Abstract
To understand the mechanisms of cadmium (Cd) tolerance during seed germination in rice, quantitative trait loci (QTLs) and epistasis were analyzed using 124 rice backcross recombinant inbred lines (BRILs) derived from a cross between indica CH891 and japonica 02428, and six additive QTLs along with 16 pairs of epistatic QTLs involving 17 loci were identified for germination rate (GR) under Cd and control conditions. The expression of these QTLs and their epistasis under Cd stress and control conditions were not the same, and more pairs of epistatic QTLs were detected under Cd stress than under control conditions, suggesting that Cd stress could induce a different gene expression network and that Cd tolerance with respect to GR is controlled by additive effects and gene interactions. To our knowledge, this is the first study of rice seed germination ability under Cd stress in a typical indica/japonica cross. Notably, all the major additive QTLs for GR were mapped to a small chromosomal region (60–980 kb). These QTLs could be highly valuable genetic factors for cadmium tolerance improvement in rice lines. Moreover, the BRILs developed in this study will serve as an appropriate choice for mapping and studying the genetic basis of complex traits in rice.
Similar content being viewed by others
References
Abe T, Nonoue Y, Ono N, Omoteno M, Kuramata M, Fukuoka S, Yamamoto T, Yano M, Ishikawa S (2013) Detection of QTLs to reduce cadmium content in rice grains using LAC23/Koshihikari chromosome segment substitution lines. Breed Sci 63(3):284–291
Ali U, Zhong M, Shar T, Fiaz S, Xie L, Jiao G, Ahmad S, Sheng Z, Tang S, Wei X, Hu P (2019) The Infuence of pH on cadmium accumulation in seedlings of Rice (Oryza sativa L.). J Plant Growth Regul. https://doi.org/10.1007/s00344-019-10034-x
Arao T, Ishikawa S, Murakami M, Abe K, Maejima Y, Makino T (2010) Heavy metal contamination of agricultural soil and countermeasures in Japan. Paddy Water Environ 8:247–257
Bian J, Zhu G, Zhu C, Peng X, Li C, He X, Chen X, Fu J, Hu L, Ouyang L, Shen X, He H, Song Y (2015) Molecular dissection of developmental behavior of tiller number and the relationship with effective panicle using indica-japonica introgression lines in rice. Mol Breeding 35:91
Cao F, Cai Y, Liu L, Zhang M, He X, Zhang G, Wu F (2015) Differences in photosynthesis, yield and grain cadmium accumulation as affected by exogenous cadmium and glutathione in the two rice genotypes. Plant Growth Regul 75(3):715–723
Clemens S, Ma J (2016) Toxic heavy metal and metalloid accumulation in crop plants and foods. Annu Rev Plant Biol 67:489–512
Huang J, Cai M, Long Q, Liu L, Lin Q, Jiang L, Chen S, Wan J (2014) OsLOX2, a rice type I lipoxygenase, confers opposite effects on seed germination and longevity. Transgenic Res 23(4):643–655
Hussain W, Campbell M, Jarquin D, Walia H, Morota G (2020) Variance heterogeneity genome-wide mapping for cadmium in bread wheat reveals novel genomic loci and epistatic interactions. The Plant Genome 13:e20011
Ishikawa S, Ae N, Yano M (2005) Chromosomal regions with quantitative trait loci controlling cadmium concentration in brown rice (Oryza sativa). New Phytol 168:345–350
Jha UC, Bohra A (2016) Genomics enabled breeding approaches for improving cadmium stress tolerance in plants. Euphytica 208:1–31
Jiang N, Shi S, Shi H, Khanzada H, Wassan GM, Zhu C, Peng X, Yu Q, Chen X, He X, Fu J, Hu L, Xu J, Ouyang L, Sun X, Zhou D, He H, Bian J (2017) Mapping QTL for seed germinating ability under low temperature using a new high-density genetic map of Rice. Front Plant Sci 8:1223
Kuriakose, Saritha V, Prasad MNV (2008) Cadmium stress affects seed germination and seedling growth in Sorghum bicolor (L.) Moench by changing the activities of hydrolyzing enzymes. Plant Growth Regul 54:143–156
Li H, Ye G, Wang J (2007) A modified algorithm for the improvement of composite interval mapping. Genetics 175:361–374
Li H, Ribaut J-M, Li Z, Wang J (2008) Inclusive composite interval mapping (ICIM) for digenic epistasis of quantitative traits in biparental populations. Theor Appl Genet 116:243–260
Li X, Ziadi N, Belanger G, Cai Z, Xu H (2011) Cadmium accumulation in wheat grain as affected by mineral N fertilizer and soil characteristics. Can J Soil Sci 91:521–531
Liu S, Yang C, Xie W, Xia C, Fan P (2012) The effects of cadmium on germination and seedling growth of Suaeda salsa. Procedia Environ Sci 16:293–298
McCouch SR, Committee on Gene Symbolization, Nomenclature, and Linkage [CGSNL] (2008) Rice genetics cooperative. Gene nomenclature system for rice. Rice 1:2–84
Meng L, Li H, Zhang L, Wang J (2015) QTL IciMapping: integrated software for genetic linkage map construction and quantitative trait locus mapping in bi-parental populations. Crop J 3:269–283
Moya JL, Ros R, Picazo I (1993) Influence of cadmium and nickel on growth, net photosynthesis and carbohydrate distribution in rice plants. Photosynth Res 36(2):75–80
Nakanishi H, Ogawa I, Ishimaru Y, Mori S, Nishizawa NK (2006) Iron deficiency enhances cadmium uptake and translocation mediated by the Fe2+ transporters OsIRT1 and OsIRT2 in rice. Soil Sci Plant Nutr 52(4):464–469
Ohta H, Shirano Y, Tanaka K, Morita Y, Shibata D (1992) cDNA cloning of rice lipoxygenase L-2 and characterization using an active enzyme expressed from the cDNA in Escherichia coli. Eur J Biochem 206(2):331–336
Saito T (2004) Cadmium input from rainfall into fields in the city of Tsukuba. NIAES Annual Report 2004. National Institute for Agro-Environmental Sciences, Tsukuba, pp. 54–55
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
Singh S, Eapen S, D’Souza SF (2006) Cadmium accumulation and its influence on lipid per oxidation and antioxidative system in an aquatic plant, Bacopa monnieri L. Chemosphere 62:233–246
Takahashi R, Ishimaru Y, Senoura T, Shimo H, Ishikawa S, Arao T, Nakanishi H, Nishizawa NK (2011) The OsNRAMP1 iron transporter is involved in Cd accumulation in rice. J Exp Bot 62(14):4843–4850
Tazib T, Ikka T, Kuroda K, Kobayashi Y, Kimura K, Koyama H (2009) Quantitative trait loci controlling resistance to cadmium rhizotoxicity in two recombinant inbred populations of Arabidopsis thaliana are partially shared by those for hydrogen peroxide resistance. Physiol Plant 136(4):395–406
Ueno D, Kono I, Yokosho K, Ando T, Yano M, Ma JF (2009) A major quantitative trait locus controlling cadmium translocation in rice (Oryza sativa). New Phytol 182(3):644–653
Ueno D, Yamaji N, Kono I, Huang CF, Ando T, Yano M, Ma JF (2010) Gene limiting cadmium accumulation in rice. Proc Natl Acad Sci U S A 107(38):16500–16505
Xue D, Chen M, Zhang G (2009) Mapping of QTLs associated with cadmium tolerance and accumulation during seedling stage in rice (Oryza sativa L.). Euphytica 165:587–596
Yan YF, Lestari P, Lee K-J, Kim MY, Lee S-H, Lee B-W (2013) Identification of quantitative trait loci for cadmium accumulation and distribution in rice (Oryza sativa). Genome 56(4):227–232
Yang X, Guo Y, Yan J, Zhang J, Song T, Rocheford T, Li JS (2010) Major and minor QTL and epistasis contribute to fatty acid compositions and oil concentration in high-oil maize. Theor Appl Genet 120:665–678
Zhang X, Fan X, Li C, Nan Z (2010) Effects of cadmium stress on seed germination, seedling growth and antioxidative enzymes in Achnatherum inebrians plants infected with a Neotyphodium endophyte. Plant Growth Regul 60:91–97
Zhang X, Chen H, Jiang H, Lu W, Pan J, Qian Q, Xue D (2015) Measuring the damage of heavy metal cadmium in rice seedlings by SRAP analysis combined with physiological and biochemical parameters. J Sci Food Agric 95(11):2292–2298
Zhou JQ, Jiang YR, Ming XQ, Wang JR, Tang WB, Sun L (2019) Introgressing the allelic variation of a major locus in reducing the grain cadmium accumulation in indica rice hybrids. Mol Breeding 39:84
Acknowledgements
We thank the anonymous referees for their critical comments on this manuscript. This research was supported by grants (20192ACBL20017; 20192BCB23010) from Project of Science and Technology Department of Jiangxi Province, grant (GJJ170241) from Project of Science and Technology Department of Department of Education of Jiangxi Province and grant (201910410003) from National Undergraduate Training Program for Innovation and Entrepreneurship.
Author information
Authors and Affiliations
Contributions
JB drafted the manuscript and annotated the data. HH designed the research work. CL, PW, GW, YW, QC, YC, DZ, CL, XZ, JT and CL performed the experiments. All the authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors have no conflicts of interest to disclose.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Li, C., Wang, P., Wu, G. et al. Additive and Epistatic QTL on Cadmium (Cd) Tolerance Associated with Seed Germinating Ability in Rice. J Plant Growth Regul 40, 2115–2123 (2021). https://doi.org/10.1007/s00344-020-10258-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-020-10258-2