Skip to main content
SpringerLink
Log in

Plastids of three Cuscuta species differing in plastid coding capacity have a common parasite-specific RNA composition

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

The chlorophyll containing holoparasitic species Cuscuta reflexa, the achlorophyllous species Cuscuta odorata and the intermediate species Cuscuta gronovii, which contains only traces of chlorophyll, were compared with respect to their plastid coding capacity and plastid gene expression at the level of RNA. While extensive deletions have taken place in the plastid DNA of the achlorophyllous species C. odorata, the green species C. reflexa has retained an almost complete plastid genome. Although the plastid genome of the intermediate species C. gronovii has suffered extensive deletions, in contrast to the plastid genome of C. odorata it has retained photosynthesis-related genes. Hybridization with radioactive 3′-labelled RNA revealed that in all three species only a small 'parasite-specific' portion of the plastid genome consisting of mainly rRNAs and tRNAs is represented at the level of steady-state RNA. Run-on transcription assays revealed that in plastids of C. reflexa the entire genome is transcribed. Hence, the subset of RNA species required for a parasitic lifestyle is preferentially stabilized in Cuscuta plastids.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2a, b.
Fig. 3.
Fig. 4.
Fig. 5.

Similar content being viewed by others

Abbreviations

accD :

gene encoding the β-subunit of acetyl-CoA carboxylase

atpB :

gene encoding the β-subunit of ATPase

clpP :

gene coding for Clp-protease subunit

LSC:

large single-copy region

NEP:

nuclear-encoded RNA polymerase

PEP:

plastid-encoded RNA polymerase

psa :

genes coding for subunits of photosystem I

psb :

genes coding for subunits of photosystem II

rbcL :

gene encoding the large subunit of Rubisco

rpo :

genes encoding subunits of PEP

rpl, rps :

genes coding for subunits of the ribosomes

SSC:

small single-copy region

trn :

genes encoding tRNAs

References

  • Allison LA, Simon LD, Maliga P (1996) Deletion of rpoB reveals a second distinct transcription system in plastids of higher plants. EMBO J 15:2802–2809

    CAS  PubMed  Google Scholar 

  • Bömmer D, Haberhausen G, Zetsche K (1993) A large deletion in the plastid DNA of the holoparasitic flowering plant Cuscuta reflexa concerning two ribosomal proteins (rpl2, rpl23), one transfer RNA (trnI) and an ORF 2280 homologue. Curr Genet 24:171–176

    Google Scholar 

  • Chang CC, Sheen J, Bligny M, Niwa Y, Lerbs-Mache S, Stern DB (1999) Functional analysis of two maize cDNAs encoding T7-like RNA polymerases. Plant Cell 11:911–926

    Article  CAS  PubMed  Google Scholar 

  • Delavault P, Thalouarn P (1994) Plastid genome evolution in Orobanchaceae and other holoparasites. In: Pieterse AH, Verkleij JAC, ter Borg SJ (eds) Proceedings of the 3rd International Workshop on Orobanche and related Striga research. Amsterdam, The Netherlands

  • DeSantis-Macciossek G, Kofer W, Bock A, Schoch S, Maier RM, Wanner G, Rüdiger W, Koop HU, Herrmann RG (1999) Targeted disruption of the plastid RNA polymerase genes rpoA, B and C1: molecular biology, biochemistry and ultrastructure. Plant J 18:477–489

    PubMed  Google Scholar 

  • Eberhard S, Drapier D, Wollmann FA (2002) Searching limiting steps in the expression of chloroplast-encoded proteins: relations between gene copy number, transcription, transcript abundance and translation rate in the chloroplast of Chlamydomonas reinhardtii. Plant J 31:149–60

    Article  CAS  PubMed  Google Scholar 

  • Falk J, Schmidt A, Krupinska K (1993) Characterization of plastid DNA transcription in ribosome deficient plastids of heat-bleached barley leaves. J Plant Physiol 141:176–181

    CAS  Google Scholar 

  • Gruissem W, Tonkyn JC (1993) Control mechanisms of plastid gene expression. Crit Rev Plant Sci 12:19–55

    CAS  Google Scholar 

  • Haberhausen G, Zetsche K (1994) Functional loss of all ndh genes in an otherwise relatively unaltered plastid genome of the holoparasitic flowering plant Cuscuta reflexa. Plant Mol Biol 24:217–222

    Google Scholar 

  • Haberhausen G, Valentin K, Zetsche K (1992) Organisation and sequence of photosynthetic genes from the plastid genome of the holoparasitic flowering plant Cuscuta reflexa. Mol Gen Genet 232:154–161

    CAS  PubMed  Google Scholar 

  • Hallick RB, Lipper C, Richards OC, Rutter WJ (1976) Isolation of a transcriptionally active chromosome from Euglena gracilis. Biochemistry 15:3039–3045

    CAS  PubMed  Google Scholar 

  • Hedtke B, Börner T, Weihe A (1997) Mitochondrial and chloroplast phage-type RNA polymerases in Arabidopsis. Science 277:809–811

    CAS  PubMed  Google Scholar 

  • Hedtke B, Legen J, Weihe A, Herrmann RG, Börner T (2002) Six active phage-type RNA polymerases in Nicotiana tabacum. Plant J 30:625–637

    Article  PubMed  Google Scholar 

  • Hess WR, Prombona A, Fieder B, Subramanian AR, Börner T (1993) Chloroplast rps15 and the rpoB/C1/C2 gene cluster are strongly transcribed in ribosome-deficient plastids: evidence for a functioning non-chloroplast-encoded RNA polymerase. EMBO J 12:563–571

    CAS  PubMed  Google Scholar 

  • Hibberd JM, Bungard RA, Press MC, Jeschke WD, Scholes JD, Quick WP (1998) Localization of photosynthetic metabolism in the parasitic angiosperm Cuscuta reflexa. Planta 205:506–513

    Article  CAS  Google Scholar 

  • Ikeda TM, Gray MW (1999) Identification and characterization of T3/T7 bacteriophage-like RNA polymerase sequences in wheat. Plant Mol Biol 40:567–578

    CAS  PubMed  Google Scholar 

  • Klein RR, Mullet JE (1990) Light-induced transcription of chloroplast genes. psbA transcription is differentially enhanced in illuminated barley. J Biol Chem 265:1895–1902

    CAS  PubMed  Google Scholar 

  • Krause K, Falk J, Humbeck K, Krupinska K (1998) Responses of the transcriptional apparatus of barley chloroplasts to a prolonged dark period and to subsequent reillumination. Physiol Plant 104:143–152

    Article  CAS  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

    CAS  PubMed  Google Scholar 

  • Krause K, Berg S, Krupinska K (2003) Plastid transcription in the holoparasitic plant genus Cuscuta: parallel loss of the rrn16 PEP-promoter and of the rpoA and rpoB genes coding for the plastid-encoded RNA polymerase. Planta 216:815–823

    CAS  PubMed  Google Scholar 

  • Krupinska K (1992) Transcriptional control of plastid gene expression during development of primary foliage leaves of barley grown under a daily light-dark-regime. Planta 186:294–303

    CAS  Google Scholar 

  • Legen J, Kemp S, Krause K, Profanter B, Herrmann RG, Maier RM (2002) Comparative analysis of plastid transcription profiles of entire plastid chromosomes from tobacco attributed to wild-type and PEP-deficient transcription machineries. Plant J 31:171–188

    Article  CAS  PubMed  Google Scholar 

  • Machado MA, Zetsche K (1990) A structural, functional and molecular analysis of plastids of the holoparasites Cuscuta reflexa and Cuscuta europaea. Planta 181:91–96

    CAS  Google Scholar 

  • Maliga P (1998) Two plastid polymerases of higher plants: an evolving story. Trends Plant Sci 3:4-6

    Article  Google Scholar 

  • Monde RA, Schuster G, Stern DB (2000) Processing and degradation of chloroplast mRNA. Biochimie 82:573–582

    CAS  Google Scholar 

  • Morden CW, Wolfe KH, dePamphilis CW, Palmer JD (1991) Plastid translation and transcription genes in a non-photosynthetic plant: intact, missing and pseudo genes. EMBO J 10:3281–3288

    CAS  PubMed  Google Scholar 

  • Mullet JE (1993) Dynamic regulation of chloroplast transcription. Plant Physiol 103:309–313

    Article  CAS  PubMed  Google Scholar 

  • Panda MM, Choudhury NK (1992) Effect of irradiance and nutrients on chlorophyll and carotenoid content and Hill reaction activity in Cuscuta reflexa. Photosynthetica 26:585–592

    CAS  Google Scholar 

  • Schuster G, Lisitsky I, Klaff P (1999) Polyadenylation and degradation of mRNA in the chloroplast. Plant Physiol 120:937–944

    CAS  PubMed  Google Scholar 

  • Sherman TD, Pettigrew WT, Vaughn KC (1999) Structural and immunological characterization of the Cuscuta pentagona L. chloroplast. Plant Cell Physiol 40:592–603

    CAS  Google Scholar 

  • Sugiura M, Shinozaki K, Zaita N, Kusuda M, Kumano M (1986) Clone bank of the tobacco (Nicotiana tabacum) chloroplast genome as a set of overlapping restriction endonuclease fragments: mapping of eleven ribosomal protein genes. Plant Sci 44:211–216

    Article  CAS  Google Scholar 

  • van der Kooij TAW, Krause K, Dörr I, Krupinska K (2000) Molecular, functional and ultrastructural characterization of plastids from six species of the parasitic flowering plant genus Cuscuta. Planta 210:701–707

    Article  PubMed  Google Scholar 

  • Wakasugi T, Sugita M, Tsudzuki T, Sugiura M (1998) Updated map of tobacco chloroplast DNA. Plant Mol Biol Rep 16:231–241

    CAS  Google Scholar 

  • Wimpee CF, Wrobel RL, Garvin DK (1991) A divergent plastid genome in Conopholis americana, an achlorophyllous parasitic plant. Plant Mol Biol 17:161–166

    CAS  PubMed  Google Scholar 

  • Wischmann B, Nielsen TH, Møller BL (1999) In vitro biosynthesis of phosphorylated starch in intact potato amyloplasts. Plant Physiol 119:455–462

    Article  CAS  PubMed  Google Scholar 

  • Wulff E, Torres S, Vigil E (2002) Protocol for DNA extraction from potato tubers. Plant Mol Biol Rep 20:187a–187e

    Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge Mario Brosch for technical help and valuable advice concerning amyloplast isolation and labelling of steady-state RNAs. S. Berg received a PhD grant from the Friedrich-Naumann foundation.

Author information

Authors and Affiliations

  1. Botanisches Institut, Christian-Albrechts-Universität Kiel, Am Botanischen Garten 1–9, 24118, Kiel, Germany

    Sabine Berg, Karin Krupinska & Kirsten Krause

Authors
  1. Sabine Berg
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karin Krupinska
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kirsten Krause
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kirsten Krause.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Berg, S., Krupinska, K. & Krause, K. Plastids of three Cuscuta species differing in plastid coding capacity have a common parasite-specific RNA composition. Planta 218, 135–142 (2003). https://doi.org/10.1007/s00425-003-1082-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-003-1082-8

Keywords

Search

Navigation