Skip to main content
Log in

Spatial organization and connectivity of wood rays in Pinus massoniana xylem based on high-resolution μCT-assisted network analysis

Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Spatial organization and connectivity of wood rays in Pinus massoniana was comprehensively viewed and regarded as anatomical adaptions to ensure the properties of rays in xylem.

Abstract

Spatial organization and connectivity of wood rays are essential for understanding the wood hierarchical architecture, but the spatial information is ambiguous due to small cell size. Herein, 3D visualization of rays in Pinus massoniana was performed using high-resolution μCT. We found brick-shaped rays were 6.5% in volume fractions, nearly twice the area fractions estimated by 2D levels. Uniseriate rays became taller and wider during the transition from earlywood to latewood, which was mainly contributed from the height increment of ray tracheids and widened ray parenchyma cells. Furthermore, both volume and surface area of ray parenchyma cells were larger than ray tracheids, so ray parenchyma took a higher proportion in rays. Moreover, three different types of pits for connectivity were segmented and revealed. Pits in both axial tracheids and ray tracheids were bordered, but the pit volume and pit aperture of earlywood axial tracheids were almost tenfold and over fourfold larger than ray tracheids. Contrarily, cross-field pits between ray parenchyma and axial tracheids were window-like with the principal axis of 31.0 μm, but its pit volume was approximately one-third of axial tracheids. Additionally, spatial organization of rays and axial resin canal was analyzed by a curved surface reformation tool, providing the first evidence of rays close to epithelial cells inward through the resin canal. Epithelial cells had various morphologies and large variations in cell size. Our results give new insights into the organization of radial system of xylem, especially the connectivity of rays with adjacent cells.

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

Access this article

Price includes VAT (Canada)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Adey-Johnson R, McLean JP, Van den Bulcke J, Van Acker J, McDonald PJ (2020) Micro-CT measurements of within-ring variability in longitudinal hydraulic pathways in Norway spruce. IAWA J 41:12–29

    Google Scholar 

  • Ahmed SA, Chun SK (2009) Observation of liquid permeability related to anatomical characteristics in Samanea saman. Turk J Agric for 33:155–163

    Google Scholar 

  • Ahmed SA, Chun SK (2011) Permeability of Tectona grandis L. as affected by wood structure. Wood Sci Technol 45:487–500

    CAS  Google Scholar 

  • Ahmed SA, Chong SH, Chun SK, Park BS (2006) Ray parenchyma and ray tracheid structure of four Korean pine wood species. J of the Korea Furnit Soc 17:101–107

    Google Scholar 

  • Bannan M (1936) Vertical resin ducts in the secondary wood of the Abietineae. New Phytol 35:11–46

    Google Scholar 

  • Barghoorn ES (1940) The ontogenetic development and phylogenetic specialization of rays in the xylem of dicotyledons. I. the primitive ray structure. Am J Bot 27:918–928

    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

    PubMed  Google Scholar 

  • Borrega M, Gibson LJ (2015) Mechanics of balsa (Ochroma pyramidale) wood. Mech Mater 84:75–90

    Google Scholar 

  • Braune W, Leman A, Taubert H (2009) Pflanzenanatomisches Praktikum I: Zur Einführung in die Anatomie der Vegetationsorgane der Samenpflanzen, vol 1. Springer-Verlag

    Google Scholar 

  • Brodersen C (2013) Visualizing wood anatomy in three dimensions with high-resolution X-ray micro-tomography (μCT ) - a review. IAWA J 34:408–424

    Google Scholar 

  • Brodersen CR, Lee EF, Choat B, Jansen S, Phillips RJ, Shackel KA, McElrone AJ, Matthews MA (2011) Automated analysis of three-dimensional xylem networks using high-resolution computed tomography. New Phytol 191:1168–1179

    CAS  PubMed  Google Scholar 

  • Brodersen CR, Choat B, Chatelet DS, Shackel KA, Matthews MA, McElrone AJ (2013) Xylem vessel relays contribute to radial connectivity in grapevine stems (Vitis vinifera and V. arizonica; Vitaceae). Am J Bot 100:314–321

    PubMed  Google Scholar 

  • Burgert I, Eckstein D (2001) The tensile strength of isolated wood rays of beech (Fagus sylvatica L.) and its significance for the biomechanics of living trees. Trees 15:168–170

    Google Scholar 

  • Burgert I, Bernasconi A, Niklas K, Eckstein D (2001) The influence of rays on the transverse elastic anisotropy in green wood of deciduous trees. Holzforschung 55:449–454

    CAS  Google Scholar 

  • Carlquist S (2012) How wood evolves: a new synthesis. Botany 90:901–940

    Google Scholar 

  • Carlquist S (2018) Living cells in wood 3. Overview; functional anatomy of the parenchyma network. Bot Rev 84:242–294

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Domec JC, Lachenbruch B, Meinzer FC (2006) Bordered pit structure and function determine spatial patterns of air-seeding thresholds in xylem of Douglas-fir (Pseudotsuga menziesii; Pinaceae) trees. Am J Bot 93:1588–1600

    PubMed  Google Scholar 

  • Fabián-Plesníková I, Sáenz-Romero C, Cruz-De-León J, Martínez-Trujillo M, Sánchez-Vargas NM, Terrazas T (2021) Heritability and characteristics of resin ducts in Pinus oocarpa stems in Michoacán, Mexico. IAWA J 42:258–278

    Google Scholar 

  • Friend AD (2020) Wood structure explained by complex spatial source-sink interactions. bioRxiv II:432

    Google Scholar 

  • Gerolamo CS, Angyalossy V (2017) Wood anatomy and conductivity in lianas, shrubs and trees of Bignoniaceae. IAWA J 38:412–432

    Google Scholar 

  • Govina JK, Apiolaza LA, Altane CM (2021) Variation and genetic parameters of axial resin canal features in clones and families of Pinus radiata. New for 52:167–176

    Google Scholar 

  • Hankinson R (1921) Investigation of crushing strength of spruce at varying angles of grain. Air Service Inf Circular 3:130

    Google Scholar 

  • Jansen S, McAdam S (2019) Pits with aspiration explain life expectancy of a conifer species. Proc Natl Acad Sci USA 116:14794–14796

    CAS  PubMed  PubMed Central  Google Scholar 

  • Klaassen RK (2008) Water flow through wooden foundation piles: A preliminary study. Int Biodeter Biodegr 61:61–68

    CAS  Google Scholar 

  • Koddenberg T, Wentzel M, Militz H (2019) Volumetric estimate of bordered pits in Pinus sylvestris based on X-ray tomography and light microscopy imaging. Micron 124:102704

    PubMed  Google Scholar 

  • Kotowska MM, Thom R, Zhang Y, Schenk HJ, Jansen S (2020) Within-tree variability and sample storage effects of bordered pit membranes in xylem of Acer pseudoplatanus. Trees 34:61–71

    Google Scholar 

  • Kuroda K (1986) Wound effects on cytodifferentiation in the secondary xylem of woody plants. Wood Res Bull Res Inst Kyoto Univ 72:67–118

    Google Scholar 

  • Li W, Zhang Z, Mei C, Kibleur P, Van Acker J, Van Den Bulcke J (2022) Understanding the mechanical strength and dynamic structural changes of wood-based products using X-ray computed tomography. Wood Mater Sci Eng 18:454–463

    Google Scholar 

  • Maire E, Withers PJ (2014) Quantitative X-Ray Tomography. Inte Mater Rev 59:1–43

    CAS  Google Scholar 

  • Martin B, Colin J, Perré P, Casalinho J, Mounkaila M, Lu P, Rémond R (2022) CT investigation of 3D liquid pathways in the anatomical structure of Norway spruce wood during imbibition. Holzforsch 76:592–603

    CAS  Google Scholar 

  • Matisons R, Dubra S, Dauškane I, Bičkovskis K, Jansons A, Gärtner H (2021) Canopy status modulates formation of wood rays in scots pine under hemiboreal conditions. Dendrochronologia 67:125822

    Google Scholar 

  • Mayo SC, Chen F, Evans R (2010) Micron-scale 3D imaging of wood and plant microstructure using high-resolution X-ray phase-contrast microtomography. J Struct Biol 171:182–188

    CAS  PubMed  Google Scholar 

  • Meng Q, Fu F, Wang J, He T, Jiang X, Zhang Y, Yin Y, Li N, Guo J (2021) Ray traits of juvenile wood and mature wood: Pinus massonia and Cunninghamia lanceolata. Forests 12:1277

    Google Scholar 

  • Morris H, Plavcová L, Cvecko P, Fichtler E, Gillingham MA, Martínez-Cabrera HI, McGlinn DJ, Wheeler E, Zheng J, Ziemińska K (2016) A global analysis of parenchyma tissue fractions in secondary xylem of seed plants. New Phytol 209:1553–1565

    CAS  PubMed  Google Scholar 

  • Nakaba S, Morimoto H, Arakawa I, Yamagishi Y, Nakada R, Funada R (2016) Responses of ray parenchyma cells to wounding differ between earlywood and latewood in the sapwood of Cryptomeria japonica. Trees 31:27–39

    Google Scholar 

  • Olsson T, Megnis M, Varna J, Lindberg H (2001) Study of the transverse liquid flow paths in pine and spruce using scanning electron microscopy. J Wood Sci 47:282–288

    Google Scholar 

  • Pereira L, Flores-Borges DN, Bittencourt PR, Mayer JL, Kiyota E, Araújo P, Jansen S, Freitas RO, Oliveira RS, Mazzafera P (2018) Infrared nanospectroscopy reveals the chemical nature of pit membranes in water-conducting cells of the plant xylem. Plant Physiol 177:1629–1638

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pfautsch S (2016) Hydraulic anatomy and function of trees-basics and critical developments. Curr for Rep 2:236–248

    Google Scholar 

  • Pfautsch S, Holtta T, Mencuccini M (2015a) Hydraulic functioning of tree stems-fusing ray anatomy, radial transfer and capacitance. Tree Physiol 35:706–722

    CAS  PubMed  Google Scholar 

  • Pfautsch S, Renard J, Tjoelker MG, Salih A (2015b) Phloem as capacitor: radial transfer of water into xylem of tree stems occurs via symplastic transport in ray parenchyma. Plant Physiol 167:963–971

    CAS  PubMed  PubMed Central  Google Scholar 

  • Phillips M (2012) Inducible and constitutive defenses in pine: the ecological role of pine oil. Pine resin: biology, chemistry and applications 49–66.

  • Qin L, Lin L, Fu F, Fan M (2017) Microstructure and quantitative micromechanical analysis of wood cell-emulsion polymer isocyanate and urea-formaldehyde interphases. Microsc Microanal 23:687–695

    CAS  PubMed  Google Scholar 

  • Qu W, Yang C, Zhang J, Ma Y, Tian X, Zhao S, Yu W (2022) Hydraulic function analysis of conifer xylem based on a model incorporating tracheids, bordered pits, and cross-field pits. Forests 13:171

    Google Scholar 

  • Rahman MM, Fujiwara S, Kanagawa Y (2005) Variations in volume and dimensions of rays and their effect on wood properties of teak. Wood Fiber Sci 37:497–504

    CAS  Google Scholar 

  • Reiterer A, Burgert I, Sinn G, Tschegg S (2002) The radial reinforcement of the wood structure and its implication on mechanical and fracture mechanical properties-a comparison between two tree species. J Mater Sci 37:935–940

    CAS  Google Scholar 

  • Rungwattana K, Hietz P, Larjavaara M (2017) Radial variation of wood functional traits reflect size-related adaptations of tree mechanics and hydraulics. Funct Ecol 32:260–272

    Google Scholar 

  • Sanabria SJ, Baensch F, Zauner M, Niemz P (2020) In-situ quantification of microscopic contributions of individual cells to macroscopic wood deformation with synchrotron computed tomography. Sci Rep 10:21615

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schmitt U, Singh AP, Kim YS (2021) Wood as an ecological niche for microorganisms: wood formation, structure, and cell wall composition. Forest Microbiology. Elsevier, Academic Press, pp 7–34

    Google Scholar 

  • Schniewind A (1959) Transverse anisotropy of wood: a function of gross anatomic structure. Forest Prod J 9:350–359

    CAS  Google Scholar 

  • Schulte PJ, Hacke UG (2021) Solid mechanics of the torus-margo in conifer intertracheid bordered pits. New Phytol 229:1431–1439

    PubMed  Google Scholar 

  • Shen W, Ma L, Zhang X, Li X, Zhao Y, Jing Y, Feng Y, Tan X, Sun F, Lin J (2020) Three-dimensional reconstruction of Picea wilsonii Mast. pollen grains using automated electron microscopy. Sci China Life Sci 63:171–179

    CAS  PubMed  Google Scholar 

  • Slupianek A, Dolzblasz A, Sokolowska K (2021) Xylem parenchyma-role and relevance in wood functioning in trees. Plants 10:1247

    CAS  PubMed  PubMed Central  Google Scholar 

  • Song K, Liu B, Jiang X, Yin Y (2011) Cellular changes of tracheids and ray parenchyma cells from cambium to heartwood in Cunninghamia lanceolata. J Trop for Sci 23:478–487

    Google Scholar 

  • Song J, Chen C, Zhu S, Zhu M, Dai J, Ray U, Li Y, Kuang Y, Li Y, Quispe N, Yao Y, Amy G, Ulrich HL, Hugh AB, Zhu J et al (2018) Processing bulk natural wood into a high-performance structural material. Nature 554:224–228

    CAS  PubMed  Google Scholar 

  • Tang Q, Fang L, Wang Y, Zou M, Guo W (2018) Anisotropic flexible transparent films from remaining wood microstructures for screen protection and AgNW conductive substrate. Nanoscale 10:4344–4353

    CAS  PubMed  Google Scholar 

  • Tixier A, Herbette S, Jansen S, Capron M, Tordjeman P, Cochard H, Badel E (2014) Modelling the mechanical behaviour of pit membranes in bordered pits with respect to cavitation resistance in angiosperms. Ann Bot-London 114:325–334

    Google Scholar 

  • Trtik P, Dual J, Keunecke D, Mannes D, Niemz P, Stahli P, Kaestner A, Groso A, Stampanoni M (2007) 3D imaging of microstructure of spruce wood. J Struct Biol 159:46–55

    CAS  PubMed  Google Scholar 

  • Usta I, Hale MD (2003) Radial permeability of sitka spruce as affected by wood structure: permeability of cross-field pits in uniseriate rays. IAWA J 24:197–204

    Google Scholar 

  • Vázquez-González C, Zas R, Erbilgin N, Ferrenberg S, Rozas V, Sampedro L (2020) Resin ducts as resistance traits in conifers: linking dendrochronology and resin-based defences. Tree Physiol 40:1313–1326

    PubMed  Google Scholar 

  • Wason J, Bouda M, Lee EF, McElrone AJ, Phillips RJ, Shackel KA, Matthews MA, Brodersen C (2021) Xylem network connectivity and embolism spread in grapevine (Vitis vinifera L.). Plant Physiol 186:373–387

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu K, Yuan S, Gao Y, Wu Y, Zhang J, Li X, Lu J (2020) Characterization of moisture states and transport in MUF resin-impregnated poplar wood using low field nuclear magnetic resonance. Drying Technol 39:791–802

    Google Scholar 

  • Yang K, Benson C (1997) Ultrastructure of pits inPinus banksiana lamb. Wood Sci Technol 31:153–169

    CAS  Google Scholar 

  • Yin Y, Berglund L, Salmén L (2011) Effect of steam treatment on the properties of wood cell walls. Biomacromol 12:194–202

    CAS  Google Scholar 

  • Yin L, Jiang X, Ma L, Liu S, He T, Jiao L, Yin Y, Yao L, Guo J (2022) Anatomical adaptions of pits in two types of ray parenchyma cells in Populus tomentosa during the xylem differentiation. J Plant Physiol 278:153830

    CAS  PubMed  Google Scholar 

  • Zhang X, Man Y, Zhuang X, Shen J, Zhang Y, Cui Y, Yu M, Xing J, Wang G, Lian N, Hu Z, Ma L, Shen W, Yang S, Xu H et al (2021) Plant multiscale networks: charting plant connectivity by multi-level analysis and imaging techniques. Sci China Life Sci 64:1392–1422

    PubMed  Google Scholar 

  • Zhao M (2021) Research progress on the resin canal and raw lacquer synthesis of Toxicodendron vernicifluum (Stokes). Plant Cell and Tissue Differentiation and Secondary Metabolites. Springer International Publishing, Cham, pp 145–165

    Google Scholar 

  • Zhu J, Shi Y, Fang L, Liu X, Ji C (2015) Patterns and determinants of wood physical and mechanical properties across major tree species in China. Sci China Life Sci 58:602–612

    PubMed  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge Mr. Yonggang Zhang from the Research Institute of Wood Industry, Chinese Academy of Forestry, for help in the sample collection. This work was supported by the National Natural Science Foundation of China (31890772), National Natural Science Foundation of China (32071691), the department of Science and Technology, National Forestry and Grassland Administration (2020132601) and Fundamental Research Funds for the Central Non-proft Research Institution of CAF (CAFYBB2021QC003).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Juan Guo.

Ethics declarations

Conflict of interest

The author(s) declare that they have no conflict of interest.

Additional information

Communicated by Anastasios Melis.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 2944 KB)

Supplementary file2 (MP4 1216 KB)

Supplementary file3 (MP4 1469 KB)

Supplementary file4 (MP4 636 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ma, L., Meng, Q., Jiang, X. et al. Spatial organization and connectivity of wood rays in Pinus massoniana xylem based on high-resolution μCT-assisted network analysis. Planta 258, 28 (2023). https://doi.org/10.1007/s00425-023-04185-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00425-023-04185-1

Keywords

Navigation