-PCR showed that the second clpP group IIa intron was not spliced (Fig. 1F). The last gene exon codes for the 85-aa residues that include two residues of a clpP catalytic triad, indicating that the mutant polypeptide is catalyt- ically inactive (14). The plastid ClpPR protease complex is re- ported to be essential in both tobacco and Arabidopsis (15). Protein-coding regions of plastid genes for the AtpF subunit of Fig. 1. Mutant bsm phenotype and plastid gene expression. (A) Shrunken dry the ATP synthase and ribosomal proteins Rpl2 and Rps12 are mutant seed, arrested embryo (Inset), and a WT seed. (B) Asynchronous ger- interrupted by group IIa introns (16). The production of the rps12 mination of the seeds with arrested embryos. (C) Mixed callus/shoot bsm ORF also requires a transsplicing event of a IIb intron. Results culture on a medium supplemented with phytohormones. (D) Albino cells are showed that rps12 transsplicing was normal but that atpF, rpl2, and bsm/bsm homozygous. HindIII-digested genomic DNA from albino cells (b/b) was compared with DNA of green homo- (B/B) and heterozygous (B/b) plants rps12 group IIa introns were not spliced in bsm cells (Fig. 1G). by hybridization analysis with radioactive probes detecting nuclear BSM and These nonspliced transcripts encode mutant proteins, of which plastid rbcL genes.
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