Skip to main content
SpringerLink
Log in

Seasonal bulk xylem pressure in temperate broadleaf eudicot trees: a case study for sugar long-distance transport and signaling

  • Opinion Paper
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

Sugars regulate growth, development, and defense in trees. Sugars are also important signaling molecules and are transported over long distances via xylem and phloem. Sucrose loading to tracheids and vessels is associated with bulk xylem pressure and occurs seasonally in temperate broadleaf eudicot trees. Following restoration of xylem hydraulic conductivity in spring, sugars are unloaded from xylem sap at apical branches and deposited as starch before growth of shoot apical meristems. Growth of cambia and shoot apical meristems leads to starch catabolism that yields hexose-phosphates to fuel cell growth and regulate other signal networks. The contrast between cell molecular biology of Arabidopsis and physiology of temperate broadleaf eudicot trees indicates the importance of phosphorylation in long-distance sugar signaling. Hexokinase, acting as a hub for signal and hormone networks, is likely an important regulator of sugar signaling in response to stimuli such as energy status, sugar status, and environmental conditions. The comparative analysis suggested here could help bridge physiology and detailed molecular mechanisms regarding physiology of trees.

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

  • Aki T, Shigyo M, Nakano R, Yoneyama T, Yanagisawa S (2008) Nano scale proteomics revealed the presence of regulatory proteins including three FT-like proteins in phloem and xylem saps from rice. Plant Cell Physiol 49:767–790

    Article  PubMed  CAS  Google Scholar 

  • Aloni R (1987) Differentiation of vascular tissues. Annu Rev Plant Physiol 38:179–204

    Article  Google Scholar 

  • Améglio T, Guilliot A, Lacointe A, Julien JL, Alves G, Valentin V, Pétel G (2000) Water relations in winter: effect on bud break of walnut tree. In: Viémont JD, Crabbé J (eds) Dormancy in plants: from whole plant behaviour to cellular control. CABI, Wallingford, pp 109–120

    Chapter  Google Scholar 

  • Améglio T, Bodet C, Lacointe A et al (2002) Winter embolism, mechanisms of xylem hydraulic conductivity recovery and springtime growth patterns in walnut and peach trees. Tree Physiol 22:1211–1220

    Article  PubMed  Google Scholar 

  • Améglio T, Decourteix M, Alves G et al (2004) Temperature effects on xylem sap osmolarity in walnut trees: evidence for a vitalistic model of winter embolism repair. Tree Physiol 24:785–793

    Article  PubMed  Google Scholar 

  • Aoki N, Hirose T, Scofield GN, Whitfeld PR, Furbank RT (2003) The sucrose transporter gene family in rice. Plant Cell Physiol 44:223–232. https://doi.org/10.1093/pcp/pcg030

    Article  PubMed  CAS  Google Scholar 

  • Baldazzi V, Bertin N, de Jong H, Génard M (2012) Towards multiscale plant models: integrating cellular networks. Trends Plant Sci 17:728–736

    Article  PubMed  CAS  Google Scholar 

  • Bonhomme M, Peuch M, Améglio T et al (2010) Carbohydrate uptake from xylem vessels and its distribution among stem tissues and buds in walnut (Juglans regia L.). Tree Physiol 30:89–102

    Article  PubMed  CAS  Google Scholar 

  • Chen LQ, Cheung LS, Feng L, Tanner W, Frommer WB (2015) Transport of sugars. Annu Rev Biochem 84:865–894

    Article  PubMed  CAS  Google Scholar 

  • Cirelli D, Jagels R, Tyree MT (2008) Toward an improved model of maple sap exudation: the location and role of osmotic barriers in sugar maple, butternut and white birch. Tree Physiol 28:1145–1155

    Article  PubMed  Google Scholar 

  • Conroy C, Ching J, Gao Y, Wang X, Rampitsch C, Xing T (2013) Knockout of AtMKK1 enhances salt tolerance and modifies metabolic activities in Arabidopsis. Plant Signal Behav 8:e24206. https://doi.org/10.4161/psb.24206

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cookson SJ, Yadav UP, Klie S, Morcuende R, Usadel B, Lunn JE, Stitt M (2016) Temporal kinetics of the transcriptional response to carbon depletion and sucrose readdition in Arabidopsis seedlings. Plant Cell Environ 39:768–786

    Article  PubMed  CAS  Google Scholar 

  • Decourteix M, Alves G, Brunel N et al (2006) JrSUT1, a putative xylem sucrose transporter, could mediate sucrose influx into xylem parenchyma cells and be up-regulated by freeze-thaw cycles over the autumn-winter period in walnut tree (Juglans regia L.). Plant Cell Environ 29:36–47

    Article  PubMed  CAS  Google Scholar 

  • Decourteix M, Alves G, Bonhomme M, Peuch M, Baaziz KB, Brunel N, Guilliot A, Rageau R, Ameglio T, Petel G, Sakr S (2008) Sucrose (JrSUT1) and hexose (JrHT1 and JrHT2) transporters in walnut xylem parenchyma cells: their potential role in early events of growth resumption. Tree Physiol 28:215–224

    Article  PubMed  CAS  Google Scholar 

  • Essiamah S, Eschrich W (1986) Water uptake in deciduous trees during winter and the role of conducting tissues in spring reactivation. IAWA J 7:31–38

    Article  Google Scholar 

  • Eveland AL, Jackson DP (2012) Sugars, signaling, and plant development. J Exp Bot 63:3367–3377

    Article  PubMed  CAS  Google Scholar 

  • Evert RF, Eichhorn SE (2006) Esau’s plant anatomy: meristems, cells, and tissues of the plant body: their structure, function, and development, 3rd edn. John Wiley, Hoboken

    Book  Google Scholar 

  • Ewers FW, Améglio T, Cochard H et al (2001) Seasonal variation in xylem pressure of walnut trees: root and stem pressures. Tree Physiol 21:1123–1132

    Article  PubMed  CAS  Google Scholar 

  • Furukawa J, Abe Y, Mizuno H, Matsuki K, Sagawa K, Kojima M, Sakakibara H, Iwai H, Satoh S (2011) Seasonal fluctuation of organic and inorganic components in xylem sap of Populus nigra. Plant Roots 5:56–62

    Article  CAS  Google Scholar 

  • Heizmann U, Kreuzwieser J, Schnitzler JP, Brüggemann N, Rennenberg H (2001) Assimilate transport in the xylem sap of pedunculate oak (Quercus robur) saplings. Plant Biol 3:132–138

    Article  CAS  Google Scholar 

  • Kühn C (2016) Post-translational crosstalk between brassinosteroid and sucrose signaling. Plant Sci 248:75–81

    Article  PubMed  CAS  Google Scholar 

  • Lalonde S, Frommer WB (2012) SUT sucrose and MST monosaccharide transporter inventory of the Selaginella genome. Front Plant Sci 3:24. https://doi.org/10.3389/fpls.2012.00024

    Article  PubMed  PubMed Central  Google Scholar 

  • Li L, Sheen J (2016) Dynamic and diverse sugar signaling. Curr Opin Plant Biol 33:116–125

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li J, Wu L, Foster R, Ruan YL (2017) Molecular regulation of sucrose catabolism and sugar transport for development, defence and phloem function. J Integr Plant Biol 59:322–335

    Article  PubMed  CAS  Google Scholar 

  • Mason MG, Ross JJ, Babst BA, Wienclaw BN, Beveridge CA (2014) Sugar demand, not auxin, is the initial regulator of apical dominance. Proc Natl Acad Sci U S A 111:6092–2097

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Morris H, Plavcova L, Cvecko P et al (2016) A global analysis of parenchyma tissue fractions in secondary xylem of seed plants. New Phytol 209:1553–1565

    Article  PubMed  CAS  Google Scholar 

  • Oh E, Zhu JY, Wang ZY (2012) Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nat Cell Biol 14:802–809

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Panchen ZA, Primack RB, Nordt B, Ellwood ER, Stevens AD, Renner SS, Willis CG, Fahey R, Whittemore A, du Y, Davis CC (2014) Leaf out times of temperate woody plants are related to phylogeny, deciduousness, growth habit and wood anatomy. New Phytol 203:1208–1219

    Article  PubMed  CAS  Google Scholar 

  • Pien S, Wyrzykowska J, Fleming AJ (2002) Novel marker genes for early leaf development indicate spatial regulation of carbohydrate metabolism within the apical meristem. Plant J 25:663–674

    Article  Google Scholar 

  • Plavcova L, Jansen S (2015) The role of xylem parenchyma in the storage and utilization of nonstructural carbohydrates. In: Hacke U (ed) Functional and ecological xylem anatomy. Springer, pp 209–234

  • Plavcova L, Hoch G, Morris H et al (2016) The amount of parenchyma and living fibers affects storage of nonstructural carbohydrates in young stems and roots of temperate trees. Am J Bot 103:603–612

    Article  PubMed  CAS  Google Scholar 

  • Ramon M, Rolland F, Sheen J (2008) Sugar sensing and signaling. The Arabidopsis book 6. https://doi.org/10.1199/tab.0117

  • Rinne P, Tuominen H, Junttila O (1994) Seasonal changes in bud dormancy in relation to bud morphology, water and starch content, and abscisic acid concentration in adult trees of Betula pubescens. Tree Physiol 14:549–561

    Article  PubMed  CAS  Google Scholar 

  • Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709

    Article  PubMed  CAS  Google Scholar 

  • Ruan YL, Jin Y, Yang YJ, Li GJ, Boyer JS (2010) Sugar input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat. Mol Plant 3:942–955

    Article  PubMed  CAS  Google Scholar 

  • Sauter JJ (1981) Evidence of sucrose efflux and hexose uptake in the xylem of Salix. Z Pflanzenphysiol 103:183–188

    Article  CAS  Google Scholar 

  • Sauter JJ (1982) Efflux and reabsorption of sugars in the xylem I. Seasonal changes in sucrose efflux in Salix. Z Pflanzenphysiol 106:325–336

    Article  CAS  Google Scholar 

  • Sauter JJ (1983) Efflux and reabsorption of sugars in the xylem II. Seasonal changes in sucrose uptake in Salix. Z Pflanzenphysiol 111:429–440

    Article  CAS  Google Scholar 

  • Sauter JJ (1988) Temperature-induced changes in starch and sugars in the stem of Populus × canadensis ‘robusta’. J Plant Physiol 132:608–612

    Article  CAS  Google Scholar 

  • Sauter JJ, Ambrosius T (1986) Changes in the partitioning of carbohydrates in the wood during bud break in Betula pendula Roth. J Plant Physiol 124:31–43

    Article  CAS  Google Scholar 

  • Sauter JJ, Iten W, Zimmermann M (1973) Studies on the release of sugar into the vessels of sugar maple (Acer saccharum). Can J Bot 51:1–8

    Article  CAS  Google Scholar 

  • Schiener P, Black KD, Stanley MS, Green DH (2015) The seasonal variation in the chemical composition of the kelp species Laminaria digitata, Laminaria hyperborea, Saccharina latissima and Alaria esculenta. J Appl Phycol 27:363–373

    Article  CAS  Google Scholar 

  • Schill V, Hartung W, Orthen B, Weisenseel MH (1996) The xylem sap of maple (Acer platanoides) trees—sap obtained by a novel method shows changes with season and height. J Exp Bot 47:123–133

    Article  CAS  Google Scholar 

  • Sheldrake AR, Northcote DH (1968) Some constituents of xylem sap and their possible relationship to xylem differentiation. J Exp Bot 19:681–689

    Article  Google Scholar 

  • Stitt M, Zeeman SC, Hibberd JM et al (2012) Starch turnover: pathways, regulation and role in growth. Curr Opin Plant Biol 15:282–292

    Article  PubMed  CAS  Google Scholar 

  • Sturm A, Tang GQ (1999) The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends Plant Sci 4:401–407

    Article  PubMed  CAS  Google Scholar 

  • Szklarczyk D, Morris JH, Cook H, Kuhn M, Wyder S, Simonovic M, Santos A, Doncheva NT, Roth A, Bork P, Jensen LJ, von Mering C (2017) The STRING database in 2017: quality-controlled protein–protein association networks, made broadly accessible. Nucleic Acids Res 45:D362–D368

    Article  PubMed  CAS  Google Scholar 

  • Tixier A, Sperling O, Orozco J, Lampinen B, Amico Roxas A, Saa S, Earles JM, Zwieniecki MA (2017) Spring bud growth depends on sugar delivery by xylem and water recirculation by phloem Münch flow in Juglans regia. Planta 246:495–508

    Article  PubMed  CAS  Google Scholar 

  • Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K (2010) Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol 51:1821–1839

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Williams LE, Lemoine R, Sauer N (2000) Sugar transporters in higher plants—a diversity of roles and complex regulation. Trends Plant Sci 5:283–290

    Article  PubMed  CAS  Google Scholar 

  • Wong BL, Baggett KL, Rye AH (2003) Seasonal patterns of reserve and soluble carbohydrates in mature sugar maple (Acer saccharum). Can J Bot 81:780–788

    Article  CAS  Google Scholar 

  • Xing T, Wang XJ (2015) Protoplasts in plant signaling analysis: moving forward in the omics era. Botany 93:325–332

    Article  Google Scholar 

  • Zhang Q, Hu W, Zhu F, Wang L, Yu Q, Ming R, Zhang J (2016) Structure, phylogeny, allelic haplotypes and expression of sucrose transporter gene families in Saccharum. BMC Genomics 17:88

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology and Institute of Biochemistry, Carleton University, Ottawa, ON, K1S 5B6, Canada

    Ross Young, Root Gorelick & Tim Xing

Authors
  1. Ross Young
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Root Gorelick
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tim Xing
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tim Xing.

Additional information

Communicated by A. Brunner

Electronic supplementary material

ESM 1

(DOCX 67 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Young, R., Gorelick, R. & Xing, T. Seasonal bulk xylem pressure in temperate broadleaf eudicot trees: a case study for sugar long-distance transport and signaling. Tree Genetics & Genomes 14, 56 (2018). https://doi.org/10.1007/s11295-018-1272-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11295-018-1272-y

Keywords

Search

Navigation