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Natural variation reveals contrasting abilities to cope with alkaline and saline soil among different Medicago truncatula genotypes

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Abstract

Background and Aims

Abiotic stress conditions cause extensive losses to agricultural production worldwide. Salinity and alkalinity affect plant growth, photosynthesis and availability of nutrients including Fe. Many studies have described the response mechanisms of plants to single abiotic stress conditions. However, in the field, crops and other plants are routinely subjected to a combination of different abiotic stresses. Salinity and alkalinity are wide-spread in Tunisia, where Medicago truncatula occurs as a native species.

Methods

We established a growth system to study the combined effects of salinity and alkalinity conditions in laboratory conditions. We screened 11 Tunisian M. truncatula lines from the SARDI collection based on their phenotypic responses to the double stress.

Results

Salinity and alkalinity affected germination rates, shoot and root dry weights, pigment contents and root morphology parameters. We were able to select among the 11 investigated lines four sensitive and tolerant lines with different abilities to respond to the double stress. Tolerant and sensitive genotypes (two lines each) differed in root flavin contents, root flavin staining patterns and concentrations of root flavins in the nutrient solution.

Conclusions

Root architecture, flavin root localization in epidermal cells and flavin secretion are relevant tolerance mechanisms for salt and alkaline stress in M. truncatula. Pairs of contrasting lines from close origins were identified that will be useful tools to identify genes for the tolerance mechanisms.

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Abbreviations

Chl :

chlorophyll

Rbfl :

riboflavin

References

  • Abadia J, Vazquez S, Rellan-Alvarez R, El-Jendoubi H, Abadia A, Alvarez-Fernandez A, Lopez-Millan AF (2011) Towards a knowledge-based correction of iron chlorosis. Plant Physiol Biochem 49:471–482. https://doi.org/10.1016/j.plaphy.2011.01.026

    Article  CAS  PubMed  Google Scholar 

  • Andaluz S, Rodríguez-Celma J, Abadía A, Abadía J, López-Millán A-F (2009) Time course induction of several key enzymes in Medicago truncatula roots in response to Fe deficiency. Plant Physiol Biochem 47:1082–1088

    Article  CAS  PubMed  Google Scholar 

  • Ariel F, Diet A, Verdenaud M, Gruber V, Frugier F, Chan R, Crespi M (2010) Environmental regulation of lateral root emergence in Medicago truncatula requires the HD-Zip I transcription factor HB1. Plant Cell 22:2171–2183. https://doi.org/10.1105/tpc.110.074823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bailey-Serres J, Voesenek LA (2010) Life in the balance: a signaling network controlling survival of flooding. Curr Opin Plant Biol 13:489–494. https://doi.org/10.1016/j.pbi.2010.08.002

    Article  CAS  PubMed  Google Scholar 

  • Basigalup D, Irwin J, Mi F, Abdelguefri-Laouar M (2014) Perspectives of alfalfa in Australia, China, Africa and Latin America. The journal of the International Legume Society: Legume Perspectives 9–10

  • Briat J-F, Dubos C, Gaymard F (2015) Iron nutrition, biomass production, and plant product quality. Trends Plant Sci 20:33–40

    Article  CAS  PubMed  Google Scholar 

  • Cramer GR, Epstein E, Läuchli A (1991) Effects of sodium, potassium and calcium on salt-stressed barley. Physiol Plant 81:197–202

    Article  CAS  Google Scholar 

  • Ellwood S, D’souza N, Kamphuis L, Burgess T, Nair R, Oliver R (2006) SSR analysis of the Medicago truncatula SARDI core collection reveals substantial diversity and unusual genotype dispersal throughout the Mediterranean basin. Theor Appl Genet 112:977–983

    Article  CAS  PubMed  Google Scholar 

  • Fenner M, Thompson K (2005) The ecology of seeds. Cambridge University Press

  • Fourcroy P, Siso-Terraza P, Sudre D, Saviron M, Reyt G, Gaymard F, Abadia A, Abadia J, Alvarez-Fernandez A, Briat JF (2014) Involvement of the ABCG37 transporter in secretion of scopoletin and derivatives by Arabidopsis roots in response to iron deficiency. New Phytol 201:155–167. https://doi.org/10.1111/nph.12471

    Article  CAS  PubMed  Google Scholar 

  • Friesen ML, Cordeiro MA, Penmetsa RV, Badri M, Huguet T, Aouani ME, Cook DR, Nuzhdin SV (2010) Population genomic analysis of Tunisian Medicago truncatula reveals candidates for local adaptation. Plant J 63:623–635

    Article  CAS  PubMed  Google Scholar 

  • Friesen ML, von Wettberg EJ, Badri M, Moriuchi KS, Barhoumi F, Chang PL, Cuellar-Ortiz S, Cordeiro MA, Vu WT, Arraouadi S (2014) The ecological genomic basis of salinity adaptation in Tunisian Medicago truncatula. BMC Genomics 15:1

    Article  Google Scholar 

  • Gao ZW, Zhu H, Gao JC, Yang CW, Mu CS, Wang DL (2011) Germination responses of Alfalfa (Medicago sativa L.) seeds to various salt-alkaline mixed stress. Afr J Agric Res 6:3793–3803

    Google Scholar 

  • Guan B, Zhou D, Zhang H, Tian Y, Japhet W, Wang P (2009) Germination responses of Medicago ruthenica seeds to salinity, alkalinity, and temperature. J Arid Environ 73:135–138. https://doi.org/10.1016/j.jaridenv.2008.08.009

    Article  Google Scholar 

  • Hanin M, Ebel C, Ngom M, Laplaze L, Masmoudi K (2016) New Insights on Plant Salt Tolerance Mechanisms and Their Potential Use for Breeding. Front Plant Sci 7:1787. https://doi.org/10.3389/fpls.2016.01787

    Article  PubMed  PubMed Central  Google Scholar 

  • Hsieh EJ, Waters BM (2016) Alkaline stress and iron deficiency regulate iron uptake and riboflavin synthesis gene expression differently in root and leaf tissue: implications for iron deficiency chlorosis. J Exp Bot 67:5671–5685. https://doi.org/10.1093/jxb/erw328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lazrek F, Roussel V, Ronfort J, Cardinet G, Chardon F, Aouani M, Huguet T (2009) The use of neutral and non-neutral SSRs to analyse the genetic structure of a Tunisian collection of Medicago truncatula lines and to reveal associations with eco-environmental variables. Genetica 135:391–402

    Article  CAS  PubMed  Google Scholar 

  • Li Q, Yang A, Zhang WH (2016) Efficient acquisition of iron confers greater tolerance to saline-alkaline stress in rice (Oryza sativa L.) J Exp Bot 67:6431–6444. https://doi.org/10.1093/jxb/erw407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livak K (1997) ABI prism 7700 sequence detection system user bulletin# 2 relative quantification of gene expression. ABI company publication

  • López-Millán AF, Morales F, Andaluz S, Gogorcena Y, Abadía A, De Las RJ, Abadía J (2000) Responses of sugar beet roots to iron deficiency. Changes in carbon assimilation and oxygen use. Plant Physiol 124:885–898

    Article  PubMed  PubMed Central  Google Scholar 

  • Lucena JJ (2000) Effects of bicarbonate, nitrate and other environmental factors on iron deficiency chlorosis. A review. J Plant Nutr 23:1591–1606

    Article  CAS  Google Scholar 

  • Naranjo-Arcos MA, Bauer P (2016) Nutritional Deficiency. Chapter 4: Iron Nutrition, Oxidative Stress, and Pathogen Defense. INTECH Open Access Publisher

  • Rabhi M, Barhoumi Z, Ksouri R, Abdelly C, Gharsalli M (2007) Interactive effects of salinity and iron deficiency in Medicago ciliaris. C R biol 330:779–788

    Article  CAS  PubMed  Google Scholar 

  • Rahoui S, Martinez Y, Sakouhi L, Ben C, Rickauer M, El Ferjani E, Gentzbittel L, Chaoui A (2016) Cadmium-induced changes in antioxidative systems and differentiation in roots of contrasted Medicago truncatula lines. Protoplasma: 1–17

  • Rengasamy P (2016) Soil Salinization. OXFORD RESEARCH ENCYCLOPEDIA, ENVIRONMENTAL SCIENCE. https://doi.org/10.1093/acrefore/9780199389414.013.65

  • Rodriguez-Celma J, Lattanzio G, Grusak MA, Abadia A, Abadia J, Lopez-Millan AF (2011a) Root responses of Medicago truncatula plants grown in two different iron deficiency conditions: changes in root protein profile and riboflavin biosynthesis. J Proteome Res 10:2590–2601. https://doi.org/10.1021/pr2000623

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Celma J, Lin WD, Fu GM, Abadia J, Lopez-Millan AF, Schmidt W (2013) Mutually exclusive alterations in secondary metabolism are critical for the uptake of insoluble iron compounds by Arabidopsis and Medicago truncatula. Plant Physiol 162:1473–1485. https://doi.org/10.1104/pp.113.220426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodriguez-Celma J, Vazquez-Reina S, Orduna J, Abadia A, Abadia J, Alvarez-Fernandez A, Lopez-Millan AF (2011b) Characterization of flavins in roots of Fe-deficient strategy I plants, with a focus on Medicago truncatula. Plant cell physiol 52:2173–2189. https://doi.org/10.1093/pcp/pcr149

    Article  CAS  PubMed  Google Scholar 

  • Schmid NB, Giehl RF, Doll S, Mock HP, Strehmel N, Scheel D, Kong X, Hider RC, von Wiren N (2014) Feruloyl-CoA 6′-Hydroxylase1-dependent coumarins mediate iron acquisition from alkaline substrates in Arabidopsis. Plant Physiol 164:160–172. https://doi.org/10.1104/pp.113.228544

    Article  CAS  PubMed  Google Scholar 

  • Sisó-Terraza P, Luis-Villarroya A, Fourcroy P, Briat JF, Abadía A, Gaymard F, Abadía J, Álvarez-Fernández A (2016a) Accumulation and Secretion of Coumarinolignans and other Coumarins in Arabidopsis thaliana Roots in Response to Iron Deficiency at High pH. Front Plant Sci 7:1711. https://doi.org/10.3389/fpls.2016.01711

    Article  PubMed  PubMed Central  Google Scholar 

  • Sisó-Terraza P, Rios JJ, Abadía J, Abadía A, Álvarez-Fernández A (2016b) Flavins secreted by roots of iron-deficient Beta vulgaris enable mining of ferric oxide via reductive mechanisms. New Phytol 209:733–745. https://doi.org/10.1111/nph.13633

    Article  PubMed  Google Scholar 

  • Skujinš J (1984) Microbial ecology of desert soils. Springer, Advances in microbial ecology

    Book  Google Scholar 

  • Susín S, Abián J, Sánchez-Baeza F, Peleato ML, Abadía A, Gelpí E, Abadía J (1993) Riboflavin 3′-and 5′-sulfate, two novel flavins accumulating in the roots of iron-deficient sugar beet (Beta vulgaris). J Biol Chem 268:20958–20965

    PubMed  Google Scholar 

  • Yousfi S, Mahmoudi H, Abdelly C, Gharsalli M (2007) Effect of salt on physiological responses of barley to iron deficiency. Plant Physiol Biochem 45:309–314

    Article  CAS  PubMed  Google Scholar 

  • Zahaf O, Blanchet S, De Zélicourt A, Alunni B, Plet J, Laffont C, De Lorenzo L, Imbeaud S, Ichanté J-L, Diet A (2012) Comparative transcriptomic analysis of salt adaptation in roots of contrasting Medicago truncatula genotypes. Mol Plant 5:1068–1081

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported partly by a DAAD Stibed stipend to H. B. A. provided through the Heinrich Heine University, and Spanish MINECO projects AGL2013-42175-R and AGL2016-75226-R (co-financed with FEDER) to J. A. and A. A.-F.

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Authors and Affiliations

  1. Institute of Botany, University of Düsseldorf, D-40225, Düsseldorf, Germany

    Heithem Ben Abdallah, Hans-Jörg Mai & Petra Bauer

  2. Department of Plant Nutrition, Aula Dei Experimental Station, Consejo Superior de Investigaciones Científicas (CSIC), P.O. Box 13034, E-50080, Zaragoza, Spain

    Ana Álvarez-Fernández & Javier Abadía

  3. Institute of Botany, Heinrich-Heine University, Universitätstrasse 1, D-40225, Düsseldorf, Germany

    Petra Bauer

Authors
  1. Heithem Ben Abdallah
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  2. Hans-Jörg Mai
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  3. Ana Álvarez-Fernández
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  4. Javier Abadía
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  5. Petra Bauer
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Correspondence to Petra Bauer.

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Ben Abdallah, H., Mai, HJ., Álvarez-Fernández, A. et al. Natural variation reveals contrasting abilities to cope with alkaline and saline soil among different Medicago truncatula genotypes. Plant Soil 418, 45–60 (2017). https://doi.org/10.1007/s11104-017-3379-6

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