S-like ribonuclease gene expression in carnivorous plants

Emi Nishimura, Minako Kawahara, Reina Kodaira, Marina Kume, Naoki Arai, Jun ichi Nishikawa, Takashi Ohyama

    Research output: Contribution to journalArticle

    11 Citations (Scopus)

    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.

    Original languageEnglish
    Pages (from-to)955-967
    Number of pages13
    JournalPlanta
    Volume238
    Issue number5
    DOIs
    Publication statusPublished - 2013 Nov

    Fingerprint

    carnivorous plants
    ribonucleases
    Dionaea muscipula
    Carnivory
    Droseraceae
    Drosera
    Gene Expression
    gene expression
    traps
    carnivores
    Cephalotus
    genes
    digestion
    promoter regions
    Genes
    Digestion
    liquids
    Mebendazole
    Pancreatic Ribonuclease
    trapping

    Keywords

    • Cephalotus follicularis
    • Dionaea muscipula
    • DNA methylation
    • Drosera adelae
    • T2 family ribonucleases
    • Transcription

    ASJC Scopus subject areas

    • Plant Science
    • Genetics

    Cite this

    Nishimura, E., Kawahara, M., Kodaira, R., Kume, M., Arai, N., Nishikawa, J. I., & Ohyama, T. (2013). S-like ribonuclease gene expression in carnivorous plants. Planta, 238(5), 955-967. https://doi.org/10.1007/s00425-013-1945-6

    S-like ribonuclease gene expression in carnivorous plants. / Nishimura, Emi; Kawahara, Minako; Kodaira, Reina; Kume, Marina; Arai, Naoki; Nishikawa, Jun ichi; Ohyama, Takashi.

    In: Planta, Vol. 238, No. 5, 11.2013, p. 955-967.

    Research output: Contribution to journalArticle

    Nishimura, E, Kawahara, M, Kodaira, R, Kume, M, Arai, N, Nishikawa, JI & Ohyama, T 2013, 'S-like ribonuclease gene expression in carnivorous plants', Planta, vol. 238, no. 5, pp. 955-967. https://doi.org/10.1007/s00425-013-1945-6
    Nishimura E, Kawahara M, Kodaira R, Kume M, Arai N, Nishikawa JI et al. S-like ribonuclease gene expression in carnivorous plants. Planta. 2013 Nov;238(5):955-967. https://doi.org/10.1007/s00425-013-1945-6
    Nishimura, Emi ; Kawahara, Minako ; Kodaira, Reina ; Kume, Marina ; Arai, Naoki ; Nishikawa, Jun ichi ; Ohyama, Takashi. / S-like ribonuclease gene expression in carnivorous plants. In: Planta. 2013 ; Vol. 238, No. 5. pp. 955-967.
    @article{ccc481aa53444baeb6de2bd146785ad6,
    title = "S-like ribonuclease gene expression in carnivorous plants",
    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.",
    keywords = "Cephalotus follicularis, Dionaea muscipula, DNA methylation, Drosera adelae, T2 family ribonucleases, Transcription",
    author = "Emi Nishimura and Minako Kawahara and Reina Kodaira and Marina Kume and Naoki Arai and Nishikawa, {Jun ichi} and Takashi Ohyama",
    year = "2013",
    month = "11",
    doi = "10.1007/s00425-013-1945-6",
    language = "English",
    volume = "238",
    pages = "955--967",
    journal = "Planta",
    issn = "0032-0935",
    publisher = "Springer Verlag",
    number = "5",

    }

    TY - JOUR

    T1 - S-like ribonuclease gene expression in carnivorous plants

    AU - Nishimura, Emi

    AU - Kawahara, Minako

    AU - Kodaira, Reina

    AU - Kume, Marina

    AU - Arai, Naoki

    AU - Nishikawa, Jun ichi

    AU - Ohyama, Takashi

    PY - 2013/11

    Y1 - 2013/11

    N2 - 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.

    AB - 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.

    KW - Cephalotus follicularis

    KW - Dionaea muscipula

    KW - DNA methylation

    KW - Drosera adelae

    KW - T2 family ribonucleases

    KW - Transcription

    UR - http://www.scopus.com/inward/record.url?scp=84886431409&partnerID=8YFLogxK

    UR - http://www.scopus.com/inward/citedby.url?scp=84886431409&partnerID=8YFLogxK

    U2 - 10.1007/s00425-013-1945-6

    DO - 10.1007/s00425-013-1945-6

    M3 - Article

    C2 - 23959189

    AN - SCOPUS:84886431409

    VL - 238

    SP - 955

    EP - 967

    JO - Planta

    JF - Planta

    SN - 0032-0935

    IS - 5

    ER -