Skip to main content
Log in

Anatomical changes to protect organelle integrity account for tolerance to alkali and salt stresses in Melilotus officinalis

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

The adaptation mechanism of Melilotus officinalis was studied to understand this species’ mechanisms.

Methods

Seedlings of Melilotus officinalis were treated with different NaHCO3 levels, with the control plants being grown without NaHCO3. Anatomical structure of three organs and ultrastruture of two organelles widespread were observed by making paraffin and ultrathin sections.

Results

The results showed that NaHCO3 treatments significantly affected vascular system of Melilotus officinalis. Vascular tissue throughout the roots, stems and leaflets underwent changes. Particularly, the diameter of xylem vessels declined significantly, which greatly limited the transportation and transverse diffusion of water; the cross section of stems was changed from near quadrangle to irregular shape, which increased the surface area of the stems and furthered the ability of photosynthesis; epidermis cell walls cutinization occurred and the diameter of xylem vessel decreased greatly, which reduced water loss through stomata and non-stomata cells. In spite of these dramatic morphological changes, organelles in cells, both chloroplast in stems and leaflets and mitochondria in roots, had minor changes. Particularly, thylakoid in chloroplast and cristae in mitochondria still had intact membrane system and sharp-edged laminated structure.

Conclusions

Vascular tissue, the cross section of stems, cell walls of epidermis and mesophyll cell all underwent changes in Melilotus officinalis under NaHCO3 stress. While organelles in cells had minor changes. Maybe structural integrity of organelle was protected by active morphological change of tissues and cells in Melilotus officinalis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abari AK, Nasr MH, Hojjati M, Bayat D (2011) Salt effects on seed germination and seedling emergence of two Acacia species. African J Plant Sci 5:52–56

    Google Scholar 

  • Akram M, Akhtar S, Javed IUH, Wahid A, Rasul E (2002) Anatomical Attributes of different wheat (Triticum aestivum) Accessions/varieties to NaCl salinity. Int J Agric Biol 4:166–168

    Google Scholar 

  • Arafa AA, Khafagy MA, El-Banna MF (2009) The effect of Glycinebetaine or Ascorbic acid on Grain germination and leaf structure of sorghum plants grown under salinity stress. Aust J Crop Sci 3:294–304

    CAS  Google Scholar 

  • Ashraf M, Noor R, Zafar ZU, Mujahid M (1994) Growth and ion distribution in Salt Stressed Melilotus indica (L.)all. and Medicago sativa L. Flora (Jena) 189:207–213

    Google Scholar 

  • Atkin OK, Macherel D (2009) The Crucial role of plant mitochondria in Orchestrating drought tolerance. Ann Bot 103:581–597

    Article  CAS  PubMed  Google Scholar 

  • Ayako N, Hiroshi S, Tatsuru M, Hiroyuki O, Ken-ichiro T (2001) Two Distinct Isopentenyl Diphosphate Isomerases in Cytosol and Plastid are Differentially Induced by Environmental Stresses in Tobacco. FEBS Lett 506:61–64

    Article  Google Scholar 

  • Bray S, Reid DM (2002) The Effect of Salinity and CO2 Enrichment on the Growth and Anatomy of the Second Trifoliate Leaf of Phaseolus vulgaris. Can J Bot 80:349–359

    Article  Google Scholar 

  • Das-Chatterjee A, Goswami L, Maitra S, Dastidar KG, Ray S, Majumder AL (2006) Introgression of a Novel Salt-tolerant L-myo-inositol 1-phosphate Synthase from Porteresia Coarctata (Roxb.) Tateoka (PcINo1) Confers Salt Tolerance to Evolutionary Diverse Organisms. FEBS Lett 580:3980–3988

    Article  CAS  PubMed  Google Scholar 

  • El-Haddad HE, Noaman MM (2001) Leaching Requirement and Salinity Threshold for the Yield and Agronomic Characteristic of Halophytes under Salt Stress. J Arid Environ 49:865–874

    Article  Google Scholar 

  • Emad A, Al S (2009) Melilotus indicus (L.) All. A Salt-tolerant Wild Leguminous Herb with High Potential for Use as a Forage Crop in Salt-affected Soils. Flora 204:737–746

    Article  Google Scholar 

  • Endress AG, Sjolund RD (1976) Ultrastructural Cytology of Callus Cultures of Trepantus Tortuosus as Affected by Temperature. Am J Bot 63:1213–1224

    Article  Google Scholar 

  • Esau K (1977) Anatomy of Seed Plants. John Wiley and Son., Inc., New York

    Google Scholar 

  • Evans PM, Kearney GA (2003) Melilotus albus (Medik.) is Productive and Regenerates Well on Saline Soils of Neutral to Alkaline Reaction in the High Rainfall Zone of South-western Victoria. Aust J Exp Agric 43:349–355

    Article  Google Scholar 

  • Fahn A (1982) Plant Anatomy. Pergamon Press, Oxford

    Google Scholar 

  • FAO (2005) Global Network on Integrated Soil Management for Sustainable Use of Salt-affected Soil. FAO Land and Plant Nutrition Management Service. Roma, Italy

    Google Scholar 

  • Flowers TJ, Yeo AR (1986) Ion Relations of Plant under Drought and Salinity. Aust J Plant Physiol 25:75–91

    Article  Google Scholar 

  • Geilfus CM, Zörb C, Mühling KH (2010) Salt Stress Differentially Affects Growth-mediating β-expansins in Resistant and Sensitive Maize (Zea mays L.). Plant Physiol Biochem 48:993–998

    Article  CAS  PubMed  Google Scholar 

  • Gulzar S, Khan MA (2001) Seed Germination of a Halophytic Grass Aeluropus Lagopoides. Ann Bot 87:319–324

    Article  Google Scholar 

  • Hamdia M, Abd E, Shaddad MAK (1996) Comparative Effect of Sodium Carbonate, Sodium Sulphate, and Sodium Chloride on the Growth and Related Metabolic Activities of Pea Plants. J Plant Nutr 19:717–728

    Article  Google Scholar 

  • Hameed M, Ashraf M, Naz N (2009) Anatomical Adaptations to Salinity in Cogon Grass [Imperata cylindrical (L.) Raeuschel] from the Salt Range, Pakinstan. Plant Soil 322:229–238

    Article  CAS  Google Scholar 

  • Hu Y, Fromm J, Schmidhalter U (2005) Effect of Salinity on Tissue Architecture in Expanding Wheat Leaves. Planta 220:838–848

    Article  CAS  PubMed  Google Scholar 

  • Hyder SZ, Yasmin S (1972) Salt Tolerance and Cation Interaction in Alkali Sacation at Germination. J Range Manag 25:390–392

    Article  CAS  Google Scholar 

  • Islam MS, Akhter MM, Sabagh AE, Liu LY, Nguyen NT, Ueda A, Masaoka Y, Saneoka H (2011) Comparative Studies on Growth and Physiological Responses to Saline and Alkaline Stresses of Foxtail Millet (Setaria italica L.) and Proso Millet (Panicum miliaceum L.). Aust J Crop Sci 5:1269–1277

    CAS  Google Scholar 

  • Katsuhara M, Kawasaki T (1996) Salt Stress Induced Nuclear and DNA Degradation Inmeristematic Cell of Barley Roots. Plant Cell Physiol 37:169–173

    Article  CAS  Google Scholar 

  • Koyro HW (1996) Ultrastructural and Physiological Changes in Root Cells of Sorghum Plants (Sorghum bicolor × S. sudanensis cv. Sweet Sioux) Induced by NaCl. J Exp Bot 48:693–706

    Article  Google Scholar 

  • Maddaloni J (1986) Forage Production on Saline and Alkaline Soil in the Humid Region of Argentina. Reclam Revegetation Res 5:11–16

    Google Scholar 

  • Maranon T, Garcia LV, Troncoso A (1989) Salinity and Germination of Annual Melilotus from the Guadalquivir Delta (SW Spain). Plant Soil 119:223–228

    Article  CAS  Google Scholar 

  • Mufarrege MM, Luca GAD, Hadad HR, Maine MA (2011) Adaptability of Typha domingensis to High pH and Salinity. Ecotoxicology 20:457–465

    Article  CAS  PubMed  Google Scholar 

  • Munns R, Termaat A (1986) Whole-plant Responses to Salinity. Aust J Plant Physiol 13:143–160

    Article  Google Scholar 

  • Nichols PGH, Malik AI, Stockdal M, Colmer TD (2009) Salt Tolerance and Avoidance Mechanism at Germination of Annual Pasture: Iimportance for Adaptation to Saline Environments. Plant Soil 315:241–255

    Article  CAS  Google Scholar 

  • Pastore D, Trono D, Laus MN, Fonzo ND, Flagella Z (2007) Possible Plant Mitochondria Involvement in Cell Adaptation to Drought Stress a Case Study: Durum Wheat Mitochondria. J Exp Bot 2:195–210

    Google Scholar 

  • Paz RC, Reinoso H, Espasandin FD, González Antivilo FA, Sansberro PA, Rocco RA, Ruiz OA, Menendez AB (2014) Akaline, saline and mixed saline–alkaline stresses induce physiological and morpho-anatomical changes in Lotus tenuis Shoots. Plant Biol 16:1042–1049

  • Peharec ŠP, Koffler T, Adler G, Bar-Zvi D (2013) Chloroplasts of Salt-grown Arabidopsis Seedlings are Impaired in Structure, Genome Copy Number and Transcript Levels. PLoS One 8:e82548

  • Reinoso H, Sosa L, Ramirez L, Luna V (2004) Salt-induced Changes in the Vegetative Anatomy of Prosopis strombulifera (Leguminosae). Can J Bot 82:618–628

    Article  Google Scholar 

  • Rogers ME, Evans PM (1996) Do Melilotus Species Have a Role for Saline Areas in Australia? In: Asghar M (ed) Proceedings of the 8th Australian Agronomy Conference Toowoomba. Australian Society of Agronomy, Toowoomba, pp. 486–489

    Google Scholar 

  • Rogers ME, Colmer TD, Frost K, Henry D, Cornwall D, Hulm E, Deretic J, Hughes SR, Craig AD (2008) Diversity in the Genus Melilotus for Tolerance to Salinity and Waterlogging. Plant Soil 304:89–101

    Article  CAS  Google Scholar 

  • Rogers ME, Colmer TD, Nichols PGH, Hughes SJ, Frost K, Cornwall D, Chandra S, Miller SM, Craig AD (2011) Salinity and Waterlogging Tolerance Amongst Accessions of Messina (Melilotus siculus). Crop Pasture Sci 62:225–235

    Article  Google Scholar 

  • Saboora A, Kiarostami K, Behroozbayati F, Hashemi SH (2006) Salinity (NaCl) Tolerance of Wheat Genotypes at Germination and Early Seedling Growth. Pak J Biol Sci 9:2009–2021

    Article  CAS  Google Scholar 

  • Serrato VG, Ferro M, Ferraro D, Riveros E (1991) Anatomical Changes in Prosopis tamarugo Phil. Seeding Growing at Different Level of NaCI Salinity. Ann Bot (London) 68:47–53

    Google Scholar 

  • Shannon MC, Grieve CM, Francois LE (1994) Whole Plant Response to Salinity. In: Wilkinson RE, Dekker M (eds) Plant-environment Interactions, Marcel Dekker. Inc, New York, pp. 199–224

    Google Scholar 

  • Smith MM, Hodson MJ, Öpik H, Wainwright SJ (1982) Salt Induced Ultrastructural Damage to Mitochondria in Root Tips of a Salt-sensitive Ecotype of Agrostis stolonifera. J Exp Bot 33:886–895

    Article  CAS  Google Scholar 

  • Solomon M, Grdalovich E, Mayer AM, Poljakoff-Mayber A (1986) Changes Induced by Salinity to the Anatomy and Morphology of Excised Roots in Culture. Ann Bot 57:811–818

    Article  Google Scholar 

  • Stevenson G (1969) An Agronomic and Taxonomic Review of the Genus Melilotus Mill. Can J Plant Sci 49:1–20

    Article  Google Scholar 

  • Suh MC, Samuels AL, Jetter R, Kunst L, Pollard M, Ohlrogge J, Beisson F (2005) Cuticular Lipid Composition, Surface Structure, and Gene Expression in Arabidopsis Stem Epidermis. Plant Physiol 139:1649–1665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terashima I, Hanba YT, Tholen D, Niinemets U (2011) Leaf Functional Anatomy in Relation to Photosynthesis. Plant Physiol 155:108–116

    Article  CAS  PubMed  Google Scholar 

  • Trinchant JC, Boscari A, Spennato G, Sype GV, Rudulier DL (2004) Proline Betaine Accumulation and Metabolism in Alfalfa Plants under Sodium Chloride Stress. Plant Physiol 135:1583–1594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang H, Wu Z, Chen Y, Yang C, Shi D (2011) Effects of Salt and Alkali Stresses on Growth and Ion Balance in Rice (Oryza sativa L.). Plant Soil Environ 57:286–294

    Google Scholar 

  • Wang, X., Wang, J.G., Liu, H.L., Zou, D.T. and Zhao, H.W. (2013) Influence of Natural Saline-alkali Stress on Chlorophyll Content and Chloroplast Ultrastructure of Two Contrasting Rice (Oryza sativa L. japonica) Cultivars. Aust J Crop Sci 7:289–292

  • Yang GH (2012) Alkali Stress Induced the Accumulation and Secretion of Organic Acids in Wheat. Afr J Agric Res 7:2844–2852

    Google Scholar 

  • Yadav RK, Kumar A, Lal D, Batra L (2004) Yield Responses of Winter (rabi) Forage Crops to Irrigation with Saline Drainage Water. Exp Agric 40:65–75

    Article  Google Scholar 

  • Yamamoto Y, Kobayashi Y, Devi SR, Rikiishi S, Matsumoto H (2002) Aluminum toxicity is Associated with Mitochondrial Dysfunction and the Production of Reactive Oxygen Species in Plant Cells. Plant Physiol 128:63–72

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang CW, Shi DC, Wang DL (2008) Comparative Effects of Salt and Alkali Stress on Growth, Osmotic Adjustment and Ionic Balance of an Alkali-resistant Halophyte Suaeda glauca (Bge.). Plant Growth Regul 56:179–190

    Article  CAS  Google Scholar 

  • Yeo AR, Flowers TJ (1980) Salt Tolerance in the Halophyte Suaeda Maritime L. Dum: Evaluation of the Effect of Salinity upon Growth Journal of Experimental Botany 31:1171–1183

    CAS  Google Scholar 

  • Yu NI, Lee SA, Lee MH, Heo JO, Chang KS, Lim J (2010) Characterization of Short-root Function in the Arabidopsis Root Vascular System. Mol Cell 30:113–119

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was funded by The Innovation Fund of Gansu Agricultural University. The authors thank Prof. ZZ Cao (Gansu Agricultural University) for providing the seeds of Melilotus officinalis, Prof. ZN Nie (Department of Environment and Primary Industries Victoria, Australia, and Gansu Agricultural University) for his critical reading and comments on this paper. YM Zhang would like to thank her colleague LX Chen and YY He for making semi-thin section and ultrathin section.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hui-ling Ma.

Ethics declarations

Funding

This study was funded by The Innovation Fund of Gansu Agricultural University.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible Editor: Frans J.M Maathuis.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, Ym., Ma, Hl., Calderón-Urrea, A. et al. Anatomical changes to protect organelle integrity account for tolerance to alkali and salt stresses in Melilotus officinalis . Plant Soil 406, 327–340 (2016). https://doi.org/10.1007/s11104-016-2875-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-016-2875-4

Keywords

Navigation