Skip to main content
Log in

Responses of ray parenchyma cells to wounding differ between earlywood and latewood in the sapwood of Cryptomeria japonica

Trees Aims and scope Submit manuscript

Abstract

Key message

Changes in cellular contents of ray parenchyma cells during the formation of reaction zone differ between earlywood and latewood in the sapwood of Cryptomeria japonica.

Abstract

Changes over time in the cellular contents of xylem parenchyma cells provide important clues to the mechanism of the early events in the wound reaction of trees. In this study, we monitored the events that occur during the death of ray parenchyma cells after wounding. We examined nuclei, starch grains, and colored substances in ray parenchyma cells by light microscopy and the autofluorescence of cell walls of tracheids by confocal laser-scanning microscopy in Cryptomeria japonica after artificial wounding. In addition, we compared cytological changes in ray parenchyma cells in the longitudinal and radial directions. Finally, we analyzed the differences between earlywood and latewood in terms of the responses of ray parenchyma cells to wounding. Behind the wound, changes in cellular contents were visible first in latewood regions in the second annual ring behind the wound. The progression of changes in cellular contents of ray parenchyma cells stopped near the growth-ring boundary. These results indicate that the growth-ring boundary might prevent the spread of some factor(s) that induces cytological changes in ray parenchyma cells. Above the wound, most colored substances were localized in ray parenchyma cells that were located near wounds in latewood regions. Thus, even at an equal distance from the wound, the amount of secondary metabolites in ray parenchyma cells differed between earlywood and latewood. Our observations suggest that differences in the anatomical features of neighboring tracheids between earlywood and latewood might influence changes in cellular contents of ray parenchyma cells during reactions to wounding in Cryptomeria japonica.

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

Access this article

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
Fig. 8
Fig. 9
Fig. 10
Fig. 11

References

  • Arbellay E, Corona C, Stoffel M, Fonti P, Decaulne A (2012a) Defining an adequate sample of earlywood vessels for retrospective injury detection in diffuse-porous species. PLoS One 7:e38824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arbellay E, Fonti P, Stoffel M (2012b) Duration and extension of anatomical changes in wood structure after cambial injury. J Exp Bot 63:3271–3277

    Article  CAS  PubMed  Google Scholar 

  • Arbellay E, Stoffel M, Sutherland EK, Smith KT, Falk DA (2014) Changes in tracheid and ray traits in fire scars of North American conifers and their ecophysiological implications. Ann Bot 114:223–232

    Article  PubMed  PubMed Central  Google Scholar 

  • Barnard DM, Lachenbruch B, McCulloh KA, Kitin P, Meinzer FC (2013) Do ray cells provide a pathway for radial water movement in the stems of conifer trees? Am J Bot 100:322–331

    Article  PubMed  Google Scholar 

  • Begum S, Nakaba S, Oribe Y, Kubo T, Funada R (2007) Induction of cambial reactivation by localized heating in a deciduous hardwood hybrid poplar (Populus sieboldii × P. grandidentata). Ann Bot 100:439–447

    Article  PubMed  PubMed Central  Google Scholar 

  • Begum S, Nakaba S, Oribe Y, Kubo T, Funada R (2010) Changes in the localization and levels of starch and lipids in cambium and phloem during cambial reactivation by artificial heating of main stems of Cryptomeria japonica trees. Ann Bot 106:885–895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boddy L, Rayner ADM (1983) Origins of decay in living deciduous trees: the role of moisture content and a re-appraisal of the expanded concept of tree decay. N Phytol 94:623–641

    Article  Google Scholar 

  • Catesson AM (1990) Cambial cytology and biochemistry. In: Iqbal M (ed) The vascular cambium. Research Studies Press, Taunton, pp 63–112

    Google Scholar 

  • Chaffey N, Barlow P (2001) The cytoskeleton facilitates a three-dimensional symplasmic continuum in the long-lived ray and axial parenchyma cells of angiosperm trees. Planta 213:811–823

    Article  CAS  PubMed  Google Scholar 

  • Coutts MP (1976) The formation of dry zones in the sapwood of conifers. I. Induction of drying in standing trees and logs by Fomes annosus and extracts of infected wood. Eur J For Pathol 6:372–381

    Article  Google Scholar 

  • Delvaux C, Sinsin B, Van Damme P, Beeckman H (2010) Wound reaction after bark harvesting: microscopic and macroscopic phenomena in ten medicinal tree species (Benin). Trees 24:941–951

    Article  Google Scholar 

  • Domec JC, Gartner BG (2002) How do water transport and storage differ in coniferous earlywood and latewood? J Exp Bot 53:2369–2379

    Article  CAS  PubMed  Google Scholar 

  • Duchesne LC, Hubbes M, Jeng RS (1992) Biochemistry and molecular biology of defense reaction in the xylem of angiosperm trees. In: Blanchette RA, Biggs AR (eds) Defense mechanisms of woody plants against fungi. Springer, Berlin, pp 133–146

    Chapter  Google Scholar 

  • Fink S (1999) Pathological and regenerative plant anatomy. Encyclopedia of plant anatomy, Part 6, vol 14. Gebrüder Borntraeger, Berlin

  • Hasegawa M, Shiroya M (1966) Translocation and transformation of sucrose in the wood of Prunus yedoensis. Bot Mag Tokyo 79:595–601

    Article  CAS  Google Scholar 

  • Hessburg PF, Hansen EM (1987) Pathological anatomy of black stain root disease of Douglas-fir. Can J Bot 65:962–971

    Article  Google Scholar 

  • Hillis WE (1987) Heartwood and tree exudates. Springer, New York, pp 1–268

    Google Scholar 

  • Imai T, Nomura M (2005) Induction of the biosynthesis of agatharesinol, a norlignan, in sapwood sticks of Cryptomeria japonica under humidity-regulated circumstances. J Wood Sci 51:537–541

    Article  CAS  Google Scholar 

  • Kemp MS, Burden RS (1986) Phytoalexins and stress metabolites in the sapwood of trees. Phytochem 25:1261–1269

    Article  CAS  Google Scholar 

  • Kitin P, Fujii T, Abe H, Takata K (2009) Anatomical features that facilitate radial flow across growth rings and from xylem to cambium in Cryptomeria japonica. Ann Bot 103:1145–1157

    Article  PubMed  PubMed Central  Google Scholar 

  • Kuroda K, Yamashita K, Fujiwara T (2009) Cellular level observation of water loss and the refilling of tracheids in the xylem of Cryptomeria japonica during heartwood formation. Trees 23:1163–1172

    Article  CAS  Google Scholar 

  • Kuroda K, Fujiwara T, Hashida K, Imai T, Kushi M, Saito K, Fukushima K (2014) The accumulation pattern of ferruginol in the heartwood-forming Cryptomeria japonica xylem as determined by time-of-flight secondary ion mass spectrometry and quantity analysis. Ann Bot 113:1029–1036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lev-Yadun S, Aloni R (1995) Differentiation of the ray system in woody plants. Bot Rev 61:45–84

    Article  Google Scholar 

  • Magel EA (2000) Biochemistry and physiology of heartwood formation. In: Savidge R, Barnett J, Napier R (eds) Cell and molecular biology of wood formation. BIOS Scientific Publishers, Oxford, pp 363–376

    Google Scholar 

  • Nakaba S, Begum S, Yamagishi Y, Jin HO, Kubo T, Funada R (2012a) Differences in the timing of cell death, differentiation and function among three different types of ray parenchyma cells in the hardwood Populus sieboldii × P. grandidentata. Trees 26:743–750

    Article  Google Scholar 

  • Nakaba S, Yamagishi Y, Sano Y, Funada R (2012b) Temporally and spatially controlled death of parenchyma cells is involved in heartwood formation in pith regions of branches of Robinia pseudoacacia var. inermis. J Wood Sci 58:69–76

    Article  CAS  Google Scholar 

  • Nakaba S, Sano Y, Funada R (2013) Disappearance of microtubules, nuclei and starch during cell death of ray parenchyma in Abies sachalinensis. IAWA J 34:135–146

    Article  Google Scholar 

  • Nakaba S, Kitin P, Yamagishi Y, Begum S, Kudo K, Nugroho WD, Funada R (2015) Three-dimensional imaging of cambium and secondary xylem cells by confocal laser scanning microscopy. In: Yeung ECT, Stasolla C, Sumner MJ, Huang BQ (eds) Plant microtechniques and protocols. Springer, Berlin, pp 431–465. ISBN 978-3-319-19943-6

    Chapter  Google Scholar 

  • Nakaba S, Arakawa I, Morimoto H, Nakada R, Bito N, Imai T, Funada R (2016) Agatharesinol biosynthesis-related changes of ray parenchyma in sapwood sticks of Cryptomeria japonica during cell death. Planta 243:1225–1236

    Article  CAS  PubMed  Google Scholar 

  • Nobuchi T, Akamatsu Y, Sato K, Harada H (1986) Early response of ray parenchyma cells following wounding in sugi (Cryptomeria japonica D. Don) wood: seasonal changes of discoloration and cytological structure. Bull Kyoto Univ For 57:290–299

    Google Scholar 

  • Ohashi H, Imai T, Yoshida K, Yasue M (1990) Characterization of physiological functions of sapwood: fluctuation of extractives in the withering process of Japanese cedar sapwood. Holzforschung 44:79–86

    Article  CAS  Google Scholar 

  • Ohashi H, Kato N, Imai T, Kawai S (1991) Characterization of physiological functions of sapwood: fluctuation of heartwood extractives in the withering process of Japanese cedar sapwood fed an inhibitor of phenylalanine ammonia-lyase. Holzforschung 45:245–252

    Article  CAS  Google Scholar 

  • Okada N, Hirakawa Y, Katayama Y (2011) Application of activable tracers to investigate radial movement of minerals in the stem of Japanese cedar (Cryptomeria japonica). J Wood Sci 57:421–428

    Article  CAS  Google Scholar 

  • Okada N, Hirakawa Y, Katayama Y (2012) Radial movement of sapwood-injected rubidium into heartwood of Japanese cedar (Cryptomeria japonica) in the growing period. J Wood Sci 58:1–8

    Article  CAS  Google Scholar 

  • Pearce RB (2000) Decay development and its restriction in trees. J Arboric 26:1–11

    Google Scholar 

  • Sauter JJ (2000) Photosynthate allocation to the vascular cambium: fact and problem. In: Savidge R, Barnett J, Napier R (eds) Cell and molecular biology of wood formation. BIOS Scientific Publishers, Oxford, pp 71–83

    Google Scholar 

  • Schmitt U, Liese W (1990) Wound reaction of the parenchyma in Betula. IAWA Bull 11:413–420

    Article  Google Scholar 

  • Shain L (1967) Resistance of sapwood in stems of Loblolly pine to infection by Fomes annosus. Phytopathol 57:1034–1045

    Google Scholar 

  • Shain L (1971) The response of sapwood of Norway spruce to infection by Fomes annosus. Phytopathol 61:301–307

    Article  CAS  Google Scholar 

  • Shain L (1979) Dynamic responses of differentiated sapwood to injury and infection. Phytopathol 69:1143–1147

    Article  Google Scholar 

  • Shigo AL (1984) Compartmentalization: a conceptual framework for understanding how trees grow and defend themselves. Ann Rev Phytopathol 22:189–214

    Article  Google Scholar 

  • Smith KT, Arbellay E, Falk DA, Sutherland EK (2016) Macroanatomy and compartmentalization of recent fire scars in three North American conifers. Can J For Res 46:535-542

    Article  Google Scholar 

  • Spicer R (2005) Senescence in secondary xylem: heartwood formation as an active developmental program. In: Holbrook NM, Zwieniecki MA (eds) Vascular transport in plants. Elsevier Academic Press, Amsterdam, pp 457–475

    Chapter  Google Scholar 

  • Spicer R (2014) Symplasmic networks in secondary vascular tissues: parenchyma distribution and activity supporting long-distance transport. J Exp Bot 65:1829–1848

    Article  CAS  PubMed  Google Scholar 

  • Utsumi Y, Sano Y, Funada R, Ohtani J, Fujikawa S (2003) Seasonal and perennial changes in the distribution of water in the sapwood of conifers in a sub-frigid zone. Plant Physiol 131:1826–1833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wardell JF, Hart JH (1970) Early responses of sapwood of Quercus bicolor to mechanical injury. Can J Bot 48:683–686

    Article  Google Scholar 

  • Yamada T (1992) Biochemistry of gymnosperm xylem responses to fungal invasion. In: Blanchette RA, Biggs AR (eds) Defense mechanisms of woody plants against fungi. Springer, Berlin, pp 147–164

    Chapter  Google Scholar 

  • Yamada T (1998) Contribution of active defense responses in the limitation of fungal spread in the sapwood of living sugi (Cryptomeria japonica) tree. J For Res 3:103–109

    Article  Google Scholar 

  • Yamada T (2001) Defense mechanisms in the sapwood of living trees against microbial infection. J For Res 6:127–137

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank the staff of the Field Museum Tama Hills of the Tokyo University of Agriculture and Technology for providing plant materials. This work was supported by the Grants-in-Aid from the Japan Society for the Promotion of Science (Nos. 23380105, 24380090, 25850121, 15H04527, 15K07508, and 16K14954).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Satoshi Nakaba.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by E. Beck.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nakaba, S., Morimoto, H., Arakawa, I. et al. Responses of ray parenchyma cells to wounding differ between earlywood and latewood in the sapwood of Cryptomeria japonica . Trees 31, 27–39 (2017). https://doi.org/10.1007/s00468-016-1452-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-016-1452-z

Keywords

Navigation