Advertisement

Plant and Soil

, Volume 426, Issue 1–2, pp 349–363 | Cite as

Different tolerance mechanism to alkaline stresses between Populus bolleana and its desert relative Populus euphratica

  • Yufang Sun
  • Yongbin Ou
  • Yongfeng Gao
  • Xuan Zhang
  • Yongmei He
  • Yuan Li
  • Yinan Yao
Regular Article
  • 203 Downloads

Abstract

Background and aims

Populus bolleana Lauche. (P. bolleana) and Populus euphratica Oliv. (P. euphratica) separately survive in mild and moderate alkaline soil conditions. The aim of this study was to explore the underlying mechanism for the different alkaline tolerance in the two poplar species.

Methods

Young saplings of two poplar species were grown in moderate alkaline soil, and the young and old leaves of the two poplars were separately analyzed by ion concentration, allocation and distribution, transcript variation of different genes involved in ion transport and nitrogen assimilation, nitrogen metabolism, organic acid, leaf pigments, and redox responses.

Results

Excess Na+ under alkali stress was mainly allocated to old leaves in P. bolleana. However, excess Na+ was allocated to both young and old leaves in P. euphratica, and was balanced by enhanced levels of Mg2+, Ca2+, and SO42−, with no change in oxidative parameter. The reduction of nitrate nitrogen occurred under alkali stress in both species; P. euphratica acclimated to alkali stress by more flexible regulation of N metabolism and nitrate absorption than P. bolleana.

Conclusions

Our results strongly indicated different alkali tolerance mechanisms in P. bolleana and P. euphratica. P. bolleana protects young tissues via profound accumulation of Na+ and confining damage effects into the old leaves under alkali stress, while P. euphratica can effectively compartmentalize excess Na+, keep its ion balance, and adjust nitrogen transport and metabolism in both young and old leaves to avoid alkali damage.

Keywords

Alkali stress Physiological indexes Nitrate nitrogen Ammonia nitrogen Young and old leaves Alkaline tolerance 

Abbreviations

NHX

Na+/H+ antiporter

SOS1

Salt overly sensitive

AMT

Ammonium transporter

NRT

Nitrate transporter

NR

Nitrate reductase

NiR

Nitrite reductase

AS

Asparagine synthetase

GS

Glutamine synthetase;1

AspAT

Aspartate aminotransferase

GDH

Glutamate dehydrogenase

NADH

Nicotinamide adenine dinucleotide

NADH-GOGAT

NADH-dependent glutamine-2-oxoglutarate aminotransferase

SOD

Superoxide dismutase

Fd-GOGAT

Ferredoxin-dependent glutamate synthase

HKT

High-affinity potassium transporter

HAK

High-affinity potassium transporter

MDA

Malondialdehyde

CAT

catalase

POD

Peroxidase

OH

Hydroxide anion

OAs

Organic acids

HPLC

High performance liquid chromatography

qRT-PCR

Qualitatively real-time PCR

ROS

Reactive oxygen species

TBARS

Thiobarbituric acid reactive substance

PE

Spectrophotometer

LSD

Least significance difference

TCA

Tricarboxylic acid cycle

Notes

Funding information

This research was supported by the Youth Foundation of Science and Technology in Sichuan, China, (No. 2014JQ0016), Natural Science Foundation of China (31770644 and 31270660), Project of Innovation research team in the Sichuan Education Administration (No. 13TD0023), and the Longshan Talent Program of Southwestern University of Science and Technology.

Supplementary material

11104_2018_3632_Fig8_ESM.gif (37 kb)
Fig. S1

Effects of alkali stress on the expression of genes involved in Na+ absorption and metabolism in young and old leaves of two poplars. White bars indicate young leaves of control (CK-Young), light gray bars indicate old leaves of control (CK-Old), gray bars indicate young leaves under alkali treatment (A-Young), and black bars indicate old leaves under alkali treatment (A-Old). Columns represent values which are means (± SE) of four biological replicates. Statistically significant between organs at same stress condition, different letters on the bars indicate significant difference. P values of the ANOVAs of species, control, alkali treatment, and their interaction are indicated. *P < 0.05; **P < 0.01; ***P < 0.001; ****P < 0.0001; ns, not significant (GIF 36 kb)

11104_2018_3632_MOESM1_ESM.tif (1.4 mb)
High resolution image (TIFF 1442 kb)
11104_2018_3632_Fig9_ESM.gif (64 kb)
Fig. S2

Effects of alkali stress on the expression of HAK gene family in young and old leaves of two poplars. White bars indicate young leaves of control (CK-Young), light gray bars indicate old leaves of control (CK-Old), gray bars indicate young leaves under alkali treatment (A-Young), and black bars indicate old leaves under alkali treatment (A-Old). Columns represent values which are means (± SE) of four biological replicates. Statistically significant between organs at same stress condition, different letters on the bars indicate significant difference. P values of the ANOVAs of species, control, alkali treatment, and their interaction are indicated. *P < 0.05; **P < 0.01; ***P < 0.001; ****P < 0.0001; ns, not significant (GIF 64 kb)

11104_2018_3632_MOESM2_ESM.tif (1.9 mb)
High resolution image (TIFF 1959 kb)
11104_2018_3632_Fig10_ESM.gif (29 kb)
Fig. S3

Effects of alkali treatment on the expression of NRT gene family in young and old leaves of two poplars. White bars indicate young leaves of control (CK-Young), light gray bars indicate old leaves of control (CK-Old), gray bars indicate young leaves under alkali treatment (A-Young), and black bars indicate old leaves under alkali treatment (A-Old). Columns represent values which are means (± SE) of four biological replicates. Statistically significant between organs at same stress condition, different letters on the bars indicate significant difference. P values of the ANOVAs of species, control, alkali treatment, and their interaction are indicated. *P < 0.05; **P < 0.01; ***P < 0.001; ****P < 0.0001; ns, not significant (GIF 28 kb)

11104_2018_3632_MOESM3_ESM.tif (1.3 mb)
High resolution image (TIFF 1334 kb)
11104_2018_3632_MOESM4_ESM.docx (21 kb)
ESM 1 (DOCX 20 kb)

References

  1. Aleman F, Nieves-Cordones M, Martínez V, Rubio F (2009) Potassium/sodium steady-state homeostasis in Thellungiella halophila and Arabidopsis thaliana under long-term salinity conditions. Plant Sci 176(6):768–774CrossRefGoogle Scholar
  2. Assaad HI, Hou Y, Zhou L, Carroll RJ, Wu G (2015) Rapid publication-ready MS-Word tables for two-way ANOVA. Springerplus 4(1):33CrossRefPubMedPubMedCentralGoogle Scholar
  3. Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161(2):559–566CrossRefPubMedGoogle Scholar
  4. Blumwald E, Aharon GS, Apse MP (2000) Sodium transport in plant cells. Biochim Biophys Acta Biomembr 1465(1):140–151CrossRefGoogle Scholar
  5. Brunner AM, Busov VB, Strauss SH (2004) Poplar genome sequence: functional genomics in an ecologically dominant plant species. Trends Plant Sci 9(1):49–56CrossRefPubMedGoogle Scholar
  6. Cazzonelli CI (2011) Carotenoids in nature: insights from plants and beyond. Funct Plant Biol 38(11):833–847CrossRefGoogle Scholar
  7. Chen S, Li J, Yin W, Wang S, Fritz E, Polle A, Hüttermann A (2002) Tissue and cellular K+, Ca2+ and Mg2+ of poplar under saline conditions. J Beijing For Univ 24(5):84–88Google Scholar
  8. Chen W, Cui P, Sun H, Guo W, Yang C, Jin H, Fang B, Shi D (2009a) Comparative effects of salt and alkali stresses on organic acid accumulation and ionic balance of seabuckthorn (Hippophae rhamnoides L.) Ind Crop Prod 30(3):351–358CrossRefGoogle Scholar
  9. Chen F, Liu X, Chen L (2009b) Developmental changes in pulp organic acid concentration and activities of acid-metabolising enzymes during the fruit development of two loquat (Eriobotrya japonica Lindl.) cultivars differing in fruit acidity. Food Chem 114(2):657–664CrossRefGoogle Scholar
  10. Couturier J, Montanini B, Martin F, Brun A, Blaudez D, Chalot M (2007) The expanded family of ammonium transporters in the perennial poplar plant. New Phytol 174(1):137–150CrossRefPubMedGoogle Scholar
  11. Crosby N (1968) Determination of ammonia by the Nessler method in waters containing hydrazine. Analyst 93(1107):406–408CrossRefGoogle Scholar
  12. De la Torre WR, Burkey KO (1990) Acclimation of barley to changes in light intensity: chlorophyll organization. Photosynth Res 24(2):117–125CrossRefPubMedGoogle Scholar
  13. Ding M, Hou P, Shen X, Wang M, Deng S, Sun J, Xiao F, Wang R, Zhou X, Lu C, Zhang D, Zheng X, Hu Z, Chen S (2010) Salt-induced expression of genes related to Na+/K+ and ROS homeostasis in leaves of salt-resistant and salt-sensitive poplar species. Plant Mol Biol 73(3):251–269CrossRefPubMedGoogle Scholar
  14. 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(2):279–293CrossRefPubMedGoogle Scholar
  15. Drechsler N, Zheng Y, Bohner A, Nobmann B, von Wiren N, Kunze R, Rausch C (2015) Nitrate-dependent control of shoot K homeostasis by the nitrate transporter1/peptide transporter family member NPF7.3/NRT1.5 and the stelar K+ outward rectifier SKOR in Arabidopsis. Plant Physiol 169(4):2832–2847PubMedPubMedCentralGoogle Scholar
  16. Dvořák J, Noaman M, Goyal S, Gorham J (1994) Enhancement of the salt tolerance of Triticum turgidum L. by the Kna1 locus transferred from the Triticum aestivum L. chromosome 4D by homoeologous recombination. TAG Theor Appl Genet 87(7):872–877CrossRefPubMedGoogle Scholar
  17. Ehlting B, Dluzniewska P, Dietrich H, Selle A, Teuber M, Hansch 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(7):796–811CrossRefPubMedGoogle Scholar
  18. Fan SC, Lin CS, Hsu PK, Lin SH, Tsay YF (2009) The Arabidopsis nitrate transporter NRT1. 7, expressed in phloem, is responsible for source-to-sink remobilization of nitrate. Plant Cell 21(9):2750–2761CrossRefPubMedPubMedCentralGoogle Scholar
  19. Flowers T, Hajibagheri M, Clipson N (1986) Halophytes. Q Rev Biol 61(3):313–337CrossRefGoogle Scholar
  20. Gorham J, Jones RW, Bristol A (1990) Partial characterization of the trait for enhanced K(+)-(Na+) discrimination in the D genome of wheat. Planta 180(4):590–597CrossRefPubMedGoogle Scholar
  21. Hajlaoui H, El Ayeb N, Garrec JP, Denden M (2010) Differential effects of salt stress on osmotic adjustment and solutes allocation on the basis of root and leaf tissue senescence of two silage maize (Zea mays L.) varieties. Ind Crop Prod 31(1):122–130CrossRefGoogle Scholar
  22. Havaux M, Tardy F (1999) Loss of chlorophyll with limited reduction of photosynthesis as an adaptive response of Syrian barley landraces to high-light and heat stress. Funct Plant Biol 26(6):569–578Google Scholar
  23. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circ Calif Agric Exp Stat 347:1–32Google Scholar
  24. Horie T, Yoshida K, Nakayama H, Yamada K, Oiki S, Shinmyo A (2001) Two types of HKT transporters with different properties of Na+ and K+ transport in Oryza sativa. Plant J 27(2):129–138CrossRefPubMedGoogle Scholar
  25. Husted JA, Cook RJ, Farewell VT, Gladman DD (2000) Methods for assessing responsiveness: a critical review and recommendations. J Clin Epidemiol 53(5):459–468CrossRefPubMedGoogle Scholar
  26. Kar M, Mishra D (1976) Catalase, peroxidase, and polyphenoloxidase activities during rice leaf senescence. Plant Physiol 57(2):315–319CrossRefPubMedPubMedCentralGoogle Scholar
  27. Kinnersley AM, Turano FJ (2000) Gamma aminobutyric acid (GABA) and plant responses to stress. Crit Rev Plant Sci 19(6):479–509CrossRefGoogle Scholar
  28. Li C, Fang B, Yang C, Shi D, Wang D (2009) Effects of various salt–alkaline mixed stresses on the state of mineral elements in nutrient solutions and the growth of alkali resistant halophyte Chloris virgata. J Plant Nutr 32(7):1137–1147CrossRefGoogle Scholar
  29. Li J, Fu Y, Pike SM, Bao J, Tian W, Zhang Y, Chen C, Zhang Y, Li H, Huang J (2010) The Arabidopsis nitrate transporter NRT1. 8 functions in nitrate removal from the xylem sap and mediates cadmium tolerance. Plant Cell 22(5):1633–1646CrossRefPubMedPubMedCentralGoogle Scholar
  30. Lin S, Kuo H, Canivenc G, Lin C, Lepetit M, Hsu PK, Tillard P, Lin HL, Wang YY, Tsai CB (2008) Mutation of the Arabidopsis NRT1. 5 nitrate transporter causes defective root-to-shoot nitrate transport. Plant Cell 20(9):2514–2528CrossRefPubMedPubMedCentralGoogle Scholar
  31. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25(4):402–408CrossRefPubMedGoogle Scholar
  32. Meng S, Peng J, He Y, Zhang G, Yi H, Fu Y, Gong J (2016) Arabidopsis NRT1.5 mediates the suppression of nitrate starvation-induced leaf senescence by modulating foliar potassium level. Mol Plant 9(3):461–470CrossRefPubMedGoogle Scholar
  33. Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25(2):239–250CrossRefPubMedGoogle Scholar
  34. Nieves-Cordones M, Alemán F, Martínez V, Rubio F (2010) The Arabidopsis thaliana HAK5 K+ transporter is required for plant growth and K+ acquisition from low K+ solutions under saline conditions. Mol Plant 3(2):326–333CrossRefPubMedGoogle Scholar
  35. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95(2):351–358CrossRefPubMedGoogle Scholar
  36. Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60(3):324–349CrossRefPubMedGoogle Scholar
  37. Rausch T, Kirsch M, Löw R, Lehr A, Viereck R, Zhigang A (1996) Salt stress responses of higher plants: the role of proton pumps and Na+/H+-antiporters. J Plant Physiol 148(3–4):425–433CrossRefGoogle Scholar
  38. Shabala S, Cuin TA (2008) Potassium transport and plant salt tolerance. Physiol Plant 133(4):651–669CrossRefPubMedGoogle Scholar
  39. Storey R, Walker RR (1999) Citrus and salinity. Sci Hortic 78:39–81CrossRefGoogle Scholar
  40. Venema K, Quintero FJ, Pardo JM, Donaire JP (2002) The Arabidopsis Na+/H+ exchanger AtNHX1 catalyzes low affinity Na+ and K+ transport in reconstituted liposomes. J Biol Chem 277(4):2413–2418CrossRefPubMedGoogle Scholar
  41. Vorob’eva LA, Pankova EI (2008) Saline-alkali soils of Russia. Eurasian Soil Sci 41(5):457–470CrossRefGoogle Scholar
  42. Wang Y, Tsay YF (2011) Arabidopsis nitrate transporter NRT1. 9 is important in phloem nitrate transport. Plant Cell Online 23(5):1945–1957CrossRefGoogle Scholar
  43. Wang Y, Ma H, Liu G, Xu C, Zhang D, Ban Q (2008) Analysis of gene expression profile of Limonium bicolor under NaHCO3 stress using cDNA microarray. Plant Mol Biol Report 26(3):241–254CrossRefGoogle Scholar
  44. Wang H, Ahan J, Wu Z, Shi D, Liu B, Yang C (2012a) Alteration of nitrogen metabolism in rice variety ‘Nipponbare’ induced by alkali stress. Plant Soil 355(1–2):131–147CrossRefGoogle Scholar
  45. Wang H, Wu Z, Han J, Zheng W, Yang C (2012b) Comparison of ion balance and nitrogen metabolism in old and young leaves of alkali-stressed rice plants. PLoS One 7(5):e37817CrossRefPubMedPubMedCentralGoogle Scholar
  46. Wang YY, Hsu PK, Tsay YF (2012c) Uptake, allocation and signaling of nitrate. Trends Plant Sci 17(8):458–467CrossRefPubMedGoogle Scholar
  47. Xie H (1999) Determination of nitrogen content in nitrate by salicylic acid colorimetry in water. Guizhou Agric Sci 27(3):40–41Google Scholar
  48. Yang C, Chong J, Li C, Kim C, Shi D, Wang D (2007) Osmotic adjustment and ion balance traits of an alkali resistant halophyte Kochia sieversiana during adaptation to salt and alkali conditions. Plant Soil 294(1–2):263–276CrossRefGoogle Scholar
  49. Yang C, Jianaer A, Li C, Shi D, Wang D (2008a) Comparison of the effects of salt-stress and alkali-stress on photosynthesis and energy storage of an alkali-resistant halophyte Chloris virgata. Photosynthetica 46(2):273–278CrossRefGoogle Scholar
  50. Yang C, Shi D, Wang D (2008b) Comparative effects of salt and alkali stresses on growth, osmotic adjustment and ionic balance of an alkali-resistant halophyte Suaeda glauca (Bge.) Plant Growth Regul 56(2):179–190CrossRefGoogle Scholar
  51. Yang C, Guo W, Shi D (2010) Physiological roles of organic acids in alkali-tolerance of the alkali-tolerant halophyte. Agron J 102(4):1081CrossRefGoogle Scholar
  52. Zhang X, Xiao X, Sun Y (2015) Different physiological response of different maturity of leaves of Populus bolleana to alkali stress. For Sci 51(12):9–16Google Scholar
  53. Zou Q (2000) Plant physiology experiment instruction. China agriculture press, BeijingGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Yufang Sun
    • 1
    • 2
  • Yongbin Ou
    • 3
  • Yongfeng Gao
    • 3
  • Xuan Zhang
    • 1
  • Yongmei He
    • 4
  • Yuan Li
    • 4
  • Yinan Yao
    • 3
  1. 1.Key Laboratory of Biogeography and Bioresources in Arid Land, Xinjiang Institute of Ecology and GeographyChinese Academy of ScienceUrumqiChina
  2. 2.University of Chinese Academy of ScienceBeijingChina
  3. 3.School of Life Science and EngineeringSouthwest University of Science and TechnologyMianyangChina
  4. 4.Yunnan Engineering Laboratory for Agro-environment Pollution Control and Eco-remediationThe Innovation Team for Farmland Non-pollution Production of Yunnan ProvinceKunmingChina

Personalised recommendations