Skip to main content
SpringerLink
Log in

S-like ribonuclease gene expression in carnivorous plants

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

Abstract

Functions of S-like ribonucleases (RNases) differ considerably from those of S-RNases that function in self-incompatibility. Expression of S-like RNases is usually induced by low nutrition, vermin damage or senescence. However, interestingly, an Australian carnivorous plant Drosera adelae (a sundew), which traps prey with a sticky digestive liquid, abundantly secretes an S-like RNase DA-I in the digestive liquid even in ordinary states. Here, using D. adelae, Dionaea muscipula (Venus flytrap) and Cephalotus follicularis (Australian pitcher plant), we show that carnivorous plants use S-like RNases for carnivory: the gene da-I encoding DA-I and its ortholog cf-I of C. follicularis are highly expressed and constitutively active in each trap/digestion organ, while the ortholog dm-I of D. muscipula becomes highly active after trapping insects. The da-I promoter is unmethylated only in its trap/digestion organ, glandular tentacles (which comprise a small percentage of the weight of the whole plant), but methylated in other organs, which explains the glandular tentacles-specific expression of the gene and indicates a very rare gene regulation system. In contrast, the promoters of dm-I, which shows induced expression, and cf-I, which has constitutive expression, were not methylated in any organs examined. Thus, it seems that the regulatory mechanisms of the da-I, dm-I and cf-I genes differ from each other and do not correlate with the phylogenetic relationship. The current study suggests that under environmental pressure in specific habitats carnivorous plants have managed to evolve their S-like RNase genes to function in carnivory.

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. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

FIS2:

FERTILIZATION INDEPENDENT SEED2

FWA:

FLOWERING WAGENINGEN

MPC:

MATERNALLY EXPRESSED PAB C-TERMINALLY

PAGE:

Polyacrylamide gel electrophoresis

RNase:

Ribonuclease

References

  • Abel S, Köck M (2001) Secretory acid ribonucleases from tomato, Lycopersicon esculentum Mill. Methods Enzymol 341:351–368

    Article  PubMed  CAS  Google Scholar 

  • Albert VA, Williams SE, Chase MW (1992) Carnivorous plants: phylogeny and structural evolution. Science 257:1491–1495

    Article  PubMed  CAS  Google Scholar 

  • Aravind L, Koonin EV (2001) A natural classification of ribonucleases. Methods Enzymol 341:3–28

    Article  PubMed  CAS  Google Scholar 

  • Bariola PA, Howard CJ, Taylor CB, Verburg MT, Jaglan VD, Green PJ (1994) The Arabidopsis ribonuclease gene RNS1 is tightly controlled in response to phosphate limitation. Plant J 6:673–685

    Article  PubMed  CAS  Google Scholar 

  • Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16:6–21

    Article  PubMed  CAS  Google Scholar 

  • Darwin C (1875) Insectivorous plants. John Murray, London

    Book  Google Scholar 

  • Dodds PN, Clarke AE, Newbigin E (1996) Molecular characterisation of an S-like RNase of Nicotiana alata that is induced by phosphate starvation. Plant Mol Biol 31:227–238

    Article  PubMed  CAS  Google Scholar 

  • Ellison AM, Gotelli NJ (2009) Energetics and the evolution of carnivorous plants—Darwin’s ‘most wonderful plants in the world’. J Exp Bot 60:19–42

    Article  PubMed  CAS  Google Scholar 

  • Hayashi T, Kobayashi D, Kariu T, Tahara M, Hada K, Kouzuma Y, Kimura M (2003) Genomic cloning of ribonucleases in Nicotiana glutinosa leaves, as induced in response to wounding or to TMV-infection, and characterization of their promoters. Biosci Biotechnol Biochem 67:2574–2583

    Article  PubMed  CAS  Google Scholar 

  • Henderson IR, Jacobsen SE (2007) Epigenetic inheritance in plants. Nature 447:418–424

    Article  PubMed  CAS  Google Scholar 

  • Jost W, Bak H, Glund K, Terpstra P, Beintema JJ (1991) Amino acid sequence of an extracellular, phosphate-starvation-induced ribonuclease from cultured tomato (Lycopersicon esculentum) cells. Eur J Biochem 198:1–6

    Article  PubMed  CAS  Google Scholar 

  • Jullien PE, Kinoshita T, Ohad N, Berger F (2006) Maintenance of DNA methylation during the Arabidopsis life cycle is essential for parental imprinting. Plant Cell 18:1360–1372

    Article  PubMed  CAS  Google Scholar 

  • Juniper BE, Robins RJ, Joel DM (1989) The carnivorous plants. Academic Press, London

    Google Scholar 

  • Kao T, Huang S (1994) Gametophytic self-incompatibility: a mechanism for self/nonself discrimination during sexual reproduction. Plant Physiol 105:461–466

    PubMed  CAS  Google Scholar 

  • Kariu T, Sano K, Shimokawa H, Itoh R, Yamasaki N, Kimura M (1998) Isolation and characterization of a wound-inducible ribonuclease from Nicotiana glutinosa leaves. Biosci Biotechnol Biochem 62:1144–1151

    Article  PubMed  CAS  Google Scholar 

  • Kinoshita T, Miura A, Choi Y, Kinoshita Y, Cao X, Jacobsen SE, Fischer RL, Kakutani T (2004) One-way control of FWA imprinting in Arabidopsis endosperm by DNA methylation. Science 303:521–523

    Article  PubMed  CAS  Google Scholar 

  • Köck M, Groß N, Stenzel I, Hause G (2004) Phloem-specific expression of the wound-inducible ribonuclease LE from tomato (Lycopersicon esculentum cv. Lukullus). Planta 219:233–242

    Article  PubMed  Google Scholar 

  • Lauria M, Rossi V (2011) Epigenetic control of gene regulation in plants. Biochim Biophys Acta 1809:369–378

    Article  PubMed  CAS  Google Scholar 

  • LeBrasseur ND, MacIntosh GC, Pérez-Amador MA, Saitoh M, Green PJ (2002) Local and systemic wound-induction of RNase and nuclease activities in Arabidopsis: RNS1 as a marker for a JA-independent systemic signaling pathway. Plant J 29:393–403

    Article  PubMed  CAS  Google Scholar 

  • Luhtala N, Parker R (2010) T2 family ribonucleases: ancient enzymes with diverse roles. Trends Biochem Sci 35:253–259

    Article  PubMed  CAS  Google Scholar 

  • Ma R-C, Oliveira MM (2000) The RNase PD2 gene of almond (Prunus dulcis) represents an evolutionarily distinct class of S-like RNase genes. Mol Gen Genet 263:925–933

    Article  PubMed  CAS  Google Scholar 

  • Ochman H, Gerber AS, Hartl DL (1988) Genetic applications of an inverse polymerase chain reaction. Genetics 120:621–623

    PubMed  CAS  Google Scholar 

  • Okabe T, Iwakiri Y, Mori H, Ogawa T, Ohyama T (2005a) An S-like ribonuclease gene is used to generate a trap-leaf enzyme in the carnivorous plant Drosera adelae. FEBS Lett 579:5729–5733

    Article  PubMed  CAS  Google Scholar 

  • Okabe T, Futatsuya C, Tanaka O, Ohyama T (2005b) Structural analysis of the gene encoding Drosera adelae S-like ribonuclease DA-I. J Adv Sci 17:218–224

    Article  CAS  Google Scholar 

  • Rubio V, Linhares F, Solano R, Martín AC, Iglesias J, Leyva A, Paz-Ares J (2001) A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev 15:2122–2133

    Article  PubMed  CAS  Google Scholar 

  • Schulze WX, Sanggaard KW, Kreuzer I, Knudsen AD, Bemm F, Thøgersen IB, Bräutigam A, Thomsen LR, Schliesky S, Dyrlund TF, Escalante-Perez M, Becker D, Schultz J, Karring H, Weber A, Højrup P, Hedrich R, Enghild JJ (2012) The protein composition of the digestive fluid from the Venus flytrap sheds light on prey digestion mechanisms. Mol Cell Proteomics 11:1306–1319

    Article  PubMed  Google Scholar 

  • Shiba H, Kakizaki T, Iwano M, Tarutani Y, Watanabe M, Isogai A, Takayama S (2006) Dominance relationships between self-incompatibility alleles controlled by DNA methylation. Nat Genet 38:297–299

    Article  PubMed  CAS  Google Scholar 

  • Tanaka N, Arai J, Inokuchi N, Koyama T, Ohgi K, Irie M, Nakamura KT (2000) Crystal structure of a plant ribonuclease, RNase LE. J Mol Biol 298:859–873

    Article  PubMed  CAS  Google Scholar 

  • Taylor CB, Bariola PA, delCardayré SB, Raines RT, Green PJ (1993) RNS2: a senescence-associated RNase of Arabidopsis that diverged from the S-RNases before speciation. Proc Natl Acad Sci USA 90:5118–5122

    Article  PubMed  CAS  Google Scholar 

  • Tiwari S, Schulz R, Ikeda Y, Dytham L, Bravo J, Mathers L, Spielman M, Guzmán P, Oakey RJ, Kinoshita T, Scott RJ (2008) Maternally expressed pab c-terminal, a novel imprinted gene in Arabidopsis, encodes the conserved C-terminal domain of polyadenylate binding proteins. Plant Cell 20:2387–2398

    Article  PubMed  CAS  Google Scholar 

  • Van Nerum I, Certal AC, Oliveira MM, Keulemans J, Broothaerts W (2000) PD1, an S-like RNase gene from a self-incompatible cultivar of almond. Plant Cell Rep 19:1108–1114

    Article  Google Scholar 

  • Website of Botanical Society of America (2013). http://www.botany.org. (see: RESOURCE/Carnivorous Plants/Insectivorous Plants) Accessed 3 Mar 2013

  • Wei J-Y, Li A-M, Li Y, Wang J, Liu X-B, Liu L-S, Xu Z-F (2006) Cloning and characterization of an RNase-related protein gene preferentially expressed in rice stems. Biosci Biotechnol Biochem 70:1041–1045

    Article  PubMed  CAS  Google Scholar 

  • Ye Z-H, Droste DL (1996) Isolation and characterization of cDNAs encoding xylogenesis-associated and wounding-induced ribonucleases in Zinnia elegans. Plant Mol Biol 30:697–709

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW-L, Chen H, Henderson IR, Shinn P, Pellegrini M, Jacobsen SE, Ecker JR (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126:1189–1201

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by a research grant from the Ministry of Education, Culture, Sports, Science and Technology of Japan (MEXT) to T.O.

Author information

Authors and Affiliations

  1. Major in Integrative Bioscience and Biomedical Engineering, Graduate School of Science and Engineering, Waseda University, 2-2 Wakamatsu-cho, Shinjuku-ku, Tokyo, 162-8480, Japan

    Emi Nishimura, Reina Kodaira, Marina Kume, Naoki Arai & Takashi Ohyama

  2. Department of Biology, Faculty of Education and Integrated Arts and Sciences, Waseda University, 2-2 Wakamatsu-cho, Shinjuku-ku, Tokyo, 162-8480, Japan

    Minako Kawahara, Jun-ichi Nishikawa & Takashi Ohyama

Authors
  1. Emi Nishimura
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Minako Kawahara
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Reina Kodaira
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marina Kume
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Naoki Arai
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jun-ichi Nishikawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Takashi Ohyama
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Takashi Ohyama.

Additional information

The nucleotide sequences reported in this paper have been submitted to DDBJ under accession numbers AB811227, AB811228, AB811229, AB811230 and AB811231.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 1158 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nishimura, E., Kawahara, M., Kodaira, R. et al. S-like ribonuclease gene expression in carnivorous plants. Planta 238, 955–967 (2013). https://doi.org/10.1007/s00425-013-1945-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-013-1945-6

Keywords

Search

Navigation