Evaluation of rice wild relatives as a source of traits for adaptation to iron toxicity and enhanced grain quality

Autoři: Birgit Bierschenk aff001;  Melle Tilahun Tagele aff001;  Basharat Ali aff001;  M. d. Ashrafuzzaman aff001;  Lin-Bo Wu aff001;  Matthias Becker aff001;  Michael Frei aff001
Působiště autorů: Institute for Crop Science and Resource Conservation (INRES), University of Bonn, Bonn, Germany aff001;  Department of Agronomy, University of Agriculture Faisalabad, Faisalabad, Pakistan aff002;  Department of Genetic Engineering & Biotechnology, Shahjalal University of Science & Technology, Sylhet, Bangladesh aff003
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.pone.0223086


Rice wild relatives (RWR) constitute an extended gene pool that can be tapped for the breeding of novel rice varieties adapted to abiotic stresses such as iron (Fe) toxicity. Therefore, we screened 75 Oryza genotypes including 16 domesticated O. sativa genotypes, one O. glaberrima, and 58 RWR representing 21 species, for tolerance to Fe toxicity. Plants were grown in a semi-artificial greenhouse setup, in which they were exposed either to control conditions, an Fe shock during the vegetative growth stage (acute treatment), or to a continuous moderately high Fe level (chronic treatment). In both stress treatments, foliar Fe concentrations were characteristic of Fe toxicity, and plants developed foliar stress symptoms, which were more pronounced in the chronic Fe stress especially toward the end of the growing season. Among the genotypes that produced seeds, only the chronic stress treatment significantly reduced yields due to increases in spikelet sterility. Moreover, a moderate but non-significant increase in grain Fe concentrations, and a significant increase in grain Zn concentrations were seen in chronic stress. Both domesticated rice and RWR exhibited substantial genotypic variation in their responses to Fe toxicity. Although no RWR strikingly outperformed domesticated rice in Fe toxic conditions, some genotypes scored highly in individual traits. Two O. meridionalis accessions were best in avoiding foliar symptom formation in acute Fe stress, while an O. rufipogon accession produced the highest grain yields in both chronic and acute Fe stress. In conclusion, this study provides the basis for using interspecific crosses for adapting rice to Fe toxicity.

Klíčová slova:

Rice – Plant resistance to abiotic stress – Leaves – Toxicity – Seeds – Domestic animals – Cereal crops – Oryza


1. Brozynska M, Furtado A, Henry RJ (2016) Genomics of crop wild relatives: expanding the gene pool for crop improvement. Plant Biotechnol J 14: 1070–1085. doi: 10.1111/pbi.12454 26311018

2. Mammadov J, Buyyarapu R, Guttikonda SK, Parliament K, Abdurakhmonov IY, Kumpatla SP (2018) Wild Relatives of Maize, Rice, Cotton, and Soybean: Treasure Troves for Tolerance to Biotic and Abiotic Stresses. Front Plant Sci 9. doi: 10.3389/fpls.2018.00886 30002665

3. GRiSP, Global Rice Science Partnership (2013) Rice Almanac, 4th edition. International Rice Research Institute, Los Banos (Philippines).

4. Huang XH, Kurata N, Wei XH, Wang ZX, Wang A, Zhao Q, et al. (2012) A map of rice genome variation reveals the origin of cultivated rice. Nature 490: 497–501. doi: 10.1038/nature11532 23034647

5. Stein JC, Yu Y, Copetti D, Zwickl DJ, Zhang L, Zhang C, et al. (2018) Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza. Nat Genet 50: 285–296. doi: 10.1038/s41588-018-0040-0 29358651

6. Wang M, Yu Y, Haberer G, Marri PR, Fan C, Goicoechea JL, et al. (2014) The genome sequence of African rice (Oryzaglaberrima) and evidence for independent domestication. Nat Genet 46: 982. doi: 10.1038/ng.3044 25064006

7. Hilbert L, Neves EG, Pugliese F, Whitney BS, Shock M, Veasey E, et al. (2017) Evidence for mid-Holocene rice domestication in the Americas. Nat Ecol Evol 1: 1693–1698. doi: 10.1038/s41559-017-0322-4 28993622

8. Menguer PK, Sperotto RA, Ricachenevsky FK (2017) A walk on the wild side: Oryza species as source for rice abiotic stress tolerance. Genet MolBiol 40: 238–252. doi: 10.1590/1678-4685-gmb-2016-0093 28323300

9. Jena KK (2010) The species of the genus Oryza and transfer of useful genes from wild species into cultivated rice, O. sativa. Breed Sci 60: 518–523. doi: 10.1270/jsbbs.60.518

10. Sweeney M, McCouch S (2007) The complex history of the domestication of rice. Ann Bot 100: 951–957. doi: 10.1093/aob/mcm128 17617555

11. Vaughan DA, Morishima H, Kadowaki K (2003) Diversity in the Oryza genus. Curr Opin Plant Biol 6: 139–146. doi: 10.1016/s1369-5266(03)00009-8 12667870

12. Prathepha P (2011) Microsatellite analysis of weedy rice (Oryza sativa f. spontanea) from Thailand and Lao PDR. Aust J Crop Sci 5: 49–54.

13. Cao QJ, Lu BR, Xia H, Rong J, Sala F, Spada A, et al. (2006) Genetic diversity and origin of weedy rice (Oryza sativa f. Spontanea) populations found in North-eastern China revealed by simple sequence repeat (SSR) markers. Ann Bot 98: 1241–1252. doi: 10.1093/aob/mcl210 17056615

14. Brar DS, Khush GS (1997) Alien introgression in rice. Plant Mol Biol 35: 35–47. doi: 10.1023/a:1005825519998 9291958

15. Hajjar R, Hodgkin T (2007) The use of wild relatives in crop improvement: A survey of developments over the last 20 years. Euphytica 156: 1–13. doi: 10.1007/s10681-007-9363-0

16. Tu J, Ona I, Zhang Q, Mew TW, Khush GS, Datta SK (1998) Transgenic rice variety ‘IR72’ with Xa21 is resistant to bacterial blight. TheorAppl Genet 97: 31–36. doi: 10.1007/s001220050863

17. Narain A, Kar MK, Kaliaperumal V, Sen P (2016) Development of monosomic alien addition lines from the wild rice (Oryzabrachyantha A. Chev. et Roehr.) for introgression of yellow stem borer (Scirpophaga incertulas Walker.) resistance into cultivated rice (Oryza sativa L.). Euphytica 209: 603–613. doi: 10.1007/s10681-016-1633-2

18. Ishimaru T, Hirabayashi H, Ida M, Takai T, San-Oh YA, Yoshinaga S, et al. (2010) A genetic resource for early-morning flowering trait of wild rice Oryza officinalis to mitigate high temperature-induced spikelet sterility at anthesis. Ann Bot 106: 515–520. doi: 10.1093/aob/mcq124 20566680

19. Mao DH, Yu L, Chen DZ, Li LY, Zhu YX, Xiao YQ, et al. (2015) Multiple cold resistance loci confer the high cold tolerance adaptation of Dongxiang wild rice (Oryza rufipogon) to its high-latitude habitat. Theor Appl Genet 128: 1359–1371. doi: 10.1007/s00122-015-2511-3 25862679

20. Hoang TML, Tran TN, Nguyen TKT, Williams B, Wurm P, Bellairs S, et al. (2016) Improvement of Salinity Stress Tolerance in Rice: Challenges and Opportunities. Agronomy 6. doi: 10.3390/agronomy6040054

21. Nguyen BD, Brar DS, Bui BC, Nguyen TV, Pham LN, Nguyen HT (2003) Identification and mapping of the QTL for aluminum tolerance introgressed from the new source, Oryza rufipogon Griff., into indica rice (Oryza sativa L.). Theor Appl Genet 106: 583–593. doi: 10.1007/s00122-002-1072-4 12595985

22. Ricachenevsky FK, Sperotto RA (2016) Into the wild: Oryza species as sources for enhanced nutrient accumulation and metal tolerance in rice. Front Plant Sci 7. doi: 10.3389/fpls.2016.00974 27446193

23. Becker M, Asch F (2005) Iron toxicity in rice—conditions and management concepts. J Plant Nutr Soil Sci 168: 558–573. doi: 10.1002/jpln.200520504

24. Sahrawat KL (2005) Iron Toxicity in Wetland Rice and the Role of Other Nutrients. J Plant Nutr 27: 1471–1504. doi: 10.1081/pln-200025869

25. Wu L-B, Ueda Y, Lai S-K, Frei M (2017) Shoot tolerance mechanisms to iron toxicity in rice (Oryza sativa L.). Plant Cell Environ 40: 570–584. doi: 10.1111/pce.12733 26991510

26. Wu L-B, Shhadi M, Gregorio G, Matthus E, Becker M, Frei M (2014) Genetic and physiological analysis of tolerance to acute iron toxicity in rice. Rice 7: 8. doi: 10.1186/s12284-014-0008-3 24920973

27. Audebert A, Fofana M (2009) Rice yield gap due to iron toxicity in West Africa. Journal of Agronomy and Crop Sci 195: 66–76. doi: 10.1111/j.1439-037X.2008.00339.x

28. Frei M, Tetteh RN, Razafindrazaka AL, Fuh MA, Wu L-B, Becker M (2016) Responses of rice to chronic and acute iron toxicity: genotypic differences and biofortification aspects. Plant Soil 408: 149–161. doi: 10.1007/s11104-016-2918-x

29. Dufey I, Hiel MP, Hakizimana P, Draye X, Lutts S, Kone B, et al. (2012) Multi-environment quantitative trait loci mapping and consistency across environments of resistance mechanisms to ferrous iron toxicity in rice. Crop Sci 52: 539–550. doi: 10.2135/cropsci2009.09.0544

30. Dufey I, Mathieu A-S, Draye X, Lutts S, Bertin P (2014) Construction of an integrated map through comparative studies allows the identification of candidate regions for resistance to ferrous iron toxicity in rice. Euphytica: 1–11. doi: 10.1007/s10681-014-1255-5

31. Arbelaez JD, Moreno LT, Singh N, Tung CW, Maron LG, Ospina Y, et al. (2015) Development and GBS-genotyping of introgression lines (ILs) using two wild species of rice, O. meridionalis and O. rufipogon, in a common recurrent parent, O. sativa cv. Curinga. Mol Breed 35: 81. doi: 10.1007/s11032-015-0276-7 25705117

32. Matthus E, Wu L-B, Ueda Y, Hoeller S, Becker M, Frei M (2015) Loci, genes, and mechanisms associated with tolerance to ferrous iron toxicity in rice (Oryza sativa L.). Theor Appl Genet 128: 2085–2098. doi: 10.1007/s00122-015-2569-y 26152574

33. Sikirou M, Saito K, Dramé KN, Saidou A, Dieng I, Ahanchédé A, et al. (2016) Soil-based screening for iron toxicity tolerance in rice using pots. Plant Prod Sci 19: 489–496. doi: 10.1080/1343943X.2016.1186496

34. Vaintraub IA, Lapteva NA (1988) Colorimetric determination of phytate in unpurified extracts of seeds and the products of their processing. Anal Biochem 175: 227–230. doi: 10.1016/0003-2697(88)90382-x 3245569

35. Dobermann A, Fairhurst. T. (2000) Rice—Nutrient Disorders and Nutrient Management. Potash & Phosphate Institute (PPI), Potash and Phosphate Institute of Canada (PPIC) and International Rice Research Institute (IRRI).

36. Quinet M, Vromman D, Clippe A, Bertin P, Lequeux H, Dufey I, et al. (2012) Combined transcriptomic and physiological approaches reveal strong differences between short- and long-term response of rice (Oryza sativa) to iron toxicity. Plant Cell Environ 35: 1837–1859. doi: 10.1111/j.1365-3040.2012.02521.x 22506799

37. Poschenrieder C, Cabot C, Martos S, Gallego B, Barceló J (2013) Do toxic ions induce hormesis in plants? Plant Sci 212: 15–25. https://doi.org/10.1016/j.plantsci.2013.07.012 24094050

38. Becana M, Moran JF, Iturbe-Ormaetxe I (1998) Iron-dependent oxygen free radical generation in plants subjected to environmental stress: toxicity and antioxidant protection. Plant Soil 201: 137–147. doi: 10.1023/a:1004375732137

39. Apel K, Hirt H (2004) Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55: 373–399. doi: 10.1146/annurev.arplant.55.031903.141701 15377225

40. Li B, Sun L, Huang J, Göschl C, Shi W, Chory J, et al. (2019) GSNOR provides plant tolerance to iron toxicity via preventing iron-dependent nitrosative and oxidative cytotocicity. Nat Comm 10, 3896.

41. Vaughan DA (1994) The Wild relatives of Rice—A Genetic Resources Handbook. IRRI, Manila, Philippines.

42. Cogle AL, Keating MA, Langford PA, Gunton J, Webb IS (2011) Runoff, soil loss, and nutrient transport from cropping systems on Red Ferrosols in tropical northern Australia. Soil Res 49: 87–97. doi: 10.1071/sr10069

43. Engel K, Asch F, Becker M (2012) Classification of rice genotypes based on their mechanisms of adaptation to iron toxicity. J Plant Nutr Soil Sci 175: 871–881. doi: 10.1002/jpln.201100421

44. Camaschella C (2015) Iron-deficiency anemia. N Engl J Med 372: 1832–1843. doi: 10.1056/NEJMra1401038 25946282

45. Sandstead HH (2013) Human Zinc Deficiency: Discovery to Initial Translation. Adv Nutr 4: 76–81. doi: 10.3945/an.112.003186 23319126

46. Trijatmiko KR, Dueñas C, Tsakirpaloglou N, Torrizo L, Arines FM, Adeva C, et al. (2016) Biofortified indica rice attains iron and zinc nutrition dietary targets in the field. Sci Rep 6: 19792. doi: 10.1038/srep19792 26806528

47. Raboy V (2002) Progress in breeding low phytate crops. J Nutr 132: 503S–505S. doi: 10.1093/jn/132.3.503S 11880580

48. Olsen LI, Hansen TH, Larue C, Osterberg JT, Hoffmann RD, Liesche J, et al. (2016) Mother-plant-mediated pumping of zinc into the developing seed. Nat Plants 2: 16036. doi: 10.1038/nplants.2016.36 27243644

49. Wang Y, Frei M (2011) Stressed food—The impact of abiotic environmental stresses on crop quality. Agr Ecosyst Environ 141: 271–286. doi: 10.1016/j.agee.2011.03.017

50. Gibson RS, Bailey KB, Gibbs M, Ferguson EL (2010) A review of phytate, iron, zinc, and calcium concentrations in plant-based complementary foods used in low-income countries and implications for bioavailability. Food Nutr Bull 31: S134–146. doi: 10.1177/15648265100312S206 20715598

Článok vyšiel v časopise


2020 Číslo 1

Najčítanejšie v tomto čísle

Tejto téme sa ďalej venujú…

Zabudnuté heslo

Nemáte účet?  Registrujte sa

Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.


Nemáte účet?  Registrujte sa