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Abstract

Rice is the major food crop grown in all over the world mitigating 60–70% requirement of calories. However, its growth has always been challenged under different abiotic stress. Iron is one such important micronutrient, which pose hazardous effects to its yield and quality under both iron (Fe) deficient and excess condition. Recent research studies have attempted to overcome these iron stress constraints by understanding the function of homeostatic genes involved in it and modulating their expression through developed molecular technologies. These technologies involved overexpression of genes in iron uptake, transport, storage, along with the transcriptomics analysis of whole genome to develop a better quality of rice progenies which can withstand various adverse effects of iron stress. Iron homeostasis pathway involves Strategy I and Strategy II followed by dicotyledonous and monocotyledonous plants. However, in the case of rice, several genes involved in both strategies have found to be responsive under Fe-deficient and excess condition. Interaction of other metals present in the soil along with pH can affect the iron uptake in rice. Transgenic rice can become a strong contender in iron stress condition controlling iron uptake, translocation and storage.

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Abbreviations

FRO:

Ferric chelate reductase

IRT:

Iron-regulated transporter

MA:

Mugineic acid

NAS:

Nicotinamide synthase

NAAT:

Nicotianamine aminotransferase

DMAS:

Deoxymugineic acid

YSL:

Yellow stripe like

NRAMPs:

Natural resistance-associated macrophage proteins

TOMs:

Transporter of mugineic acid

PEZ:

Phenolics efflux zero

IDEF:

Iron-deficiency element factor (transcription factor)

FER:

Ferritin

References

  1. Bishwajit G, Sarker S, Kpoghomou MK, Gao H, Jun L, Yin D, Ghosh S (2013) Self- sufficiency in rice and food security: a South Asian perspective. Agric Food Secur 2:1–6. https://doi.org/10.1186/2048-7010-2-10

    Article  Google Scholar 

  2. Rout GR, Sahoo S (2015) Role of Iron in plant growth and mechanism. Rev Agric Sci 3:1–24. https://doi.org/10.7831/ras.3.1

    Article  Google Scholar 

  3. Asch F, Becker M, Kpongor DS (2005) A quick and efficient screen for resistance to iron toxicity in lowland rice. J Plant Nutr Soil Sci 168:1–10. https://doi.org/10.1002/jpln.200520540

    Article  CAS  Google Scholar 

  4. Dorlodot SD, Lutts S, Bertin P (2005) Effects of ferrous iron toxicity on the growth and mineral composition of an interspecific rice. J Plant Nutr 28:1–20. https://doi.org/10.1081/PLN-200042144

    Article  CAS  Google Scholar 

  5. Kobayashi T, Nishizawa NK (2012) Iron uptake, translocation, and regulation in higher plants. Ann Rev Plant Soil 63:132–152. https://doi.org/10.1146/annurev-arplant-042811-105522

    Article  CAS  Google Scholar 

  6. Sikirou M, Saito K, Dako EGA, Drame KN, Adam A, Venuprasad R (2015) Genetic improvement of iron toxicity tolerance in rice progress, challenges and prospects in West Africa. Plant Prod Sci 18:423–434. https://doi.org/10.1626/pps.18.423

    Article  CAS  Google Scholar 

  7. Kobayashi T, Itai RN, Nishizawa NK (2014) Iron deficiency responses in rice roots. Rice 7:1–21. https://doi.org/10.1186/s12284-014-0027-0

    Article  Google Scholar 

  8. Romheld V, Marschner H (1986) Evidence for a specific uptake system for iron phytosiderophore in roots of grasses. Plant Physiol 80:175–180. https://doi.org/10.1104/pp.80.1.175

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Bashir K, Ishimaru Y, Nishizawa NK (2010) Iron uptake and loading into rice grains. Rice 3:122–130. https://doi.org/10.1007/s12284-010-9042-y

    Article  Google Scholar 

  10. Inoue H, Kobayashi T, Nozoye T, Takahashi M, Kakei Y, Suzuki K, Nakazono M, Nakanishi H, Mori S, Nishizawa NK (2008) 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 284:3470–3479. https://doi.org/10.1074/jbc.M806042200

    Article  PubMed  CAS  Google Scholar 

  11. Lee S, Chieko JC, Kim SA, Walker EL, Lee Y (2009) Disruption of OsYSL15 leads to Iron inefficiency in rice plants. Plant Physiol 150:786–800. https://doi.org/10.1104/pp.109.135418

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Shabala S (2011) Physiological and cellular aspects of phytotoxicity tolerance in plants: the role of membrane transporters and implications for crop breeding for water logging tolerance. New Phytol 190:289–298. https://doi.org/10.1111/j.1469-8137.2010.03575.x

    Article  PubMed  CAS  Google Scholar 

  13. Li S, Pan XX, Berry JO, Wang Y, Naren MaS, Tan S, **ao W, Zhao WZ, Sheng XY, Ying LP (2015) OsSec24, a functional Sec24- like protein in rice, improves tolerance to iron deficient and high pH by enhancing H+ secretion mediated by PM-H+ ATPase. Plant Sci 233:61–71. https://doi.org/10.1016/j.plantsci.2015.01.001

    Article  PubMed  CAS  Google Scholar 

  14. Connorton JM, Balk J, Celma JR (2017) Iron homeostasis: a brief overview. Metallomics 9(7):813–823. https://doi.org/10.1039/c7mt00136c

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Ishimaru Y, Suzuki M, Tsukamoto T, Suzuki K, Nakazono M, Kobayashi T, Wada Y, Watanabe S, Matsuhashi S, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2006) Rice plants take up iron as an Fe3+-phytosiderophore and as Fe2+. Plant J 45:335–346. https://doi.org/10.1111/j.1365-313X.2005.02624.x

    Article  PubMed  CAS  Google Scholar 

  16. 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 133:1102–1110. https://doi.org/10.1104/pp.103.025122

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Pereira MP, Santos C, Gomes A, Vasconcelos MW (2014) Cultivar variability of iron uptake mechanisms in rice (Oryza sativa L.). Plant Physiol Biochem 85:21–30. https://doi.org/10.1016/j.plaphy.2014.10.007

    Article  PubMed  CAS  Google Scholar 

  18. Yokosho K, Yamaji N, Feng Ma J (2016) OsFRDL1 expressed in nodes is required for distribution of iron into grains in rice. J Exp Bot 67:5485–5494. https://doi.org/10.1093/jxb/erw314

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Kim S et al (2006) Localisation of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science 314:1295–1298. https://doi.org/10.1126/science.1132563

    Article  PubMed  CAS  Google Scholar 

  20. Darbani B, Brait JF, Holm PB, Husted S, Noeparvar S, Norg S (2013) Dissecting plant iron homeostasis under short and long-term iron fluctuation. Biotechnol Adv 31:1292–1307. https://doi.org/10.1016/j.biotechadv.2013.05.003

    Article  PubMed  CAS  Google Scholar 

  21. Belouchi A, Kwan T, Gros P (1996) Cloning and characterization of the OsNRAMP family from Oryza sativa, a new family of membrane proteins possibly implicated in the transport of metal ions. Plant Mol Biol 33:1085–1092. https://doi.org/10.1023/A%3A1005723304911

    Article  Google Scholar 

  22. Briat JF, Duc C, Ravet K, Gaymard F (2010) Ferritins and iron storage in plants. Biochem Biophy Acta 1800:806–814. https://doi.org/10.1016/j.bbagen.2009.12.003

    Article  CAS  Google Scholar 

  23. Gross J, Stein RS, Fett-neto AG, Fett JP (2003) Iron homeostasis related genes in rice. Genet Mol Biol 26:1415–4757. https://doi.org/10.1590/S14157572003000400012

    Article  Google Scholar 

  24. Stein RJ, Ricachenevsky FK, Fett JP (2009) Differential regulation of the two rice ferritin genes (OsFER1 and OsFER2). Plant Sci 177:563–569. https://doi.org/10.1016/j.plantsci.2009.08.001

    Article  CAS  Google Scholar 

  25. Shahid M, Nayak AK, Shukla AK, Tripathi R, Kumar A, Raja R, Panda BB, Meher J, Bhattacharyya P, Das D (2014) Mitigation of iron toxicity and Iron, Zinc and Manganese nutrition of wetland rice cultivars (Oryza sativa L.) grown in iron toxic soil. CLEAN Soil Air Water 42(11):1604–1609. https://doi.org/10.1002/clen.201300178

    Article  CAS  Google Scholar 

  26. Maheshwari M, Murthy ANG, Shanker AK (2017) 12-Nitrogen nutrition in crops and its importance in crop quality. Indian Nitrogen Assess 1:175–186. https://doi.org/10.1016/B978-0-12-811836-8.00012-4

    Article  Google Scholar 

  27. Banakar R, Fernandez AA, Benito PD, Abadia J, Capell T, Christou P (2017) Phytosiderophores determine thresholds for iron and zinc accumulation in biofortified rice endosperm while inhibiting the accumulation of cadmium. J Exp Bot 68(17):4983–4995. https://doi.org/10.1093/jxb/erx304

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Ishimaru Y, Masuda H, Bashir K, Inoue H, Tsukamoto T, Takahashi M, Nakanishi H, Aoki N, Hirose T, Ohsugi R, Nishizawa NK (2010) Rice metal-nicotianamine transporter, OsYSL2, is required for the long-distance transport of iron and manganese. Plant J 62:379–390. https://doi.org/10.1111/j.1365-313X.2010.04158.x

    Article  PubMed  CAS  Google Scholar 

  29. Wang M, Gruissem W, Bhullar NK (2013) Nicotianamine synthase overexpression positively modulates iron homeostasis-related genes in high iron rice. Front Plant Sci 4:1–15. https://doi.org/10.3389/fpls.2013.00156

    Article  Google Scholar 

  30. Inoue H, Takahashi M, Kobayashi T, Suzuki M, Nakanishi H, Mori S, Nishizawa NK (2008) Identification and localization of the rice nicotianamine aminotransferase gene OsNAAT1 expression suggests the site of phytosiderophore synthesis in rice. Plant Mol Biol 66:193–203. https://doi.org/10.1007/s11103-007-9262-8

    Article  PubMed  CAS  Google Scholar 

  31. Bashir K, Hanada K, Shimizu M, Seki M, Nakanishi H, Nishizawa NK (2014) Transcriptomic analysis of rice in response to iron deficiency and excess. Rice 7:1–15. https://doi.org/10.1186/s12284-014-0018-1

    Article  Google Scholar 

  32. Ishimaru Y, Bashir K, Nakanishi H, Nishizawa NK (2011) A rice phenolics efflux transporter in solubilizing apoplasmic iron. Plant Signal Behav 46:1624–1626. https://doi.org/10.1074/jbc.M111.221168

    Article  CAS  Google Scholar 

  33. Bashir K, Ishimaru Y, Itai RN, Senoura T, Takahashi M, An G, Oikawa T, Ueda M, Sato A, Uozumi N, Nakanishi H, Nishizawa NK (2015) Iron deficiency regulated OsOPT7 is essential for iron homeostasis in rice. Plant Mol Biol 88:165–176. https://doi.org/10.1007/s11103-015-0315-0

    Article  PubMed  CAS  Google Scholar 

  34. Yang A, Zhang WH (2016) A small GTPase, OsRab6q, is involved in the regulation of iron homeostasis in rice. Plant Cell Physiol 57:1271–1280. https://doi.org/10.1093/jxb/erq301

    Article  PubMed  CAS  Google Scholar 

  35. Kobayashi T, Suzuki M, Inoue H, Itai RN, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2005) Expression of iron-acquisition-related genes in iron-deficient rice is coordinately induced by partially conserved iron-deficiency-responsive elements. J Exp Bot 56:1305–1316. https://doi.org/10.1093/jxb/eri131

    Article  PubMed  CAS  Google Scholar 

  36. Zheng L, Ying Y, Wang L, Wang F, Whelan J, Shou H (2012) Identification of a novel iron regulated basic helix loop helix protein involved in Fe homeostasis in Oryza sativa. BMC Plant Biol 10:1–9. https://doi.org/10.1186/1471-2229-10-166

    Article  CAS  Google Scholar 

  37. Khong GN, Richaud F, Coudert Y, Pati PK, Santi C, Perin C, Breitler JC, Meynard D, Vinh DN, Guiderdoni E, Gantet P (2008) Modulating rice stress by transcription factors. Biotechnol Genet Eng 25:381–404. https://doi.org/10.5661/bger-25-381

    Article  CAS  Google Scholar 

  38. Thompson MJ, De Ocampo M, Egdane J, Rahman MA, Sajise AG, Adorada DL, Tumimbang-Raiz E, Blumwald E, Seraj ZI, Singh RK, Gregorio GB, Ismail AM (2010) Characterizing the Saltol quantitative trait locus for salinity tolerance in rice. Rice 3:148–160. https://doi.org/10.1007/s12284-010-9053-8

    Article  Google Scholar 

  39. Dufey I, Hakizimana P, Draye X, Lutts S, Bertin P (2009) QTL map** for biomass and physiological parameters linked to resistance mechanisms to ferrous iron toxicity in rice. Euphytica 167:143–160. https://doi.org/10.1007/s10681-008-9870

    Article  CAS  Google Scholar 

  40. Shimizu A (2009) QTL analysis of genetic tolerance to Iron toxicity in rice (Oryza sativa L.) by quantification of bronzing score. J New Seeds 10:171–179. https://doi.org/10.1080/15228860903064989

    Article  Google Scholar 

  41. Lb Wu, Shhadi MY, Gregorio G, Matthus E, Becker M, Frei M (2014) Genetic and physiological analysis of tolerance to acute iron toxicity in rice. Rice 7:1–12. https://doi.org/10.1186/s12284-014-0008-3

    Article  Google Scholar 

  42. Suzuki M, Takahashi M, Tsukamoto T, Watanabe S, Matsuhashi S (2006) Biosynthesis and secretion of mugineic acid family phytosiderophores in zinc-deficient barley. Plant J 48:85–97. https://doi.org/10.1111/j.1365-313X.2006.02853.x

    Article  PubMed  CAS  Google Scholar 

  43. Ishimaru Y, Kim S, Tsukamoto T, Oki H, Kobayashi T, Watanabe S, Matsuhashi S, Takahshi M, Nakanishi H, Mori S, Nishizawa NK (2007) Mutational reconstructed ferric chelate reductase confers enhanced tolerance in rice to iron deficiency in calcareous soil. Proc Natl Acad Sci 104:7373–7378. https://doi.org/10.1073/pnas.0610555104

    Article  PubMed  CAS  Google Scholar 

  44. Masuda H, Aung MA, Nishizawa NK (2013) Iron biofortification of rice using different transgenic approaches. Rice 6:1–40. https://doi.org/10.1186/1939-8433-6-40

    Article  Google Scholar 

  45. Finnato T, Oliveira AC, Chaparro C, Maia LC, Farias DR, Woyann LG, Mistura CC, Bresolin APS, Lauro C, Panaud O, Picault N (2015) Abiotic stress and genome dynamics: specific genes and transposable elements response to iron excess in rice. Rice 8:1–13. https://doi.org/10.1186/s12284-015-0045-6

    Article  Google Scholar 

  46. Liu CW, Sung Y, Chen BC, Lai HY (2014) Effects of nitrogen fertilizer on growth and nitrate and nitrate content of lettuce (Lactuca sativa L.). Int J Environ Res Public Health 11:4427–4440. https://doi.org/10.3390/ijerph110404427

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Chen L, Wang G, Chen P, Zhu H, Wang S, Ding Y (2018) Shoot-root communication plays a key role in physiological alterations of rice (Oryza sativa) under iron deficiency. Front Plant Sci 9:1–12. https://doi.org/10.3389/fpls.2018.00757

    Article  Google Scholar 

  48. Masuda H, Shimochi E, Hamada T, Senoura T, Kobayashi T, Aung MA, Ishimaru Y, Ogo Y, Nakanishi H, Nishizawa NK (2017) A new transgenic rice line exhibiting enhanced ferric ion reduction and phytosiderophore production confers tolerance to low iron availability in calcareous soil. PLoS ONE 12(3):e0173441. https://doi.org/10.1371/journal.pone.0173441

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Correspondence to Sanjib Kumar Panda.

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Significance Statement

Understanding the genetic responses of rice plant along with the morphological changes under uttermost shift in concentrations of iron, the authors can go for the biotechnological interventions to develop the tolerant varieties of the crop that can withstand both excess and deficit condition of iron in the soil.

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Kar, S., Panda, S.K. Iron Homeostasis in Rice: Deficit and Excess. Proc. Natl. Acad. Sci., India, Sect. B Biol. Sci. 90, 227–235 (2020). https://doi.org/10.1007/s40011-018-1052-3

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