Abstract
Lowland rice is often subject to iron toxicity which may lead to yield reduction. In order to cope with this nutrient disorder, plants have developed resistance strategies. The aim of this research was to assess morphological and physiological parameters linked to iron toxicity resistance mechanisms and to identify quantitative trait loci (QTLs) involved in their genetic determinism. A segregating population consisting of 164 recombinant inbred lines (RILs) derived from a cross between Azucena and IR64 was tested twice in hydroponics at the vegetative stage at 0 and 250 mg Fe2+ l−1. Morphological traits were measured on all 164 RILs. Physiological traits, which were too time-consuming to allow their measurement on all the population, were measured on the two parents and extreme individuals only, selected on the basis of their leaf bronzing index and shoot dry weight. A total of 24 putative QTLs was identified on chromosomes 1, 2, 3, 4, 7 and 11 for leaf bronzing index, shoot water content, shoot and root dry weight, relative variation of shoot and root dry weight, shoot iron concentration, stomatal resistance and chlorophyll content index. Several QTLs were detected in overlapping regions for different parameters. The pertinence of phenotyping extreme RILs only for a QTL analysis is discussed in this study. The QTL analysis allowed to better understand the physiological response of rice in the presence of an excess of ferrous iron, inclusive the relations existing between the stomata closure, the shoot water content reduction and the oxidative stress linked to these growth conditions.
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References
Abdoul KC (2006) Testing and developing tolerant rice varieties to iron toxicity in lower guinea (CRA kilissi and koba). In: Audebert A, Narteh LT, Kiepe P, Millar D, Beks B (eds) Iron toxicity in rice-based system in West Africa. Africa Rice Center (WARDA), Cotonou, Bénin, pp 64–74
Ahmadi N, Dubreuil-Tranchant C, Courtois B, Foncéka D, This D, Mc Couch SR, et al. (2005) New resources and integrated maps for IR64 × Azucena, a reference population in rice. In: IRRI 5th International Rice Genetics Symposium and 3rd International Rice Functional Genomics Symposium, Manila, Philip, 19–23 November 2005. sl:sn, 1p. International Rice Genetics Symposium. 5, 2005-11-19/2005-11-23, Manille
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 168:764–773. doi:10.1002/jpln.200520540
Audebert A (2006a) Diagnostic of risk and approaches to iron toxicity management in lowland rice farming. In: Audebert A, Narteh LT, Kiepe P, Millar D, Beks B (eds) Iron toxicity in rice-based system in West Africa. Africa Rice Center (WARDA), Cotonou, Bénin, pp 6–17
Audebert A (2006b) Iron toxicity in rice—environmental conditions and symptoms. In: Audebert A, Narteh LT, Kiepe P, Millar D, Beks B (eds) Iron toxicity in rice-based system in West Africa. Africa Rice Center (WARDA), Cotonou, Bénin, pp 18–33
Audebert A (2006c) Iron partitioning as a mechanism for iron toxicity tolerance in lowland rice. In: Audebert A, Narteh LT, Kiepe P, Millar D, Beks B (eds) Iron toxicity in rice-based system in West Africa. Africa Rice Center (WARDA), Cotonou, Bénin, pp 34–45
Audebert A, Sahrawat KL (2000) Mechanisms for iron toxicity tolerance in lowland rice. J Plant Nutr 23:1877–1885
Awal MA, Ikeda T (2002) Recovery strategy following the imposition of episodic soil moisture deficit in stands of peanut (Arachis hypogaea L.). J Agron Crop Sci 188:185–192. doi:10.1046/j.1439-037X.2002.00558.x
Baruah KK, Nath B (1996) Changes in growth, iron uptake and metabolism of rice (Oryza sativa L.) seedlings at excess iron in growth medium. Indian J Plant Physiol 1:114–118
Basten CJ, Weir BS, Zeng Z-B (1994) Zmap-a QTL cartographer In: Smith C, Gavora JS, Benkel B, Chesnais J, Fairfull W, Gibson JP, Kennedy BW, Burnside EB (eds) Proceedings of the 5th World congress on genetics applied to livestock production: computing strategies and software, 22:65–66. Published by the Organizing Committee, 5th world congress on genetics applied to livestock production, Guelph, Ontario
Basten CJ, Weir BS, Zeng Z-B (2004) QTL Cartographer, Version 1.17. Department of Statistics, North Carolina State University, Raleigh
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
Becker M, Asch F (2005) Iron toxicity in rice—conditions and management concepts. J Plant Nutr Soil Sci 168(4):558–573. doi:10.1002/jpln.200520504
Bode K, Döring O, Lüthje S, Neue H-U, Böttger M (1995) The role of active oxygen in iron tolerance of rice (Oryza sativa L.). Protoplasm 184:249–255. doi:10.1007/BF01276928
Briat J-F (1996) Roles of ferritin in plants. J Plant Nutr 19:1331–1342
Briat J-F, Vert G (2004) Acquisition et gestion du fer par les plantes. Cah Agric 13:183–201
Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971
Colmant G, Bertin P (2004) Ferrous iron toxicity in rice: impact of dissolved oxygen in nutrient solution. Belg J Bot 137(1):105–120
Darvasi A, Soller M (1992) Selective genotyping for determination of linkage between a marker locus and a quantitative trait locus. Theor Appl Genet 85:353–359. doi:10.1007/BF00222881
de Dorlodot S, 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. doi:10.1081/PLN-200042144
Dingkuhn M, Audebert A, Jones MP, Etienne K, Sow A (1999) Control of stomatal conductance and leaf rolling in O. sativa and O. glaberrima upland rice. Field Crops Res 61:223–236. doi:10.1016/S0378-4290(98)00165-8
Doerge RW, Zeng Z-B, Weir BS (1997) Statistical issues in the search for genes affecting quantitative traits in experimental populations. Stat Sci 12(3):195–219. doi:10.1214/ss/1030037909
Doran G, Eberbach P, Helliwell S (2006) The impact of rice plant roots on the reducing conditions in flooded rice soil. Chemosphere 63:1892–1902. doi:10.1016/j.chemosphere.2005.10.027
Fang W-C, Wang J-W, Lin CC, Kao CH (2001) Iron induction of lipid peroxidation and effects on antioxidative enzyme activities in rice leaves. Plant Growth Regul 35:75–80. doi:10.1023/A:1013879019368
Genon JG, de Hepcee N, Dufey JE, Delvaux B, Hennebert PA (1994) Iron toxicity and other chemical soil constraints to rice in highland swamps of Burundi. Plant Soil 166:109–115. doi:10.1007/BF02185487
Goicoechea N, Aguirreolea J, Cenoz S, Garcia-Mina JM (2001) Gas exchange and flowering in Verticillium-wilted pepper plants. J Phytopathol 149:281–286. doi:10.1046/j.1439-0434.2001.00622.x
Gridley HE, Efisue A, Tolou B, Bakayako T (2006) Breeding for tolerance to iron toxicity at WARDA. In: Audebert A, Narteh LT, Kiepe P, Millar D, Beks B (eds) Iron toxicity in rice-based system in West Africa. Africa Rice Center (WARDA), Cotonou, Bénin, pp 96–111
Gross J, Stein RJ, Fett-Neto AG, Fett JP (2003) Iron homeostasis related genes in rice. Genet Mol Biol 26(4):477–497. doi:10.1590/S1415-47572003000400012
Hernández JA, Rubio M, Olmos E, Ros-Barceló A, Martinez-Gómez P (2004) Oxidative stress induced by long-term plum pox virus infection in peach (Prunus persica). Physiol Plant 122:486–495. doi:10.1111/j.1399-3054.2004.00431.x
Hu ML, Wang CM, Yang QH, Zhai HQ, Lu W, Zhang RX et al (2005) QTL analysis for traits associated with photosynthetic functions in rice (Oryza sativa L.). Yi Chuan Xue Bao 32(8):818–824
INGER (International Network for Genetic Evaluation of Rice) (1996) Standard evaluation system for rice, 4th edn. International Rice Research Institute, Manila 52
IRRI (International Rice Research Institute) (1965) Annual Report 1964, Los Banos p 335
Ishimaru K (2003) Identification of a locus increasing rice yield and physiological analysis of its function. Plant Physiol 133:1081–1088. doi:10.1104/pp.103.027607
Jansen RC, Van Ooijen JW, Stam P, Lister C, Dean C (1995) Genotype-by-environment interaction in genetic mapping of multiple quantitative trait loci. Theor Appl Genet 91:33–37. doi:10.1007/BF00220855
Jiang C, Zeng Z-B (1995) Multiple trait analysis of genetic mapping for quantitative trait loci. Genetics 140:1111–1127
Jusu MS, Mansaray MS, Fomba SN, Jalloh AB (2006) Combating iron toxicity in rice in inland valley swamps of Sierra Leone through varietal improvement. In: Audebert A, Narteh LT, Kiepe P, Millar D, Beks B (eds) Iron toxicity in rice-based system in West Africa. Africa Rice Center (WARDA), Cotonou, Bénin, pp 112–124
Lander ES, Botstein D (1989) Mapping mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199
Lander E, Kruglyak L (1995) Genetic dissection of complex traits: guidelines for interpreting and reporting linkage results. Nat Genet 11:241–247. doi:10.1038/ng1195-241
Lobréaux S, Hardy T, Briat J-F (1993) Abscisic acid is involved in the iron-induced synthesis of maize ferritin. EMBO J 12(2):651–657
Mackill DJ, Nguyen HT, Zhang J (1999) Use of molecular markers in plant improvement programs for rainfed lowland rice. Field Crops Res 64:177–185. doi:10.1016/S0378-4290(99)00058-1
Majerus V, Bertin P, Swenden A, Fortemps A, Lobréaux S, Lutts S (2007a) Organ-dependent responses of the African rice to short-term iron toxicity: ferritin regulation and antioxidative responses. Biol Plant 51(2):303–312. doi:10.1007/s10535-007-0060-6
Majerus V, Bertin P, Swenden A, Fortemps A, Lobréaux S, Lutts S (2007b) Effects of iron toxicity on osmotic potential, osmolytes and polyamines concentrations in the African rice (Oryza glaberrima Steud.). Plant Sci 173:96–105. doi:10.1016/j.plantsci.2007.04.003
Masahiro Y, Sasaki T (1997) Genetic and molecular dissection of quantitative traits in rice. Plant Mol Biol 35:145–153. doi:10.1023/A:1005764209331
Montás Ramírez L, Claassen N, Amílcar Ubiera A, Werner H, Moawad AM (2002) Effect of phosphorus, potassium and zinc fertilizers on iron toxicity in wetland rice (Oryza sativa L.). Plant Soil 239:197–206. doi:10.1023/A:1015099422778
Müller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566. doi:10.1104/pp.125.4.1558
Neue HU, Quijano C, Senadhira D, Setter T (1998) Strategies for dealing with micronutrient disorders and salinity in lowland rice systems. Field Crops Res 56:139–155. doi:10.1016/S0378-4290(97)00125-1
Nipah JO, Safo-Kantanka O, Jones MP, Singh BN (1999) Genetics of tolerance for iron toxicity in rice. Int Rice Res Notes 24:11
Nyamangyoku O, Lutts S, Bertin P (2006). Mechanisms of resistance to ferrous iron toxicity at the vegetative stage in cultivated rices: Oryza sativa L., Oryza glaberrima Steud., and interspecific hybrids. In: Nyamangyoku O. Ferrous iron toxicity: mechanisms of resistance and impact on nutrient elements at the vegetative stage in cultivated rices (Oryza sativa L., Oryza glaberrima Steud., and interspecific hybrids), PhD Thesis, Université Catholique de Louvain, p 164
Ota Y (1969) Studies on the occurrence of the physiological disease called ‘bronzing’. Bull Natl Inst Agric Sci (Japan) D 18:31–104
Pathirana R, Wijithawarna WA, Jagoda K, Ranawaka AL (2002) Selection of rice for iron toxicity tolerance through irradiated caryopsis culture. J Plant Cell Tissue Organ Cult 70:83–90. doi:10.1023/A:1016025728740
Peng XX, Yamauchi M (1993) Ethylene production in rice bronzing leaves induces by ferrous iron. Plant Soil 149:227–234. doi:10.1007/BF00016613
Ponnamperuma FN, Bradfield R, Peech M (1955) Physiological disease of rice attributable to iron toxicity. Nature 175:265. doi:10.1038/175265a0
Sahrawat KL (2004) Iron toxicity in wetland rice and the role of other nutrients. J Plant Nutr 27(8):1471–1504. doi:10.1081/PLN-200025869
Sahrawat KL, Sika M (2002) Comparative tolerance of Oryza sativa and Oryza glaberrima rice cultivars for iron toxicity in West Africa. Int Rice Res Notes 27(2):30–31
Sahu SK, Sandha B, Dev G (2001) Relationship between applied potassium and iron toxicity in rice. Int Rice Res Notes 26(2):52–53
Sairam RK, Saxena DC (2000) Oxidative stress and antioxidants in wheat genotypes: possible mechanism of water stress tolerance. J Agron Crop Sci 184:55–61. doi:10.1046/j.1439-037x.2000.00358.x
Shimizu A, Yanagihara S, Kawasaki S, Ikehashi H (2004) Phosphorus deficiency-induced root elongation and its QTL in rice (Oryza sativa L.). Theor Appl Genet 109:1361–1368. doi:10.1007/s00122-004-1751-4
Taylor GJ, Crowder AA (1983) Use of the DCB technique for extraction of hydrous iron oxides from roots of wetland plants. Am J Bot 70(8):1254–1257. doi:10.2307/2443295
Teng S, Qian Q, Zeng D, Kunihiro Y, Fujimoto K, Huang D et al (2004) QTL analysis of leaf photosynthetic rate and related physiological traits in rice (Oryza sativa L.). Euphytica 135:1–7. doi:10.1023/B:EUPH.0000009487.89270.e9
Thongbai P, Goodman BA (2000) Free radical generation and post-anoxic injury in rice grown in an iron-toxic soil. J Plant Nutr 23(11&12):1887–1900
WARDA (West Africa Rice Development Association) (2002) Painting the rice red: iron toxicity in the lowlands, Annual report 2001–2002, pp 29–37
Wan JL, Zhai HQ, Wan JM, Ikehashi H (2003a) Detection and analysis of QTLs for ferrous iron toxicity tolerance in rice, Oryza sativa L. Euphytica 131:201–206. doi:10.1023/A:1023915710103
Wan JL, Zhai HQ, Wan JM, Yasui H, Yoshimura A (2003b) Mapping QTL for traits associated with resistance to ferrous iron toxicity in rice (Oryza sativa L.), using japonica chromosome segment substitution lines. Yi Chuan Xue Bao 30(10):893–898
Wan JL, Zhai HQ, Wan JM, Yasui H, Yoshimura A (2004) Detection and analysis of QTLs associated with resistance to ferrous iron toxicity in rice (Oryza sativa L.), using recombinant inbred lines. Acta agronomica sinica 30(4):329–333
Wan JL, Zhai HQ, Wan JM (2005) Mapping of QTLs for ferrous iron toxicity tolerance in rice (Oryza sativa L.). Yi Chuan Xue Bao 32(11):1156–1166
Wu P, Luo A, Zhu J, Yang J, Huang N, Senadhira D (1997) Molecular markers linked to genes underlying seedling tolerance for ferrous iron toxicity. Plant Soil 196(2):317–320. doi:10.1023/A:1004288427140
Wu P, Hu B, Liao CY, Zhu JM, Wu YR, Senadhira D et al (1998) Characterization of tissue tolerance to iron by molecular markers in different lines of rice. Plant Soil 203:217–226. doi:10.1023/A:1004321218387
Yamauchi M (1989) Rice bronzing in Nigeria caused by nutrient imbalances and its control by potassium sulfate application. Plant Soil 117:275–286. doi:10.1007/BF02220722
Yang QH, Lu W, Hu ML, Wang CM, Zhang RX, Yano M et al (2003) QTL and epistatic interaction underlying leaf chlorophyll and H2O2 content variation in rice (Oryza sativa L.). Yi Chuan Xue Bao 30(3):245–250
Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Laboratory manual for physiological studies of rice, 3rd edn. Int Rice Res Inst, Manila
Zeng Z-B (1994) Precision mapping of quantitative trait loci. Genetics 136:1457–1468
Acknowledgments
We thanks the Research Institute for Development (IRD) and the International Cooperation Center in Agronomical Research for Development (CIRAD) in Montpellier (France) for their collaboration in this study by providing the segregating population and the genotypic map of the markers for the recombinant inbred lines (RILs)—European project EGRAM. We are also thankful to the Fonds National de la Recherche Scientifique (FNRS, Belgium, FRFC 2.4556.00) and the Fonds Scientifique de Recherche (FSR, UCL, Belgium) for their financial contribution.
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Dufey, I., Hakizimana, P., Draye, X. et al. QTL mapping for biomass and physiological parameters linked to resistance mechanisms to ferrous iron toxicity in rice. Euphytica 167, 143–160 (2009). https://doi.org/10.1007/s10681-008-9870-7
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DOI: https://doi.org/10.1007/s10681-008-9870-7