Salinity tolerance of Populus

Plant Biology

Volumn 12, Issue 2, 2010, Pages 317-333

  Chen, S ^a,b   Polle, A ^c  

^a BEIJING FORESTRY UNIVERSITY   (China)

^b HUBEI UNIVERSITY FOR NATIONALITIES   (China)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Gene transformation; Ion relations; NaCl; Osmoregulation; Potassium transporter and channel; ROS homeostasis; Salt stress signalling; Sodium proton antiporter

Indexed keywords

ANTIPORTER; CALCIUM; CHLORIDE; POTASSIUM; REACTIVE OXYGEN METABOLITE; SODIUM; SODIUM CHLORIDE; WATER;

ADAPTATION; BIOTECHNOLOGY; CROP PLANT; DICOTYLEDON; ECOTYPE; GENETIC ANALYSIS; ION; MORPHOLOGY; OSMOREGULATION; SALINITY TOLERANCE; SODIUM CHLORIDE;

ADAPTATION; ASPEN; DROUGHT; GENETICS; GENOTYPE; HALOPHYTE; METABOLISM; PHYSIOLOGY; REVIEW; SOIL; TRANSGENIC PLANT;

ADAPTATION, PHYSIOLOGICAL; ANTIPORTERS; CALCIUM; CHLORIDES; DROUGHTS; GENOTYPE; PLANTS, GENETICALLY MODIFIED; POPULUS; POTASSIUM; REACTIVE OXYGEN SPECIES; SALT-TOLERANT PLANTS; SODIUM; SODIUM CHLORIDE; SOIL; WATER;

POPULUS; POPULUS EUPHRATICA;

EID: 77952525618     PISSN: 14358603     EISSN: 14388677     Source Type: Journal    
DOI: 10.1111/j.1438-8677.2009.00301.x     Document Type: Review

References (122)

1. Arndt SK, Arampatsis C, Foetzki A, Li X, Zeng F, Zhang X. Contrasting patterns of leaf solute accumulation and salt adaptation in four phreatophytic desert plants in a hyperarid desert with saline groundwater. Journal of Arid Environments 2004, 59:259-270.
2. Arshi A, Abdin MZ, Lqbal M. Ameliorative effects of CaCl2 on growth, ionic relations, and proline content of senna under salinity stress. Journal of Plant Nutrition 2005, 28:101-125.
3. Barrero-Gil J, Rodríguez-Navarro A, Benito B. Cloning of the PpNHAD1 transporter of Physcomitrella patens, a chloroplast transporter highly conserved in photosynthetic eukaryotic organisms. Journal of Experimental Botany 2007, 58:2839-2849.
4. Beritognolo I, Piazzai M, Benucci S, Kuzminsky E, Sabatti M, Mugnozza GS, Muleo R. Functional characterisation of three Italian Populus alba L. genotypes under salinity stress. Trees - Structure and Function 2007, 21:465-477.
5. Blumwald E, Aharon GS, Apse MP. Sodium transport in plant cells. Biochimica et Biophysica Acta 2000, 1465:140-151.
6. Bogeat-Triboulot M, Brosché M, Renaut J, Jouve L, Le Thiec D, Fayyaz P, Vinocur B, Witters E, Laukens K, Teichmann T, Altman A, Hausman JF, Polle A, Kangasjärvi J, Dreyer E. Gradual soil water depletion results in reversible changes of gene expression, protein profiles, ecophysiology and growth performance in Populus euphratica, a poplar growing in arid regions. Plant Physiology 2007, 143:876-892.
7. Bohnert HJ, Gong Q, Li P, Ma S. Unraveling abiotic stress tolerance mechanisms - getting genomics going. Current Opinion in Plant Biology 2006, 9:180-188.
8. Bolu WH, Polle A. Growth and stress reactions in roots and shoots of a salt-sensitive poplar species (Populus × canescens). Tropical Ecology 2004, 45:161-171.
9. Brosché M, Vinocur B, Alatalo ER, Lamminmäki A, Teichmann T, Ottow EA, Djilianov D, Afif D, Bogeat-Triboulot M-B, Altman A, Polle A, Dreyer E, Rudd S, Paulin L, Auvinen P, Kangasjärvi J. Gene expression and metabolite profiling of Populus euphratica growing in the Negev Desert. Genome Biology 2005, 6:R101. 1-17
10. Caines AM, Shennan C. Interactive effects of Ca2+ and NaCl salinity on the growth of two tomato genotypes differing in Ca2+ use efficiency. Plant Physiology and Biochemistry 1999, 37:569-576.
11. Chang Y, Chen S, Yin W, Wang R, Liu Y, Shi Y, Shen Y, Li Y, Jiang J, Liu Y. Growth, gas exchange, ABA and CaM response to salt stress in three poplars. Journal of Integrative Plant Biology 2006, 48:286-293.
12. Chen C. PeNhaD1 gene transformation and salt resistance of transgenic Populus tomentosa. 2007, PhD dissertation, Beijing Forestry University, Beijing, China, in Chinese with English abstract
13. Chen S, Li J, Wang S, Hüttermann A, Altman A. Salt, nutrient uptake and transport and ABA of Populus euphratica; a hybrid in response to increasing soil NaCl. Trees - Structure and Function 2001, 15:186-194.
14. Chen S, Li J, Fritz E, Wang S, Hüttermann A. Sodium and chloride distribution in roots and transport in three poplar genotypes under increasing NaCl stress. Forest Ecology and Management 2002a, 168:217-230.
15. Chen S, Li J, Wang T, Wang S, Polle A, Hüttermann A. Osmotic stress and ion-specific effects on xylem abscisic acid and the relevance to salinity tolerance in poplar. Journal of Plant Growth Regulation 2002b, 21:224-233.
16. Chen S, Li J, Wang S, Fritz E, Hüttermann A, Altman A. Effects of NaCl on shoot growth, transpiration, ion compartmentation and transport in regenerated plants of Populus euphratica and Populus tomentosa. Canadian Journal of Forest Research 2003a, 33:967-975.
17. Chen S, Li J, Wang T, Wang S, Polle A, Hüttermann A. Gas exchange, xylem ions and abscisic acid response to Na+-salts and Cl--salts in Populus euphratica. Acta Botanica Sinica 2003b, 45:561-566.
18. Chen S, Zomorodi M, Fritz E, Wang S, Hüttermann A. Hydrogel modified uptake of salt ions and calcium in Populus euphratica under saline conditions. Trees - Structure and Function 2004, 18:175-183.
19. Chen Z, Newman I, Zhou M, Mendham N, Zhang G, Shabala S. Screening plants for salt tolerance by measuring K+ flux: a case study for barley. Plant, cell & environment 2005, 28:1230-1246.
20. Chen Z, Pottosin II, Cuin TA, Fuglsang AT, Tester M, Jha D, Zepeda-Jazo I, Zhou M, Palmgren MG, Newman IA, Shabala S. Root plasma membrane transporters controlling K+/Na+ homeostasis in salt stressed barley. Plant Physiology 2007, 145:1714-1725.
21. Chen S, Olbrich A, Langenfeld-Heyser R, Fritz E, Polle A. Quantitative X-ray microanalysis of hydrogen peroxide within plant cells. Microscopy Research and Technique 2009, 72:49-60.
22. Cuin TA, Betts SA, Chalmandrier R, Shabala S. A root's ability to retain K+ correlates with salt tolerance in wheat. Journal of Experimental Botany 2008, 59:2697-2706.
23. Dai S, Chen S, Fritz E, Olbrich A, Kettner C, Polle A, Hüttermann A. Ion compartmentation in leaf cells of Populus euphratica and P. tomentosa under salt stress. Journal of Beijing Forestry University 2006, 28:1-5. in Chinese with English abstract
24. Davenport RJ, Muñoz-Mayor A, Jha D, Essah PA, Rus A, Tester M. The Na+ transporter AtHKT1;1 controls retrieval of Na+ from the xylem in Arabidopsis. Plant, cell & environment 2007, 30:497-507.
25. Demidchik V, Maathuis FJM. Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development. New Phytologist 2007, 175:387-404.
26. Demidchik V, Davenport RJ, Tester MA. Nonselective cation channels in plants. Annual Review of Plant Biology 2002, 53:67-107.
27. Dluzniewska P, Gessler A, Dietrich H, Schnitzler J-P, Teuber M, Rennenberg H. Nitrogen uptake and metabolism in Populus × canescens as affected by salinity. New Phytologist 2007, 173:279-293.
28. Ehlting B, Dluzniewska P, Dietrich H, Selle A, Teuber M, Hänsch R, Nehls U, Polle A, Schnitzler J-P, Rennenberg H, Gessler A. Interaction of nitrogen nutrition and salinity in Grey poplar (Populus tremula × alba). Plant, cell & environment 2007, 30:796-811.
29. Escalante-Pérez M, Lautner S, Nehls U, Selle A, Teuber M, Schnitzler JP, Teichmann T, Fayyaz P, Hartung W, Polle A, Fromm J, Hedrich R, Ache P. Salt stress affects xylem differentiation of grey poplar (Populus × canescens). Planta 2009, 229:299-309.
30. Fayyaz P. Effects of salt stress on ecophysiological and molecular characteristics of Populus euphratica Olive., Populus × canescens (Aiton) Sm., and Arabidopsis thaliana. 2008, Thesis, Georg-August University Göttingen, Cuvillier Verlag Germany, pp
31. Finkelstein RR, Gampala SSL, Rock CD. Abscisic acid signaling in seeds and seedlings. Plant Cell 2002, 14:15-45.
32. Fukuda A, Nakamura A, Tagiri A, Tanaka H, Miyao A, Hirochika H, Tanaka Y. Function, intracellular localization and the importance in salt tolerance of a vacuolar Na+/H+ antiporter from rice. Plant and Cell Physiology 2004, 45:146-159.
33. Fung LE, Wang S, Altman A, Hüttermann A. Effect of NaCl on growth, photosynthesis, ion and water relations of four poplar genotypes. Forest Ecology and Management 1998, 107:135-146.
34. Gafur A, Schützendübel A, Langenfeld-Heyser R, Fritz E, Polle A. Compatible and incompetent Paxillus involutus isolates for ectomycorrhiza formation in vitro with poplar (Populus × canescens) differ in H2O2 production. Plant Biology 2004, 6:91-99.
35. Garbarino J, Dupont FM. NaCl induces a Na+/H+ antiport in tonoplast vesicles from barley roots. Plant Physiology 1988, 86:231-236.
36. Gries D, Zeng F, Foetzki A, Arndt SK, Bruelheide H, Thomas FM, Zhang X, Runge M. Growth and water relations of Tamarix ramosissima and Populus euphratica on Taklamakan Desert dunes in relation to depth to a permanent water table. Plant, cell & environment 2003, 26:725-736.
37. Gu R, Fonseca S, Puskás LG, Hackler LJ, Zvara A, Dudits D, Pais MS. Transcript identification and profiling during salt stress and recovery of Populus euphratica. Tree Physiology 2004a, 24:265-276.
38. Gu R, Liu Q, Pei D, Jiang X. Understanding saline and osmotic tolerance of Populus euphratica suspended cells. Plant Cell Tissue and Organ Culture 2004b, 78:261-265.
39. Guan L, Scandalios JG. Effects of the plant growth regulator abscisic acid and high osmoticum on the developmental expression of the maize catalase genes. Physiologia Plantarum 1998a, 104:413-422.
40. Guan L, Scandalios JG. Two structurally similar maize cytosolic superoxide dismutase genes, Sod4 and Sod4A, respond differentially to abscisic acid and high osmoticum. Plant Physiology 1998b, 117:217-224.
41. Guan LM, Zhao J, Scandalios JG. Cis-element and trans factors that regulate expression of maize Cat1 antioxidant gene in response to ABA and osmotic stress: H2O2 is the likely intermediary signaling molecule for the response. Plant Journal 2000, 22:87-95.
42. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ. Plant cellular and molecular responses to high salinity. Annual Review of Plant Physiology and Plant Molecular Biology 2000, 51:463-499.
43. Hibino T, Kaku N, Yoshikawa H, Takabe T, Takabe T. Molecular characterization of DnaK from the halotolerant cyanobacterium Aphanothece halophytica for ATPase, protein folding, and copper binding under various salinity conditions. Plant Molecular Biology 1999, 40:409-418.
44. Hu L, Lu H, Liu Q, Chen X, Jiang X. Overexpression of mtlD gene in transgenic Populus tomentosa improves salt tolerance through accumulation of mannitol. Tree Physiology 2005, 25:1273-1281.
45. Hukin D, Cochard H, Dreyer E, Le Thiec D, Bogeat-Triboulot MB. Cavitation vulnerability in roots and shoots: does Populus euphratica Oliv., a poplar from arid areas of Central Asia, differ from other poplar species? Journal of Experimental Botany 2005, 56:2003-2010.
46. Jouve L, Hoffmann L, Hausman JF. Polyamine, carbohydrate, and proline content changes during salt stress exposure of aspen (Populus tremula L.): involvement of oxidation and osmoregulation metabolism. Plant Biology 2004, 6:74-80.
47. Junghans U, Polle A, Düchting P, Weiler E, Kuhlman B, Gruber F, Teichmann T. Adaptation to high salinity in poplar involves changes in xylem anatomy and auxin physiology. Plant, cell & environment 2006, 29:1519-1531.
48. Kawano T, Kawano N, Muto S, Lapeyrie F. Cation-induced superoxide generation in tobacco cell suspension culture is dependent on ion valence. Plant, cell & environment 2001, 24:1235-1241.
49. Keitel C, Adams MA, Holst T, Matzarakis A, Mayer H, Rennenberg H, Geßler A. Carbon and oxygen isotope composition of organic compounds in the phloem sap provides a short-time measure for stomatal conductance of European beech (Fagus sylvativa). Plant, cell & environment 2003, 26:1157-1168.
50. Khamzina A, Lamers John PA, Martius C, Worbes M, Vlek PLG. Potential of nine multipurpose tree species to reduce saline groundwater tables in the lower Amu Darya River region of Uzbekistan. Agroforestry Systems 2006, 68:151-165.
51. Knight H, Knight MR. Abiotic stress signaling pathways: specificity and cross-talk. Trends in Plant Science 2001, 6:262-267.
52. Langenfeld-Heyser R, Gao J, Ducic T, Tachd P, Lu C, Fritz E, Gafur A, Polle A. Paxillus involutus mycorrhiza attenuate NaCl-stress responses in the salt-sensitive hybrid poplar Populus × canescens. Mycorrhiza 2007, 17:121-131.
53. Leung J, Giraudat J. Abscisic acid signal transduction. Annual Review of Plant Physiology and Plant Molecular Biology 1998, 49:199-222.
54. Liphschitz N, Waisel Y. The effect of water stresses on radial growth of Populus euphratica Oliv. La Yaaran 1970, 20(3):53-63. 74-80
55. Little CHA, Eidt DC. Effects of abscisic acid on budbreak and transpiration in woody species. Nature 1968, 220:498-499.
56. Liu J, Zhu JK. An Arabidopsis mutant that requires increased calcium for potassium nutrition and salt tolerance. Proceedings of the National Academy of Sciences USA 1997, 94:14960-14964.
57. Liu J, Zhu JK. A calcium sensor homolog required for plant salt tolerance. Science 1998, 280:1943-1945.
58. Lü P, Hu J, Chen S, Shen X, Yin W, Chen Y, Sun Y, Hu Z. Function of the putative Na+/H+ antiporter gene PeNhaD1 from salt-resistant Populus euphratica Oliv. Journal of Plant Physiology and Molecular Biology 2007, 33:173-178. in Chinese with English abstract
59. Luan S, Kudla J, Rodriguez-Concepcion M, Yalovsky S, Gruissem W. Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants. Plant Cell 2002, 14:389-400.
60. Luo ZB, Polle A. Wood composition and energy content in a poplar short rotation plantation on fertilized agricultural land in a future CO2 atmosphere. Global Change Biology 2009, 15:38-47.
61. Luo ZB, Janz D, Jiang XN, Göbel C, Wildhagen H, Tan YP, Rennenberg H, Feussner I, Polle A. Upgrading root physiology for stress tolerance by ectomycorrhizas: insights from metabolite and transcriptional profiling into reprogramming for stress anticipation. Plant Physiology 2009a, 151:1902-1917.
62. Luo ZB, Li K, Jiang XN, Polle A. The ectomycorrhizal fungus (Paxillus involutus) and hydrogels affect drought tolerance of Populus euphratica. Annals of Forest Science 2009b, 106:1-10.
63. Ma H, Fung L, Wang S, Altman A, Hüttermann A. Photosynthetic response of Populus euphratica to salt stress. Forest Ecology and Management 1997, 93:55-61.
64. Ma T, Liu Q, Li Z, Zhang X. Tonoplast H+-ATPase in response to salt stress in Populus euphratica cell suspensions. Plant Science 2002, 163:499-505.
65. Mittelheuser CJ, Van Steveninck RFM. Stomatal closure and inhibition of transpiration induced by (RS)-abscisic acid. Nature 1969, 221:281-282.
66. Munns R. Genes and salt tolerance: bring them together. New Phytologist 2005, 167:645-663.
67. Munns R, Tester M. Mechanisms of salinity tolerance. Annual Review of Plant Biology 2008, 59:651-681.
68. Nilsson J, Karlberg A, Antti H, Lopez-Vernaza M, Mellerowicz E, Perrot-Rechenmann C, Sandberg G, Bhalerao RP. Dissecting the molecular basis of the regulation of wood formation by auxin in hybrid aspen. Plant Cell 2008, 20:843-855.
69. Ottow EA. Molecular and ecophysiological responses of Populus euphratica (Oliv.) and Arabidopsis thaliana (L.) to salt stress. 2005, Thesis, University of Göttingen, Cuvillier, ISBN 3-86537-379-8*Kt, pp
70. Ottow EA, Brinker M, Teichmann T, Fritz E, Kaiser W, Brosché M, Kangasjärvi J, Jiang X, Polle A. Populus euphratica displays apoplastic sodium accumulation, osmotic adjustment by decreases in calcium and soluble carbohydrates, and develops leaf succulence under salt stress. Plant Physiology 2005a, 139:1762-1772.
71. Ottow EA, Polle A, Brosché M, Kangasjärvi J, Dibrov P, Zörb C, Teichmann T. Molecular characterization of PeNhaD1: the first member of the NhaD Na+/H+ antiporter family of plant origin. Plant Molecular Biology 2005b, 58:73-86.
72. Peuke AD, Rennenberg H. Heavy metal resistance and phytoremediation with transgenic trees. Tree transgenesis - recent developments 2006, 137-155. Fladung M, Ewald D. In, Eds, Springer, Heidelberg, pp
73. Polle A. Dissecting the superoxide dismutase-ascorbate-glutathione-pathway in chloroplasts by metabolic modeling. computer simulations as a step towards flux analysis. Plant Physiology 2001, 126:445-462.
74. Popko J, Hänsch R, Mendel R-R, Polle A, Teichmann T. The role of abscisic acid and auxin in the response of poplar to abiotic stress. Plant Biology 2010, 12:242-258.
75. Quintero EJ, Ohta M, Shi H, Zhu JK, Pardo JM. Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na+ homeostasis. Proceedings of the National Academy of Sciences USA 2002, 99:9061-9066.
76. Rajagopal J, Khurana DK, Srivastava PS, Lakshmikumaran M. Analysis of repetitive DNA elements in Populus species and their use in study of phylogenetic relationships. IPC- Abstracts of papers and posters presented at the 21st session of the commission 2000, 125-126. Isebrands JG, Richardson J, In, Eds, Portland, Oregon, USA, pp
77. Renault S. Response of red-osier dogwood (Cornus stolonifera) seedlings to sodium sulphate salinity: effects of supplemental calcium. Physiologia Plantarum 2005, 123:75-81.
78. Rowland DL, Sher AA, Marshall DL. Inter- and intra-population variation in seedling performance of Rio Grande cottonwood under low and high salinity. Canadian Journal of Forest Research 2004, 34:1458-1466.
79. Shabala S, Cuin TA. Potassium transport and plant salt tolerance. Physiologia Plantarum 2008, 133:651-669.
80. Shabala S, Shabala L, Volkenburgh E. Effect of calcium on root development and root ion fluxes in salinised barley seedlings. Functional Plant Biology 2003, 30:507-514.
81. Shabala L, Cuin TA, Newman IA, Shabala S. Salinity-induced ion flux patterns from the excised roots of Arabidopsis sos mutants. Planta 2005, 222:1041-1050.
82. Shabala S, Demidchik V, Shabala L, Cuin TA, Smith SJ, Miller AJ, Davies JM, Newman IA. Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+-permeable channels. Plant Physiology 2006, 141:1653-1665.
83. Shao J, Chen S, Wang R, Zhang X, Jiang J. Enhancement of hydrogel on salt resistance of P. popularis'35-44'. Journal of Beijing Forestry University 2007, 29:79-84. in Chinese with English Abstract
84. Shi H, Ishitani M, Kim C, Zhu JK. The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proceedings of the National Academy of Sciences USA 2000, 97:6896-6901.
85. Shi H, Lee BH, Wu SJ, Zhu JK. Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nature Biotechnology 2003, 21:81-85.
86. Shinozaki K, Yamaguchi-Shinozaki K. Molecular responses to dehydration and low temperature: Differences and cross-talk between two stress signaling pathways. Current Opinion in Plant Biology 2000, 3:217-223.
87. Singh M, Jain M, Pant RC. Clonal variability in photosynthetic and growth characteristics of Populus deltoides under saline conditions. Photosynthetica 1999, 36:605-609.
88. Sixto H, Grau JM, Alba N, Alía R. Response to sodium chloride in different species and clones of genus Populus L. Forestry 2005, 78:93-104.
89. Sixto H, Aranda I, Grau JM. Assessment of salt tolerance in Populus alba clones using chlorophyll fluorescence. Photosynthetica 2006, 44:169-173.
90. Song C-P, Guo Y, Qiu Q, Lambert G, Galbraith DW, Jagendorf A, Zhu J-K. Probable Na+(K+)/H+ exchanger on the chloroplast envelope functions in pH homeostasis and chloroplast development in Arabidopsis thaliana. Proceedings of the National Academy of Sciences USA 2004, 101:10211-10216.
91. Steppuhn H, Kort J, Wall KG. First year growth response of selected hybrid poplar cuttings to root-zone salinity. Canadian Journal of Plant Science 2008, 88:473-483.
92. Suarez N, Sobrado MA. Adjustments in leaf water relations of mangrove (Avicennia germinans) seedlings grown in a salinity gradient. Tree Physiology 1998, 20:277-282.
93. Sun J, Chen S, Dai S, Wang R, Li N, Shen X, Zhou X, Lu C, Zheng X, Hu Z, Zhang Z, Song J, Xu Y. NaCl-Induced alternations of cellular and tissue ion fluxes in roots of salt-resistant and salt-sensitive poplar species. Plant Physiology 2009a, 149:1141-1153.
94. Sun J, Dai S, Wang R, Chen S, Li N, Zhou X, Lu C, Shen X, Zheng X, Hu Z, Zhang Z, Song J, Xu Y. Calcium mediates root K+/Na+ homeostasis in poplar species differing in salt tolerance. Tree Physiology 2009b, 29:1175-1186.
95. Takabe T, Uchida A, Shinagawa F, Terada Y, Kajita H, Tanaka Y, Takabe T, Hayashi T, Kawai T, Takabe T. Overexpression of DnaK from a halotolerant cyanobacterium Aphanothece halophytica enhances growth rate as well as abiotic stress tolerance of poplar plants. Plant Growth Regulation 2008, 56:265-273.
96. Teichmann T, Bolu-Arianto WH, Olbrich A, Langenfeld-Heyser R, Gobel C, Grzeganek P, Feussner I, Hansch R, Polle A. GH3::GUS reflects cell-specific developmental patterns and stress-induced changes in wood anatomy in the poplar stem. Tree Physiology 2008, 28:1305-1315.
97. Tester M, Davenport R. Na+ tolerance and Na+ transport in higher plants. Annals of Botany 2003, 91:503-527.
98. Teuber M, Zimmer I, Kreuzwieser J, Ache P, Polle A, Rennenberg H, Schnitzler JP. VOC emissions of Grey poplar leaves as affected by salt stress and different N sources. Plant Biology 2008, 10:86-96.
99. Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen G-L, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Déjardin A, dePamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan B, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjärvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leplé CJ, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi P, Ritland K, Rouzé P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai C-J, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, Van de Peer Y, Rokhsar D. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 2006, 313:1596-1604.
100. Diagnosis and improvement of saline and alkaline soils 1969, Agriculture Handbook No. 60, Department of Agriculture, USA
101. Wang R. Salt-induced oxidative stress and the relevance to salt tolerance in poplar. 2007, PhD dissertation, Beijing Forestry University, Beijing, China, in Chinese with English abstract
102. Wang S, Chen Q, Wang W, Wang X, Lu M. Salt tolerance conferred by over-expression of OsNHX1 gene in Poplar 84K. Chinese Science Bulletin 2005, 50:224-228.
103. Wang R, Chen S, Deng L, Fritz E, Hüttermann A, Polle A. Leaf photosynthesis, fluorescence response to salinity and the relevance to chloroplast salt compartmentation and anti-oxidative stress in two poplars. Trees - Structure and Function 2007, 21:581-591.
104. Wang R, Chen S, Zhou X, Shen X, Deng L, Zhu H, Shao J, Shi Y, Dai S, Fritz E, Hüttermann A, Polle A. Ionic homeostasis and reactive oxygen species control in leaves and xylem sap of two poplars subjected to NaCl stress. Tree Physiology 2008, 28:947-957.
105. Watanabe S, Kojima K, Ide Y, Sasaki S. Effects of saline and osmotic stress on proline and sugar accumulation in Populus euphratica in vitro. Plant Cell Tissue and Organ Culture 2000, 63:199-206.
106. Wei Q. Euphratica Poplar 1993, China Forestry Publishing, Beijing, in Chinese
107. Wu Y, Ding N, Zhao X, Zhao M, Chang Z, Liu J, Zhang L. Molecular characterization of PeSOS1: the putative Na+/H+ antiporter of Populus euphratica. Plant Molecular Biology 2007, 65:1-11.
108. Xiong L, Schumaker KS, Zhu JK. Cell signaling during cold, drought and salt stresses. Plant Cell 2002, 14:165-183.
109. Yang T, Poovaiah BW. Hydrogen peroxide homeostasis: activation of plant catalase by calcium/calmodulin. Proceedings of the National Academy of Sciences USA 2002, 99:4097-4102.
110. Yang YL, Zhang F, Zhao M, An L, Zhang L, Chen N. Properties of plasma membrane H+-ATPase in salt-treated Populus euphratica callus. Plant Cell Reports 2007a, 26:229-235.
111. Yang YQ, Hu L, Chen X, Ottow EA, Polle A, Jiang X. A novel method to quantify H+-ATPase-dependent Na+ transport across plasma membrane vesicles. Biochimica et Biophysica Acta 2007b, 1768:2078-2088.
112. Yi H, Polanco MC, MacKinnon MD, Zwiazek JJ. Responses of ectomycorrhizal Populus tremuloides and Betula papyrifera seedlings to salinity. Environmental and Experimental Botany 2008, 62:357-363.
113. Zalesny JA, Zalesny RS, Wiese AH, Sexton B, Hall RB. Sodium and chloride accumulation in leaf, woody, and root tissue of Populus after irrigation with landfill leachate. Environmental Pollution 2008, 155:72-80.
114. Zhang F, Yang Y, He W, Zhao X, Zhang L. Effects of salinity on growth and compatible solutes of callus induced from Populus euphratica. In Vitro Cellular & Developmental Biology-Plant 2004, 40:491-494.
115. Zhang F, Wang Y, Yang YL, Wu H, Wang D, Liu JQ. Involvement of hydrogen peroxide and nitric oxide in salt resistance in the calluses from Populus euphratica. Plant Cell and Environment 2007, 30:775-785.
116. Zhang H, Yin W, Xia X. Calcineurin B-Like family in Populus: comparative genome analysis and expression pattern under cold, drought and salt stress treatment. Plant Growth Regulation 2008a, 56:129-140.
117. Zhang T, Song Y, Liu Y, Guo X, Zhu C, Wen F. Overexpression of phospholipase Dα gene enhances drought and salt tolerance of Populus tomentosa. Chinese Science Bulletin 2008b, 53:3656-3665.
118. Zhu JK. Plant salt tolerance. Trends in Plant Science 2001, 6:66-71.
119. Zhu JK. Salt and drought stress signal transduction plants. Annual Review of Plant Biology 2002, 53:247-273.
120. Zhu D, Scandalios JG. Differential accumulation of manganese-superoxide dismutase transcripts in maize in response to abscisic acid and high osmoticum. Plant Physiology 1994, 106:173-178.
121. Zong H, Liu E, Guo Z, Li M. Preliminary report on relationship between Ca2+-CAM messenger system and stress resistance of rice seedling. Journal of South China Agriculture University 2000, 21:63-67. in Chinese with an English abstract
122. Zsuffa L. A summary review of interspecific breeding in the genus Populus L. Proceedings of the 14th meeting of the Canadian Tree Improvement Association, part 2 1975, 107-123. Fowler DPYeatman CW. In, Eds, Canadian Forestry Service, Ottawa, Ontario, Canada, pp