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Vessel development and the importance of lateral flow in water transport within developing bundles of current-year shoots of grapevine (Vitis vinifera L.)

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Abstract

In the developing xylem bundles of young stems, the presence of immature living vessel elements can strongly restrict or even block axial hydraulic conductance, especially in newly matured vessels. Lateral connections between vessels may provide an alternative pathway for water movement to bypass these closed, living elements. Using the grapevine as a model system, the present study aimed to demonstrate the effects of living vessel elements on water movement patterns, and the importance of lateral flow for effective water conductivity in the developing bundles. Living vessel elements were detected using dye staining and the pattern of vessel development and maturation was then monitored. The importance of lateral flow was confirmed using several approaches: (1) capacity for lateral flow, (2) effect of increasing the distance of water transport, and (3) effect of ion concentrations. Living vessel elements were found along the developing bundles, they occupied a significant proportion of the distal and peripheral parts of the flow path, forming a substantial barrier to apoplastic water flow. Water in the developing xylem bundles could move easily from vessel to vessel and between secondary and primary xylem. Furthermore, data from increasing the transport length and altering the ion concentrations supported the critical contribution of the lateral flow to the total hydraulic conductance within the developing bundles. The hydraulic architecture of the developing xylem bundles is described. The results are discussed in terms of reliability and efficiency of water transport during shoot growth and development.

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References

  • Bull TA, Gayler KR, Glasziou KT (1972) Lateral movement of water and sugar across xylem in sugarcane stalks. Plant Physiol 49:1007–1011

    Article  PubMed  CAS  Google Scholar 

  • Burggraaf PD (1972) Some observations on the course of the vessels in the wood of Fraxinus excelsior L. Acta Bot Neer 21:32–47

    Google Scholar 

  • Chatelet DS, Matthews MA, Rost TL (2006) Xylem structure and connectivity in grapevine (Vitis vinifera) shoots provides a passive mechanism for the spread of bacteria in grape plants. Ann Bot 98:483–494

    Article  PubMed  Google Scholar 

  • Chaves T, Regalado AP, Chen M, Ricardo CP, Showalter AM (2002) Programmed cell death induced by (β-d-galactosyl)3 Yariv reagent in Nicotiana tabacum BY-2 suspension-cultured cells. Physiol Plant 116:548–553

    Article  CAS  Google Scholar 

  • Comstock JP, Sperry JS (2000) Theoretical considerations for optimal conduit length for water transport in vascular plants. New Phytol 148:195–218

    Article  Google Scholar 

  • Cronshaw J, Bouck GB (1965) The fine structure of differentiating xylem elements. J Cell Biol 24:415–431

    Article  PubMed  CAS  Google Scholar 

  • Ellmore GS, Zanne AE, Orians CM (2006) Comparative sectoriality in temperate hardwoods: hydraulics and xylem anatomy. Bot J Linn Soc 150:61–71

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Frensch J, Steudle E (1989) Axial and radial hydraulic resistance to roots of maize (Zea mays L.). Plant Physiol 91:719–726

    Article  PubMed  CAS  Google Scholar 

  • Fujii T, Lee SJ, Kuroda N, Suzuki Y (2001) Conductive function of intervessel pits through a growth ring boundary of Machilus thunbergii. IAWA J 22:1–14

    Google Scholar 

  • Hacke UG, Sperry JS, Wheeler JK, Castro L (2006) Scaling of angiosperm xylem structure with safety and efficiency. Tree Physiol 26:619–701

    Article  Google Scholar 

  • Kitin P, Sano Y, Funada R (2001) Analysis of cambium and differentiating vessel elements in kalopanax pictus using resin cast replicas. IAWA J 22:15–28

    Google Scholar 

  • Kitin PB, Fujii T, Abe H, Funada R (2004) Anatomy of the vessel network within and between tree rings of Fraxinus lanuginosa (Oleaceae). Am J Bot 91:779–788

    Article  PubMed  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  Google Scholar 

  • Marshall C (1996) Sectoriality and physiological organization in herbaceous plants: an overview. Vegetation 127:9–16

    Article  Google Scholar 

  • McCulley M (1995) How do real roots work? Plant Physiol 109:1–6

    Google Scholar 

  • Meuser J, Frensch J (1998) Hydraulic properties of living late metaxylem and interactions between transpiration and xylem pressure in maize. J Exp Bot 49:69–77

    CAS  Google Scholar 

  • Milburn JA (1996) Sap ascent in vascular plants: challengers to the Cohesion theory ignore the significance of immature xylem and the recycling of Munch water. Ann Bot 78:399–407

    Article  Google Scholar 

  • Orians CM, Jones CG (2001) Plants as resource mosaics: a functional model for predicting patterns of within-plant resource heterogeneity to consumers based on vascular architecture and local environmental variability. Oikos 94:493–504

    Article  Google Scholar 

  • Orians CM, van Vuuren MM, Harris NL, Babst BA, Ellmore GS (2004) Differential sectoriality in long distance transport in temperate tree species, evidence from dye flow, 15 N transport, and vessel element pitting. Trees 18:501–509

    Article  Google Scholar 

  • Orians CM, Smith SDP, Sack L (2005) How are leaves plumbed inside a branch? Differences in leaf-to-leaf hydraulic sectoriality among six temperate tree species. J Exp Bot 56:2267–2273

    Article  PubMed  CAS  Google Scholar 

  • Salleo S, LoGullo MA, Oliveri F (1985) Hydraulic parameters measured in 1-year-old twigs of some Mediterranean species with diffuse-porous wood. J Exp Bot 36:1–11

    Article  Google Scholar 

  • Schubert A, Lovisolo C, Peterlunger E (1999) Shoot orientation effects vessel size, shoot hydraulic conductivity and shoot growth rate in Vitis vinifera L. Plant Cell Environ 22:197–204

    Article  PubMed  CAS  Google Scholar 

  • Shane MW, McCully ME, Canny MJ (2000) Architecture of branch root junctions in maize: structure of the connecting xylem and the porosity of pit membranes. Ann Bot 85:613–624

    Article  Google Scholar 

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

    Article  Google Scholar 

  • St Aubin G, Canny MJ, McCully ME (1986) Living vessel elements in the late metaxylem of sheathed maize roots. Ann Bot 58:577–588

    Article  Google Scholar 

  • Stevenson JF, Matthews MA, Greve LC, Labavitch JM, Rost TL (2004) Grapevine susceptibility to Pierce’s disease. I. Relevance of hydraulic architecture. Am J Enol Vitic 55:228–237

    Google Scholar 

  • Sun Q, Rost TL, Matthews MA (2006) Pruning-induced tylose development stem of current-year shoots of Vitis vinifera (Vitaceae). Am J Bot 93:1567–1576

    Article  PubMed  CAS  Google Scholar 

  • Taneda H, Tateno M (2007) Effects of transverse movement of water in xylem on patterns of water transport within current-year shoots of kudzu vine, Pueraria lobata. Funct Ecol 21:226–234

    Article  Google Scholar 

  • Thorne ET, Young BM, Young GM, Stevenson JF, Labavitch JM, Matthews MA (2006) The structure of xylem vessels in grapevine and a possible passive mechanism for the systemic spread of bacterial disease. Am J Bot 93:497–504

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Tyree MT, Davis SD, Cochard H (1994) Biophysical perspective of xylem evolution: is there a tradeoff of hydraulic efficiency for vulnerability to disfunction? IAWA J 15:335–360

    Google Scholar 

  • Tyree MT, Zimmermann MH (2002) Xylem structure and the ascent of sap, 2nd edn. Springer, Berlin

    Google Scholar 

  • Van Ieperen W, Van Meeteren U, Van Gelder H (2000) Fluid ionic composition influences hydraulic conductance of xylem conduits. J Exp Bot 51:769–776

    Article  PubMed  Google Scholar 

  • Vuorisalo T, Hutchings MJ (1996) On plant sectoriality, or how to combine the benefits of autonomy and integration. Vegetation 127:3–8

    Article  Google Scholar 

  • Wheeler JK, Sperry JS, Hacke UG, Hoang N (2005) Intervessel 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

    Article  Google Scholar 

  • Zanne AE, Sweeney K, Sharma M, Orians CM (2006) Patterns and consequences of differential vascular sectoriality in 18 temperate trees and shrub species. Funct Ecol 20:200–206

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Zwieniecki MA, Melcher PJ, Holbrook NM (2001a) Hydrogel control of xylem hydraulic resistance in plants. Science 29:1059–1062

    Article  Google Scholar 

  • Zwieniecki MA, Melcher PJ, Holbrook NM (2001b) Hydraulic properties of individual xylem vessels of Fraxinus americana. J Exp Bot 52:1–8

    Article  Google Scholar 

  • Zwieniecki MA, Orians CM, Melcher PJ, Holbrook NM (2003) Ionic control of the lateral exchange of water between vascular bundles in tomato. Ann Bot 54:1399–1405

    CAS  Google Scholar 

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Acknowledgments

We thank Abdelaziz Labidi and Belgacem Hadid for their support and assistance. Special thanks are extended to Drs. Hocine Bensaha, Mohamed Amine Benhadia, Mohamed Hocine Benaissa, Nouredine Slimani and the anonymous referees for helpful comments on earlier versions of this manuscript. We are also grateful to Sofiane Amira, Ali Lahcini, Abdessalem Bougafla and Saci Djouwahi for their technical support.

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Authors and Affiliations

  1. Laboratory of Biomolecules and Plant Amelioration, Larbi Benmhidi University of Oum El Bouaghi, BP 358, Constantine Road, 04000, Oum El Bouaghi, Algeria

    Youcef Halis, Samah Djehichi & Mohamed Mourad Senoussi

  2. Scientific and Technical Research Centre for Arid Areas (CRSTRA), Biophysical Station, 3240, Nezla, Touggourt, Algeria

    Youcef Halis

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  1. Youcef Halis
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  2. Samah Djehichi
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  3. Mohamed Mourad Senoussi
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Correspondence to Youcef Halis.

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Communicated by S. Mayr.

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Halis, Y., Djehichi, S. & Senoussi, M.M. Vessel development and the importance of lateral flow in water transport within developing bundles of current-year shoots of grapevine (Vitis vinifera L.). Trees 26, 705–714 (2012). https://doi.org/10.1007/s00468-011-0637-8

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  • DOI: https://doi.org/10.1007/s00468-011-0637-8

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