Skip to main content
SpringerLink
Log in

Comparative axial widening of phloem and xylem conduits in small woody plants

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

Abstract

Key message

Along the stem axis phloem’s sieve elements increase in diameter basally at rates comparable to those of xylem conduits and in agreement with principles of hydraulic optimization.

Abstract

Plant physiology relies on the efficiency of the two long-distance transport systems of xylem and phloem. Xylem architecture comprises conduits of small dimensions towards the stem apex, where transpiration-induced tensions are the highest along the root-to-leaves hydraulic pathway, and widen basally to minimize the path length resistance to water flow. Instead, information on phloem anatomy and allometry is extremely scarce, although potentially relevant for the efficiency of sugar transportation. We measured the hydraulic diameter (Dh) of both xylem conduits and phloem sieve elements in parallel at different heights along the stem of a small tree of Picea abies, Fraxinus excelsior and Salix eleagnos. Dh increased from the stem apex to base in both xylem and phloem, with a higher scaling exponent (b) of sieve elements than that of tracheids in the conifer (0.19 vs. 0.14) and lower than that of vessels in the angiosperms (0.14–0.22 vs. 0.19–0.40). In addition, sieve elements were larger than tracheids in P. abies and narrower than angiosperms vessels at any height along the stem. In conclusion, axial conduit widening would seem to be a key feature of both xylem and phloem long-distance transport architectures.

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

Similar content being viewed by others

References

  • 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

    Article  PubMed  Google Scholar 

  • Anfodillo T, Petit G, Crivellaro A (2013) Axial conduit widening in woody species: a still neglected anatomical pattern. IAWA 34:352–364

    Article  Google Scholar 

  • Angeles G, Bond B, Boyer JS, Brodribb T, Brooks JR, Burns MJ, Cavender-Bares J, Clearwater M, Cochard H, Comstock J, Davis SD, Domec JC, Donovan L, Ewers F, Gartner B, Hacke U, Hinckley T, Holbrook NM, Jones HG, Kavanagh K, Law B, Lopez-Portillo J, Lovisolo C, Martin T, Martinez-Vilalta J, Mayr S, Meinzer FC, Melcher P, Mencuccini M, Mulkey S, Nardini A, Neufeld HS, Passioura J, Pockman WT, Pratt RB, Rambal S, Richter H, Sack L, Salleo S, Schubert A, Schulte P, Sparks JP, Sperry J, Teskey R, Tyree M (2004) The cohesion-tension theory. New Phytol 163:451–452

    Article  Google Scholar 

  • Becker P, Gribben RJ, Lim CM (2000) Tapered conduits can buffer hydraulic conductance from path-length effects. Tree Physiol 20:965–967

    Article  CAS  PubMed  Google Scholar 

  • Bettiati D, Petit G, Anfodillo T (2012) Testing the equi-resistance principle of the xylem transport system in a small ash tree: empirical support from anatomical analyses. Tree Physiol 32:171–177

    Article  PubMed  Google Scholar 

  • Bohonak AJ (2004) RMA: software for reduced major axis regression v.1.17. University of San Diego

  • Brodribb TJ, Holbrook NM (2003) Stomatal closure during leaf dehydration, correlation with other leaf physiological traits. Plant Physiol 132:2166–2173

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Brodribb TJ, Holbrook NM, Edwards EJ, Gutiérrez MV (2003) Relations between stomatal closure, leaf turgor and xylem vulnerability in eight tropical dry forest trees. Plant Cell Environ 26:443–450

    Article  Google Scholar 

  • Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ, Feild TS, Gleason SM, Hacke UG, Jacobsen AL, Lens F, Maherali H, Martínez-Vilalta J, Mayr S, Mencuccini M, Mitchell PJ, Nardini A, Pittermann J, Pratt RB, Sperry JS, Westboy M, Wright IJ, Zanne AE (2012) Global convergence in the vulnerability of forests to drought. Nature 491:752–755

    CAS  PubMed  Google Scholar 

  • Davison AC, Hinkley DV (1997) Bootstrap methods and their applications. Cambridge University Press, New York

    Book  Google Scholar 

  • De Schepper V, Steppe K (2010) Development and verification of a water and sugar transport model using measured stem diameter variations. J Exp Bot 61:2083–2099

    Article  PubMed  Google Scholar 

  • De Schepper V, De Swaef T, Bauweraerts I, Steppe K (2013) Phloem transport: a review of mechanisms and controls. J Exp Bot 64:4839–4850

    Google Scholar 

  • Ewers F, Fisher J (1991) Why vines have narrow stems: histological trends in Bauhinia (Fabaceae). Oecologia 88:233–237

    Article  Google Scholar 

  • Hacke UG, Sperry JS, Pockman WT, Davis SD, McCulloch KA (2001) Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 126:457–461

    Article  Google Scholar 

  • Ho LC, Nichols R (1975) The role of phloem transport in the translocation of sucrose along the stem of carnation cut flowers. Ann Bot 39:439–446

    CAS  Google Scholar 

  • Höltta 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

    Article  PubMed  Google Scholar 

  • Hölttä T, Vesala T, Perämäki M, Nikinmaa E (2006) Refilling of embolised conduits as a consequence of ‘Münch water’ circulation. Funct Plant Biol 33:949–959

    Article  Google Scholar 

  • Jensen KH, Lee J, Bohr T, Bruus H, Holbrook NM, Zwieniecki MA (2011) Optimality of the Münch mechanism for translocation of sugars in plants. J R Soc Interface 8:1155–1165

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jensen KH, Liesche J, Bohr T, Schulz A (2012) Universality of phloem transport in seed plants. Plant Cell Environ 35:1065–1076

    Article  CAS  PubMed  Google Scholar 

  • Knoblauch M, van Bel AJE (1998) Sieve tubes in action. Plant Cell 10:35–50

    Article  CAS  PubMed Central  Google Scholar 

  • Köckenberger W, Pope JM, Xia Y, Jeffrey KR, Komor E, Callaghan PT (1997) A non-invasive measurement of phloem and xylem water flow in castor bean seedlings by nuclear magnetic resonance microimaging. Planta 201:53–63

    Article  Google Scholar 

  • Kolb KJ, Sperry JS (1999) Differences in drought adaptation between subspecies of sagebrush (Artemisia tridentata). Ecology 80:2373–2384

    Article  Google Scholar 

  • Lacointe A, Minchin PEH (2008) Modelling phloem and xylem transport within a complex architecture. Funct Plant Biol 35:772–780

    Article  Google Scholar 

  • Lampinen MJ, Noponen T (2003) Thermodynamic analysis of the interaction of the xylem water and phloem sugar solution and its significance for the cohesion theory. J Theor Biol 224:285–298

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739

    Article  PubMed  Google Scholar 

  • Mencuccini M, Hölttä T, Martinez-Vilalta J (2011) Comparative criteria for models of the vascular transport systems of tall trees. In: Meinzer FC, Lachenbruch B, Dawson TE (eds) Size- and age-related changes in tree structure and function, vol 4. Springer, Netherlands, pp 309–339

    Chapter  Google Scholar 

  • Minchin PEH, Lacointe A (2005) New understanding on phloem physiology and possible consequences for modelling long-distance carbon transport. New Phytol 166:771–779

    Article  CAS  PubMed  Google Scholar 

  • Nardini A, Lo Gullo MA, Salleo S (2011) Refilling embolized xylem conduits: is it a matter of phloem unloading? Plant Sci 180:604–611

    Article  CAS  PubMed  Google Scholar 

  • Nepstad DC, Tohver IM, Ray D, Moutinho P, Cardinot G (2007) Mortality of large trees and lianas following experimental drought in an Amazon forest. Ecology 88:2259–2269

    Article  PubMed  Google Scholar 

  • Olson ME, Rosell JA (2012) Vessel diameter-stem diameter scaling across woody angiosperms and the ecological causes of xylem vessel diameter variation. New Phytol 197:1204–1213

    Article  PubMed  Google Scholar 

  • Petit G, Anfodillo T (2009) Plant physiology in theory and practice: an analysis of the WBE model for vascular plants. J Theor Biol 259:1–4

    Article  PubMed  Google Scholar 

  • Petit G, Anfodillo T, Mencuccini M (2008) Tapering of xylem conduits and hydraulic limitations in sycamore (Acer pseudoplatanus) trees. New Phytol 177:653–664

    Article  PubMed  Google Scholar 

  • Petit G, Anfodillo T, De Zan C (2009) Degree of tapering of xylem conduits in stems and roots of small Pinus cembra and Larix decidua trees. Botany 87:501–508

    Article  Google Scholar 

  • Petit G, Anfodillo T, Carraro V, Grani F, Carrer M (2011) Hydraulic constraints limit height growth in trees at high altitude. New Phytol 189:241–252

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Rosner S, Baier P, Kikuta S (2001) Osmotic potential of Norway spruce [Picea abies (L.) Karst.] secondary phloem in relation to anatomy. Trees 15:472–482

    Article  Google Scholar 

  • Ryan MG, Asao S (2014) Phloem transport in trees. Tree Physiol 34:1–4

    Article  PubMed  Google Scholar 

  • Ryan MG, Phillips N, Bond BJ (2006) The hydraulic limitation hypothesis revisited. Plant Cell Environ 29:367–381

    Article  PubMed  Google Scholar 

  • Sala A, Piper F, Hoch G (2010) Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytol 186:274–281

    Article  PubMed  Google Scholar 

  • Sevanto S, Höltta T, Holbrook NM (2011) Effects of the hydraulic coupling between xylem and phloem on diurnal phloem diameter variation. Plant Cell Environ 34:690–703

    Article  CAS  PubMed  Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry. WH Freeman, New York

    Google Scholar 

  • West GB, Brown JH, Enquist BJ (1999) A general model for the structure and allometry of plant vascular systems. Nature 400:664–667

    Article  CAS  Google Scholar 

  • Woodruff DR (2014) The impacts of water stress on phloem transport in Douglas-fir trees. Tree Physiol 34:5–14

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The manuscript was inspired and supported by the EU COST Action FP1106 (STReESS). Alan Crivellaro received financial support from the University of Padova (“Assegno di Ricerca Junior” CPDr124554/12).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Dipartimento Territorio e Sistemi Agro-Forestali, Università degli Studi di Padova, Viale dell’Università, 16, 35020, Legnaro, PD, Italy

    Giai Petit & Alan Crivellaro

Authors
  1. Giai Petit
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alan Crivellaro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Giai Petit.

Additional information

Communicated by M. Adams.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Petit, G., Crivellaro, A. Comparative axial widening of phloem and xylem conduits in small woody plants. Trees 28, 915–921 (2014). https://doi.org/10.1007/s00468-014-1006-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-014-1006-1

Keywords

Search

Navigation