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Purine biosynthetic enzyme ATase2 is involved in the regulation of early chloroplast development and chloroplast gene expression in Arabidopsis

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Abstract

To investigate the molecular mechanism of chloroplast biogenesis and development, we characterized an Arabidopsis mutant (dg169, delayed greening 169) which showed growth retardation and delayed greening phenotype in leaves. Newly emerged chlorotic leaves recovered gradually with leaf development in the mutant, and the mature leaves showed similar phenotype to those of wild-typewild-type plants. Compared with wild-type, the chloroplasts were oval-shaped and smaller and the thylakoid membranes were less abundant in yellow section of young leaves of dg169. In addition, the functions of photosystem II (PSII) and photosystem I (PSI) were also impaired. Furthermore, the amount of core subunits of PSII and PSI, as well as PSII and PSI complexes reduced in yellow section of young leaves of dg169. Map-based positional cloning identified that phenotype of dg169 was attributed to a point mutation of ATase2 which converts the conserved Ile-155 residue to Asn. ATase2 catalyzes the first step of de novo purine biosynthesis. This mutation resulted in impaired purine synthesis and a significant decrease in ATP, ADP, GTP and GDP contents. The analysis of ATase2-GFP protein fusion showed that ATase2 was localized to nucleoid of chloroplasts. Our results further demonstrated that the levels of PEP-dependent transcripts in yellow section of young leaves of dg169 were decreased while NEP-dependent and both PEP- and NEP-dependent transcripts and chloroplast DNA replications were increased. The results in this study suggest that ATase2 plays an essential role in early chloroplast development through maintaining PEP function.

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References

  • Allison LA (2000) The role of sigma factors in plastid transcription. Biochimie 82:537–548

    Article  CAS  PubMed  Google Scholar 

  • Arsova B, Hoja U, Wimmelbacher M, Greiner E, Ustun S, Melzer M, Petersen K, Lein W, Bornke F (2010) Plastidial thioredoxin z interacts with two fructokinase-like proteins in a thiol-dependent manner: evidence for an essential role in chloroplast development in Arabidopsis and Nicotiana benthamiana. Plant Cell 22:1498–1515

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Boudreau E, Nickelsen J, Lemaire SD, Ossenbuhl F, Rochaix JD (2000) The Nac2 gene of Chlamydomonas encodes a chloroplast TPR-like protein involved in psbD mRNA stability. EMBO J 19:3366–3376

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bruce Cahoon A, Stern DB (2001) Plastid transcription: a menage a trois? Trends Plant Sci 6:45–46

    Article  CAS  PubMed  Google Scholar 

  • Chi W, Ma J, Zhang D, Guo J, Chen F, Lu C, Zhang L (2008) The pentratricopeptide repeat protein DELAYED GREENING1 is involved in the regulation of early chloroplast development and chloroplast gene expression in Arabidopsis. Plant Physiol 147:573–584

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chi W, Mao J, Li Q, Ji D, Zou M, Lu C, Zhang L (2010) Interaction of the pentatricopeptide-repeat protein DELAYED GREENING 1 with sigma factor SIG6 in the regulation of chloroplast gene expression in Arabidopsis cotyledons. Plant J 64:14–25

    Article  CAS  PubMed  Google Scholar 

  • Chi W, He B, Mao J, Li Q, Ma J, Ji D, Zou M, Zhang L (2012) The function of RH22, a DEAD RNA helicase, in the biogenesis of the 50S ribosomal subunits of Arabidopsis chloroplasts. Plant Physiol 158:693–707

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Gao ZP, Yu QB, Zhao TT, Ma Q, Chen GX, Yang ZN (2011) A functional component of the transcriptionally active chromosome complex, Arabidopsis pTAC14, interacts with pTAC12/HEMERA and regulates plastid gene expression. Plant Physiol 157:1733–1745

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Garcia M, Myouga F, Takechi K, Sato H, Nabeshima K, Nagata N, Takio S, Shinozaki K, Takano H (2008) An Arabidopsis homolog of the bacterial peptidoglycan synthesis enzyme MurE has an essential role in chloroplast development. Plant J 53:924–934

    Article  CAS  PubMed  Google Scholar 

  • Garton S, Knight H, Warren GJ, Knight MR, Thorlby GJ (2007) crinkled leaves 8–a mutation in the large subunit of ribonucleotide reductase–leads to defects in leaf development and chloroplast division in Arabidopsis thaliana. Plant J 50:118–127

    Article  CAS  PubMed  Google Scholar 

  • Geigenberger P, Reimholz R, Geiger M, Merlo L, Canale V, Stitt M (1997) Regulation of sucrose and starch metabolism in potato tubers in response to short-term water deficit. Planta 201:502–518

    Article  CAS  Google Scholar 

  • Gilkerson J, Perez-Ruiz JM, Chory J, Callis J (2012) The plastid-localized pfkB-type carbohydrate kinases FRUCTOKINASE-LIKE 1 and 2 are essential for growth and development of Arabidopsis thaliana. BMC Plant Biol 12:102

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hajdukiewicz PT, Allison LA, Maliga P (1997) The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids. EMBO J 16:4041–4048

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hajirezaei MR, Bornke F, Peisker M, Takahata Y, Lerchl J, Kirakosyan A, Sonnewald U (2003) Decreased sucrose content triggers starch breakdown and respiration in stored potato tubers (Solanum tuberosum). J Exp Bot 54:477–488

    Article  CAS  PubMed  Google Scholar 

  • Hanaoka M, Kanamaru K, Fujiwara M, Takahashi H, Tanaka K (2005) Glutamyl-tRNA mediates a switch in RNA polymerase use during chloroplast biogenesis. EMBO Rep 6:545–550

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hanson AD, Gregory JF 3rd (2002) Synthesis and turnover of folates in plants. Curr Opin Plant Biol 5:244–249

    Article  CAS  PubMed  Google Scholar 

  • Herz S, Eberhardt S, Bacher A (2000) Biosynthesis of riboflavin in plants. The ribA gene of Arabidopsis thaliana specifies a bifunctional GTP cyclohydrolase II/3,4-dihydroxy-2-butanone 4-phosphate synthase. Phytochemistry 53:723–731

    Article  CAS  PubMed  Google Scholar 

  • Hung WF, Chen LJ, Boldt R, Sun CW, Li HM (2004) Characterization of Arabidopsis glutamine phosphoribosyl pyrophosphate amidotransferase-deficient mutants. Plant Physiol 135:1314–1323

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ishizaki Y, Tsunoyama Y, Hatano K, Ando K, Shinmyo A, Kobori M, Takeba G, Nakahira Y, Shiina T (2005) A nuclear-encoded sigma factor, Arabidopsis SIG6, recognizes sigma-70 type chloroplast promoters and regulates early chloroplast development in cotyledons. Plant J 42:133–144

    Article  CAS  PubMed  Google Scholar 

  • Krause K, Maier RM, Kofer W, Krupinska K, Herrmann RG (2000) Disruption of plastid-encoded RNA polymerase genes in tobacco: Expression of only a distinct set of genes is not based on selective transcription of the plastid chromosome. Mol Gen Genet 263:1022–1030

    Article  CAS  PubMed  Google Scholar 

  • Lerbs-Mache S (2011) Function of plastid sigma factors in higher plants: regulation of gene expression or just preservation of constitutive transcription? Plant Mol Biol 76:235–249

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Rodermel SR, Yu F (2010) A var2 leaf variegation suppressor locus, SUPPRESSOR OF VARIEGATION3, encodes a putative chloroplast translation elongation factor that is important for chloroplast development in the cold. BMC Plant Biol 10:287

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu J, Yang H, Lu Q, Wen X, Chen F, Peng L, Zhang L, Lu C (2012) PsbP-domain protein1, a nuclear-encoded thylakoid lumenal protein, is essential for photosystem I assembly in Arabidopsis. Plant Cell 24:4992–5006

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Martinez-Garcia JF, Monte E, Quail PH (1999) A simple, rapid and quantitative method for preparing Arabidopsis protein extracts for immunoblot analysis. Plant J 20:251–257

    Article  CAS  PubMed  Google Scholar 

  • Meurer J, Meierhoff K, Westhoff P (1996) Isolation of high-chlorophyll-fluorescence mutants of Arabidopsis thaliana and their characterisation by spectroscopy, immunoblotting and northern hybridisation. Planta 198:385–396

    Article  CAS  PubMed  Google Scholar 

  • Meurer J, Lezhneva L, Amann K, Godel M, Bezhani S, Sherameti I, Oelmuller R (2002) A peptide chain release factor 2 affects the stability of UGA-containing transcripts in Arabidopsis chloroplasts. Plant Cell 14:3255–3269

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Myouga F, Hosoda C, Umezawa T, Iizumi H, Kuromori T, Motohashi R, Shono Y, Nagata N, Ikeuchi M, Shinozaki K (2008) A heterocomplex of iron superoxide dismutases defends chloroplast nucleoids against oxidative stress and is essential for chloroplast development in Arabidopsis. Plant Cell 20:3148–3162

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Neuhaus HE, Emes MJ (2000) Nonphotosynthetic metabolism in plastids. Annu Rev Plant Physiol Plant Mol Biol 51:111–140

    Article  CAS  PubMed  Google Scholar 

  • Peng L, Ma J, Chi W, Guo J, Zhu S, Lu Q, Lu C, Zhang L (2006) LOW PSII ACCUMULATION1 is involved in efficient assembly of photosystem II in Arabidopsis thaliana. Plant Cell 18:955–969

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pfalz J, Pfannschmidt T (2013) Essential nucleoid proteins in early chloroplast development. Trends Plant Sci 18:186–194

    Article  CAS  PubMed  Google Scholar 

  • Pfalz J, Liere K, Kandlbinder A, Dietz KJ, Oelmuller R (2006) pTAC2, -6, and -12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression. Plant Cell 18:176–197

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pogson BJ, Albrecht V (2011) Genetic dissection of chloroplast biogenesis and development: an overview. Plant Physiol 155:1545–1551

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophyll a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394

    Article  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Schult K, Meierhoff K, Paradies S, Toller T, Wolff P, Westhoff P (2007) The nuclear-encoded factor HCF173 is involved in the initiation of translation of the psbA mRNA in Arabidopsis thaliana. Plant Cell 19:1329–1346

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schweer J, Turkeri H, Kolpack A, Link G (2010) Role and regulation of plastid sigma factors and their functional interactors during chloroplast transcription—recent lessons from Arabidopsis thaliana. Eur J Cell Biol 89:940–946

    Article  CAS  PubMed  Google Scholar 

  • Senecoff JF, McKinney EC, Meagher RB (1996) De novo purine synthesis in Arabidopsis thaliana. II. The PUR7 gene encoding 5′-phosphoribosyl-4-(N-succinocarboxamide)-5-aminoimidazole synthetase is expressed in rapidly dividing tissues. Plant Physiol 112:905–917

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Serino G, Maliga P (1998) RNA polymerase subunits encoded by the plastid rpo genes are not shared with the nucleus-encoded plastid enzyme. Plant Physiol 117:1165–1170

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Smith PM, Atkins CA (2002) Purine biosynthesis. Big in cell division, even bigger in nitrogen assimilation. Plant Physiol 128:793–802

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sun X, Ouyang M, Guo J, Ma J, Lu C, Adam Z, Zhang L (2010) The thylakoid protease Deg1 is involved in photosystem-II assembly in Arabidopsis thaliana. Plant J 62:240–249

    Article  CAS  PubMed  Google Scholar 

  • Tiller N, Bock R (2014) The translational apparatus of plastids and its role in plant development. Mol Plant 7:1105–1120

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • van der Graaff E, Hooykaas P, Lein W, Lerchl J, Kunze G, Sonnewald U, Boldt R (2004) Molecular analysis of “de novo” purine biosynthesis in solanaceous species and in Arabidopsis thaliana. Front Biosci 9:1803–1816

    Article  PubMed  Google Scholar 

  • Walsh TA, Bauer T, Neal R, Merlo AO, Schmitzer PR, Hicks GR, Honma M, Matsumura W, Wolff K, Davies JP (2007) Chemical genetic identification of glutamine phosphoribosylpyrophosphate amidotransferase as the target for a novel bleaching herbicide in Arabidopsis. Plant Physiol 144:1292–1304

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Woo NS, Gordon MJ, Graham SR, Rossel JB, Badger MR, Pogson BJ (2011) A mutation in the purine biosynthetic enzyme ATASE2 impacts high light signalling and acclimation responses in green and chlorotic sectors of Arabidopsis leaves. Funct Plant Biol 38:401–419

    Article  CAS  Google Scholar 

  • Yagi Y, Ishizaki Y, Nakahira Y, Tozawa Y, Shiina T (2012) Eukaryotic-type plastid nucleoid protein pTAC3 is essential for transcription by the bacterial-type plastid RNA polymerase. Proc Natl Acad Sci USA 109:7541–7546

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yu F, Liu X, Alsheikh M, Park S, Rodermel S (2008) Mutations in SUPPRESSOR OF VARIEGATION1, a factor required for normal chloroplast translation, suppress var2-mediated leaf variegation in Arabidopsis. Plant Cell 20:1786–1804

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yu QB, Lu Y, Ma Q, Zhao TT, Huang C, Zhao HF, Zhang XL, Lv RH, Yang ZN (2013) TAC7, an essential component of the plastid transcriptionally active chromosome complex, interacts with FLN1, TAC10, TAC12 and TAC14 to regulate chloroplast gene expression in Arabidopsis thaliana. Physiol Plant 148:408–421

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Ding S, Lu Q, Yang Z, Wen X, Zhang L, Lu C (2011) Characterization of photosystem II in transgenic tobacco plants with decreased iron superoxide dismutase. Biochim Biophys Acta 1807:391–403

    Article  CAS  PubMed  Google Scholar 

  • Zhong L, Zhou W, Wang H, Ding S, Lu Q, Wen X, Peng L, Zhang L, Lu C (2013) Chloroplast small heat shock protein HSP21 interacts with plastid nucleoid protein pTAC5 and is essential for chloroplast development in Arabidopsis under heat stress. Plant Cell 25:2925–2943

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zrenner R, Stitt M, Sonnewald U, Boldt R (2006) Pyrimidine and purine biosynthesis and degradation in plants. Annu Rev Plant Biol 57:805–836

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the State Key Basic Research and Development Plan of China (2015CB150105) and the Key Research Programme of the Chinese Academy of Sciences (KGZD-EW-T05).

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Authors and Affiliations

  1. Photosynthesis Research Center, Key Laboratory of Photobiology, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China

    Zhipan Yang, Zengzhen Shang, Lei Wang, Qingtao Lu, Xiaogang Wen, Wei Chi, Lixin Zhang & Congming Lu

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Zengzhen Shang & Lei Wang

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  1. Zhipan Yang
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Correspondence to Congming Lu.

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Yang, Z., Shang, Z., Wang, L. et al. Purine biosynthetic enzyme ATase2 is involved in the regulation of early chloroplast development and chloroplast gene expression in Arabidopsis . Photosynth Res 126, 285–300 (2015). https://doi.org/10.1007/s11120-015-0131-z

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