Skip to main content
SpringerLink
Log in

Co-occurrence of tannin and tannin-less vacuoles in sensitive plants

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

Abstract

Vacuoles of different types frequently coexist in the same plant cell, but the duality of the tannin/tannin-less vacuoles observed in Mimosa pudica L. is rare. In this plant, which is characterized by highly motile leaves, the development and original features of the double vacuolar compartment were detailed in primary pulvini from the young to the mature leaf stage. In young pulvini, the differentiation of tannin vacuoles first occurred in the epidermis and progressively spread toward the inner cortex. In motor cells of nonmotile pulvini, tannin deposits first lined the membranes of small vacuole profiles and then formed opaque clusters that joined together to form a large tannin vacuole (TV), the proportion of which in the cell was approximately 45 %. At this stage, transparent vacuole profiles were rare and small, but as the parenchyma cells enlarged, these profiles coalesced to form a transparent vacuole with a convexity toward the larger-sized tannin vacuole. When leaf motility began to occur, the two vacuole types reached the same relative proportion (approximately 30 %). Finally, in mature cells displaying maximum motility, the large transparent colloidal vacuole (CV) showed a relative proportion increasing to approximately 50 %. At this stage, the proportion of the tannin vacuole, occurring in the vicinity of the nucleus, decreased to approximately 10 %. The presence of the condensed type of tannins (proanthocyanidins) was proven by detecting their fluorescence under UV light and by specific chemical staining. This dual vacuolar profile was also observed in nonmotile parts of M. pudica (e.g., the petiole and the stem). Additional observations of leaflet pulvini showing more or less rapid movements showed that this double vacuolar structure was present in certain plants (Mimosa spegazzinii and Desmodium gyrans), but absent in others (Albizzia julibrissin, Biophytum sensitivum, and Cassia fasciculata). Taken together, these observations strongly suggest that a direct correlation cannot be found between the presence of a tannin vacuole and the osmoregulated motility of pulvini.

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

CV:

Colloidal vacuole

HPF:

High-pressure freezing

PAs:

Proanthocyanidins

TEM:

Transmission electron microscopy

TV:

Tannin vacuole

References

  • Abrahams S, Tanner GJ, Larkin PJ, Ashton AR (2002) Identification and biochemical characterization of mutants in the proanthocyanidin pathway in Arabidopsis. Plant Physiol 130:561–573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barahona-Rosales R (1999) Condensed tannins in tropical forage legumes: their characterization and study of their nutritional impact from the standpoint of structure-activity relationships. PHD, Reading, Kansas State Univ

  • Brillouet JM, Romieu C, Schoefs B, Solymosi K, Cheynier V, Fulcrand H, Verdeil JL, Conéjéro G (2013) The tannosome is an organelle forming condensed tannins in the chlorophyllous organs of Tracheophyta. Ann Bot 112:1003–1014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buer CS, Imin N, Djordjevic MA (2010) Flavonoids: new roles for old molecules. J Integr Plant Biol 52:98–111

    Article  CAS  PubMed  Google Scholar 

  • Campbell NA, Garber RC (1980) Vacuolar reorganization in the motor cells of Albizzia during leaf movement. Planta 148:251–255

    Article  CAS  PubMed  Google Scholar 

  • Campbell NA, Thomson WW (1977) Multivacuolate motor cells in Mimosa L. Ann Bot 41:1361–1362

    Google Scholar 

  • Campbell NA, Stika KM, Morrison GH (1979) Calcium and potassium in the motor organs of the sensitive plant: localization by ion microscopy. Science 204:181–186

    Article  Google Scholar 

  • Chafe SC, Durzan DJ (1973) Tannin inclusions in cell suspensions cultures of white spruce. Planta 113:251–262

    Article  CAS  PubMed  Google Scholar 

  • Debeaujon I, Nesi N, Perez P, Devic M, Grandjean O, Caboche C, Lepiniec L (2003) Proanthocyanidin-accumulating cells in Arabidopsis testa: regulation of differentiation and role in seed development. Plant Cell 15:2514–2531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dédaldéchamp F, Uhel C (1999) Induction of anthocyanin synthesis in nonpigmented grape cell suspensions by acting on DFR substrate availability or precursors level. Enzym Microb Technol 25:316–321

    Article  Google Scholar 

  • Diaz AM, Caldas GV, Blair MW (2010) Concentrations of condensed tannins and anthocyanins in common bean seed coats. Food Res Int 43:595–601

    Article  CAS  Google Scholar 

  • Diekmann W, Hedrich R, Raschke K, Robinson DG (1993) Osmocytosis and vacuolar fragmentation in guard cell protoplasts: their relevance to osmotically-induced volume changes in guard cells. J Exp Bot 44:1569–1577

    Article  Google Scholar 

  • Dixon RA, Liu C, Jun H (2013) Metabolic engineering of anthocyanins and condensed tannins in plants. Curr Opin Biotechnol 24:329–335

    Article  CAS  PubMed  Google Scholar 

  • Downey MO, Dokoozlian NK, Krstic MP (2006) Cultural practice and environmental impacts on the flavonoid composition of grapes and wine: a review of recent research. Am J Enol Vitic 57:257–268

    CAS  Google Scholar 

  • Erdei L, Szabo-Nagy A, Lazlavir M (1994) Effects of tannins and phenolics on the H+-ATPase activity in plant plasma membrane. J Plant Physiol 144:49–52

    Article  CAS  Google Scholar 

  • Esau K (1965) Plant anatomy, 2nd edn. J Wiley and Sons, New-York

    Google Scholar 

  • Feucht W, Treutter D, Polster J (2004) Flavanol binding of nuclei from tree species. Plant Cell Rep 22:430–436

    Article  CAS  PubMed  Google Scholar 

  • Feucht W, Treutter D, Dithmar H, Polster J (2008) Microspore development of three coniferous species: affinity of nuclei for flavonoids. Tree Physiol 28:1783–1791

    Article  PubMed  Google Scholar 

  • Feucht W, Schmid M, Treutter D (2011) Nuclei of Tsuga canadensis: role of flavanols in chromatin organization. Int J Mol Sci 12:6834–6855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fleurat-Lessard P (1981) Ultrastructural features of the starch sheath cells of the primary pulvinus after gravistimulation of the sensitive plant (Mimosa pudica L.). Protoplasma 105:177–184

    Article  Google Scholar 

  • Fleurat-Lessard P (1988) Structural and ultrastructural features of cortical cells in motor organs of sensitive plants. Biol Rev 63:1–22

    Article  Google Scholar 

  • Fleurat-Lessard P (1990) Structure and ultrastructure of the pulvinus in nyctinastic legumes. In: RL Satter, HL Gorton, TC Vogelmann (eds) The pulvinus motor organ for leaf movement. Am Soc Plant Physiol, pp 101–129

  • Fleurat-Lessard P, Millet B (1984) Ultrastructural features of cortical parenchyma cells (motor cells) in stamen filaments of Berberis canadensis Mill. and tertiary pulvini of Mimosa pudica. J Exp Bot 35:1332–1341

    Article  Google Scholar 

  • Fleurat-Lessard P, Satter R (1985) Relationship between structure and motility of Albizzia motor organs: changes in ultrastructure of cortical cells during dark-induced closure. Protoplasma 128:72–79

    Article  Google Scholar 

  • Fleurat-Lessard P, Schmitt AC, Vantard M, Stoeckel H, Roblin G (1993) Characterization and immunocytochemical distribution of microtubules and F-actin filaments in protoplasts of Mimosa pudica motor cells. Plant Physiol Biochem 31:757–764

    CAS  Google Scholar 

  • Fleurat-Lessard P, Frangne N, Maeshima M, Ratajczak R, Bonnemain JL, Martinoia E (1997) Increased expression of vacuolar aquaporin and H+ ATPase related to motor cell function in Mimosa pudica L. Plant Physiol 114:827–834

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gao XQ, Li CG, Wei PC, Zhang XY, Chen J, Wang XC (2005) The dynamic changes of tonoplasts in guard cells are important for stomatal movement in Vicia faba. Plant Physiol 139:1207–1216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grundhöfer P, Gross GG (2001) Immunocytochemical studies on the origin and deposition sites of hydrolysable tannins. Plant Sci 160:987–995

    Article  PubMed  Google Scholar 

  • Hollins DL, Jaffé MJ (1997) On the role of tannin vacuoles in several nastic leaf responses. Protoplasma 199:215–222

    Article  CAS  Google Scholar 

  • Imaji A, Seiwa K (2010) Carbon allocation to defense, storage and growth in seedlings of two temperate broad-leaves tree species. Oecologia 162:273–281

    Article  PubMed  Google Scholar 

  • Kanzawa N, Hoshino Y, Chiba M, Hoshino D, Kobayashi H, Kamasawa N, Kishi Y, Osumi M, Sameshima M, Tsuchiya T (2006) Change in the actin cytoskeleton during seismonastic movement of Mimosa pudica. Plant Cell Physiol 47:531–539

    Article  CAS  PubMed  Google Scholar 

  • Kumon K, Suda S (1984) Ionic fluxes from pulvinar cells during the rapid movement of Mimosa pudica L. Plant Cell Physiol 25:975–979

  • Lacampagne S (2010) Localisation et caractérisation des tannins dans la pellicule du raisin: etude de l’impact de l’organisation physico-chimique des parois cellulaires sur la composante tannique, la qualité du fruit et la typicité des raisins de Bordeaux. Thèse Doct. Université, Bordeaux 2

  • Lattandio V, Lattandio VMT, Cardinali A (2006) Role of phenolics in the resistance mechanisms of plants against fungal pathogens and insects. In: Filippo Imperato (ed) Phytochemistry. Advances in research, pp 23–67

  • Lazzaro MD, Thomson WW (1996) The vacuolar-tubular continuum in living trichomes of chickpea (Cicer arietinum) provides a rapid means of solute delivery from base to tip. Protoplasma 193:181–190

    Article  Google Scholar 

  • Li LJ, Ren F, Gao XQ, Wei PC, Wang XC (2012) The reorganization of actin filaments is required for vacuolar fusion of guard cells during stomatal opening in Arabidopsis. Plant Cell Environ 36:484–497

    Article  PubMed  Google Scholar 

  • Martinoia E, Maeshima M, Neuhaus HE (2007) Vacuolar transporters and their essential role in plant metabolism. J Exp Bot 58:83–102

    Article  CAS  PubMed  Google Scholar 

  • Martinoia H, Meyer S, De Angeli A, Nagy R (2012) Vacuolar transporters in their physiological context. Annu Rev Plant Biol 63:183–213

    Article  CAS  PubMed  Google Scholar 

  • Marty F (1978) Cytochemical studies on GERL, provacuoles, and vacuoles in root meristematic cells of Euphorbia. Proc Natl Acad Sci U S A 75:852–856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marty F (1999) Plant vacuoles. Plant Cell 11:587–599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miranda M, Ralph SG, Mellway R, White R, Heath MC, Bohlmann J, Constabel CP (2007) The transcriptional response of hybrid poplar (Populus trichocarpa x P. deltoids) to infection by Melampsora medusae leaf rust involves induction of flavonoid pathway genes leading to the accumlulation of proanthocyanidins. Mol Plant-Microbe Interact 20:816–831

    Article  CAS  PubMed  Google Scholar 

  • Moran N (2007) Osmoregulation of leaf motor cells. FEBS Lett 581:2337–2347

    Article  CAS  PubMed  Google Scholar 

  • Morse MJ, Satter RL (1979) Relationship between motor cell ultrastructure and leaf movements in Samanea saman. Physiol Plant 46:338–346

    Article  Google Scholar 

  • Moysset L, Simons E (1991) Secondary pulvinus of Robinia pseudoacacia (Leguminosae): structural and ultrastructural features. Am J Bot 78:1467–1486

    Article  Google Scholar 

  • Murakami S, Isobe Y, Kijima H, Nagai H, Muramatu M, Otomo S (1991) Inhibition of gastric H+, K+-ATPase and acid secretion by ellagic acid. Planta Med 57:305–308

    Article  CAS  PubMed  Google Scholar 

  • Paris N, Stanley M, Jones RL, Rogers JC (1996) Plant cells contain two functionally distinct vacuolar compartments. Cell 85:563–572

    Article  CAS  PubMed  Google Scholar 

  • Peters DJ, Constabel CP (2002) Molecular analysis of herbivore induced condensed tannin synthesis: cloning and expression of dihydroflavonol reductase from trembling aspen (Populus tremuloides). Plant J 32:701–712

    Article  CAS  PubMed  Google Scholar 

  • Pinelo M, Arnous A, Meyer AS (2006) Upgrading of grape skins: significance of plant cell-wall structural components and extraction techniques for phenol release. Trends Food Sci Technol 17:579–590

    Article  CAS  Google Scholar 

  • Reisen D, Marty F, Leborgne-Castel N (2005) New insights into the tonoplast architecture of plant vacuoles and vacuolar dynamics during osmotic stress. BMC Plant Biol 5:1–13

    Article  Google Scholar 

  • Robbins MP, Paolocciz F, Hughes JW, Turchettiz V, Allison G, Arcioniz S, Morris P, Damianiz F (2003) Sn, a maize bHLH gene, modulates anthocyanin and condensed tannin pathways in Lotus corniculatus. J Exp Bot 54:234–248

    Article  Google Scholar 

  • Robert D, Roland JC (1989) Les vacuoles. In: Doin (ed) Biologie Végétale, Tome I, chap IV, pp 191–238

  • Roblin G (1979) Mimosa pudica: a model for the study of the excitability in plants. Biol Rev 54:135–153

    Article  Google Scholar 

  • Rogers JC (2008) Multiple vacuoles in plant cells. Plant Physiol 146:1024–1027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Samejima M, Sibaoka T (1980) Changes in the extracellular ion concentration in the main pulvinus of Mimosa pudica during rapid movement and recovery. Plant Cell Physiol 21:467–479

    CAS  Google Scholar 

  • Satter R (1979) Movements using turgor mechanisms. Leaf movements and tendril curling. In: Haupt W, Feinleib M (eds) Encyclopedia of plant physiology, physiology of movements, vol 7. Springer-Verlag, Berlin, pp 442–484

    Google Scholar 

  • Satter R, Galston AW (1981) Mechanism of control of leaf movements. Annu Rev Plant Physiol 32:83–110

    Article  CAS  Google Scholar 

  • Satter R, Schrempf M, Chaudri J, Galston AW (1977) Phytochrome and circadian clocks in Samanea. Rhythmic redistribution of potassium and chloride within the pulvinus during long dark periods. Plant Physiol 59:231–235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terrier N, Torregrosa L, Ageorges A, Vialte S, Verriés C, Cheynier V, Romieu C (2009) Ectopic expression of VvMybPA2 promotes proanthocyanidin biosynthesis in grapevine and suggests additional targets in the pathway. Plant Physiol 149:1028–1041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thiery JP (1967) Mise en évidence des polysaccharides sur coupes fines en microscopie électronique. J Microsc 6:987–1018

    CAS  Google Scholar 

  • Toriyama H (1955) Observational and experimental studies on sensitive plants V- The development of the tannin vacuole in the motor cell of the pulvinus. Bot Mag Tokyo 68:204–208

    Article  Google Scholar 

  • Toriyama H (1957) Observational and experimental studies on sensitive plants VII-Vital staining of the thread like apparatus. Cytologia 22:60–68

    Article  Google Scholar 

  • Toriyama H (1967a) Distribution of tannins vacuoles in the main pulvinus of Mimosa pudica L. Proc Jpn Acad 43:384–388

    Google Scholar 

  • Toriyama H (1967b) On the relation between tannin vacuoles and protoplasm in the motor cell of Mimosa pudica L. Proc Jpn Acad 43:777–782

    Google Scholar 

  • Toriyama H, Jaffé MJ (1972) Migration of Calcium and its role in the regulation of seismonasty in the motor cell of Mimosa pudica L. Plant Physiol 49:72–81

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toriyama H, Komada Y (1971) The recovery process of the tannin vacuole in the motor cell of Mimosa pudica L. Cytologia 36:690–697

    Article  CAS  Google Scholar 

  • Turnquist HM, Allen NS, Jaffé MJ (1993) A Pharmalogical study of calcium flux mechanisms in the tannin vacuoles of Mimosa pudica L. motor cells. Protoplasma 176:91–99

    Article  CAS  Google Scholar 

  • Valtaud C, Thibault F, Larignon P, Bertsch C, Fleurat-Lessard P, Bourbouloux A (2011) Systemic damage in leaf metabolism caused by esca infection in grapevines. Aust J Grape Wine Res 17:101–110

    Article  Google Scholar 

  • Visnovitz T, Vilàgi I, Carro P, Kristol Z (2007) Mechanoreceptor cells on the tertiary pulvini of Mimosa pudica L. Plant Signal Behav 2:462–466

    Article  PubMed  PubMed Central  Google Scholar 

  • Wardrop AB, Cronshaw J (1962) Formation of phenolic substances in the ray parenchyma of angiosperms. Nature 193:90–92

    Article  CAS  Google Scholar 

  • Weston LA, Mathesius U (2013) Flavonoids: their structure, biosynthesis and role in the rhizosphere, including allelopathy. J Chem Ecol 39:283–297

    Article  CAS  PubMed  Google Scholar 

  • Whitecross MI, Plovanic N (1982) Structure of the motor region of pulvinules of Desmodium gyrans leaflet. Micron 13:337–338

    Google Scholar 

  • Zhang C, Hicks GR, Raikhel N (2014) Plant morphology and vacuolar trafficking. Plant Sci 5:1–9

    Google Scholar 

Download references

Acknowledgments

The authors are grateful to JM. Pérault, F. Thibault, and B. Merceron for skillful technical assistance.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Laboratoire EBI (Ecologie et Biologie des Interactions), UMR CNRS 7267, Equipe SÈVE (Sucres & Échanges Végétaux- Environnement), Université de Poitiers, Bât. B 31, 3 rue Jacques Fort, TSA 51106, 86073, Poitiers Cedex 9, France

    Pierrette Fleurat-Lessard, Magali Lallemand, Fabienne Dédaldéchamp & Gabriel Roblin

  2. Image UP, Service de Microscopie Electronique et Photonique, Pôle Biologie Santé, Université de Poitiers, 1 rue Georges Bonnet, TSA 51106, Poitiers Cedex 9, France

    Emile Béré

Authors
  1. Pierrette Fleurat-Lessard
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emile Béré
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Magali Lallemand
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fabienne Dédaldéchamp
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gabriel Roblin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fabienne Dédaldéchamp.

Additional information

Handling Editor: Friedrich W. Bentrup

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fleurat-Lessard, P., Béré, E., Lallemand, M. et al. Co-occurrence of tannin and tannin-less vacuoles in sensitive plants. Protoplasma 253, 821–834 (2016). https://doi.org/10.1007/s00709-015-0844-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-015-0844-z

Keywords

Search

Navigation