Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Intra-organismal variation in the structure of plant vascular transport tissues in poplar trees

Abstract

Key message

Phloem and xylem conduit structure vary greatly throughout the body of Populus trichocarpa trees, particularly between roots and shoots. This has implications for understanding organ and whole plant vascular function.

Abstract

Woody plant vascular transport occurs predominantly within secondary xylem and phloem, which are both produced by the vascular cambium during secondary growth. We examined how vessel and sieve tube structure varied throughout the plant body of P. trichocarpa trees and whether xylem and phloem conduit structure was correlated across different positions within the plant. We excavated entire juvenile P. trichocarpa trees and measured vessel and sieve tube structural traits of current-year growth in 1 m increments along the main root:shoot axis. Trees were > 4 m tall and had roots that extended 4–5 m at their longest length. We found that both sieve tube and vessel diameters greatly varied throughout the plant body and with organ diameter. Roots had wider diameter conduits than shoots. Sieve tube diameter was strongly correlated with vessel diameter, which may be related to their common developmental origin. Other structural traits, such as pit membrane area and pit density for xylem, and sieve plate area and number of sieve areas per plate for phloem, also varied and were correlated with changes in conduit diameter. The median air-seeding pressure of vessels (Pm) and vessel length did not differ between roots and shoots. Understanding plant vascular function will likely require increased knowledge of whole plant structure and function, since plant performance may be limited by any point along the transport pathway. Considering intra-organismal variation may be a way to evaluate structure–function hypotheses while controlling for confounding sources of variation that may impact inter-specific comparisons.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

References

  1. Alder NN, Sperry JS. Pockman WT (1996) Root and stem xylem embolism, stomatal conductance, and leaf turgor in Acer grandidentatum populations along a soil moisture gradient. Oecologia 105:293–301

  2. Aloni R (2010) The induction of vascular tissues by auxin. Davies PJ (ed) Plant hormones (pp 485–518). Springer, Dordrecht

  3. Aloni R, Zimmermann MH (1983) The control of vessel size and density along the plant axis: a new hypothesis. Differentiation 24:203–208

  4. Anfodillo T, Carraro V, Carrer M, Fior C, Rossi S (2006) Convergent tapering of xylem conduits in different woody species. New Phytol 169:279–290

  5. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

  6. Butterfield BG (1973) Variation in the size of fusiform cambial initials and vessel members in Hoheria angustifolia Raoul. N Z J Bot 11:391–410

  7. Christman MA, Sperry JS (2010) Single-vessel flow measurements indicate scalariform perforation plates confer higher flow resistance than previously estimated. Plant Cell Environ 33:431–443

  8. Davis JD, Evert RF (1968) Seasonal development of the secondary phloem in Populus tremuloides. Bot Gaz 129:1–8

  9. Davis SD, Sperry JS, Hacke UG (1999) The relationship between xylem conduit diameter and cavitation caused by freezing. Am J Bot 86:1367–1372

  10. Domec JC, Gartner BL (2002) Age- and position-related changes in hydraulic versus mechanical dysfunction of xylem: inferring the design criteria for Douglas-fir wood structure. Tree Physiol 22:91–104

  11. Domec JC, Warren JM, Meinzer FC, Lachenbruch B (2009) Safety factors for xylem failure by implosion and air-seeding within roots, trunks and branches of young and old conifer trees. IAWA J 30:100–120

  12. Engelbrecht BMJ, Velez V, Tyree MT (2000) Hydraulic conductance of two co-occurring neotropical understory shrubs with different habitat preferences. Annales des Sciences Forestieres 57:201–208

  13. Ewers FW, Fisher JB (1989) Variation in vessel length and diameter in stems of six tropical and subtropical lianas. Am J Bot 76:1452–1459

  14. Ewers FW, Fisher JB, Chiu ST (1990) A survey of vessel dimensions in stems of tropical lianas and other growth forms. Oecologia 84:544–552

  15. Ewers FW, Carlton MR, Fisher JB, Kolb KJ, Tyree MT (1997) Vessel diameters in roots versus stems of tropical lianas and other growth forms. IAWA J 18:261–279

  16. Givnish TJ, Wong SC, Stuart-Williams H, Holloway-Phillips M, Farquhar GD (2014) Determinants of maximum tree height in Eucalyptus species along a rainfall gradient in Victoria, Australia. Ecology 95:2991–3007

  17. Greenidge K (1952) An approach to the study of vessel length in hardwood species. Am J Bot 39:570–574

  18. Hacke U, Sauter JJ (1996) Drought-induced xylem dysfunction in petioles, branches, and roots of Populus balsamifera L. and Alnus glutinosa (L.) Gaertn. Plant Physiol 111:413–417

  19. Hacke UG, Sperry JS (2001) Functional and ecological xylem anatomy. Perspect Plant Ecol 4:97–115

  20. Hacke UG, Sperry JS, Pittermann J (2000) Drought experience and cavitation resistance in six shrubs from the Great Basin, Utah. Basic Appl Ecol 1:31–41

  21. Hacke UG, Sperry JS, Wheeler JK, Castro L (2006) Scaling of angiosperm xylem structure with safety and efficiency. Tree Physiol 26:689–701

  22. Hölttä T, Mencuccini M, Nikinmaa E (2009) Linking phloem function to structure: analysis with a coupled xylem–phloem transport model. J Theor Biol 259:325–337

  23. Hukin D, Cochard H, Dreyer E, Thiec DL, Bogeat-Triboulot MB (2005) Cavitation vulnerability in roots and shoots: does Populus euphratica Oliv., a poplar from arid areas of Central Asia, differ from other poplar species? J Exp Bot 56:2003–2010

  24. Jacobsen AL, Pratt RB, Tobin MF, Hacke UG, Ewers FW (2012) A global analysis of xylem vessel length in woody plants. Am J Bot 99:1583–1591

  25. Jacobsen AL, Tobin MF, Toschi HS, Percolla MI, Pratt RB (2016) Structural determinants of increased susceptibility to dehydration-induced cavitation in post-fire resprouting chaparral shrubs. Plant Cell Environ 39:2473–2485

  26. Jensen KH, Mullendore DL, Holbrook NM, Bohr T, Knoblauch M, Bruus H (2012) Modeling the hydrodynamics of phloem sieve plates. Front Plant Sci 3(151):1–11

  27. Jyske T, Hölttä T (2015) Comparison of phloem and xylem hydraulic architecture in Picea abies stems. New Phytol 205:102–115

  28. Kolb KJ, Sperry JS, Lamont BB (1996) A method for measuring xylem hydraulic conductance and embolism in entire root and shoot systems. J Exp Bot 47:1805–1810

  29. Langan SJ, Ewers FW, Davis SD (1997) Xylem dysfunction caused by water stress and freezing in two species of co-occurring chaparral shrubs. Plant Cell Environ 20:425–437

  30. Lens F, Sperry JS, Christman MA, Choat B, Rabaey D, Jansen S (2011) Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer. New Phytol 190:709–723

  31. Lintunen A, Kalliokoski T (2010) The effect of tree architecture on conduit diameter and frequency from small distal roots to branch tips in Betula pendula, Picea abies and Pinus sylvestris. Tree Physiol 30:1433–1447

  32. Liu M, Pan R, Tyree MT (2018) Intra-specific relationship between vessel length and vessel diameter of four species with long-to-short species-average vessel lengths: further validation of the computation algorithm. Trees 32(1):51–60

  33. Maherali H, Pockman WT, Jackson RB (2004) Adaptive variation in the vulnerability of woody plants to xylem cavitation. Ecology 85:2184–2199

  34. Martínez-Vilalta J, Prat E, Oliveras I, Piñol J (2002) Xylem hydraulic properties of roots and stems of nine Mediterranean woody species. Oecologia 133:19–29

  35. McCulloh KA, Sperry JS, Adler FR (2003) Water transport in plants obeys Murray’s law. Nature 421:939–942

  36. McCulloh KA, Sperry JS, Lachenbruch B, Meinzer FC, Reich PB, Voelker S (2010) Moving water well: comparing hydraulic efficiency in twigs and trunks of coniferous, ring-porous, and diffuse-porous saplings from temperate and tropical forests. New Phytol 186:439–450

  37. McElrone AJ, Pockman WT, Martínez-Vilalta J, Jackson RB (2004) Variation in xylem structure and function in stems and roots of trees to 20 m depth. New Phytol 163:507–517

  38. Mullendore DL, Windt CW, Van As H, Knoblauch M (2010) Sieve tube geometry in relation to phloem flow. Plant Cell 22:579–593

  39. Niklas KJ, Spatz HC (2004) Growth and hydraulic (not mechanical) constraints govern the scaling of tree height and mass. PNAS 101:15661–15663

  40. Nygren P, Pallardy SG (2008) Applying a universal scaling model to vascular allometry in a single-stemmed, monopodially branching deciduous tree (Attim’s model). Tree Physiol 28:1–10

  41. Olson ME, Anfodillo T, Rosell JA, Petit G, Crivellaro A, Isnard S, León-Gómez C, Alvarado-Cárdenas LO, Castorena M (2014) Universal hydraulics of the flowering plants: vessel diameter scales with stem length across angiosperm lineages, habits and climates. Ecol Lett 17:988–997

  42. Petit G, Crivellaro A (2014) Comparative axial widening of phloem and xylem conduits in small woody plants. Trees 28:915–921

  43. Pittermann J, Sperry JS (2003) Tracheid diameter is the key trait determining the extent of freezing-induced embolism in conifers. Tree Physiol 23:907–914

  44. Pratt RB, Jacobsen AL, Ewers FW, Davis SD (2007) Relationships among xylem transport, biomechanics and storage in stems and roots of nine Rhamnaceae species of the California chaparrral. New Phytol 178:87–798

  45. Pratt RB, North GB, Jacobsen AL, Ewers FW, Davis SD (2010) Xylem root and shoot hydraulics is linked to life history type in chaparral seedlings. Funct Ecol 24:70–81

  46. Pratt RB, MacKinnon ED, Venturas MD, Crous CJ, Jacobsen AL (2015) Root resistance to cavitation is accurately measured using a centrifuge technique. Tree Physiol 35:185–196

  47. Quilhó T, Pereira H, Richter HG (2000) Within–tree variation in phloem cell dimensions and proportions in Eucalyptus globulus. IAWA J 21:31–40

  48. R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  49. Ridoutt BG, Sands R (1993) Within-tree variation in cambial anatomy and xylem cell differentiation in Eucalyptus globulus. Trees 8:18–22

  50. Schuldt B, Leuschner C, Brock N, Horna V (2013) Changes in wood density, wood anatomy and hydraulic properties of the xylem along the root-to-shoot flow path in tropical rainforest trees. Tree Physiol 33:161–174

  51. Sperry JS, Hacke UG (2004) Analysis of circular bordered pit function I. Angiosperm vessels with homogenous pit membranes. Am J Bot 91:369–385

  52. Sperry JS, Saliendra NZ (1994) Intra- and inter-plant variation in xylem cavitation in Betula occidentalis. Plant Cell Environ 17:1233–1241

  53. Sperry JS, Hacke UG, Wheeler JK (2005) Comparative analysis of end wall resistivity in xylem conduits. Plant Cell Environ 28:456–465

  54. Tyree MT, Ewers FW (1991) The hydraulic architecture of trees and other woody plants. New Phytol 119:345–360

  55. Venturas MD, Rodriguez-Zaccaro FD, Percolla MI, Crous CJ, Jacobsen AL, Pratt RB (2016) Single vessel air injection estimates of xylem resistance to cavitation are affected by vessel network characteristics and sample length. Tree Physiol 36:1247–1259

  56. Wheeler JK, Sperry JS, Hacke UG, Hoang N (2005) Inter-vessel pitting and cavitation in woody Rosaceae and other vesselled plants: a basis for a safety versus efficiency trade-off in xylem transport. Plant Cell Environ 28:800–812

  57. Zhao X (2015) Effects of cambial age and flow path-length on vessel characteristics in birch. J For Res 20:175–185

  58. Zimmermann MH, Jeje AA (1981) Vessel-length distribution in stems of some American woody plants. Can J Bot 59:1882–1892

  59. Zimmermann MH, Potter D (1982) Vessel-length distribution in branches, stem and roots of Acer rubrum L. IAWA Bull 3:103–109

Download references

Acknowledgements

The National Science Foundation (NSF) is acknowledged for support (Division of Integrative Organismal Systems; IOS-1252232 and Division of Human Resource Development; HRD-1547784). We thank Chevron for support to the California State University, Bakersfield (CSUB) Research Experience Vitalizing Science University Program (REVS-UP) which supported high school student researchers who assisted with data collection: Daisy Buenrostro, Viviana Firo, and Brooke Herrera.

Author information

Correspondence to Anna L. Jacobsen.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by E. Magel.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 14 KB)

Supplementary material 2 (DOCX 21 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Jacobsen, A.L., Valdovinos-Ayala, J., Rodriguez-Zaccaro, F.D. et al. Intra-organismal variation in the structure of plant vascular transport tissues in poplar trees. Trees 32, 1335–1346 (2018). https://doi.org/10.1007/s00468-018-1714-z

Download citation

Keywords

  • Anatomy
  • Development
  • Phloem
  • Pit membrane
  • Sieve area
  • Sieve plate
  • Single-vessel air injection
  • Transport
  • Xylem