Acta Physiologiae Plantarum

, 41:157 | Cite as

Architectural traits in response to salinity of wheat primary roots

  • Nina TerletskayaEmail author
  • Ulshan Duisenbayeva
  • Aiman Rysbekova
  • Meruert Kurmanbayeva
  • Irina Blavachinskaya
Original Article


This article provides a study on morphological and anatomical changes during post-embryonic development of roots in plants under saline stress. The influence of salinity on the architecture of root related to the species-specificity of wheat plants is shown. The important roles of thickness of the epiblema and length of root hairs, the thickness of the endoderm and the diameter of the central cylinder under salt stress appear worthy of note. It is shown that both the water content of roots cells and its chromosomal apparatus are affected by salt stress. In addition to a very strong plasmolysis, the compression and fragmentation of the nuclei were noted, which resulted into their destruction and cell death. On the basis of all considered parameters the studied species can be arranged in the following according their resistance to salinity: T. polonicum < T. compactum < T. aestivum < T. dicoccum. This is confirmed by the data of ion balance of Na+, K+, and Ca2+ in primary roots of different wheat species.


Wheat species Primary roots Salinity Morphology Anatomy Ion balance 



This research was supported by the Ministry for Science and Education of Kazakhstan. We are grateful to Dr. Nina Khailenko for her excellent consultation assistance and important experimental suggestions.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interests.

Human and animal rights

This research did not involve experiments with human or animal participants.

Informed consent

Informed consent was obtained from all individual participants included in the study and in this article.


  1. Adem G, Roy SJ, Zhou M, Bowman JP, Shabala S (2014) Evaluating contribution of ionic, osmotic and oxidative stress components towards salinity tolerance in barley. BMC Plant Biol 14:113CrossRefGoogle Scholar
  2. Albacete A, Ghanem ME, Martinez-Andujar C, Acosta M, Sanchez-Bravo J, Martinez V, Lutts S, Dodd IC, Perez-Alfocea F (2008) Hormonal changes in relation to biomass partitioning and shoot growth impairment in salinized tomato (Solanum lycopersicum L.) plants. J Exp Bot 59:4119–4131CrossRefGoogle Scholar
  3. Annunziata MG, Ciarmiello LF, Woodrow P, Maximova E, Fuggi A, Carillo P (2017) Durum wheat roots adapt to salinity remodeling the cellular content of nitrogen metabolites and sucrose. Front Plant Sci 7:2035. CrossRefPubMedPubMedCentralGoogle Scholar
  4. Aroca R, Porcel R, Ruis-Lozano JM (2011) Regulation of root water uptake under drought stress conditions. J Exp Bot 63(1):43–57CrossRefGoogle Scholar
  5. Ashraf MY, Sarwar G (2002) Salt tolerance potential in some members of Brassicaceae. Physiological studies on water relations and mineral contents. In: Ahmad R, Malik KA (eds) In prospects for Saline Agriculture. Kluwer Academic Publishers, Netherlands, pp 237–245CrossRefGoogle Scholar
  6. Atabayeva S, Nurmahanova A, Minocha S, Ahmetova A, Kenzhebayeva S, Aidosova S, Nurzhanova A, Zhardamalieva A, Asrandina S, Alybayeva R, Li T (2013) The effect of salinity on growth and anatomical attributes of barley seedling (Hordeum vulgare L.). AJB 12(18):2366–2377. CrossRefGoogle Scholar
  7. Atabayeva S, Nurmahanova A, Ahmetova A, Narmuratova M, Asrandina S, Beisenova A, Alybayeva R, Lee T (2016) Anatomical peculiarities in wheat (Triticum aestivum L.) Varieties under copper stress. Pak J Bot 48(4):1399–1405Google Scholar
  8. Atkin O, Macherel D (2009) The crucial role of plant mitochondria in orchestrating drought tolerance. Ann Bot 103:581–597CrossRefGoogle Scholar
  9. Barykina RP, Veselova TD, Deviatov AG, Dzhalilova KK, Ilyina GM, Chubatova NV (2004) Handbook of botanical microtechiques. The fundamentals and methods. Lomonosov Moskow State University, MoscowGoogle Scholar
  10. Bramley H, Turner NC, Turner DW, Tyerman SD (2009) Roles of morphology, anatomy, and aquaporins in determining contrasting hydraulic behavior of roots. Plant Physiol 150:348–364. CrossRefPubMedPubMedCentralGoogle Scholar
  11. Carden DE, Walker DJ, Flowers TJ, Miller AJ (2003) Single-cell measurements of the contributions of cytosolic Na+ and K+ to salt tolerance. Plant Physiol 131:676–683CrossRefGoogle Scholar
  12. Carillo P (2018) GABA shunt in durum wheat. Front Plant Sci 9:100. CrossRefPubMedPubMedCentralGoogle Scholar
  13. Ceccoli G, Ramos JC, Ortega LI, Acosta JM, Perreta MG (2011) Salinity induced anatomical and morphological changes in Chloris gayana Kunth roots. Biocell 35(1):9–17PubMedGoogle Scholar
  14. Chen Z, Newman I, Zhou M, Mendham N, Zhang G, Shabala S (2005) Screening plants for salt tolerance by measuring K+ flux: a case study for barley. Plant Cell Environ 28:1230–1246CrossRefGoogle Scholar
  15. Cockcroft CE, den Boer BG, Healy JM, Murray JA (2000) Cyclin D control of growth rate in plants. Nature 405:575–579CrossRefGoogle Scholar
  16. Cuin TA, Betts SA, Chalmandrier R, Shabala S (2008) A root’s ability to retain K+ correlates with salt tolerance in wheat. J Exp Bot 59(10):2697–2706. CrossRefPubMedPubMedCentralGoogle Scholar
  17. De Veylder L, Beeckman T, Beemster GTS, de Almeida Engler J, Ormenese S, Maes S, Naudts M, Van Der Schueren E, Jacqmard A, Engler G, Inzé D (2002) Control of proliferation, endoreduplication and differentiation by the Arabidopsis E2Fa-Dpa transcription factor. EMBO J 21:1360–1368CrossRefGoogle Scholar
  18. DoVale J, Fritsche-Neto R (2015) Root phenomics. In: Fritsche-Neto R, Borém A (eds) Phenomics. Springer, Cham, pp 49–66. CrossRefGoogle Scholar
  19. El-Hendawy SE, Hu Y, Schmidhalter U (2005) Growth, ion content, gas exchange, and water relations of wheat genotypes differing in salt tolerances. Aust J Agric Res 56:123–134CrossRefGoogle Scholar
  20. El-Iklil Y, Karrou M, Mrabet R, Benichou M (2002) Effet du stress salin sur la variation de certains métabolites chez Lycopersicon esculentum et Lycopersicon sheesmanii = Salt stress effect on metabolite concentrations of Lycopersicon esculentum and Lycopersicon sheesmanii. Can J Plant Sci 82(1):177–183CrossRefGoogle Scholar
  21. Ferchichi S, Hessini K, Dell’Aversana E, D’Amelia L, Woodrow P, Ciarmiello LF, Fuggi A, Carillo P (2018) Hordeum vulgare and Hordeum maritimum respond to extended salinity stress displaying different temporal accumulation pattern of metabolites. Funct Plant Biol 45(11):1096–1109. CrossRefGoogle Scholar
  22. Gahoonia TS, Nielsen NE, Joshi PA, Jahoor AA (2001) Root hairless barley mutant for elucidating genetic of root hairs and phosphorus uptake. Plant Soil 235:211–219CrossRefGoogle Scholar
  23. García R, Báez AP (2012) Atomic absorption spectrometry (AAS). In: Farrukh MA (ed) Atomic absorption spectroscopy. InTech, Europe, pp 1–12Google Scholar
  24. Geisler M, Frangne N, Gomиs E, Martinoia E, Palmgren MG (2000) The ACA4 gene of arabidopsis encodes a vacuolar membrane calcium pump that improves salt tolerance in yeast. Plant Physiol 124:1814–1827CrossRefGoogle Scholar
  25. Gerrit W, Dirk I, Gerrit TS (2004) Beemster cell cycle modulation in the response of the primary root of arabidopsis to salt stress. Plant Physiol 135:1050–1058CrossRefGoogle Scholar
  26. Giehl RF, Gruber BD, von Wirén N (2014) It’s time to make changes: modulation of root system architecture by nutrient signals. J Exp Bot 65:769–778. CrossRefPubMedGoogle Scholar
  27. Gorban OI (2012) The importance of root system of spring durum wheat in conditions of the low volga region. Bulletin of saratov state agrarian university in honor of NI Vavilov 5:6–8Google Scholar
  28. Guo-yong, Fa-cai D, Nan H, Chun-peng S (2002) Calcium modulation of the membrane potential of the cytoplasm and the absorption of K+ in response to salt stress in the cells of the roots of wheat. An Htnandaxuexutbao. Zizan. Kexue ban = J Henan Univ Natur Sci 32(3):25–48Google Scholar
  29. Hameed M, Ashraf M, Naz N, Al-Qurainy F (2010) Anatomical adaptations of cynodon dactylon (l.) Pers., from the salt range pakistan, to salinity stress. I. Root and stem anatomy. Pak J Bot 42(1):279–289Google Scholar
  30. Hasanuzzaman M, Nahar K, Fujita M (2013) Plant response to salt stress and role of exogenous protectants to mitigate salt-induced damages. In: Ahmad P, Azooz MM, Prasad PNV (eds) Ecophysiology and responses of plants under salt stress. Springer, New York, pp 25–87CrossRefGoogle Scholar
  31. Horie T, Schroeder JI (2004) Sodium transporters in plants. Diverse genes and physiological functions. Plant Physiol 136:2457–2462CrossRefGoogle Scholar
  32. Hose E, Clarkson DT, Steudle E, Schreiber L, Hartung W (2001) The exodermis: variable apoplastic barrier. J Exp Bo 52(365):2245–3364CrossRefGoogle Scholar
  33. James RA, Rivelli AR, Munns R, von Caemmerer S (2002) Factors affecting CO2 assimilation, leaf injury and growth in salt-stressed durum wheat. Funct Plant Biol 29:1393–1403CrossRefGoogle Scholar
  34. Khan A, Gemenet DC, Villordon A (2016) Root system architecture and abiotic stress tolerance: current knowledge in root and tuber crops. Front Plant Sci 7(442):1584. CrossRefPubMedPubMedCentralGoogle Scholar
  35. Kozhushko NN (1991) Study of the drought resistance of the world gene pool of spring wheat for breeding purposes (methodological guidance). WIR, Leningrad, p 90Google Scholar
  36. Lovelli S, Perniola M, Di Tommaso T, Bochicchio R, Amato M (2012) Specific root length and diameter of hydroponically-grown tomato plants under salinity. J Agron 11:101–106CrossRefGoogle Scholar
  37. Manschadi AM, Hammer GL, Christopher JT, deVoil P (2008) Genotypic variation in seedling root architectural traits and implications for drought adaptation in wheat (Triticum aestivum L.). Plant Soil 303:115–129. CrossRefGoogle Scholar
  38. Mori IC, Schroeder JI (2004) Reactive oxygen species activation of plant Ca2+ channels. A signaling mechanism in polar growth, hormone transduction, stress signaling, and hypothetically mechanotransduction. Plant Physiol 135:702–708CrossRefGoogle Scholar
  39. Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250CrossRefGoogle Scholar
  40. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681CrossRefGoogle Scholar
  41. Munns R, James RA, Islam A, Colmer TD (2011) Hordeum marinum—wheat amphiploids maintain higher leaf K+: Na+ and suffer less leaf injury than wheat parents in saline conditions. Plant Soil 348:365–377CrossRefGoogle Scholar
  42. Neumann PM (1995) Inhibition of root growth by salinity stress: toxicity or an adaptive biophysical response? In: Baluska F, Ciamporova M, Gasparikova O, Barlow PW (eds) Structure and function of roots. Kluwer, Dordrecht, pp 299–304CrossRefGoogle Scholar
  43. Paez-Garcia A, Motes CM, Scheible W, Chen R, Blancaflor EB, Monteros MJ (2015) Root traits and phenotyping strategies for plant improvement. Plants 4:334–355. CrossRefPubMedPubMedCentralGoogle Scholar
  44. Pausheva ZP (1974) Plant cytology workshop. Moskow, RussiaGoogle Scholar
  45. Permyakova AI (1988) Microtechnique. MSU, MoscowGoogle Scholar
  46. Prozina MN (1960) Botanical microtechnique. Vysschaya Schkola, MoscowGoogle Scholar
  47. Rand PJ (2001) Cliffs quick review plant biology. Houghton Mifflin Harcourt, Boston, p 256Google Scholar
  48. Rewald B, Rachmilevitch S, McCue MD, Ephrath JE (2011) Influence of saline drip irrigation on fine root and sap-flow densities of two mature olive varieties. Environ Exp Bot 72:107–114CrossRefGoogle Scholar
  49. Rewald B, Shelef O, Ephrath JE, Rachmilevitch S (2013) Adaptive plasticity of salt-stressed root systems. Chapter 6. In: Ahmad P, Azooz MM, Prasad MNV (eds) Ecophysiology and responses of plants under salt stress. Springer, New York, pp 169–202. CrossRefGoogle Scholar
  50. Sacks MM, Silk WK, Burman P (1997) Effect of water stress on cortical cell division rates within the apical meristem of primary roots of maize. Plant Physiol 114:519–527CrossRefGoogle Scholar
  51. Sairam R, Srivastava G (2002) Changes in antioxidant activity in subcellular fractions of tolerant and susceptible wheat genotypes in response to long term salt stress. Plant Sci 162:897–904CrossRefGoogle Scholar
  52. Samarajeewa PK, Barrero RA, Umeda-Hara C, Kawai M, Uchimiya H (1999) Cortical cell death, cell proliferation, macromolecular movements and rTip1 expression pattern in roots of rice (Oryza sativa L.) under NaCl stress. Planta 207:354–361CrossRefGoogle Scholar
  53. Sánchez-Calderón L, Ibarra-Cortés ME, Zepeda-Jazo I (2013) Root development and abiotic stress adaptation. In: Vahdati K, Leslie C (eds) Abiotic stress - plant responses and applications in agriculture. InTech, pp 135–168Google Scholar
  54. Shafi M, Guoping Z, Bakht J, Khan MA, Islam EU, Khan MD, Raziuddin GZ (2010) Effect of cadmium and salinity stresses on root morphology of wheat. Pak J Bot 42(4):2747–2754Google Scholar
  55. Stevović S, Mikovilović VS, Ćalić-Dragosavac D (2010) Environmental impact on morphological and anatomical structure of Tansy. AJB 9(16):2413–2421. CrossRefGoogle Scholar
  56. Tanaka N, Kato M, Tomioka R, Kurata R, Fukao Y, Aoyama T, Maeshima M (2014) Characteristics of a root hair-less line of Arabidopsis thaliana under physiological stresses. J Exp Bot 65:1497–1512CrossRefGoogle Scholar
  57. Tardieu F (2007) Plant tolerance to water deficit: physical limits and possibilities for progress. Comptes Rendus Geosci 337:57–67CrossRefGoogle Scholar
  58. Terletskaya N, Rysbekova A, Iskakova A, Khailenko N, Polimbetova F (2011a) Saline stress response of plantlets of common wheat (Triticum aestivum) and its wild congeners. J Agr Sci Tech B 6:198–204. CrossRefGoogle Scholar
  59. Terletskaya N, Sarsenbayev B, Kirshibayev E (2011b) Influence of saline stress on saline stress on ionic balance of wheat (Triticum aestivum) and its wild congeners. J Life Sci 5(8):618–624. CrossRefGoogle Scholar
  60. Valenti GS, Ferro M, Ferraro D, Riveros F (1991) Anatomical changes in Prosopis tamarugo PHIL. seedlings growing at different levels of NaCl salinity. Ann Bot 68:47–53CrossRefGoogle Scholar
  61. Villordon AQ, Firon N, Clark CA, Smith A (2014). Manipulating root system architecture in sweetpotato for global food security: progress prospects and applications. Paper Presented at the society for experimental biology meeting, roots for global food security session, Manchester.
  62. Wang Y, Zhang W, Li K, Sun F, Han C, Wang Y, Li X (2008) Salt-induced plasticity of root hair development is caused by ion disequilibrium in Arabidopsis thaliana. J Plant Res 121:87–96CrossRefGoogle Scholar
  63. Wasson AP, Richards RA, Chatrath R, Misra SC, Prasad SV, Rebetzke GJ, Kirkegaard JA, Christopher J, Watt M (2012) Traits and selection strategies to improve root systems and water uptake in water-limited wheat crops. J Exp Bot 63:3485–3498CrossRefGoogle Scholar
  64. Woodrow P, Ciarmiello LF, Annunziata MG, Pacifico S, Iannuzzi F, Mirto A, D’Amelia L, Dell’Aversana E, Piccolella S, Fuggi A, Carillo P (2017) Durum wheat seedling responses to simultaneous high light and salinity involve a fine reconfiguration of amino acids and carbohydrate metabolism. Physiol Plant 159(3):290–312. CrossRefPubMedGoogle Scholar
  65. Wu H, Shabala L, Liu X, Azzarello E, Zhou M, Pandolfi C, Chen ZH, Bose J, Mancuso S, Shabala S (2015) Linking salinity stress tolerance with tissue-specific Na+ sequestration in wheat roots. Front Plant Sci 6:71PubMedPubMedCentralGoogle Scholar
  66. Yang Y, Chen L, Li N, Zhang Q (2016) Effect of root moisture content and diameter on root tensile properties. PLoS One 11(3):e0151791CrossRefGoogle Scholar
  67. Yi LP, Ma J, Li Y (2007) Impact of salt stress on the features and activities of root system for three desert halophyte species in their seedling stage. Sci China Ser D 50:97–106CrossRefGoogle Scholar
  68. Zhao Y, Dong W, Zhang N, Ai X, Wang M, Huang Z, Xiao L, Xia G (2014) A wheat allene oxide cyclase gene enhances salinity tolerance via jasmonate signaling. Plant Physiol 164:1068–1076CrossRefGoogle Scholar
  69. Zhuchenko A (2004) Ecological genetics of cultivated plants and problems agrosphere (theory and practice). Moskow, AgrorusGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2019

Authors and Affiliations

  1. 1.Institute of Plant Biology and Biotechnology of Science (IPBB)AlmatyKazakhstan
  2. 2.Al-Farabi Kazakh National UniversityAlmatyKazakhstan
  3. 3.S. Seifullin Kazakh Agrotechnical UniversityAstanaKazakhstan

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