Abstract
Waterlogging stress disturbs plant metabolism through increased ion (manganese and iron) toxicity resulting from the changes in the soil redox potential under hypoxic conditions. Our previous study found a significant correlation between the tolerance to Mn2+ toxicity and waterlogging stress tolerance in barley, suggesting that waterlogging tolerance could be increased by improving the tolerance to Mn2+ toxicity. In this study, a doubled-haploid (DH) population from the cross between barley varieties Yerong and Franklin (waterlogging-tolerant and -sensitive, respectively) was used to identify QTL controlling tolerance to Mn2+ toxicity based on chlorophyll content and plant survival as selection criteria. Four significant QTL for plant survival under Mn2+ stress (QSur.yf.1H, QSur.yf.3H, QSur.yf.4H, and QSur.yf.6H) were identified in this population at the seedling stage. Two significant QTL (QLC.yf.3H and QLC.yf.6H) controlling leaf chlorosis under Mn2+ stress were identified on chromosomes 3H and 6H close to QSur.yf.3H and QSur.yf.6H. The major QTL QSur.yf.3H, located near the marker Bmag0013, explained 21% of the phenotypic variation. The major QTL for plant survival on 3H was validated in a different DH population (TX9425/Naso Nijo). This major QTL could potentially be used in breeding programmes to enhance tolerance to both manganese toxicity and waterlogging.
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References
Ahmed F, Rafii MY, Ismail MR, Juraimi AS, Rahim HA, Asfaliza R, Latif MA (2012) Waterlogging tolerance of crops: breeding, mechanism of tolerance, molecular approaches, and future prospects. Biomed Res Int 2013:963525
Bailey-Serres J, Voesenek LACJ (2008) Flooding stress: acclimations and genetic diversity. Annu Rev Plant Biol 59(1):313–339. https://doi.org/10.1146/annurev.arplant.59.032607.092752
Cailliatte R, Schikora A, Briat J-F, Mari S, Curie C (2010) High-affinity manganese uptake by the metal transporter NRAMP1 is essential for Arabidopsis growth in low manganese conditions. Plant Cell 22(3):904–917. https://doi.org/10.1105/tpc.109.073023
Chen Z, Fujii Y, Yamaji N, Masuda S, Takemoto Y, Kamiya T, Yusuyin Y, Iwasaki K, Kato S-i, Maeshima M, Ma JF, Ueno D (2013) Mn tolerance in rice is mediated by MTP8.1, a member of the cation diffusion facilitator family. J Exp Bot 64(14):4375–4387. https://doi.org/10.1093/jxb/ert243
Demidchik V, Cuin T, Svistunenko D, Smith S, Miller A, Shabala S, Sokolik A, Yurin V (2010) Arabidopsis root K+-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. J Cell Sci 123(9):1468–1479. https://doi.org/10.1242/jcs.064352
Demidchik V, Maathuis F (2007) Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development. New Phytol 175(3):387–404. https://doi.org/10.1111/j.1469-8137.2007.02128.x
Demidchik V, Shabala S, Coutts K, Tester M, Davies J (2003) Free oxygen radicals regulate plasma membrane Ca2+- and K+- permeable channels in plant root cells. J Cell Sci 116(1):81–88. https://doi.org/10.1242/jcs.00201
Demirevska-Kepova K, Simova-Stoilova L, Stoyanova Z, Hölzer R, Feller U (2004) Biochemical changes in barley plants after excessive supply of copper and manganese. Environ Exp Bot 52(3):253–266. https://doi.org/10.1016/j.envexpbot.2004.02.004
Deng F, Yamaji N, Xia J, Ma J (2013) A member of the heavy metal P-type ATPase OsHMA5 is involved in xylem loading of copper in rice. Plant Physiol 163(3):1353–1362. https://doi.org/10.1104/pp.113.226225
Dreyer I, Uozumi N (2011) Potassium channels in plant cells. FEBS J 278(22):4293–4303. https://doi.org/10.1111/j.1742-4658.2011.08371.x
Hebbern CA, Pedas P, Schjoerring JK, Knudsen L, Husted S (2005) Genotypic differences in manganese efficiency: field experiments with winter barley (Hordeum vulgare L.) Plant Soil 272(1):233–244. https://doi.org/10.1007/s11104-004-5048-9
Huang X, Deng F, Yamaji N, Pinson SRM, Fuji-Kashino M, Danku J, Douglas A, Guerinot ML, Salt DE, Ma J (2016) A heavy metal P-type ATPase OsHMA4 prevents copper accumulation in rice grain. Nat Commun 7:12138. https://doi.org/10.1038/ncomms12138
Huang X, Shabala S, Shabala L, Rengel Z, Wu X, Zhang G, Zhou M (2015) Linking waterlogging tolerance with Mn2+ toxicity: a case study for barley. Plant Biol 17(1):26–33. https://doi.org/10.1111/plb.12188
Hwang H, Yoon J, Kim HY, Min MK, Kim J, Choi E, Lan W, Bae Y, Luan S, Cho H, Kim B (2013) Unique features of two potassium channels, OsKAT2 and OsKAT3, expressed in rice guard cells. PLoS One 8(8):e72541. https://doi.org/10.1371/journal.pone.0072541
Kearsey MJ, Farquhar AG (1998) QTL analysis in plants: where are we now? Heredity 80(2):137–142. https://doi.org/10.1046/j.1365-2540.1998.00500.x
Khabaz-Saberi H, Barker SJ, Rengel Z (2012) Tolerance to ion toxicities enhances wheat (Triticum aestivum L.) grain yield in waterlogged acidic soils. Plant Soil 354(1-2):371–381. https://doi.org/10.1007/s11104-011-1073-7
Khabaz-Saberi H, Rengel Z (2010) Aluminum, manganese, and iron tolerance improves performance of wheat genotypes in waterlogged acidic soils. J Plant Nutr Soil Sci 173(3):461–468. https://doi.org/10.1002/jpln.200900316
Khabaz-Saberi H, Setter T, Waters I (2006) Waterlogging induces high to toxic concentrations of iron, aluminum, and manganese in wheat varieties on acidic soil. J Plant Nutr 29(5):899–911. https://doi.org/10.1080/01904160600649161
Kirk G, Solivas J, Alberto M (2003) Effects of flooding and redox conditions on solute diffusion in soil. Eur J Soil Sci 54(3):617–624. https://doi.org/10.1046/j.1365-2389.2003.00532.x
Li H, Vaillancourt R, Mendham N, Zhou M (2008) Comparative mapping of quantitative trait loci associated with waterlogging tolerance in barley (Hordeum vulgare L.) BMC Genomics 9(1):401. https://doi.org/10.1186/1471-2164-9-401
Lidon FC, Teixeira MG (2000) Oxy radicals production and control in the chloroplast of Mn-treated rice. Plant Sci 152(1):7–15. https://doi.org/10.1016/S0168-9452(99)00179-X
Mascher M, Gundlach H, Himmelbach A, Beier S, Twardziok S, Wicker T, Radchuk V, Dockter C, Hedley P, Russell J, Bayer M, Ramsay L, Liu H, Haberer G, Zhang X, Zhang Q, Barrero R, Li L, Taudien S, Groth M, Felder M, Hastie A, Šimková H, Staňková H, Vrána J, Chan S, María Muñoz-Amatriaín, Ounit R, Wanamaker S, Bolser D, Colmsee C, Schmutzer T, Aliyeva-Schnorr L, Grasso S, Tanskanen J, Chailyan A, Sampath D, Heavens D, Clissold L, Cao S, Chapman B, Dai F, Han Y, Li H, Li X, Lin C, McCooke J, Tan C, Wang P, Wang S, Yin S, Zhou G, Poland J, Bellgard M, Borisjuk L, Houben A, Doležel J, Ayling S, Lonardi S, Kersey P, Langridge P, Muehlbauer G, Clark M, Caccamo M, Schulman A, Mayer K, Platzer M, Close T, Scholz U, Hansson M, Zhang G, Braumann I, Spannagl M, Li C, Waugh R, Stein N (2017) A chromosome conformation capture ordered sequence of the barley genome. Nature 544(7651):427–433
McDonald GK, Graham RD, Lloyd J, Lewis J, Lonergan P, Khabas-Saberi H (2001) Breeding for improved zinc and manganese efficiency in wheat and barley. In: Proceedings of the 10th Australian Agronomy Conference, Hobart, Tasmania, Australia
Pallotta MA, Graham RD, Langridge P, Sparrow DHB, Barker SJ (2000) RFLP mapping of manganese efficiency in barley. Theor Appl Genet 101(7):1100–1108. https://doi.org/10.1007/s001220051585
Pang J, Cuin T, Shabala L, Zhou M, Mendham N, Shabala S (2007) Effect of secondary metabolites associated with anaerobic soil conditions on ion fluxes and electrophysiology in barley roots. Plant Physiol 145(1):266–276. https://doi.org/10.1104/pp.107.102624
Pedas P, Ytting CK, Fuglsang AT, Jahn TP, Schjoerring JK, Husted S (2008) Manganese efficiency in barley: identification and characterization of the metal ion transporter HvIRT1. Plant Physiol 148(1):455–466. https://doi.org/10.1104/pp.108.118851
Pezeshki SR, DeLaune RD, Anderson PH (1999) Effect of flooding on elemental uptake and biomass allocation in seedlings of three bottomland tree species. J Plant Nutr 22(9):1481–1494. https://doi.org/10.1080/01904169909365729
Pittman JK (2005) Managing the manganese: molecular mechanisms of manganese transport and homeostasis. New Phytol 167(3):733–742. https://doi.org/10.1111/j.1469-8137.2005.01453.x
Qiu F, Zheng Y, Zhang Z, Xu S (2007) Mapping of QTL associated with waterlogging tolerance during the seedling stage in maize. Ann Bot-London 99(6):1067–1081. https://doi.org/10.1093/aob/mcm055
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(5):2155–2167. https://doi.org/10.1105/tpc.112.096925
Satoh-Nagasawa N, Mori M, Skurai K, Takahashi H, Watanabe A, Akagi H (2013) Functional relationship heavy metal P-type ATPases (OsHMA2 and OsHMA3) of rice (Oryza sativa) using RNAi. Plant Biotechnol 30(5):511–515. https://doi.org/10.5511/plantbiotechnology.13.0616a
Shabala S (2011) Physiological and cellular aspects of phytotoxicity tolerance in plants: the role of membrane transporters and implications for crop breeding for waterlogging tolerance. New Phytol 190(2):289–298. https://doi.org/10.1111/j.1469-8137.2010.03575.x
Shabala S, Shabala S, Cuin T, Pang J, Percey W, Chen Z, Conn S, Eing C, Wegner L (2010) Xylem ionic relations and salinity tolerance in barley. Plant J 61:839–853
Sharma T, Dreyer I, Riedelsberger J (2013) The role of K+ channels in uptake and redistribution of potassium in the model plant Arabidopsis thaliana. Front Plant Sci 4:224
Smethurst CF, Garnett T, Shabala S (2005) Nutritional and chlorophyll fluorescence responses of lucerne (Medicago sativa) to waterlogging and subsequent recovery. Plant Soil 270(1):31–45. https://doi.org/10.1007/s11104-004-1082-x
Takahashi R, Ishimaru Y, Shimo H, Ogo Y, Senoura T, Nishizawa NK, Nakanishi H (2012) The OsHMA2 transporter is involved in root-to-shoot translocation of Zn and Cd in rice. Plant Cell Environ 35(11):1948–1957. https://doi.org/10.1111/j.1365-3040.2012.02527.x
Teakle NL, Amtmann A, Real D, Colmer TD (2010) Lotus tenuis tolerates combined salinity and waterlogging: maintaining O2 transport to roots and expression of an NHX1-like gene contribute to regulation of Na+ transport. Physiol Plant 139(4):358–374. https://doi.org/10.1111/j.1399-3054.2010.01373.x
Van Ooijen JW (2006) JoinMap 4, software for the calculation of genetic linkage maps in experimental populations. Kyazma BV Wageningen, Netherlands
Van Ooijen JW (2009) MapQTL 6, software for the mapping of quantitative trait loci in experimental populations of diploid species. Kyazma BV Wageningen, Netherlands
Voorrips RE (2002) MAPCHART: software for the graphical presentation of linkage maps and QTLs. J Heredity 93(1):77–78. https://doi.org/10.1093/jhered/93.1.77
Wang J, Yang J, Jia Q, Zhu J, Shang Y, Hua W, Zhou M (2014) A new QTL for plant height in barley (Hordeum vulgare L.) showing no negative effects on grain yield. PLoS ONE 9(2):e90144. https://doi.org/10.1371/journal.pone.0090144
Xu R, Wang J, Li C, Johnson P, Lu C, Zhou M (2012) A single locus is responsible for salinity tolerance in a Chinese landrace barley (Hordeum vulgare L.) PLoS One 7(8):e43079. https://doi.org/10.1371/journal.pone.0043079
Zepeda-Jazo I, Velarde-Buendía AM, Enríquez-Figueroa R, Bose J, Shabala S, Muñiz-Murguía J, Pottosin I (2011) Polyamines interact with hydroxyl radicals in activating Ca2+ and K+ transport across the root epidermal plasma membranes. Plant Physiol 157(4):2167–2180. https://doi.org/10.1104/pp.111.179671
Zhang X, Tang B, Yu F, Li L, Wang M, Xue Y, Zhang Z, Yan J, Yue B, Zheng Y, Qiu F (2013) Identification of major QTL for waterlogging tolerance using genome-wide association and linkage mapping of maize seedlings. Plant Mol Biol Res 31(3):594–606
Zhou M (2010) Improvement of plant waterlogging tolerance. In: Mancuso S, Shabala S (eds) Waterlogging signalling and tolerance in plants. Springer, Heidelberg, pp 267–285. https://doi.org/10.1007/978-3-642-10305-6_13
Zhou M (2011) Accurate phenotyping reveals better QTL for waterlogging tolerance in barley. Plant Breed 130(2):203–208. https://doi.org/10.1111/j.1439-0523.2010.01792.x
Zhou M, Li H, Mendham N (2007) Combining ability of waterlogging tolerance in barley. Crop Sci 47:278–284. https://doi.org/10.2135/cropsci2006.02.0065
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This work was supported by the Australian Research Council Linkage grant to SS, MZ, and LS (project LP120200516) and the Grains Research and Development Corporation (GRDC) of Australia.
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Huang, X., Fan, Y., Shabala, L. et al. A major QTL controlling the tolerance to manganese toxicity in barley (Hordeum vulgare L.). Mol Breeding 38, 16 (2018). https://doi.org/10.1007/s11032-017-0767-9
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DOI: https://doi.org/10.1007/s11032-017-0767-9