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Phloem loading, plant growth form, and climate

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Abstract

Plasmodesmatal frequencies in the phloem of leaf minor veins vary considerably, suggesting that photoassimilate is loaded into the phloem by different strategies. The ecophysiological basis for multiple loading types is unknown. We updated the analysis of van Bel and Gamalei (Plant Cell Environ 15: 265–270, 1992) with more current phylogenetic data and by treating separately two symplastic loading types, those that load actively by polymer trapping (synthesis of raffinose family oligosaccharides—RFOs), and those that load passively, by diffusion. The results indicate a stronger association between passive, symplastic loading and the tree growth form than previously recognized. Apoplastic loading is highly correlated with the herbaceous habit. There is no correlation between RFO families and growth form. At the family level, there are no correlations between minor vein types and climate that cannot be explained by the dearth of woody plants in the arctic for reasons unassociated with phloem loading. However, at the species level, a floristic analysis uncovered a correlation between the RFO trait and species frequency in tropical and subtropical regions of the world. The correlations between loading types and both growth form and climate are subtle, probably indirect, and poorly understood.

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References

  • Albach DC, Meudt HM, Oxelman B (2005) Piecing together the “new” Plantaginaceae. Am J Bot 92:297–315

    Article  Google Scholar 

  • Amiard V, Demmig-Adams B, Mueh KE, Turgeon R, Combs AF, Adams WW III (2007) Role of light and jasmonic acid signaling in regulating foliar phloem cell wall ingrowth development. New Phytol 173:722–731

    Article  CAS  PubMed  Google Scholar 

  • Arnold TH, de Wet BC (1993) Plants of southern Africa: names and distributions. National Botanical Institute, Pretoria

    Google Scholar 

  • Bachmann M, Matile P, Keller F (1994) Metabolism of the raffinose family oligosaccharides in leaves of Ajuga reptans L. Cold acclimation, translocation, and sink to source transition: discovery of chain elongation enzyme. Plant Physiol 105:1335–1345

    CAS  PubMed  Google Scholar 

  • Balick MJ, Nee MH, Atha DE (2000) Checklist of the vascular plants of Belize, with common names and uses. New York Botanical Garden, Bronx

    Google Scholar 

  • Brochmann C, Rustan O, Lobin W, Kilian N (1997) The endemic vascular plants of the Cape Verde Islands, W. Africa. Botanical Garden and Museum, University of Oslo, Oslo

    Google Scholar 

  • Cabrera AL (1953) Manual de la Flora de los Alrededores de Buenos Aires. Editorial Acme, S.A, Buenos Aires

    Google Scholar 

  • Casali C (1901) Flora Irpina. R. Scuola di viticoltura ed enologia di Avellino, Avellino

    Google Scholar 

  • Clokey IW (1951) Flora of the Charleston Mountains, Clark County, Nevada. University of California Press, Berkeley

    Google Scholar 

  • Croat TB (1978) Flora of Barro Colorado Island. Stanford University Press, Stanford

    Google Scholar 

  • deVol CE, Hsu S-T, Huang T-C, Jeng Y-C, Kuo C-M, Li H-L, Liu T-S, Lu T-S (1979) Flora of Taiwan. Epoch Press, Taipei

    Google Scholar 

  • Dinant S, Lemoine R (2010) The phloem pathway: new issues and old debates. C R Biol 333:307–319

    Article  CAS  PubMed  Google Scholar 

  • Dodson CH, Gentry AH (1978) Flora of the Rîo Palenque Science Center. Los Rîos, Equador. Marie Selby Botanical Gardens, Sarasota

    Google Scholar 

  • Eggers HFA (1897) The Flora of St. Croix and the Virgin Islands. Government Printing Office, Washington

    Google Scholar 

  • Farr EM (1907) Contributions to a catalog of the Flora of the Canadian Rocky Mountains and the Selkirk Range. University of Pennsylvania, Philadelphia

    Google Scholar 

  • Fisher DG (1986) Ultrastructure, plasmodesmatal frequency, and solute concentration in green areas of variegated Coleus blumei Benth. leaves. Planta 169:141–152

    Article  Google Scholar 

  • Flora LL, Madore MA (1993) Stachyose and mannitol transport in olive (Olea europaea L.). Planta 189:484–490

    Article  CAS  Google Scholar 

  • Flora LL, Madore MA (1996) Significance of minor-vein anatomy to carbohydrate transport. Planta 198:171–178

    Article  CAS  Google Scholar 

  • Fosberg FR, Renvoize SA (1980) The Flora of Aldabra and neighbouring islands. H. M. Stationery Office, London

    Google Scholar 

  • Gamalei Y (1989) Structure and function of leaf minor veins in trees and herbs. Trees 3:96–110

    Article  Google Scholar 

  • Gamalei Y (1991) Phloem loading and its development related to plant evolution from trees to herbs. Trees 5:50–64

    Article  Google Scholar 

  • Gamalei Y (2007) The role of mesophyll cell tonoplast in determining the route of phloem loading. Thirty years of the studies of phloem loading. Russ J Plant Physiol 54:1–9

    Article  CAS  Google Scholar 

  • Gooding E, Loveless AR, Proctor GR (1965) Flora of Barbados. H. M. Stationary Office, London

    Google Scholar 

  • Gould LL, Ender RW, Champlin RE, Stuckey IH (1998) Vascular Flora of Rhode Island. Rhode Island Natural History Survey, Kingston

    Google Scholar 

  • Greenwell RA (1935) A Flora of Nelson County, Kentucky. Nazateth College, Louisville

    Google Scholar 

  • Grusak MA, Beebe DU, Turgeon R (1996) Phloem loading. In: Zamski E, Schaffer AA (eds) Photoassimilate distribution in plants and crops. Marcel Dekker, New York, pp 209–277

    Google Scholar 

  • Guha Bakshi DN (1984) Flora of Murshidabad District, West Bengal, India. Scientific, Jodhpur

    Google Scholar 

  • Haritatos E, Medville R, Turgeon R (2000) Minor vein structure and sugar transport in Arabidopsis thaliana. Planta 211:105–111

    Article  CAS  PubMed  Google Scholar 

  • Haslam SM, Sell PD, Wolseley PA (1977) A Flora of the Maltese Islands. Malta University Press, Malta

    Google Scholar 

  • Heywood VH (1978) Flowering plants of the world. Mayflower Books, New York

    Google Scholar 

  • Heywood VH, Brummitt RK, Culham A, Seberg O (2007) Flowering plant families of the world. Firefly Books, Buffalo

    Google Scholar 

  • Higley W, Raddin CS (1891) The Flora of Cook County, Illinois, and a part of Lake County, Indiana. Chicago Academy of Sciences, Chicago

    Google Scholar 

  • Hillebrand W (1888) Flora of the Hawaiian Islands: a description of their phanerogams and vascular crytogams. Williams & Norgate, London

    Google Scholar 

  • Hobbie SE, Chapin FS (1998) An experimental test of limits to tree establishment in Arctic tundra. J Ecol 86:449–461

    Article  Google Scholar 

  • Holthaus U, Schmitz K (1991) Distribution and immunolocalization of stachyose synthase in Cucumis melo L. Planta 185:479–486

    Article  CAS  Google Scholar 

  • Jelliffe SE (1899) The Flora of Long Island. The New Era Printing Company, Lancaster

    Google Scholar 

  • Jessop J (1981) Flora of Central Australia. AH & AW Reed, Sydney

    Google Scholar 

  • Kandler O (1967) Biosynthesis of poly- and oligosaccharides during photosynthesis in green plants. In: San Pietro A, Greer FA, Army TJ (eds) Harvesting the sun. Photosynthesis in plant life. Academic, New York, pp 131–152

    Google Scholar 

  • King RW, Zeevaart JAD (1974) Enhancement of phloem exudation from cut petioles by chelating agents. Plant Physiol 53:96–103

    Article  CAS  PubMed  Google Scholar 

  • Körner C (1998) A re-assessment of high elevation treeline positions and their explanation. Oecologia 115:445–459

    Article  Google Scholar 

  • Madore MA (1990) Carbohydrate metabolism in photosynthetic and nonphotosynthetic tissues of variegated leaves of Coleus blumei Benth. Plant Physiol 93:617–622

    Article  CAS  PubMed  Google Scholar 

  • Madore MA, Mitchell DE, Boyd CM (1988) Stachyose synthesis in source leaf tissues of the CAM plant Xerosicyos danguyi H. Humb. Plant Physiol 87:588–591

    Article  CAS  PubMed  Google Scholar 

  • Maheshwari JK (1963) The Flora of Delhi. Council of Scientific & Industrial Research, New Delhi

    Google Scholar 

  • McVaugh R (1958) Flora of the Columbia County Area, New York. University of the State of New York, Albany

    Google Scholar 

  • Metz MC (1934) A Flora of Bexar County, Texas. Catholic University of America, Washington

    Google Scholar 

  • Moore DM (1968) The vascular Flora of the Falkland Islands. Natural Environment Research Council, London

    Google Scholar 

  • Moss EH (1983) Flora of Alberta: a manual of flowering plants, conifers, ferns, and fern allies found growing without cultivation in the Province of Alberta, 2nd edn. University of Toronto, Toronto

    Google Scholar 

  • Niland S, Schmitz K (1995) Sugar transport into storage tubers of Stachys sieboldii Miq.: evidence for symplastic unloading and stachyose uptake into storage vacuoles by an H+-antiport mechanism. Bot Acta 108:24–33

    CAS  Google Scholar 

  • Olmstead RG, dePamphilis CW, Wolfe AD, Young ND, Elisons WJ, Reeves PA (2001) Disintegration of the Scrophulariaceae. Am J Bot 88:348–361

    Article  CAS  PubMed  Google Scholar 

  • Pate JS, Gunning BES (1969) Vascular transfer cells in angiosperm leaves. A taxonomic and morphological survey. Protoplasma 68:135–156

    Article  Google Scholar 

  • Porsild AE (1973) Illustrated Flora of the Canadian Arctic Archipelago. National Museums of Canada, Ottawa

    Google Scholar 

  • Robertson SA (1989) Flowering plants of Seychelles. Royal Botanic Gardens, Kew

    Google Scholar 

  • Sauer N (2007) Molecular physiology of higher plant sucrose transporters. FEBS Lett 581:2309–2317

    Article  CAS  PubMed  Google Scholar 

  • Schrier AA, Hoffmann-Thoma G, van Bel AJE (2000) Temperature effects on symplasmic and apoplasmic phloem loading and loading-associated carbohydrate processing. Aust J Plant Physiol 27:769–778

    CAS  Google Scholar 

  • Schulz A (2005) Role of plasmodesmata in solute loading and unloading. In: Oparka KJ (ed) Plasmodesmata. Blackwell, Oxford, pp 135–161

    Chapter  Google Scholar 

  • Senser M, Kandler O (1967) Galactinol, ein Galactosyldonor für die Biosynthese der Zucker der Raffinosefamilie in Blättern. Z Pflanzenphysiol 57:376–388

    CAS  Google Scholar 

  • Slewinski TL, Braun DM (2010) Current perspectives on the regulation of whole-plant carbohydrate partitioning. Plant Sci 178:341–349

    Article  CAS  Google Scholar 

  • Smith CF (1976) A Flora of the Santa Barbara region, California. Santa Barbara Museum of Natural History, Santa Barbara

    Google Scholar 

  • Smith GL, Wheeler CR (1992) A Flora of the vascular plants of Mendocino County, California. University of San Francisco, San Francisco

    Google Scholar 

  • Soper JH, Glauce EG, Given DR (1989) Flora of the north shore of Lake Superior. National Museums of Canada, Ottawa

    Google Scholar 

  • Turgeon R (2010) The role of phloem loading reconsidered. Plant Physiol 152:1817–1823

    Article  CAS  PubMed  Google Scholar 

  • Turgeon R, Ayre BG (2005) Pathways and mechanisms of phloem loading. In: Holbrook NM, Zwieniecki MA (eds) Vascular transport in plants. Elsevier/Academic, Oxford, pp 45–67

    Chapter  Google Scholar 

  • Turgeon R, Medville R (2004) Phloem loading. A reevaluation of the relationship between plasmodesmatal frequencies and loading strategies. Plant Physiol 136:3795–3803

    Article  CAS  PubMed  Google Scholar 

  • Turgeon R, Medville R (2010) Amborella trichopoda, plasmodesmata and the evolution of phloem loading. Protoplasma (in press; this volume)

  • Turgeon R, Wolf S (2009) Phloem transport: cellular pathways and molecular trafficking. Annu Rev Plant Biol 60:207–210

    Article  CAS  PubMed  Google Scholar 

  • Turgeon R, Webb JA, Evert RF (1975) Ultrastructure of minor veins in Cucurbita pepo leaves. Protoplasma 83:217–231

    Article  Google Scholar 

  • Turgeon R, Beebe DU, Gowan E (1993) The intermediary cell: minor-vein anatomy and raffinose oligosaccharide synthesis in the Scrophulariaceae. Planta 191:446–456

    Article  CAS  Google Scholar 

  • Turgeon R, Medville R, Nixon KC (2001) The evolution of minor vein phloem and phloem loading. Am J Bot 88:1331–1339

    Article  Google Scholar 

  • van Bel AJE (2003) The phloem, a miracle of ingenuity. Plant Cell Environ 26:125–149

    Article  Google Scholar 

  • van Bel AJE, Gamalei YV (1992) Ecophysiology of phloem loading in source leaves. Plant Cell Environ 15:265–270

    Article  Google Scholar 

  • van Bel AJE, Gamalei YV, Ammerlaan A, Bik LPM (1992) Dissimilar phloem loading in leaves with symplasmic or apoplasmic minor-vein configurations. Planta 186:518–525

    Article  Google Scholar 

  • Vásquez R (1997) Flórula de las reservas biológicas de Iquitos, Perú. Missouri Botanical Garden, St. Louis

    Google Scholar 

  • Vazquez J, Cuevas R, Cochrane TS, Iltis HH, Santana FJ, Guzman L (1995) Flora de Mantalan. Botanical Research Institute of Texas, Fort Worth

    Google Scholar 

  • Voitsekhovskaja OV, Koroleva OA, Batashev DR, Knop C, Tomos AD, Gamalei YV, Heldt HW, Lohaus G (2006) Phloem loading in two Scrophulariaceae species. What can drive symplastic flow via plasmodesmata? Plant Physiol 140:383–395

    Article  CAS  PubMed  Google Scholar 

  • Voitsekhovskaja OV, Rudashevskaya EL, Demchenko KN, Pakhomova MV, Batashev DR, Gamalei YV, Lohaus G, Pawlowski K (2009) Evidence for functional heterogeneity of sieve element–companion cell complexes in minor vein phloem of Alonsoa meridionalis. J Exp Bot 60:1873–1883

    Article  CAS  PubMed  Google Scholar 

  • Walker EH (1976) Flora of Okinawa and the Southern Ryuku Islands. Smithsonian Institution Press, Washington

    Google Scholar 

  • Wiegand KM, Eames AJ (1926) The Flora of the Cayuga Lake basin, New York. Cornell University, Ithaca

    Google Scholar 

  • Wiggens IL, Thomas JH (1945) A Flora of the Alaskan Arctic slope. University of Toronto Press, Toronto

    Google Scholar 

  • Wiggins IL, Porter DM (1971) Flora of the Galápagos Islands. Stanford University Press, Stanford

    Google Scholar 

  • Yuncker TG (1943) The Flora of Niue Island. Bishop Museum Bulletin 178:1–130

    Google Scholar 

  • Yuncker TG (1945) Plants of the Manua Islands. Bishop Mus Bull 184:1–73

    Google Scholar 

  • Zimmermann M, Ziegler H (1975) List of sugars and sugar alcohols in sieve-tube exudates. In: Zimmermann MH, Milburn JA (eds) Encyclopedia of plant physiology, N. S., vol. 1 Transport in plants. 1: Phloem transport. Springer, New York, pp 480–503

    Google Scholar 

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Acknowledgments

We thank Kevin C. Nixon for advice and encouragement. This work was supported by the U.S.–Israel Binational Agricultural Research and Development Fund (grant no. IS-3884-06).

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The authors declare that they have no conflict of interest.

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Correspondence to Robert Turgeon.

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Davidson, A., Keller, F. & Turgeon, R. Phloem loading, plant growth form, and climate. Protoplasma 248, 153–163 (2011). https://doi.org/10.1007/s00709-010-0240-7

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