Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

Iron-deficiency response and differential expression of iron homeostasis related genes in spring wheat (Triticum aestivum) mutant lines with increased grain iron content

Saule S. Kenzhebayeva https://orcid.org/0000-0003-0238-2607 A C , Saule D. Atabayeva A and Fatma Sarsu B
+ Author Affiliations
- Author Affiliations

A Faculty of Biology and Biotechnology, Al-Farabi Kazakh National University, 040050, Al-Farabi, 71, Almaty, Kazakhstan.

B Plant Breeding and Genetics Section, Joint FAO/IAEA Division, International Atomic Energy Agency, Vienna, Austria.

C Corresponding author. Email: kenzhebaevas@mail.ru, S.Kenzhebaeva@kaznu.kz

Crop and Pasture Science - https://doi.org/10.1071/CP21136
Submitted: 27 February 2021  Accepted: 4 June 2021   Published online: 27 October 2021

Abstract

Iron (Fe) is essential for plant growth and human health. Fe deficiency reduces yield and quality traits of wheat (Triticum aestivum L.). Grains of modern bread wheat varieties contain low levels of Fe, and Fe uptake and translocation in wheat grown in Fe conditions have not been studied in detail. This study investigates Fe homeostasis and biofortification in genetically stable spring wheat Almaken and Zhenis M5 mutant lines, developed with 200 Gy for higher grain Fe content. Mutant lines and parents were analysed for the expression of genes involved in Fe homeostasis under normal and deficient Fe. Wheat homologues of genes that participated in phytosiderophore (PS) synthesis and transport were significantly upregulated in the Fe-limited roots of Almaken M/1 and both Zhenis M/2 mutant lines, emphasising the role of deoxymugineic acid (DMA) in iron acquisition. The combined overexpression of SAMS, NAS1, TaNAAT, DMAS and TOM was also revealed in the roots of Almaken M/1 and both Zhenis M5 mutant lines, suggesting their involvement in PS synthesis, Fe chelation and transport. Under Fe deficiency, levels of TaYS1A encoding the wheat homologues of the metal-NA transporter YSL, also showed 2.6-, 5.1- and 5.9-fold increases in the roots of Almaken M/1 and both Zhenis M5 mutant lines, respectively. Vacuolar iron transporters (VIT2), natural resistance associated-macrophage protein (NRAMP) genes and the transcription factor basic-loop-helix (bHLH) were significantly upregulated under Fe starvation in shoots. Fe-deficiency-related genotype-dependent and tissue-specific gene expression differences provide new insights into genes involved in iron homeostasis and biofortification genes in wheat.

Keywords: gene expression, iron homeostasis, iron deficiency, spring wheat, mutant lines.


References

Abbaspour N, Hurrell R, Kelishadi R (2014) Review on iron and its importance for human health. Journal Res Medical Science 19, 164–174.

Araki R, Murata J, Murata Y (2011) A novel barley yellow stripe 1-like transporter (HvYSL2) localized to the root endodermis transports metal–phytosiderophore complexes. Plant & Cell Physiology 52, 1931–1940.
A novel barley yellow stripe 1-like transporter (HvYSL2) localized to the root endodermis transports metal–phytosiderophore complexes.Crossref | GoogleScholarGoogle Scholar |

Beasley JT, Bonneau JP, Johnson AAT (2017) Characterization of the nicotianamine aminotransferase and deoxymugineic acid synthase genes essential to strategy II Fe uptake in bread wheat (Triticum aestivum L.). PLoS One 12, e0177061
Characterization of the nicotianamine aminotransferase and deoxymugineic acid synthase genes essential to strategy II Fe uptake in bread wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar | 28475636PubMed |

Black C, Moon G, Baird J (2014) Dietary inequalities: what is the evidence for the effect of the neighborhood food environment? Health & Place 27, 229–242.
Dietary inequalities: what is the evidence for the effect of the neighborhood food environment?Crossref | GoogleScholarGoogle Scholar |

Bonneau J, Baumann U, Beasley J, Li Y, Johnson AAT (2016) Identification and molecular characterization of the nicotianamine synthase gene family in bread wheat. Plant Biotechnology Journal 14, 2228–2239.
Identification and molecular characterization of the nicotianamine synthase gene family in bread wheat.Crossref | GoogleScholarGoogle Scholar | 27155533PubMed |

Borrill P, Connorton JM, Balk J, Miller AJ, Sanders D, Uauy C (2014) Biofortification of wheat grain with Fe and zinc: integrating novel genomic resources and knowledge from model crops. Frontiers in Plant Science 5, 1–8.
Biofortification of wheat grain with Fe and zinc: integrating novel genomic resources and knowledge from model crops.Crossref | GoogleScholarGoogle Scholar |

Bouis HE, Saltzman A (2017) Improving nutrition through biofortification: A review of evidence from HarvestPlus, 2003 through 2016. Global Food Security 12, 49–58.
Improving nutrition through biofortification: A review of evidence from HarvestPlus, 2003 through 2016.Crossref | GoogleScholarGoogle Scholar | 28580239PubMed |

Briat JF, Duc C, Ravet K, Gaymard F (2010) Ferritins and iron storage in plants. Biochimica et Biophysica Acta 1800, 806–814.
Ferritins and iron storage in plants.Crossref | GoogleScholarGoogle Scholar | 20026187PubMed |

Connorton JM, Balk J, Rodríguez-Celma J (2017) Fe homeostasis in plants – a brief overview. Metallomics 9, 813–823.
Fe homeostasis in plants – a brief overview.Crossref | GoogleScholarGoogle Scholar | 28686269PubMed |

Curie C, Cassin G, Couch D, Divol F, Higuchi K, Jean ML, Misson J, Schikora A, Czernic P, Mari S (2008) Metal movement within the plant: contribution of nicotianamine and YELLOW STRIPE 1-LIKE transporters. Annals of Botany 103, 1–11.
Metal movement within the plant: contribution of nicotianamine and YELLOW STRIPE 1-LIKE transporters.Crossref | GoogleScholarGoogle Scholar | 18977764PubMed |

Fan MS, Zhao FJ, Fairweather-Tait SJ, Poulton PR, Dunham SJ, McGrath SP (2008) Evidence of decreasing mineral density in wheat grain over the last 160 years. Journal of Trace Elements in Medicine and Biology 22, 315–324.
Evidence of decreasing mineral density in wheat grain over the last 160 years.Crossref | GoogleScholarGoogle Scholar | 19013359PubMed |

Feng Ma J, Taketa S, Chang Y-C, Takeda K, Matsumoto H (1999) Biosynthesis of phytosiderophores in several Triticeae species with different genomes. Journal of Experimental Botany 50, 723–726.

Gao H, Xie W, Yang C, Xu J, Li J, Wang H, Chen X, Huang CF (2018) NRAMP2, a trans-Golgi network-localized manganese transporter, is required for Arabidopsis root growth under manganese deficiency. New Phytologist 217, 179–193.
NRAMP2, a trans-Golgi network-localized manganese transporter, is required for Arabidopsis root growth under manganese deficiency.Crossref | GoogleScholarGoogle Scholar |

Gao F, Robe K, Gaymard F, Izquierdo E, Dubos C (2019) The Transcriptional control of Fe homeostasis in plants: a tale of bHLH transcription factors? Frontiers in Plant Science 10, 6
The Transcriptional control of Fe homeostasis in plants: a tale of bHLH transcription factors?Crossref | GoogleScholarGoogle Scholar | 30713541PubMed |

Grillet L, Schmidt W (2019) Iron acquisition strategies in land plants: not so different after all. New Phytologist 224, 11–18.
Iron acquisition strategies in land plants: not so different after all.Crossref | GoogleScholarGoogle Scholar |

Gupta PK, Balyan HS, Sharma Sh, Kumar R (2021) Biofortification and bioavailability of Zn, Fe and Se in wheat: present status and future prospects. Theoretical and Applied Genetics 134, 1–35.

Haydon MJ, Cobbett CS (2007) A novel major facilitator superfamily protein at the tonoplast influences zinc tolerance and accumulation in Arabidopsis. Plant Physiology 143, 1705–1719.
A novel major facilitator superfamily protein at the tonoplast influences zinc tolerance and accumulation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 17277087PubMed |

Kaur G, Shukla V, Kumar A, Kaur M, Goel P, Singh P, Shukla A, Meena V, Kaur J, Singh J, Mantri Sh, Rouached H, Pandey AK (2019) Integrative analysis of hexaploid 1 wheat roots identifies signature components during Fe starvation. Journal of Experimental Botany 70, 6141–6161.
Integrative analysis of hexaploid 1 wheat roots identifies signature components during Fe starvation.Crossref | GoogleScholarGoogle Scholar | 31738431PubMed |

Kenzhebayeva SS, Doktyrbay G, Capstaff NM, Sarsu F, Omirbekova NZh, Eilam T, Tashenev DK, Miller AJ (2017) Searching a spring wheat mutation resource for correlations between yield, grain size, and quality parameters. Journal of Crop Improvement 31, 209–228.
Searching a spring wheat mutation resource for correlations between yield, grain size, and quality parameters.Crossref | GoogleScholarGoogle Scholar |

Kenzhebayeva S, Abekova A, Atabayeva S, Yernazarova G, Omirbekova N, Zhang G, Turasheva S, Asrandina S, Sarsu F, Wang Y (2019) Mutant lines of spring wheat with increased iron, zinc, and micronutrients in grains and enhanced bioavailability for human health. BioMed Research International 2019, 9692053
Mutant lines of spring wheat with increased iron, zinc, and micronutrients in grains and enhanced bioavailability for human health.Crossref | GoogleScholarGoogle Scholar | 31001559PubMed |

Kim SA, Guerinot ML (2007) Mining iron: iron uptake and transport in plants. FEBS Letters 581, 2273–2280.
Mining iron: iron uptake and transport in plants.Crossref | GoogleScholarGoogle Scholar | 17485078PubMed |

Kobayashi T, Nishizawa NK (2012) Iron uptake, translocation, and regulation in higher plants. Annual Review of Plant Biology 63, 131–152.
Iron uptake, translocation, and regulation in higher plants.Crossref | GoogleScholarGoogle Scholar | 22404471PubMed |

Kobayashi T, Nakanishi H, Nishizawa NK (2010) Recent insights into Fe homeostasis and their application in graminaceous crops. Proceedings of the Japan Academy. Series B, Physical and Biological Sciences 86, 900–913.
Recent insights into Fe homeostasis and their application in graminaceous crops.Crossref | GoogleScholarGoogle Scholar | 21084773PubMed |

Kobayashi T, Ozu A, Kobayashi S, et al (2019) OsbHLH058 and Osb- HLH059 transcription factors positively regulate iron deficiency responses in rice. Plant Molecular Biology 101, 471–486.
OsbHLH058 and Osb- HLH059 transcription factors positively regulate iron deficiency responses in rice.Crossref | GoogleScholarGoogle Scholar | 31552586PubMed |

Koike S, Inoue H, Mizuno D, Takahashi M, Nakanishi H, Mori S, et al (2004) OsYSL2 is a rice metal-nicotianamine transporter that is regulated by iron and expressed in the phloem. The Plant Journal 39, 415–424.
OsYSL2 is a rice metal-nicotianamine transporter that is regulated by iron and expressed in the phloem.Crossref | GoogleScholarGoogle Scholar | 15255870PubMed |

Kumar A, Kaur G, Goel P, Bhati KK, Kaur M, Shukla V, Pandey AK (2019) Genome-wide analysis of oligopeptide transporters and detailed characterization of yellow stripe transporter genes in hexaploid wheat. Functional & Integrative Genomics 19, 75–90.
Genome-wide analysis of oligopeptide transporters and detailed characterization of yellow stripe transporter genes in hexaploid wheat.Crossref | GoogleScholarGoogle Scholar |

Nozoye T, Nagasaka S, Kobayashi T, Sato Y, Uozumi N, Nakanishi H, Nishizawa NK (2015) The phytosiderophore efflux transporter TOM2 is involved in metal transport in rice. Journal Biological Chemistry 290, 27688–27699.
The phytosiderophore efflux transporter TOM2 is involved in metal transport in rice.Crossref | GoogleScholarGoogle Scholar |

Parry MA, Madgwick PJ, Bayon C, Tearall K, Hernandez-Lopez A, Baudo M, Rakszegi M, Hamada W, Al-Yassin Ouabbou A, Labhilili M, Phillips AL (2009) Mutation discovery for crop improvement Journal of Experimental Botany 60, 2817–2825.
Mutation discovery for crop improvementCrossref | GoogleScholarGoogle Scholar | 19516074PubMed |

Paul S, Ali N, Sarkar SN, Swapan K, Datta SK, Datta K (2013) Loading and bioavailability of Fe in cereal grains. Plant Cell, Tissue and Organ Culture 113, 363–373.
Loading and bioavailability of Fe in cereal grains.Crossref | GoogleScholarGoogle Scholar |

Perez-Massot E, Banakar R, Gomez-Galera S, Zorrilla-Lopez U, Sanahuja G, Arjo G, Miralpeix B, Vamvaka E, Farre G, Rivera SM, Dashevskaya S, Berman J, Sabalza M, Yuan D, Bai C, Bassie L, Twyman RM, Capell T, Christou P, Zhu C (2013) The contribution of transgenic plants to better health through improved nutrition: opportunities and constraints. Genes & Nutrition 8, 29–41.
The contribution of transgenic plants to better health through improved nutrition: opportunities and constraints.Crossref | GoogleScholarGoogle Scholar |

Qin L, Han P, Chen L, Walk TC, Li Y, Hu X, Xie L, Liao H, Liao X (2017) Genome-wide identification and expression analysis of NRAMP family genes in soybean (Glycine max L.). Frontiers in Plant Science 8, 1436
Genome-wide identification and expression analysis of NRAMP family genes in soybean (Glycine max L.).Crossref | GoogleScholarGoogle Scholar | 28868061PubMed |

Sasaki A, Yamaji N, Yokosho K, Ma JF (2012) Nramp5 is a major transporter responsible for man-ganese and cadmium uptake in rice. The Plant Cell 24, 2155–2167.
Nramp5 is a major transporter responsible for man-ganese and cadmium uptake in rice.Crossref | GoogleScholarGoogle Scholar | 22589467PubMed |

Sauter M, Moffatt B, Saechao MCh, Hell R, Wirtz M (2013) Methionine salvage and S-adenosylmethionine: essential links between sulfur, ethylene and polyamine biosynthesis. The Biochemical Journal 451, 145–154.
Methionine salvage and S-adenosylmethionine: essential links between sulfur, ethylene and polyamine biosynthesis.Crossref | GoogleScholarGoogle Scholar | 23535167PubMed |

Schefe JH, Lehmann KE, Buschmann IR, Unger T, Funke-Kaiser H (2006) Quantitative real-time RT-PCR data analysis: current concepts and the novel “gene expression’s CT difference” formula. Journal of Molecular Medicine 84, 901–910.
Quantitative real-time RT-PCR data analysis: current concepts and the novel “gene expression’s CT difference” formula.Crossref | GoogleScholarGoogle Scholar | 16972087PubMed |

Sharma S, Kaur G, Kumar A Meena V, Ram H, Kaur J, Pandet AK (2020) Gene expression pattern of vacuolar-iron transporter-like (VTL) genes in hexaploid wheat during metal stress. Plants 9, 229
Gene expression pattern of vacuolar-iron transporter-like (VTL) genes in hexaploid wheat during metal stress.Crossref | GoogleScholarGoogle Scholar |

Takahashi M, Terada Y, Nakai I, Nakanishi H, Yoshimura E, Mori S, Nishizawa NK (2003) Role of nicotianamine in the intracellular delivery of metals and plant reproductive development. The Plant Cell 15, 1263–1280.
Role of nicotianamine in the intracellular delivery of metals and plant reproductive development.Crossref | GoogleScholarGoogle Scholar | 12782722PubMed |

Tejada-Jiménez M, Castro-Rodríguez R, Kryvoruchko I, Lucas MM, Udvardi M, Imperial J, et al (2015) Medicago truncatula natural resistance-associated macrophage protein1 is required for Fe uptake by rhizobia-infected nodule cells. Plant Physiology 168, 258–272.
Medicago truncatula natural resistance-associated macrophage protein1 is required for Fe uptake by rhizobia-infected nodule cells.Crossref | GoogleScholarGoogle Scholar | 25818701PubMed |

Wang M, Kawakami Y, Bhullar NK (2019) Molecular analysis of iron deficiency response in hexaploid wheat. Frontiers in Sustainable Food Systems 3, 67
Molecular analysis of iron deficiency response in hexaploid wheat.Crossref | GoogleScholarGoogle Scholar |

Yordem BK, Conte SS, Ma JF, Yokosho K, Vasques KA, Gopalsamy SN, Walker EL (2011) Brachypodium distachyon as a new model system for understanding iron homeostasis in grasses: phylogenetic and expression analysis of yellow stripe-like (YSL) transporters. Annals of Botany 108, 821–833.
Brachypodium distachyon as a new model system for understanding iron homeostasis in grasses: phylogenetic and expression analysis of yellow stripe-like (YSL) transporters.Crossref | GoogleScholarGoogle Scholar | 21831857PubMed |