Abstract
Nearly 2 billion people worldwide are suffering from iron (Fe) deficiency anemia and zinc (Zn) deficiency. The available elite bread wheat cultivars have inherently low grain micronutrient content. Biofortification for grain Fe and Zn content is one of the most feasible and cost-effective approach for combating widespread deficiency of the micronutrients. QTL controlling high grain Fe and Zn have been mapped on groups 2 and 7 chromosomes of Triticeae. The present study was initiated for precise transfers of genes for high grain Fe and Zn on group 2 and 7 chromosomes of wheat-Aegilops substitution lines to wheat cultivars using pollen radiation hybridization. The pollen radiation hybrids (PRH1) derived from 1.75 krad irradiated spikes showed the presence of univalents and multivalents in meiotic metaphase-I indicating the effectiveness of radiation dose. In the advanced generation PRH5, the plants selected with stable chromosome number and high grain Fe and Zn content were analyzed with wheat groups 2 and 7 chromosome specific intron targeted amplified polymorphism (ITAP) markers of the metal homeostasis genes to monitor the transfers of alien genes from the substituted Aegilops chromosomes. The group 2 chromosome derivatives showed the presence of NAS2, FRO2, VIT1, and ZIP2 Aegilops genes whereas the group 7 derivatives had YSL15, NAM, NRAMP5, IRO3, and IRT2 Aegilops genes. The pollen radiation hybrids of both the groups 2 and 7 chromosomes showed more than 30% increase in grain Fe and Zn content with improved yield than the elite wheat cultivar PBW343 LrP indicating small and compensating transfers of metal homeostasis genes of Aegilops into wheat.
Similar content being viewed by others
References
Bailey RL, West KP Jr, Black RE (2015) The epidemiology of global micronutrient deficiencies. Ann Nutr Metab 66(2):22–33
Benoist BD, McLean E, Egll I, Cogswell M (2008) Worldwide prevalence of anaemia 1993–2005: WHO global database on anaemia.Geneva
Bie T, Wang L, He H, Qi Z, Feng Y, Chen Q, Li H, Chen P (2007) Molecular cytogenetic analysis of a Triticum aestivum-Haynaldia villosa reciprocal chromosomal translocation induced by pollen irradiation. Acta Agron Sin 33:1432–1438
Cakmak I, Ozkan H, Braun H, Welch R, Romheld V (2000) Zinc and iron concentrations in seeds of wild, primitive, and modern wheats. Food Nutr Bull 21(4):401–403
Cakmak I, Pfeiffer WH, McClafferty B (2010) Review: biofortification of durum wheat with zinc and iron. Cereal Chem 87(1):10–20
Calderini DF, Ortiz-Monasterio I (2003) Grain position affects grain macronutrient and micronutrient concentrations in wheat. Crop Sci 43(1):141–151
Copenhagen Consensus Centre (2008) Copenhagen consensus 2008
Chen P, You C, Hu Y, Chen S, Zhou B, Cao A, Wang X (2013) Radiation induced translocations with reduced Haynaldia villosa chromatin at the Pm21 locus for powdery mildew resistance in wheat. Mol Breeding 31:477–484
Chhuneja P, Dhaliwal HS, Bains NS, Singh K (2006) Aegilops kotschyi and Aegilops tauschii as sources for higher levels of grain iron and zinc. Plant Breed 125(5):529–531
Connolly EL, Campbell NH, Grotz N, Prichard CL, Guerinot ML (2003) Overexpression of the FRO2 ferric chelate reductase confers tolerance to growth on low iron and uncovers posttranscriptional control. Plant Physiol 133(3):1102–1110
Dixon J, Braun H, Crouch J (2009) Overview: transitioning wheat research to serve the future needs of the developing world. In: Wheat facts and futures,CIMMYT pp 1–25
Dvorak J, Knott DR (1977) Homoeologous chromatin exchange in a radiation-induced gene transfer. Can J Genet Cytol 19:125–131
Farkas A, Molnár I, Dulai S, Rapi S, Oldal V, Cseh A, Kruppa K, Molnár-Láng M (2014) Increased micronutrient content (Zn, Mn) in the 3Mb (4B) wheat–Aegilops biuncialis substitution and 3Mb. 4BS translocation identified by GISH and FISH. Genome 57(2):61–67
Friebe B, Qi L, Nasuda S, Zhang P, Tuleen N, Gill B (2000) Development of a complete set of Triticum aestivum-Aegilops speltoides chromosome addition lines. Theor Appl Genet 101(1):51–58
Friebe B, Jiang J, Gill BS, Dyck PL (1993) Radiation-induced nonhomoeologous wheat-Agropyron intermedium chromosomal translocations conferring resistance to leaf rust. Theor Appl Genet 86:141–149
Genc Y, Verbyla A, Torun A, Cakmak I, Willsmore K, Wallwork H, McDonald G (2009) Quantitative trait loci analysis of zinc efficiency and grain zinc concentration in wheat using whole genome average interval mapping. Plant Soil 314(1–2):49–66
Gómez-Galera S, Rojas E, Sudhakar D, Zhu C, Pelacho AM, Capell T, Christou P (2010) Critical evaluation of strategies for mineral fortification of staple food crops. Transgenic Res 19(2):165–180
Hunt JR (2002) Moving toward a plant-based diet: are iron and zinc at risk? Nutr Res 60(5):127–134
Inoue H, Kobayashi T, Nozoye T, Takahashi M, Kakei Y, Suzuki K, Nakazono M, Nakanishi H, Mori S, Nishizawa NK (2009) Rice OsYSL15 is an iron-regulated iron (III)-deoxymugineic acid transporter expressed in the roots and is essential for iron uptake in early growth of the seedlings. J Biol Chem 284(6):3470–3479
Ishimaru Y, Takahashi R, Bashir K, Shimo H, Senoura T, Sugimoto K, Ono K, Yano M, Ishikawa S, Arao T, Nakanishi H, Nishizawa NK (2012) Characterizing the role of rice NRAMP5 in manganese, iron and cadmium transport. Sci Rep 2:286
Jorhem L, Engman J (2000) Determination of lead, cadmium, zinc, copper, and iron in foods by atomic absorption spectrometry after microwave digestion: NMKL1 collaborative study. J AOAC Int 83(5):1189–1203
Kim SA, Punshon T, Lanzirotti A, Li L, Alonso JM, Ecker JR, Kaplan J, Guerinot ML (2006) Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science 314(5803):1295–1298
Klatte M, Schuler M, Wirtz M, Fink-Straube C, Hell R, Bauer P (2009) The analysis of Arabidopsis nicotianamine synthase mutants reveals functions for nicotianamine in seed iron loading and iron deficiency responses. Plant Physiol 150(1):257–271
Kordas K, Stoltzfus RJ (2004) New evidence of iron and zinc interplay at the enterocyte and neural tissues. J Nutr 134(6):1295–1298
Lee S, Chiecko JC, Kim SA, Walker EL, Lee Y, Guerinot ML, An G (2009) Disruption of OsYSL15 leads to iron inefficiency in rice plants. Plant Physiol 150:786–800
Li L, Chen OS, Ward DM, Kaplan J (2001) CCC1 is a transporter that mediates vacuolar iron storage in yeast. J Biol Chem 276:29515–29519
Mayer JE, Pfeiffer WH, Beyer P (2008) Biofortified crops to alleviate micronutrient malnutrition. Curr Opin Plant Biol 11(2):166–170
Milner MJ, Seamon J, Craft E, Kochian LV (2013) Transport properties of members of the ZIP family in plants and their role in Zn and Mn homeostasis. J Exp Biol 64(1):369–381
Mukai Y, Friebe B, Hatchett JH, Yamamoto M, Gill BS (1993) Molecular cytogenetic analysis of radiation-induced wheat-rye terminal and intercalary chromosomal translocations and the detection of rye chromatin specifying resistance to Hessian fly. Chromosoma 102:88–95
Murray M, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8(19):4321–4326
Muthayya S, Rah JH, Sugimoto JD, Roos FF, Kraemer K, Black RE (2013) The global hidden hunger indices and maps: an advocacy tool for action. PLoS One 8(6):e67860
Neelam K, Rawat N, Tiwari VK, Kumar S, Chhuneja P, Singh K, Randhawa GS, Dhaliwal HS (2011) Introgression of group 4 and 7 chromosomes of Ae. peregrina in wheat enhances grain iron and zinc density. Mol Breeding 28(4):623–634
Ortiz-Monasterio J, Palacios-Rojas N, Meng E, Pixley K, Trethowan R, Pena R (2007) Enhancing the mineral and vitamin content of wheat and maize through plant breeding. J Cereal Sci 46(3):293–307
Patel A, Mamtani M, Dibley MJ, Badhoniya N, Kulkarni H (2010) Therapeutic value of zinc supplementation in acute and persistent diarrhea: a systematic review. PLoS One 5(4):e10386
Peleg Z, Saranga Y, Yazici A, Fahima T, Ozturk L, Cakmak I (2008) Grain zinc, iron and protein concentrations and zinc-efficiency in wild emmer wheat under contrasting irrigation regimes. Plant Soil 306(1–2):57–67
Pfeiffer WH, McClafferty B (2007) Biofortification: breeding micronutrient-dense crops. In: Kang MS, Priyadarshan PM (eds) Breeding major food staples. Blackwell Publishing, Iowa, pp 61–91.
Qi L, Friebe B, Zhang P, Gill BS (2007) Homoeologous recombination, chromosome engineering and crop improvement. Chromosom Res 15(1):3–19
Rakhmatullina EM, Sanamyan MF (2007) Estimation of efficiency of seed irradiation by thermal neutrons for inducing chromosomal aberration in M2 of cotton Gossypium hirsutum L. Russ J Genet 43:518–524
Raupp W, Gill BS, Friebe B, Wilson D, Cox T, Sears R (1995) Proc 8th Int Wheat Genet Symp. In: The Wheat Genetics Resource Center: germ plasm conservation, evaluation and utilization. China Agricultural Scientech Press, Beijing, China, pp 469–475
Rawat N, Neelam K, Tiwari VK, Randhawa GS, Friebe B, Gill BS, Dhaliwal HS (2011) Development and molecular characterization of wheat–Aegilops kotschyi addition and substitution lines with high grain protein, iron, and zinc. Genome 54(11):943–953
Rawat N, Tiwari VK, Singh N, Randhawa GS, Singh K, Chhuneja P, Dhaliwal HS (2009) Evaluation and utilization of Aegilops and wild Triticum species for enhancing iron and zinc content in wheat. Genet Resour Crop Ev 56(1):53–64
Rawat N, Neelam K, Tiwari VK, Dhaliwal HS (2013) Biofortification of cereals to overcome hidden hunger. Plant Breed 132:437–445.
Sasaki A, Yamaji N, Yokosho K, Ma JF (2012) Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24:2155–2167
Sharma P, Sheikh I, Singh D, Kumar S, Verma SK, Kumar R, Vyas P, Dhaliwal HS (2017) Uptake, distribution, and remobilization of iron and zinc among various tissues of wheat-Aegilops substitution lines at different growth stages. Acta Physiol Plant 39:185
Sheikh I, Sharma P, Verma SK, Kumar S, Kumar R, Vyas P, Dhaliwal HS (2018) Development of intron targeted amplified polymorphic markers of metal homeostasis genes for monitoring their transfers from Aegilops species to wheat. Mol Breeding 38:47
Singh J, Sheikh I, Sharma P, Kumar S, Verma SK, Kumar R, Mathpal P, Kumar S, Vyas P, Dhaliwal HS (2016) Transfer of HMW glutenin subunits from Aegilops kotschyi to wheat through radiation hybridization. J Food Sci Technol 53(9):3543–3549
Snape J, Parker B, Simpson E, Ainsworth C, Payne P, Law C (1983) The use of irradiated pollen for differential gene transfer in wheat (Triticum aestivum). Theor Appl Genet 65(2):103–111
Somers DJ, Isaac P, Edwards K (2004) A high-density microsatellite consensus map for bread wheat (Triticum aestivum L.). Theor Appl Genet 109(6):1105–1114
Tiong J, McDonald GK, Genc Y, Pedas P, Hayes JE, Toubia J, Langridge P, Huang CY (2014) HvZIP7 mediates zinc accumulation in barley (Hordeum vulgare) at moderately high zinc supply. New Phytol 201(1):131–143
Tiwari VK, Rawat N, Chhuneja P, Neelam K, Aggarwal R, Randhawa GS, Dhaliwal HS, Keller B, Singh K (2009) Mapping of quantitative trait loci for grain iron and zinc concentration in diploid A genome wheat. J Hered 100(6):771–776
Tiwari VK, Rawat N, Neelam K, Kumar S, Randhawa GS, Dhaliwal HS (2010) Substitutions of 2S and 7U chromosomes of Aegilops kotschyi in wheat enhance grain iron and zinc concentration. Theor Appl Genet 121(2):259–269
Tiwari VK, Riera-Lizarazu O, Gunn HL, Lopez K, Iqbal MJ, Kianian SF, Leonard JM (2012) Endosperm tolerance of paternal aneuploidy allows radiation hybrid mapping of the wheat D-genome and a measure of γ ray-induced chromosome breaks. PLoS One 7(11):e48815
Uauy C, Distelfeld A, Fahima T, Blechl A, Dubcovsky J (2006) A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Sci 314:1298–1301
Verma SK, Kumar S, Sheikh I, Malik S, Mathpal P, Chugh V, Kumar S, Prasad R, Dhaliwal HS (2016a) Transfer of useful variability of high grain iron and zinc from Aegilops kotschyi into wheat through seed irradiation approach. Int J Radiant Biol 92(3):132–139
Verma SK, Kumar S, Sheikh I, Sharma P, Mathpal P, Malik S, Kundu P, Awasthi A, Kumar S, Prasad R, Dhaliwal HS (2016b) Induced homoeologous pairing for transfer of useful variability for high grain Fe and Zn from Aegilops kotschyi into wheat. Plant Mol Biol Report 34(6):1083–1094
Vert G, Briat JF, Curie C (2001) Arabidopsis IRT2 gene encodes a root-periphery iron transporter. Plant J 26:181–189
Wang L, Chen P, Wang X (2010) Molecular cytogenetic analysis of Triticum aestivum-Leymus racemosus reciprocal chromosomal translocation T7DS5LrL/T5LrS7DL. Chin Sci Bull 55:1026–1031
Wei H, Dhanaraj AL, Rowland LJ, Fu Y, Krebs SL, Arora R (2005) Comparative analysis of expressed sequence tags from cold-acclimated and non-acclimated leaves of Rhododendron catawbiense Michx. Planta 221(3):406–416
White PJ, Broadley MR (2011) Physiological limits to zinc biofortification of edible crops. Front Plant Sci 2:80
WHO (2012) UNFPA, The World Bank. Trends in maternal mortality: 1990 to 2010. World Health Organization, UNICEF, UNFPA
Acknowledgements
The authors acknowledge the Department of Biotechnology, Government of India for Grant (BT/AGR/Wheat Bioforti/PH-II/2010) through a network project “Biofortification of wheat for micronutrients through conventional and molecular approaches—phase-II”. The authors also acknowledge the Akal College of Agriculture for providing infrastructural facilities to carry out this work.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
ESM 1
(DOCX 2.60 mb)
Rights and permissions
About this article
Cite this article
Sharma, P., Sheikh, I., Kumar, S. et al. Precise transfers of genes for high grain iron and zinc from wheat-Aegilops substitution lines into wheat through pollen irradiation. Mol Breeding 38, 81 (2018). https://doi.org/10.1007/s11032-018-0836-8
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11032-018-0836-8