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Salt stress affects xylem differentiation of grey poplar (Populus × canescens)

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Abstract

In this study the impact of salt stress on the physiology and wood structure of the salt-sensitive Populus × canescens was investigated. Two weeks of salt stress altered wood anatomy significantly. The xylem differentiation zone was reduced and the resulting vessels exhibited reduced lumina. To understand this phenomenon, ion composition, levels of corresponding transcripts and of the stress hormone ABA were analysed. With increasing sodium and chloride concentrations, a general reduction of potassium was found in roots and shoots, but not in leaves. Consequently, the corresponding K+ channel transcripts in roots favoured K+ release. The overall osmolarity in leaves was up to fourfold higher than in roots or shoots. Therefore, adjustment of the K+/Na+ balance seemed not to be required in leaves. Sodium increased gradually from roots to shoots and then to leaves indicating that sodium storage took place first in roots, then in shoots, and finally in leaves to protect photosynthesis from salt effects as long as possible. Since leaf abscisic acid levels markedly increased, stomatal closure seemed to limit CO2 uptake. As a consequence, diminished nutrient supply to the cambium in combination with lowered shoot K+ content led to decreased vessel lumina, and a reduction of the radial cambium was observed. Thus, xylem differentiation was curtailed and the development of full size vessels was impaired.

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Abbreviations

ABA:

Abscisic acid

PCR:

Polymerase chain reaction

TEM:

Transmission electron microscopy

EDXA:

Energy-dispersive X-ray analysis

References

  • An YQ, McDowell JM, Huang S, McKinney EC, Chambliss S, Meagher RB (1996) Strong, constitutive expression of the Arabidopsis ACT2/ACT8 actin subclass in vegetative tissues. Plant J 10:107–121

    Article  PubMed  CAS  Google Scholar 

  • Arend M, Stinzing A, Wind C, Langer K, Latz A, Ache P, Fromm J, Hedrich R (2005) Polar localised poplar K+ channel capable of controlling electrical properties of wood forming cells. Planta 223:140–148

    Article  PubMed  CAS  Google Scholar 

  • Behl R, Jeschke WD, Hartung W (1981) A compartmental analysis of abscisic acid in roots of Hordeum distichon. J Exp Bot 32:889–897

    Article  CAS  Google Scholar 

  • Bolu WH, Polle A (2002) Growth and stress reactions in roots and shoots of a salt-sensitive poplar species (Populus canescens). J Tropic Ecol 45:161–171

    Google Scholar 

  • Brüggemann N, Schnitzler JP (2002) Comparison of isoprene emission, intercellular isoprene concentration and photosynthetic performance in water-limited oak (Quercus pubescens Willd. and Quercus robur L.) saplings. Plant Biol 4:456–463

    Article  Google Scholar 

  • Chang Y, Chen SL, Yin WL, Wang RG, Liu YF, Shi Y, Shen YY, Li Y, Jiang J, Liu Y (2006) Growth, gas exchange, abscisic acid, and calmodulin response to salt stress in three poplars. J Integr Plant Biol 48:286–293

    Article  CAS  Google Scholar 

  • Chen S, Li J, Wang S, Hüttermann A, Altman A (2001) Salt, nutrient uptake and transport, and ABA of Populus euphratica; a hybrid in response to increasing soil NaCl. Trees 15:186–194

    Article  CAS  Google Scholar 

  • Chen S, Li J, Wang T, Wang S, Polle A, Hüttermann A (2002) Osmotic stress and ion-specific effects on xylem abscisic acid and the relevance to salinity tolerance in poplar. J Plant Growth Regul 21:224–233

    Article  CAS  Google Scholar 

  • Cheong YH, Chang HS, Gupta R, Wang X, Zhu T, Luan S (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol 129:661–677

    Article  PubMed  CAS  Google Scholar 

  • Dluzniewska P, Gessler A, Dietrich H, Schnitzler JP, Teuber M, Rennenberg H (2007) Nitrogen uptake and metabolism in Populus × canescens as affected by salinity. New Phytol 173:279–293

    Article  PubMed  CAS  Google Scholar 

  • Ehlting B, Dluzniewska P, Dietrich H, Selle A, Teuber M, Hänsch R, Nehls U, Polle A, Schnitzler JP, Rennenberg H, Gessler A (2007) Interaction of nitrogen nutrition and salinity in Grey poplar (Populus tremula × alba). Plant Cell Environ 30:796–811

    Article  PubMed  CAS  Google Scholar 

  • Emmerlich V, Linka N, Reinhold T, Hurth MA, Traub M, Martinoia E, Neuhaus HE (2003) The plant homolog to the human sodium/dicarboxylic cotransporter is the vacuolar malate carrier. Proc Natl Acad Sci USA 100:11122–11126

    Article  PubMed  CAS  Google Scholar 

  • Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55:307–319

    Article  PubMed  CAS  Google Scholar 

  • Fung LE, Wang SS, Altman A, Hütterman A (1998) Effect of NaCl on growth, photosynthesis, ion and water relations of four poplar genotypes. Forest Ecol Manage 107:135–146

    Article  Google Scholar 

  • Gaymard F, Pilot G, Lacombe B, Bouchez D, Bruneau D, Boucherez J, Michaux-Ferrière N, Thibaud JB, Sentenac H (1998) Identification and disruption of a plant shaker-like outward channel involved in K+ release into the xylem sap. Cell 94:647–655

    Article  PubMed  CAS  Google Scholar 

  • Gerlach D (1969) A rapid safranin-crystal violet-light green staining sequence for paraffin sections of plant materials. Stain Technol 44:210–211

    PubMed  CAS  Google Scholar 

  • Gorham J, Bridges J, Dubcovsky J, Dvorak J, Hollington PA, Luo MC, Kahn JA (1997) Genetic analysis and physiology of a trait for enhanced K+/Na+ discrimination in wheat. New Phytol 137:109–116

    Article  CAS  Google Scholar 

  • Hedrich R, Kudla J (2006) Calcium signalling networks channel plant K+ uptake. Cell 125:1221–1223

    Article  PubMed  CAS  Google Scholar 

  • Hewitt EJ (1966) Sand and water culture methods used in the study of plant nutrition. In: Commonwelth Bureau of Horticulture and Plantation Crops, East Malling, Technical Communication No. 22, 2nd rev edn, Commonwealth Agriculture Bureau Farnham Royal, UK, pp 430–439

  • Hoagland DR, Snijder WC (1933) Nutrition of strawberry plants under controlled conditions. Proc Am Soc Hortic 30:288–296

    Google Scholar 

  • Hu L, Lu H, Liu Q, Chen X, Jiang X (2005) Overexpression of mtlD gene in transgenic Populus tomentosa improves salt tolerance through accumulation of mannitol. Tree Physiol 25:1273–1281

    PubMed  CAS  Google Scholar 

  • Hurth MA, Suh SJ, Kretzschmar T, Geis T, Bregante M, Gambale F, Martinoia E, Neuhaus HE (2005) Impaired pH homeostasis in Arabidopsis lacking the vacuolar dicarboxylate transporter and analysis of carboxylic acid transport across the tonoplast. Plant Physiol 137:901–910

    Article  PubMed  CAS  Google Scholar 

  • Jia W, Wang Y, Zhang S, Zhang J (2002) Salt-stress-induced ABA accumulation is more sensitively triggered in roots than in shoots. J Exp Bot 53:2201–2206

    Article  PubMed  CAS  Google Scholar 

  • Junghans U, Polle A, Düchting P, Weiler E, Kuhlman B, Gruber F, Teichmann T (2006) Adaptation to high salinity in poplar involves changes in xylem anatomy and auxin physiology. Plant Cell Environ 29:1519–1531

    Article  PubMed  CAS  Google Scholar 

  • Karmoker JL, van Steveninck RFM (1979) The effect of abscisic acid on the uptake and distribution of ions in intact seedlings of Phaseolus vulgaris cv. Redland Pioneer. Physiol Plantarum 45:453–459

    Article  CAS  Google Scholar 

  • Kozlowski TT (1997) Responses of woody plants to flooding and salinity. Tree Physiol Monographs No. 1. Heron Publishing, Victoria

    Google Scholar 

  • Kurkela S, Borg-Franck M (1992) Structure and expression of kin2, one of two cold- and ABA-induced genes of Arabidopsis thaliana. Plant Mol Biol 19:689–692

    Article  PubMed  CAS  Google Scholar 

  • Langer K, Ache P, Geiger D, Stinzing A, Arend M, Wind C, Regan S, Fromm J, Hedrich R (2002) Poplar potassium transporters capable of controlling K+ homeostasis and K+-dependent xylogenesis. Plant J 32:997–1009

    Article  PubMed  CAS  Google Scholar 

  • Langer K, Levchenko V, Fromm J, Geiger D, Steinmeyer R, Lautner S, Ache P, Hedrich R (2004) The poplar K+ channel KPT1 is associated with K+ uptake during stomatal opening and bud development. Plant J 37:828–838

    Article  PubMed  CAS  Google Scholar 

  • Lautner S, Ehlting B, Windeisen E, Rennenberg H, Matyssek R, Fromm J (2007) Calcium nutrition has a significant influence on wood formation in poplar. New Phytol 173:743–752

    Article  PubMed  CAS  Google Scholar 

  • Liu W, Fairbairn DJ, Reid RJ, Schachtman DP (2001) Characterization of two HKT1 homologues from Eucalyptus camaldulensis that display intrinsic osmosensing capability. Plant Physiol 127:283–294

    Article  PubMed  CAS  Google Scholar 

  • Ma H, Fung L, Wang S, Altman A, Hüttermann A (1996) Preliminary study on the salt resistance mechanisms of Populus euphratica. J Beijing For Univ 5:31–40

    Google Scholar 

  • Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158

    Article  PubMed  CAS  Google Scholar 

  • Mertens RJ, Deus-Neumann B, Weiler EW (1985) Monoclonal antibodies for the detection and quantitation of endogenous plant growth regulator, abcisc acid. FEBS Lett 160:269–272

    Article  Google Scholar 

  • Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167:645–663

    Article  PubMed  CAS  Google Scholar 

  • Ottow EA, Polle A, Brosche M, Kangasjarvi J, Dibrov P, Zorb C, Teichmann T (2005a) Molecular characterization of PeNhaD1: the first member of the NhaD Na+/H+ antiporter family of plant origin. Plant Mol Biol 58:75–88

    Article  PubMed  CAS  Google Scholar 

  • Ottow EA, Brinker M, Teichmann T, Fritz E, Kaiser W, Brosche M, Kangasjarvi J, Jiang X, Polle A (2005b) Populus euphratica displays apoplastic sodium accumulation, osmotic adjustment by decreases in calcium and soluble carbohydrates, and develops leaf succulence under salt stress. Plant Physiol 139:1762–1772

    Article  PubMed  CAS  Google Scholar 

  • Peuke AD, Jeschke WD, Hartung W (1994) The uptake and flow of C, N and ions between roots and shoots in Ricinus communis L. III. Long-distance transport of abscisic acid depending on nitrogen nutrition and salt stress. J Exp Bot 45:741–747

    Article  CAS  Google Scholar 

  • Rubio F, Gassmann W, Schroeder JI (1995) Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science 270:1660–1663

    Article  PubMed  CAS  Google Scholar 

  • Rus A, Lee BH, Munoz-Mayor A, Sharkhuu A, Miura K, Zhu JK, Bressan RA, Hasegawa PM (2004) AtHKT1 facilitates Na homeostasis and K nutrition in planta. Plant Physiol 136:2500–2511

    Article  PubMed  CAS  Google Scholar 

  • Sanderson JB (1994) Biological microtechnique. Microscopy handbooks 28, Royal Microscopical Society. Bios Scientific Publishers, Oxford

    Google Scholar 

  • Shi H, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci USA 97:6896–6901

    Article  PubMed  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217–223

    PubMed  CAS  Google Scholar 

  • Spurr AE (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–41

    Article  PubMed  CAS  Google Scholar 

  • Szyroki A, Ivashikina N, Dietrich P, Roelfsema MR, Ache P, Reintanz B, Deeken R, Godde M, Felle H, Steinmeyer R, Palme K, Hedrich R (2001) KAT1 is not essential for stomatal opening. Proc Natl Acad Sci USA 98:2917–2921

    Article  PubMed  CAS  Google Scholar 

  • Teuber M, Zimmer I, Kreuzwieser J, Ache P, Polle A, Rennenberg H, Schnitzler J-P (2008) VOC emission of Grey poplar leaves as affected by salt stress and different N sources. Plant Biol 10:86–96

    PubMed  CAS  Google Scholar 

  • Uozumi N, Kim EJ, Rubio F, Yamaguchi T, Muto S, Tsuboi A, Bakker EP, Nakamura T, Schroeder JI (2000) The Arabidopsis HKT1 gene homolog mediates inward Na+ currents in xenopus laevis oocytes and Na+ uptake in Saccharomyces cerevisiae. Plant Physiol 122:1249–1259

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Datla R, Georges F, Loewen M, Cutler AJ (1995) Promoters from kin1 and cor6.6, two homologous Arabidopsis thaliana genes: transcriptional regulation and gene expression induced by low temperature, ABA, osmoticum and dehydration. Plant Mol Biol 28:605–617

    Article  PubMed  CAS  Google Scholar 

  • Webb MS, Gilmour SJ, Thomashow MF, Steponkus PL (1996) Effects of COR6.6 and COR15am polypeptides encoded by COR cold-regulated) genes of Arabidopsis thaliana on dehydration-induced phase transitions of phospholipid membranes. Plant Physiol 111:301–312

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi T, Blumwald E (2005) Developing salt-tolerant crop plants: challenges and opportunities. Trends Plant Sci 10:615–620

    Article  PubMed  CAS  Google Scholar 

  • Zhang JZ, Creelman RA, Zhu JK (2004) From laboratory to field. Using information from Arabidopsis to engineer salt, cold, and drought tolerance in crops. Plant Physiol 135:615–621

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Ute Neef for technical assistance and Duncan Cameron (University of Sheffield, UK) and Lois Banta (Haverford College, PA, USA) for carefully reading of the manuscript and helpful comments. The study was supported financially by the German Science Foundation (DFG; Ache: AC97/4-2, Schnitzler: SCHN653/4, Nehls: Ne332/9-1, Fromm: Fr955/10-2, and Polle: PO362/13) within the German joint research group ‘Poplar—A model to address tree-specific questions’.

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Correspondence to Peter Ache.

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María Escalante-Pérez and Silke Lautner contributed equally to this work.

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Escalante-Pérez, M., Lautner, S., Nehls, U. et al. Salt stress affects xylem differentiation of grey poplar (Populus × canescens). Planta 229, 299–309 (2009). https://doi.org/10.1007/s00425-008-0829-7

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