Skip to main content
Log in

Hybridization of wheat and Aegilops cylindrica: development, karyomorphology, DNA barcoding and salt tolerance of the amphidiploids

  • Original Article
  • Published:
Journal of Plant Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

The development of salt‐tolerant genotypes is key to a better utilization of salinized irrigated lands. Given the relatively low genetic diversity within the cultivated wheats for salt tolerance, exploring the Aegilops cylindrica's genetic diversity for salt tolerance is thus crucial to breed wheat for saline environments. In the current study, wheat genotypes were hybridized with Ae. cylindrica (a hyper salt-tolerant genotype), and amphidiploid plants were produced using embryo rescue and chromosome doubling techniques. Crossability and cytological examinations of amphidiploids and BC1 were performed before sequencing the ITS4/5 and trnE/trnF DNAs to explore the phylogenetic relationships of the amphidiploids and their parents. Finally, amphidiploids were assessed for salt tolerance. Only two common wheat cultivars (‘Chinese Spring’ and ‘Roshan’) were crossable with Ae. cylindrica. The resultant intergeneric hybrids possessed 70 chromosomes, and morphologically either were similar to the male parent in ‘Chinese Spring’ × Ae. cylindrica or tended to be intermediate between parents in ‘Roshan’ × Ae. cylindrica. The phylogenetic tree divided the genotypes into two groups, in which Clade I contained Ae. cylindrica and three amphidiploids, and Clade II consisted of female parents and one amphidiploid. Amphidiploids exhibited significantly higher tolerance to salt stress compared to the female parents (wheat cultivars) in terms of a higher dry matter, lower accumulation of Na, higher K, and higher K/Na ratio in their root and leaf tissues. Taken together, the amphiploid plants might contain valuable salt tolerance factors.

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

Similar content being viewed by others

Abbreviations

CS :

Chinese Spring

DW :

Dry weight

FW :

Fresh weight

ITS :

Ribosomal internal transcribed spacer

NCBI :

National Center for Biotechnology Information

PPFD :

Photosynthetic photon flux density

SNP :

Single nucleotide polymorphisms

trnL-F :

Chloroplast-encoded trnL (UAA) 5′ exon – trnF (GAA) exon region

References

  • Alvarez I, Wendel JF (2003) Ribosomal its sequences and plant phylogenetic inference. Mol Phylogenet Evo 29:417–434

    CAS  Google Scholar 

  • Arabbeigi M, Arzani A, Majidi MM, Kiani R, Tabatabaei BES, Habibi F (2014) Salinity tolerance of Aegilops cylindrica genotypes collected from hyper-saline shores of uremia salt lake using physiological traits and SSR markers. Acta Physiol Plant 36:2243–2251

    CAS  Google Scholar 

  • Arzani A (2008) Improving salinity tolerance in crop plants: A biotechnological view. Vitro Cell Dev Biol Plant 44:373–383

    CAS  Google Scholar 

  • Arzani A, Ashraf M (2016) Smart engineering of genetic resources for enhanced salinity tolerance in crop plants. Crit Rev Plant Sci 35:146–189

    CAS  Google Scholar 

  • Arzani A, Ashraf M (2017) Cultivated ancient wheats (triticum spp.): a potential source of health-beneficial food products. Compr Rev Food Sci Saf 16:477–488

    Google Scholar 

  • Arzani A, Darvey NL (2001) The effect of colchicine on triticale anther-derived plants: microspore pre-treatment and haploid-plant treatment using a hydroponic recovery system. Euphytica 122:235–241

    CAS  Google Scholar 

  • Baldwin BG, Sanderson MJ, Porter JM, Wojciechowski MF, Campbell CS, Donoghue MJ (1995) The ITS region of nuclear ribosomal DNA: a valuable source of evidence on angiosperm phylogeny. Ann Missouri Bot Gard 82:247–277

    Google Scholar 

  • Colmer TD, Flowers TJ, Munns R (2006) Use of wild relatives to improve salt tolerance in wheat. J Exp Bot 57:1059–1078

    CAS  PubMed  Google Scholar 

  • De Storme N, Mason A (2014) Plant speciation through chromosome instability and ploidy change: cellular mechanisms, molecular factors and evolutionary relevance. Curr Plant Biol 1:10–33

    Google Scholar 

  • Dizkirici A, Kansu C, Onde S (2016) Molecular phylogeny of Triticum and Aegilops genera based on ITS and matK sequence data. Pak J Bot 48:143–153

    CAS  Google Scholar 

  • Fakhri Z, Mirzaghaderi G, Ahmadian S, Mason AS (2016) Unreduced gamete formation in wheat × Aegilops spp. hybrids is genotype specific and prevented by shared homologous subgenomes. Plant Cell Rep 35:1143–1154

    CAS  PubMed  Google Scholar 

  • Ganal MW, Polley A, Graner EM, Plieske J, Wieseke R, Luerssen H, Durstewitz G (2012) Large SNP arrays for genotyping in crop plants. J Biosci 37:821–828

    CAS  PubMed  Google Scholar 

  • Ganopoulos I, Kapazoglou A, Bosmali I, Xanthopoulou A, Nianiou-Obeidat I, Tsaftaris A, Madesis P (2017) Application of the ITS2 region for barcoding plants of the genus Triticum L. and Aegilops L. Cereal Res Commun 45:381–389

    CAS  Google Scholar 

  • Goryunova SV, Chikida NN, Gori M, Kochieva EZ (2005) Analysis of nucleotide sequence polymorphism of internal transcribed spacers of ribosomal genes in diploid Aegilops (L.) species. Mol Biol 39:173–176

    CAS  Google Scholar 

  • Guadagnuolo R, Savova-Bianchi Felber F (2001) Gene flow from wheat (Triticum aestivum L.) to jointed goatgrass (Aegilops cylindrica Host.), as revealed by RAPD and microsatellite markers. Theor Appl Genet 103:1–8

    CAS  Google Scholar 

  • Han Y, Yin S, Huang L, Wu X, Zeng J, Liu X, Zhang G (2018) A sodium transporter HvHKT1; 1 confers salt tolerance in barley via regulating tissue and cell ion homeostasis. Plant Cell Physiol 59:1976–1989

    CAS  PubMed  Google Scholar 

  • He G, Zhu X, Elling AA, Chen L, Wang X, Guo L, Qi Y (2010) Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell 22:17–33

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hegde SG, Waines JG (2004) Hybridization and introgression between bread wheat and wild and weedy relatives in North America. Crop Sci 44:1145–1155

    Google Scholar 

  • Houshmand S, Arzani A, Maibody SAM, Feizi M (2005) Evaluation of salt-tolerant genotypes of durum wheat derived from in vitro and field experiments. Field Crops Res 91:345–354

    Google Scholar 

  • Jauhar PP, Chibbar RN (1999) Chromosome-mediated and direct gene transfers in wheat. Genome 42:570–583

    CAS  Google Scholar 

  • Kaplan Z, Fehrer J (2004) Evidence for the hybrid origin of potamogeton × cooperi (Potamogetonaceae): Traditional morphology-based taxonomy and molecular techniques in concert. Folia Geobot 39:431–453

    Google Scholar 

  • Kiani R, Arzani A, Habibi F (2015) Physiology of salinity tolerance in Aegilops cylindrica. Acta Physiol Plant 37:135

    Google Scholar 

  • Kiani R, Arzani A, Maibody SM, Rahimmalek M, Razavi K (2021a) Morpho-physiological and gene expression responses of wheat by Aegilops cylindrica amphidiploids to salt stress. Plant Cell Tiss Org Cult 144:619–639

    CAS  Google Scholar 

  • Kiani R, Arzani A, Mirmohammady Maibody SAM (2021b) Polyphenols, flavonoids, and antioxidant activity involved in salt tolerance in wheat, Aegilops cylindrica and their amphidiploids. Front Plant Sci 12:493

    Google Scholar 

  • Kilian B, Mammen K, Millet E, Sharma R, Graner A, Salamini F, Ozkan H (2011) Aegilops. In: Kole C (ed) Wild crop relatives: Genomic and Breeding Resources. Springer, Berlin, pp 1–76

    Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    CAS  PubMed  Google Scholar 

  • King J, Grewal S, Yang CY, Hubbart S, Scholefield D, Ashling S, Davassi A (2017) A step change in the transfer of interspecific variation into wheat from Amblyopyrum muticum. Plant Biotechnol J 15:217–226

    CAS  PubMed  Google Scholar 

  • King J, Newell C, Grewal S, Edwards S, Yang C, Scholefield D, King IP (2019) Development of stable homozygous wheat/Amblyopyrum muticum (Aegilops mutica) introgression lines and their cytogenetic and molecular characterisation. Front Plant Sci 10:34

    PubMed  PubMed Central  Google Scholar 

  • Koch MA, Dobes C, Mitchell-Olds T (2003) Multiple hybrid formation in natural populations: concerted evolution of the internal transcribed spacer of nuclear ribosomal DNA (ITS) in North American Arabis divaricarpa (Brassicaceae). Mol Biol Evol 20:338–350

    CAS  PubMed  Google Scholar 

  • Kress WJ, Wurdack KJ, Zimmer EA, Weigt LA, Janzen DH (2005) Use of DNA barcodes to identify flowering plants. Proc Natl Acad Sci USA 102:8369–8374

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Beena AS, Awana M, Singh A (2017) Physiological, biochemical, epigenetic and molecular analyses of wheat (Triticum aestivum) genotypes with contrasting salt tolerance. Front Plant Sci 8:1151

    PubMed  PubMed Central  Google Scholar 

  • Kwiatek MT, Wiśniewska H, Ślusarkiewicz-Jarzina A, Majka J, Majka M, Belter J, Pudelska H (2017) Gametocidal factor transferred from Aegilops geniculata Roth can be adapted for large-scale chromosome manipulations in cereals. Front Plant Sci 8:409

    PubMed  PubMed Central  Google Scholar 

  • Kwok PY, Chen X (2003) Detection of single nucleotide polymorphisms. Curr Issues Mol Biol 5:43–60

    CAS  PubMed  Google Scholar 

  • Li H, Liu X, Zhang M, Feng Z, Liu D, Ayliffe M, Chen X (2018) Development and identification of new synthetic T. turgidumT. monococcum amphiploids. Plant Genet Resour 16:555–563

    CAS  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    CAS  PubMed  Google Scholar 

  • Lin Y (2001) Risk assessment of bar gene transfer from B and D genomes of transformed wheat (Triticum aestivum) lines to jointed goatgrass (Aegilops cylindrica). J Anhui Agric Univ 28:115–118

    CAS  Google Scholar 

  • Liu Q, Ge S, Tang H, Zhang X, Zhu G, Lu BR (2006) Phylogenetic relationships in Elymus (Poaceae: Triticeae) based on the nuclear ribosomal internal transcribed spacer and chloroplast trnL-F sequences. New Phytol 170:411–420

    CAS  PubMed  Google Scholar 

  • Marais GF, Kotze L, Eksteen A (2010) Allosyndetic recombinants of the Aegilops peregrina-derived Lr59 translocation in common wheat. Plant Breed 129:356–361

    CAS  Google Scholar 

  • Mason AS, Wendel JF (2020) Homoeologous exchanges, segmental allopolyploidy, and polyploid genome evolution. Front Genet 11:1014. https://doi.org/10.3389/fgene.2020.01014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Munns R, James RA (2003) Screening methods for salinity tolerance: a case study with tetraploid wheat. Plant Soil 253:201–218

    CAS  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    CAS  PubMed  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucl Acids Res 8:4321–4326

    CAS  PubMed  PubMed Central  Google Scholar 

  • Negrao S, Schmockel SM, Tester M (2017) Evaluating physiological responses of plants to salinity stress. Ann Bot 119:1–11

    CAS  PubMed  Google Scholar 

  • Nemeth C, Yang CY, Kasprzak P, Hubbart S, Scholefield D, Mehra S, King J (2015) Generation of amphidiploids from hybrids of wheat and related species from the genera Aegilops, Secale, Thinopyrum, and Triticum as a source of genetic variation for wheat improvement. Genome 58:71–79

    CAS  PubMed  Google Scholar 

  • Niranjana M (2017) Gametocidal genes of Aegilops: segregation distorters in wheat–Aegilops wide hybridization. Genome 60:639–647

    CAS  PubMed  Google Scholar 

  • Polgari D, Mihok E, Sagi L (2019) Composition and random elimination of paternal chromosomes in a large population of wheat × barley (Triticum aestivum L.× Hordeum vulgare L.) hybrids. Plant Cell Rep 38:767–775

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rimbert H, Darrier B, Navarro J, Kitt J, Choulet F, Leveugle M et al (2018) High throughput SNP discovery and genotyping in hexaploid wheat. PLoS ONE 13:e0186329

    PubMed  PubMed Central  Google Scholar 

  • Rubio F, Nieves-Cordones M, Horie T, Shabala S (2020) Doing ‘business as usual’comes with a cost: evaluating energy cost of maintaining plant intracellular K+ homeostasis under saline conditions. New Phytol 225:1097–1104

    CAS  PubMed  Google Scholar 

  • Safari Z, Mehrabi AA (2019) Molecular phylogeny of Aegilops L. and Triticum L. species revealed by internal transcribed spacers of ribosomal genes. J Agric Sci Technol 21:699–714

    Google Scholar 

  • SAS Institute (2011) Base SAS 9.3 procedures guide. SAS Institute Inc, Cary

  • Sasanuma T, Chabane K, Endo TR, Valkoun J (2004) Characterization of genetic variation in and phylogenetic relationships among diploid Aegilops species by AFLP: incongruity of chloroplast and nuclear data. Theor Appl Genet 108:612–618

    CAS  PubMed  Google Scholar 

  • Shabala S, Pottosin I (2014) Regulation of potassium transport in plants under hostile conditions: implications for abiotic and biotic stress tolerance. Physiol Plant 151:257–279

    CAS  PubMed  Google Scholar 

  • Sheikh I, Sharma P, Verma SK, Kumar S, Malik S, Mathpal P, Dhaliwal HS (2016) Characterization of interspecific hybrids of Triticum aestivum × Aegilops sp. without 5B chromosome for induced homoeologous pairing. J Plant Biochem Biotechnol 25:117–120

    Google Scholar 

  • Song Z, Dai S, Jia Y, Zhao L, Kang L, Liu D, Yan Z (2019) Development and characterization of Triticum turgidumAegilops umbellulata amphidiploids. Plant Genet Resour 17:24–32

    CAS  Google Scholar 

  • Taberlet P, Coissac E, Pompanon F, Gielly L, Miquel C, Valentini A, Vermat T, Corthier G, Brochmann C, Willerslev E (2007) Power and limitations of the chloroplast trn L (UAA) intron for plant DNA barcoding. Nucl Acids Res 35:14

    Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tayale A, Parisod C (2013) Natural pathways to polyploidy in plants and consequences for genome reorganization. Cytogenet Genome Res 140:79–96

    CAS  PubMed  Google Scholar 

  • Vimala Y, Lavania UC (2021) Genomic territories in inter-genomic hybrids: the winners and losers with hybrid fixation. Nucleus 64:1–6

    Google Scholar 

  • Wang QD, Zhang T, Wang JB (2007) Phylogenetic relationships and hybrid origin of Potamogeton species (Potamogetonaceae) distributed in China: insights from the nuclear ribosomal internal transcribed spacer sequence (ITS). Plant Syst Evol 267:65–78

    CAS  Google Scholar 

  • Wang M, Wang S, Liang Z, Shi W, Gao C, Xia G (2018) From genetic stock to genome editing: gene exploitation in wheat. Trends Biotechnol 36:160–172

    CAS  PubMed  Google Scholar 

  • Yang Y, Fan X, Wang L, ZhangSha HQLN, Wang Y, Kang HY, Zeng J, Yu XF, Zhou YH (2017) Phylogeny and maternal donors of elytrigia desv sensu lato triticeae; poaceae inferred from nuclear internal-transcribed spacer and trnL-F sequences. BMC Plant Biol 17:207

    PubMed  PubMed Central  Google Scholar 

  • Zemetra RS, Hansen J, Mallory-Smith CA (1998) Potential for gene transfer between wheat (Triticum aestivum) and jointed goatgrass (Aegilops cylindrica). Weed Sci 46:313–317

    CAS  Google Scholar 

  • Zhang W, Qu L, Gu H, Gao W, Liu M, Chen J, Chen Z (2002) Studies on the origin and evolution of tetraploid wheats based on the internal transcribed spacer (ITS) sequences of nuclear ribosomal DNA. Theor Appl Genet 104:1099–1106

    CAS  PubMed  Google Scholar 

  • Zhang J, Di H, Luo K, Jahufer Z, Wu F, Duan Z, Wang Y (2018) Coumarin content, morphological variation, and molecular phylogenetics of Melilotus. Molecules 23:810

    PubMed Central  Google Scholar 

  • Zhu M, Shabala S, Shabala L, Fan Y, Zhou MX (2016) Evaluating predictive values of various physiological indices for salinity stress tolerance in wheat. J Agron Crop Sci 202:115–124

    CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by funds from the Iran National Science Foundation (INSF) under Grant No. 96009225. Part of this research was done while the second author was on sabbatical leave at Northern Arizona University.

Author information

Authors and Affiliations

Authors

Contributions

AA conceived and designed the research. The experiments were conducted by RK with the supervision of AA, SAMMM, except the molecular analysis that was carried out by AA with the supervision of TA. The data were analyzed by RK, who also wrote the paper, with significant inputs from AA.

Corresponding authors

Correspondence to Ahmad Arzani or Tina Ayers.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 477 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kiani, R., Arzani, A., Maibody, S.A.M.M. et al. Hybridization of wheat and Aegilops cylindrica: development, karyomorphology, DNA barcoding and salt tolerance of the amphidiploids. J. Plant Biochem. Biotechnol. 30, 943–959 (2021). https://doi.org/10.1007/s13562-021-00694-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13562-021-00694-w

Keywords

Navigation