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

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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.

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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

References

  • 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):768–774

    Article  CAS  Google Scholar 

  • Assaad HI, Hou Y, Zhou L, Carroll RJ, Wu G (2015) Rapid publication-ready MS-Word tables for two-way ANOVA. Springerplus 4(1):33

    Article  PubMed  PubMed Central  Google Scholar 

  • Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161(2):559–566

    Article  CAS  PubMed  Google Scholar 

  • Blumwald E, Aharon GS, Apse MP (2000) Sodium transport in plant cells. Biochim Biophys Acta Biomembr 1465(1):140–151

    Article  CAS  Google Scholar 

  • Brunner AM, Busov VB, Strauss SH (2004) Poplar genome sequence: functional genomics in an ecologically dominant plant species. Trends Plant Sci 9(1):49–56

    Article  CAS  PubMed  Google Scholar 

  • Cazzonelli CI (2011) Carotenoids in nature: insights from plants and beyond. Funct Plant Biol 38(11):833–847

    Article  CAS  Google Scholar 

  • 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):84–88

    Google Scholar 

  • 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):351–358

    Article  Google Scholar 

  • 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):657–664

    Article  CAS  Google Scholar 

  • 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):137–150

    Article  CAS  PubMed  Google Scholar 

  • Crosby N (1968) Determination of ammonia by the Nessler method in waters containing hydrazine. Analyst 93(1107):406–408

    Article  CAS  Google Scholar 

  • De la Torre WR, Burkey KO (1990) Acclimation of barley to changes in light intensity: chlorophyll organization. Photosynth Res 24(2):117–125

    Article  PubMed  Google Scholar 

  • 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):251–269

    Article  CAS  PubMed  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(2):279–293

    Article  CAS  PubMed  Google Scholar 

  • 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):2832–2847

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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):872–877

    Article  PubMed  Google Scholar 

  • 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):796–811

    Article  CAS  PubMed  Google Scholar 

  • 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):2750–2761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flowers T, Hajibagheri M, Clipson N (1986) Halophytes. Q Rev Biol 61(3):313–337

    Article  Google Scholar 

  • 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):590–597

    Article  CAS  PubMed  Google Scholar 

  • 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):122–130

    Article  CAS  Google Scholar 

  • 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):569–578

    CAS  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circ Calif Agric Exp Stat 347:1–32

    Google Scholar 

  • 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):129–138

    Article  CAS  PubMed  Google Scholar 

  • Husted JA, Cook RJ, Farewell VT, Gladman DD (2000) Methods for assessing responsiveness: a critical review and recommendations. J Clin Epidemiol 53(5):459–468

    Article  CAS  PubMed  Google Scholar 

  • Kar M, Mishra D (1976) Catalase, peroxidase, and polyphenoloxidase activities during rice leaf senescence. Plant Physiol 57(2):315–319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kinnersley AM, Turano FJ (2000) Gamma aminobutyric acid (GABA) and plant responses to stress. Crit Rev Plant Sci 19(6):479–509

    Article  CAS  Google Scholar 

  • 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):1137–1147

    Article  CAS  Google Scholar 

  • 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):1633–1646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):2514–2528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25(4):402–408

    Article  CAS  PubMed  Google Scholar 

  • 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):461–470

    Article  CAS  PubMed  Google Scholar 

  • Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25(2):239–250

    Article  CAS  PubMed  Google Scholar 

  • 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):326–333

    Article  CAS  PubMed  Google Scholar 

  • Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95(2):351–358

    Article  CAS  PubMed  Google Scholar 

  • Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60(3):324–349

    Article  CAS  PubMed  Google Scholar 

  • 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):425–433

    Article  CAS  Google Scholar 

  • Shabala S, Cuin TA (2008) Potassium transport and plant salt tolerance. Physiol Plant 133(4):651–669

    Article  CAS  PubMed  Google Scholar 

  • Storey R, Walker RR (1999) Citrus and salinity. Sci Hortic 78:39–81

    Article  CAS  Google Scholar 

  • 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):2413–2418

    Article  CAS  PubMed  Google Scholar 

  • Vorob’eva LA, Pankova EI (2008) Saline-alkali soils of Russia. Eurasian Soil Sci 41(5):457–470

    Article  Google Scholar 

  • Wang Y, Tsay YF (2011) Arabidopsis nitrate transporter NRT1. 9 is important in phloem nitrate transport. Plant Cell Online 23(5):1945–1957

    Article  CAS  Google Scholar 

  • 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):241–254

    Article  CAS  Google Scholar 

  • 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):131–147

    Article  CAS  Google Scholar 

  • 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):e37817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang YY, Hsu PK, Tsay YF (2012c) Uptake, allocation and signaling of nitrate. Trends Plant Sci 17(8):458–467

    Article  CAS  PubMed  Google Scholar 

  • Xie H (1999) Determination of nitrogen content in nitrate by salicylic acid colorimetry in water. Guizhou Agric Sci 27(3):40–41

    Google Scholar 

  • 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):263–276

    Article  CAS  Google Scholar 

  • 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):273–278

    Article  CAS  Google Scholar 

  • 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):179–190

    Article  CAS  Google Scholar 

  • Yang C, Guo W, Shi D (2010) Physiological roles of organic acids in alkali-tolerance of the alkali-tolerant halophyte. Agron J 102(4):1081

    Article  CAS  Google Scholar 

  • 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):9–16

    Google Scholar 

  • Zou Q (2000) Plant physiology experiment instruction. China agriculture press, Beijing

    Google Scholar 

Download references

Funding

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.

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Authors and Affiliations

  1. Key Laboratory of Biogeography and Bioresources in Arid Land, Xinjiang Institute of Ecology and Geography, Chinese Academy of Science, Urumqi, 830011, China

    Yufang Sun & Xuan Zhang

  2. University of Chinese Academy of Science, Beijing, 100010, China

    Yufang Sun

  3. School of Life Science and Engineering, Southwest University of Science and Technology, Mianyang, 621010, China

    Yongbin Ou, Yongfeng Gao & Yinan Yao

  4. Yunnan Engineering Laboratory for Agro-environment Pollution Control and Eco-remediation, The Innovation Team for Farmland Non-pollution Production of Yunnan Province, Kunming, 650201, China

    Yongmei He & Yuan Li

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  1. Yufang Sun
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  2. Yongbin Ou
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  3. Yongfeng Gao
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  4. Xuan Zhang
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  5. Yongmei He
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  6. Yuan Li
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  7. Yinan Yao
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Correspondence to Yinan Yao.

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Responsible Editor: Honghua He

Electronic supplementary material

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)

High resolution image (TIFF 1442 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)

High resolution image (TIFF 1959 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)

High resolution image (TIFF 1334 kb)

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Sun, Y., Ou, Y., Gao, Y. et al. Different tolerance mechanism to alkaline stresses between Populus bolleana and its desert relative Populus euphratica. Plant Soil 426, 349–363 (2018). https://doi.org/10.1007/s11104-018-3632-7

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  • DOI: https://doi.org/10.1007/s11104-018-3632-7

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