Advertisement

Planta

, Volume 248, Issue 1, pp 257–265 | Cite as

Trans-splicing of plastid rps12 transcripts, mediated by AtPPR4, is essential for embryo patterning in Arabidopsis thaliana

  • Luca Tadini
  • Roberto Ferrari
  • Marie-Kristin Lehniger
  • Chiara Mizzotti
  • Fabio Moratti
  • Francesca Resentini
  • Monica Colombo
  • Alex Costa
  • Simona Masiero
  • Paolo Pesaresi
Short Communication

Abstract

Main conclusion

AtPPR4-mediated trans-splicing of plastid rps12 transcripts is essential for key embryo morphogenetic events such as development of cotyledons, determination of provascular tissue, and organization of the shoot apical meristem (SAM), but not for the formation of the protodermal layer.

Members of the pentatricopeptide repeat (PPR) containing protein family have emerged as key regulators of the organelle post-transcriptional processing and to be essential for proper plant embryo development. In this study, we report the functional characterization of the AtPPR4 (At5g04810) gene encoding a plastid nucleoid PPR protein. In-situ hybridization analysis reveals the presence of AtPPR4 transcripts already at the transition stage of embryo development. As a consequence, embryos lacking the AtPPR4 protein arrest their development at the transition/early-heart stages and show defects in the determination of the provascular tissue and organization of SAM. This complex phenotype is due to the specific role of AtPPR4 in the trans-splicing of the plastid rps12 transcripts, as shown by northern and slot-blot hybridizations, and the consequent defect in 70S ribosome accumulation and plastid protein synthesis, in agreement with the role proposed for the maize orthologue, ZmPPR4.

Keywords

Chloroplast Embryo development Pentatricopeptide repeat protein Protein synthesis RNA metabolism 

Abbreviations

PPR

Pentatricopeptide repeat

SAM

Shoot apical meristem

Notes

Acknowledgements

We are grateful to Christian Schmitz-Linneweber and members of his lab for their support in nucleotide immunoprecipitation and slot-blot analysis, and to Matteo Arosio for the help with the isolation of atppr4 mutant lines. We thank Valerio Parravicini and Mario Beretta for their excellent care of plants.

Funding

R. F. was supported by a Ph.D. fellowship from the Università degli Studi di Milano, C. M. and L. T. by a MIUR post-doc fellowship. Work in the lab of S. M. and P. P. was funded by CARIPLO Foundation (Grant no. 2011-2257).

Supplementary material

425_2018_2896_MOESM1_ESM.docx (37.4 mb)
Supplementary material 1 (DOCX 38282 kb)
425_2018_2896_MOESM2_ESM.xlsx (16 kb)
Supplementary material 2 (XLSX 15 kb)

References

  1. Alonso JM, Stepanova AN, Leisse TJ et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657CrossRefPubMedGoogle Scholar
  2. Barkan A, Small I (2014) Pentatricopeptide repeat proteins in plants. Annu Rev Plant Biol 65:415–442CrossRefPubMedGoogle Scholar
  3. Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602CrossRefPubMedGoogle Scholar
  4. Bobik K, Burch-Smith TM (2015) Chloroplast signaling within, between and beyond cells. Front Plant Sci 6:781CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bryant N, Lloyd J, Sweeney C, Myouga F, Meinke D (2011) Identification of nuclear genes encoding chloroplast-localized proteins required for embryo development in Arabidopsis. Plant Physiol 155:1678–1689CrossRefPubMedGoogle Scholar
  6. Capron A, Chatfie S, Provart N, Berleth T (2009) Embryogenesis: pattern formation from a single cell. Arabidopsis Book 7:e0126CrossRefPubMedPubMedCentralGoogle Scholar
  7. Cheng S, Gutmann B, Zhong X et al (2016) Redefining the structural motifs that determine RNA binding and RNA editing by pentatricopeptide repeat proteins in land plants. Plant J 85:532–547CrossRefPubMedGoogle Scholar
  8. Costa A, Gutla PV, Boccaccio A et al (2012) The Arabidopsis central vacuole as an expression system for intracellular transporters: functional characterization of the Cl/H+ exchanger CLC-7. J Physiol 590:3421–3430CrossRefPubMedPubMedCentralGoogle Scholar
  9. Cushing DA, Forsthoefel NR, Gestaut DR, Vernon DV (2005) Arabidopsis emb175 and other ppr knockout mutants reveal essential roles for pentatricopeptide repeat (PPR) proteins in plant embryogenesis. Planta 221:424–436CrossRefPubMedGoogle Scholar
  10. Ding YH, Liu NY, Tang ZS, Liu J, Yang WC (2006) Arabidopsis GLUTAMINE-RICH PROTEIN23 is essential for early embryogenesis and encodes a novel nuclear PPR motif protein that interacts with RNA polymerase II subunit III. Plant Cell 18:815–830CrossRefPubMedPubMedCentralGoogle Scholar
  11. Ferrari R, Tadini L, Moratti F, Lehniger MK, Costa A, Rossi F, Colombo M, Masiero S, Schmitz-Linneweber C, Pesaresi P (2017) CRP1 protein: (dis)similarities between Arabidopsis thaliana and Zea mays. Front Plant Sci 8:163CrossRefPubMedPubMedCentralGoogle Scholar
  12. Gillmor CS, Park MY, Smith MR, Pepitone R, Kerstetter RA, Poethig RS (2010) The MED12-MED13 module of mediator regulates the timing of embryo patterning in Arabidopsis. Development 137:113–122CrossRefPubMedPubMedCentralGoogle Scholar
  13. Gregis V, Sessa A, Dorca-Fornell C, Kater MM (2009) The Arabidopsis floral meristem identity genes AP1, AGL24 and SVP directly repress class B and C floral homeotic genes. Plant J 60:626–663CrossRefPubMedGoogle Scholar
  14. Hsu SC, Belmonte MF, Harada JJ, Inoue K (2010) Indispensable roles of plastids in Arabidopsis thaliana embryogenesis. Curr Genom 11:338–349CrossRefGoogle Scholar
  15. Ihnatowicz A, Pesaresi P, Varotto C, Richly E, Schneider A, Jahns P, Salamini F, Leister D (2004) Mutants for photosystem I subunit D of Arabidopsis thaliana: effects on photosynthesis, photosystem I stability and expression of nuclear genes for chloroplast functions. Plant J 37:839–852CrossRefPubMedGoogle Scholar
  16. Inhatowicz A, Pesaresi P, Leister D (2007) The E subunit of photosystem I is not essential for linear electron flow and photoautotrophic growth in Arabidopsis thaliana. Planta 226:889–895CrossRefGoogle Scholar
  17. Kirch T, Simon R, Grünewald M, Werr W (2003) The DORNRÖSCHEN/ENHANCER OF SHOOT REGENERATION1 gene of Arabidopsis acts in the control of meristem cell fate and lateral organ development. Plant Cell 15:694–705CrossRefPubMedPubMedCentralGoogle Scholar
  18. Kocábek T, Repková J, Dudová M, Hoyerová K, Vrba L (2006) Isolation and characterization of a novel semi-lethal Arabidopsis thaliana mutant of gene for pentatricopeptide (PPR) repeat-containing protein. Genetica 128:395–407CrossRefPubMedGoogle Scholar
  19. Kunst L (1998) Preparation of physiologically active chloroplasts from Arabidopsis. Methods Mol Biol 82:43–48PubMedGoogle Scholar
  20. Kupsch C, Ruwe H, Gusewski S, Tillich M, Small I, Schmitz-Linneweber C (2012) Arabidopsis chloroplast RNA binding proteins CP31A and CP29A associate with large transcript pools and confer cold stress tolerance by influencing multiple chloroplast RNA processing steps. Plant Cell 24:4266–4280CrossRefPubMedPubMedCentralGoogle Scholar
  21. Long JA, Barton MK (1998) The development of apical embryonic pattern in Arabidopsis. Development 125:3027–3035PubMedGoogle Scholar
  22. Mansfield SG, Briarty LG (1991) Early embryogenesis in Arabidopsis thaliana. II. The developing embryo. Can J Bot 69:461–476CrossRefGoogle Scholar
  23. McConnell JR, Emery J, Eshed Y, Bao N, Bowman J, Barton MK (2001) Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411:709–713CrossRefPubMedGoogle Scholar
  24. Meinke D, Muralla R, Sweeney C, Dickerman A (2008) Identifying essential genes in Arabidopsis thaliana. Trends Plant Sci 13:483–491CrossRefPubMedGoogle Scholar
  25. Meurer J, Lezhneva L, Amann K, Gödel M, Bezhani S, Sherameti I, Oelmüller R (2002) A peptide chain release factor 2 affects the stability of UGA-containing transcripts in Arabidopsis chloroplasts. Plant Cell 14:3255–3269CrossRefPubMedPubMedCentralGoogle Scholar
  26. Mizzotti C, Galliani BM, Dreni L, Sommer H, Bombarely A, Masiero S (2017) ERAMOSA controls lateral branching in snapdragon. Sci Rep 7:41319CrossRefPubMedPubMedCentralGoogle Scholar
  27. Möller B, Weijers D (2009) Auxin control of embryo patterning. Cold Spring Harb Perspect Biol 1(5):a001545.  https://doi.org/10.1101/cshperspect.a001545 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Mukherjee K, Brocchieri L, Bürglin TR (2009) A comprehensive classification and evolutionary analysis of plant homeobox genes. Mol Biol Evol 26:2775–2794CrossRefPubMedPubMedCentralGoogle Scholar
  29. Olinares PD, Ponnala L, Van Wijk KJ (2010) Megadalton complexes in the chloroplast stroma of Arabidopsis thaliana characterized by size exclusion chromatography, mass spectrometry, and hierarchical clustering. Mol Cell Proteom 9:1594–1615CrossRefGoogle Scholar
  30. Remans T, Smeets K, Opdenakker K, Mathijsen D, Vangronsveld J, Cuypers A (2008) Normalisation of real-time RT-PCR gene expression measurements in Arabidopsis thaliana exposed to increased metal concentrations. Planta 227:1343–1349CrossRefPubMedGoogle Scholar
  31. Resentini F, Cyprys P, Steffen JG et al (2017) SUPRESSOR OF FRIGIDA (SUF4) supports gamete fusion via regulating Arabidopsis EC1 gene expression. Plant Physiol 173:155–166CrossRefPubMedGoogle Scholar
  32. Romani I, Tadini L, Rossi F, Masiero S, Pribil M, Jahns P, Kater M, Leister D, Pesaresi P (2012) Versatile roles of Arabidopsis plastid ribosomal proteins in plant growth and development. Plant J 72:922–934CrossRefPubMedGoogle Scholar
  33. Schagger H, von Jagow G (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166:368–379CrossRefPubMedGoogle Scholar
  34. Schindelin J, Arganda-Carreras I, Frise E et al (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682CrossRefPubMedGoogle Scholar
  35. Schmitz-Linneweber C, Williams-Carrier RE, Williams-Voelker PM, Kroeger TS, Vichas A, Barkan A (2006) A pentatricopeptide repeat protein facilitates the trans-splicing of the maize chloroplast rps12 pre-mRNA. Plant Cell 18:2650–2663CrossRefPubMedPubMedCentralGoogle Scholar
  36. Takada S, Jürgens G (2007) Transcriptional regulation of epidermal cell fate in the Arabidopsis embryo. Development 134:1141–1150CrossRefPubMedGoogle Scholar
  37. ten Hove CA, Lu KJ, Weijers D (2015) Building a plant: cell fate specification in the early Arabidopsis embryo. Development 142:420–430CrossRefPubMedGoogle Scholar
  38. Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2:1565–1572CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Dipartimento di BioscienzeUniversità degli Studi di MilanoMilanItaly
  2. 2.Molecular Genetics, Institute of BiologyHumboldt University of BerlinBerlinGermany
  3. 3.Max-Planck-Institut für Molekulare PflanzenphysiologiePotsdam-GolmGermany
  4. 4.Instituto de Biologıa Molecular y Celular de Plantas (CSIC-Universidad Politécnica de Valencia)ValenciaSpain
  5. 5.Centro Ricerca e InnovazioneFondazione Edmund MachSan Michele all’AdigeItaly
  6. 6.Dipartimento di Scienze Agrarie e Ambientali - Produzione, Territorio, AgroenergiaUniversità degli studi di MilanoMilanItaly

Personalised recommendations