Plastid gene expression during chloroplast differentiation and dedifferentiation into non-photosynthetic plastids during seed formation
Arabidopsis seed formation is coupled with two plastid differentiation processes. Chloroplast formation starts during embryogenesis and ends with the maturation phase. It is followed by chloroplast dedifferentiation/degeneration that starts at the end of the maturation phase and leads to the presence of small non-photosynthetic plastids in dry seeds. We have analysed mRNA and protein levels of nucleus- and plastid-encoded (NEP and PEP) components of the plastid transcriptional machinery, mRNA and protein levels of some plastid RNA polymerase target genes, changes in plastid transcriptome profiles and mRNA and protein levels of some selected nucleus-encoded plastid-related genes in developing seeds during embryogenesis, maturation and desiccation. As expected, most of the mRNAs and proteins increase in abundance during maturation and decrease during desiccation, when plastids dedifferentiate/degenerate. In contrast, mRNAs and proteins of components of the plastid transcriptional apparatus do not decrease or even still increase during the period of plastid dedifferentiation. Results suggest that proteins of the plastid transcriptional machinery are specifically protected from degradation during the desiccation period and conserved in dry seeds to allow immediate regain of plastid transcriptional activity during stratification/germination. In addition, results reveal accumulation and storage of mRNAs coding for RNA polymerase components and sigma factors in dry seeds. They should provide immediately-to-use templates for translation on cytoplasmic ribosomes in order to enhance RNA polymerase protein levels and to provide regulatory proteins for stored PEP to guaranty efficient plastid genome transcription during germination.
KeywordsArabidopsis Plastids Dedifferentiation Transcriptome profiling RNA polymerase
Financial support was obtained from the French agency of research (GENOPLANTE project ANR-07-GPLA-013-001), the Centre National de la Recherche Scientifique and the Ministère de l’Enseignement Supérieur et de la Recherche. The authors declare that they have no conflict of interest and they thank D. Job for critical reading of the manuscript.
- Allorent G, Lambert E, Lerbs-Mache S, Courtois F (2010) RNA isolation from developing Arabidopsis thaliana seeds suitable for gene expression analyses. J Endocytobiosis Cell Res 20:26–33Google Scholar
- Belmonte MF, Kirikbride RC, Stone SL et al (2013) Comprehensive developmental profiles of gene activity in regions and subregions of the Arabidopsis seed. Proc Natl Acad Sci USA 14:E435–E444Google Scholar
- Budziszewski GJ, Lewis SP, Glover LW, Reineke J, Jones G, Schlate Ziemnik L, Lonowski J, Nyfeler B, Aux G, Zhou Q, McElver J, Patton DA, Martienssen R, Grossniklaus U, Ma H, Law M, Levin JZ (2001) Arabidopsis genes essential for seedling viability: isolation of insertional mutants and molecular cloning. Genetics 159:1765–1778PubMedGoogle Scholar
- Debeaujon I, Lepiniec L, Pourcel L and Routaboul JM (2007) Seeds coat development and dormancy. In: Bradford K, Nonogaki H (eds) Seed development, dormancy and germination. Blackwell Publishing vol. 27, pp 24–43Google Scholar
- Hedtke B, Börner T, Weihe A (2000) One RNA polymerase serving two genomes. EMBO rep 11:435–440Google Scholar
- Howell KA, Narsai R, Carroll A, Ivanova A, Lohse M, Usadel B, Millar AH, Whelan J (2009) Mapping metabolic and transcript temporal switches during germination in rice highlights specific transcription factors and the role of RNA instability in the germination process. Plant Physiol 149:961–980PubMedCrossRefGoogle Scholar
- Ishizaki Y, Tsunoyamz Y, Hatano K, Ando K, Kato 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 regulated early chloroplast development in cotyledons. Plant J 42:133–144PubMedCrossRefGoogle Scholar
- Le BH, Cheng C, Bui AQ, Wagmaister JA, Henry KF, Pelletier J, Kwong L, Belmonte M, Kirkbride R, Horvath S, Drews GN, Fischer RL, Okamuro JK, Harada JJ, Goldberg RB (2010) Global analysis of gene activity during Arabidopsis seed development and identification of seed-specific transcription factors. Proc Natl Acad Sci USA 107:8063–8070PubMedCrossRefGoogle Scholar