Skip to main content
SpringerLink
Log in

Light and temperature induce variations in the density and ultrastructure of the secretory spaces in the diesel-tree (Copaifera langsdorffii Desf.—Leguminosae)

  • Original Paper
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Key message

This manuscript shows experimentally that light and temperature significantly influence the density and cellular features of the secretory spaces in C . langsdorffii , an economically important legume tree in Brazil.

Abstract

Copaifera langsdorffii is known for its production of terpenes, which are exploited by several industrial sectors. In this species, secretory cavities and canals are present in seedlings and adult plants and constitute an important defense mechanism against herbivores and pathogens. Evidence suggests that exogenous factors modify the production of secretions in this species; however, the influence of these factors on the secretory system structure is unknown. We investigated the effects of light and temperature on the density of secretory canals and cavities in C. langsdorffii seedlings, and the influence of temperature on the ultrastructure of the epithelial cells. Seedlings were maintained in different light intensities (460, 230, and 46 μmol m−2 s−1) and temperatures (15, 25, and 35 °C) in 3 × 3 combinations. The densities of secretory spaces in epicotyls and eophylls were calculated in cross sections under a light microscope. For ultrastructural studies, samples of eophylls were prepared following the conventional techniques of transmission electron microscopy. Seedlings at 25 °C/230 μmol m−2 s−1 and 25 °C/460 μmol m−2 s−1 showed increased density of cavities and canals, respectively, suggesting an improved protection of the plants in these conditions. Ultrastructurally, the epithelial cells of seedlings observed at 25 °C contained dense cytoplasm rich in organelles, indicating intense secretory activity. At 15 and 35 °C, seedlings showed morphological alterations in mitochondria, plastids, and endoplasmic reticulum. The epithelial cells presented signs of intense lysing at 35 °C, indicating impaired secretory activity. Our data proved that light and temperature can induce alterations in the secretory system of C. langsdorffii seedlings, suggesting changes to their defense system.

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

Similar content being viewed by others

References

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Ann Rev Plant Biol 55:373–399

    Article  CAS  Google Scholar 

  • Cacas J-L (2010) Devil inside: does plant programmed cell death involve the endomembrane system? Plant Cell Environ 33:1453–1473

    CAS  PubMed  Google Scholar 

  • Corrêa MP (1984) Dicionário de plantas úteis do Brasil e das exóticas cultivadas. Ministério da Agricultura, Instituto Brasileiro de Desenvolvimento Florestal, Rio de Janeiro

  • Dünisch O, Bass P (2006) On the origin of intercellular canals in the secondary xylem of selected Meliaceae species. IAWA Bull 27:281–297

    Google Scholar 

  • Evert RF (2006) Esau’s plant anatomy. Meristems, cells and tissues of the plant body—their structure, function and development, 3rd edn. Wiley, New Jersey

  • Eyles A, Davies NW, Mohammed CM (2004) Traumatic oil glands induced by pruning in the wound-associated phloem of Eucalyptus globules: chemistry and histology. Trees 18:204–210

    Article  Google Scholar 

  • Fahn A (1979) Secretory tissues in plants. Academic Press, London

    Google Scholar 

  • Fahn A, Benayoun J (1976) Ultrastructure of resin ducts in Pinus halepensis development, possible sites of resin synthesis, and mode of its elimination from the protoplast. Ann Bot 40:857–863

    Google Scholar 

  • Feibert EB, Langenheim JH (1988) Leaf resin variation in Copaifera langsdorffi: relation to irradiance and herbivory. Phytochemistry 7:2527–2532

    Article  Google Scholar 

  • Franco AC (2002) Ecophysiology of woody plants. In: Oliveira PS, Marquis RJ (eds) The cerrados of Brazil. Columbia University Press, New York, pp 178–197

    Google Scholar 

  • Gamalei YV, Van Bel AJE, Pakhomova MV, Sjutkina V (1994) Effects of temperature on the conformation of the endoplasmic reticulum and on starch accumulation in leaves with the symplastic minor-vein configuration. Planta 194:443–453

    Article  CAS  Google Scholar 

  • Gerrits PO (1991) The application of glycol methacrylate in histotechnology; some fundamental principles. Department of Anatomy and Embryology State University Groningen, The Netherlands

    Google Scholar 

  • Gross D, Parthier B (1994) Novel natural substances acting in plant growth regulation. J Plant Growth Regul 13:93–114

    Article  CAS  Google Scholar 

  • Huang WP, Klionsky DJ (2002) Autophagy in yeast: a review of the molecular machinery. Cell Struct Funct 27:409–420

    Article  CAS  PubMed  Google Scholar 

  • Imlay JA (2003) Pathways of oxidative damage. Ann Rev Microbiol 57:395–418

    Article  CAS  Google Scholar 

  • Ishikawa HA (1996) Ultrastructural features of chilling injury: injured cells and the early events during chilling of suspension-cultured mung bean cells. Am J Bot 83:825–835

    Article  Google Scholar 

  • Johansen DA (1940) Plant Microtechnique. McGraw-Hill, New York

    Google Scholar 

  • Johnson RH, Young BL, Alstad D (1997) Responses of Ponderosa pine growth and volatile terpene concentrations to manipulation of soil water and sunlight availability. Can J For Res 27:1794–1804

    Article  Google Scholar 

  • Kandasamy MK, Kristen U (1989) Ultrastructural responses of tobacco pollen tubes to heat shock. Protoplasma 153:104–110

    Article  Google Scholar 

  • Kilpeläinen A, Gerendiain AZ, Luostarinen K, Peltola H, Kellomäki S (2007) Elevated temperature and CO2 concentration effects on xylem anatomy of Scots pine. Tree Physiol 27:1329–1338

    Article  PubMed  Google Scholar 

  • Köppen W (1931) Climatologia. Fondo de Cultura Econômica, Buenos Aires

    Google Scholar 

  • Langenheim JH (2003) Plant resins: chemistry, evolution, ecology, ethnobotany. Timber Press, Cambridge

    Google Scholar 

  • Langenheim JH, Stubblebine WH (1983) Variation in leaf resin composition between parent tree and progeny in Hymenaea: implications for herbivory in the humid tropics. Biochem Syst Ecol 11:97–106

    Article  CAS  Google Scholar 

  • Langenheim JH, Stubblebine WH, Lincoln DE, Foster CE (1978) Implications of variation in resin composition among organs, tissues and populations in the tropical legume Hymenaea. Biochem Syst Ecol 6:299–313

    Article  CAS  Google Scholar 

  • Langenheim JH, Arrhenius SP, Nascimento JC (1981) Relationship of light intensity to leaf resin composition and yield in the tropical leguminous genera Hymenaea and Copaifera. Biochem Syst Ecol 9:27–37

    Article  Google Scholar 

  • Langenheim JH, Clovis CL, Macedo CA, Stubblebine WH (1986) Hymenae and Copaifera leaf sesquiterpenes in relation to Lepidopteran herbivory in southeastern Brazil. Biochem Syst Ecol 14:41–49

    Article  CAS  Google Scholar 

  • Leite AMC, Lleras E (1993) Áreas prioritárias na Amazônia para a conservação dos recursos genéticos de espécies florestais nativas: fase preliminar. Acta Bot Bras 7:61–94

    Google Scholar 

  • Leite AMC, Salomão AN (1992) Estrutura populacional de regenerantes de copaíba (Copaifera langsdorffii Desf.) em mata ciliar do Distrito Federal. Acta Bot Bras 6:123–133

    Article  Google Scholar 

  • Li D-M, Guo Y-K, Li Q, Zhang J, Wang X-J, Bai J-G (2012) The pretreatment of cucumber with methyl jasmonate regulates antioxidant enzyme activities and protects chloroplast and mitochondrial ultrastructure in chilling-stressed leaves. Sci Hortic 143:135–143

    Article  CAS  Google Scholar 

  • Lin J, Sampson DA, Ceulemans R (2001) The effect of crown position and tree age on resin-canal density in Scots pine (Pinus sylvestris L.) needles. Can J Bot 79:1257–1261

    Google Scholar 

  • Lorenzi H (1998) Árvores Brasileiras: Manual de identificação e cultivo de plantas arbóreas nativas do Brasil. Plantarum, Nova Odessa

    Google Scholar 

  • Machado SR, Rodrigues TM (2004) Anatomia e ultra-estrutura do pulvino primário de Pterodon pubescens Benth. (Fabaceae-Faboideae). Rev Bras Bot 27:135–147

    Article  Google Scholar 

  • Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Ann Rev Plant Physiol Plant Mol Biol 50:333–359

    Article  CAS  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Ann Rev Plant Physiol Plant Mol Biol 49:249–279

    Article  CAS  Google Scholar 

  • O’Brien TP, Feder N, McCully ME (1964) Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59:368–373

    Article  Google Scholar 

  • Oliveira DMT (2001) Morfologia comparada de plântulas e plantas jovens de leguminosas arbóreas nativas: espécies de Phaseoleae, Sophoreae, Swartzieae e Tephrosieae. Rev Bras Bot 24:85–97

    Article  Google Scholar 

  • Oliveira-Filho AT, Ratter JA (2002) Vegetation physiognomies and woody flora of the cerrado biome. In: Oliveira PS, Marquis RJ (eds) The cerrados of Brazil: ecology and natural history of a neotropical savanna. Columbia University Press, New York, pp 91–120

    Google Scholar 

  • Paiva EAS, Machado SR (2007) Structural and ultrastructural aspects of ontogenesis and differentiation of resin secretory cavities in Hymenaea stigonocarpa (Fabaceae-Caesalpinioideae) leaves. Nord J Bot 24:423–431

    Article  Google Scholar 

  • Pareek A, Singla SL, Grover A (1997) Short-term salinity and high temperature stress-associated ultrastructure alterations in young leaf cells of Oryza sativa L. Ann Bot 80:629–639

    Article  Google Scholar 

  • Plowden C (2003) Production ecology of copaíba (Copaifera spp.) oleoresin in the eastern Brazilian Amazon. Econ Bot 57:491–501

    Article  Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rigling A, Brühlhart H, Bräke ROU, Foster T, Schweingruber FH (2003) Effects of irrigation on diameter growth and vertical resin duct production in Pinus sylvestris L. on dry sites in the central Alps, Switzerland. For Ecol Manag 175:285–296

    Article  Google Scholar 

  • Rodrigues TM, Machado SR (2012) Oil glands in Pterodon pubescens Benth. (Leguminosae-Papilionoideae): distribution, structure and secretion mechanisms. Int J Plant Sci 173:984–992

    Article  Google Scholar 

  • Rodrigues TM, Teixeira SP, Machado SR (2011a) The oleoresin secretory system in seedlings and adult plants of copaíba (Copaifera langsdorffii Desf., Leguminosae-Caesalpinioideae). Flora 206:585–594

    Article  Google Scholar 

  • Rodrigues TM, Santos DC, Machado SR (2011b) The role of the parenchyma sheath and PCD during the development of oil cavities in Pterodon pubescens (Leguminosae-Papilionoideae). Compt Rend Biol 334:535–543

    Article  Google Scholar 

  • Ronquim CC, Prado CHBA, Souza JP (2009) Growth, photosynthesis and leaf water potential in young plants of Copaifera langsdorffii Desf. (Caesalpiniaceae) under contrasting irradiances. Braz J Plant Physiol 21:197–208

    Google Scholar 

  • Sam O, Núñez M, Ruiz-Sánchez MC, Dell’Amico J, Falcón V, De La Rosa MC, Seoane J (2001) Effect of a brassinosteroid analogue and high temperature stress on leaf ultrastructure of Lycopersicon esculentum. Biol Plant 44:213–218

    Article  Google Scholar 

  • Thompson AR, Vierstra RD (2005) Autophagic recycling: lessons from yeast help define the process in plants. Plant Biol 8:165–173

    CAS  Google Scholar 

  • Van Doorn WG, Woltering EJ (2005) Many ways to exit? Cell death categories in plants. Trend Plant Sci 10:117–122

    Article  Google Scholar 

  • Van Doorn WG, Beers EP, Dangl JL, Franklin-Tong VE, Gallois P, Hara-Nishimura I, Jones AM, Kawai-Yamada M, Lam E, Mundy J, Mur LAJ, Petersen M, Smertenko A, Taliansky M, Van Breusegem F, Wolpert T, Woltering E, Zhivotovsky B, Bozhkov PV (2011) Morphological classification of plant cell deaths. Cell Death Differ 18:1241–1246

    Article  PubMed Central  PubMed  Google Scholar 

  • Veiga Júnior VF, Pinto AC (2002) O gênero Copaifera L. Quím Nova 25:273–286

    Article  Google Scholar 

  • Von Arnim A, Deng X (1996) Light control of seedling development. Ann Rev Plant Physiol Plant Mol Biol 47:215–243

    Article  Google Scholar 

  • Wimmer R, Grabner M (1997) Effects of climate on vertical resin duct density and radial growth of Norway spruce (Picea abies (L.) Karst.). Trees 11:271–276

    Google Scholar 

  • Wimmer R, Grabner M (2000) A comparison of tree-ring features in Picea abies as correlated with climate. IAWA 21:403–416

    Article  Google Scholar 

  • Zamski E (1972) Temperature and photoperiodic effects on xylem and vertical resin duct formation in Pinus halepensis Mill. Isr J Bot 21:99–107

    Google Scholar 

  • Zulak KG, Bohlmann J (2010) Terpenoid biosynthesis and specialized vascular cells of conifer defense. J Integr Plant Biol 52:86–97

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank the São Paulo Research Foundation (FAPESP) for financial support (BIOTA 2008/55434-7) and for the Scientific Initiation scholarship to A.C. Coneglian (2010/15153-9); PROPE/UNESP for financial support and for the Scientific Initiation scholarship to D.C. Reis (PROPE Edital 05/2010); CAPES for the Master’s scholarship to P.F.S.M. Buarque; Centro de Microscopia Eletrônica, IBB, for helping to prepare the samples for TEM; and S.R. Machado, IBB, UNESP for valuable suggestions.

Conflict of interest

The authors declare that they have no conflicts of interest.

Author information

Authors and Affiliations

  1. Department of Botany, Institute of Biosciences of Botucatu-IBB, São Paulo State University-UNESP, Botucatu, São Paulo, 18618-970, Brazil

    T. M. Rodrigues, P. F. S. M. Buarque, A. G. Coneglian & D. C. Reis

Authors
  1. T. M. Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. F. S. M. Buarque
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. G. Coneglian
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. D. C. Reis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to T. M. Rodrigues.

Additional information

Communicated by Y. Sano.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rodrigues, T.M., Buarque, P.F.S.M., Coneglian, A.G. et al. Light and temperature induce variations in the density and ultrastructure of the secretory spaces in the diesel-tree (Copaifera langsdorffii Desf.—Leguminosae). Trees 28, 613–623 (2014). https://doi.org/10.1007/s00468-013-0976-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-013-0976-8

Keywords

Search

Navigation