Advertisement

Plant Growth Regulation

, Volume 85, Issue 2, pp 329–335 | Cite as

New QTLs identified for leaf correlative traits in rice seedlings under cadmium stress

  • Jiahui Wang
  • Yunxia Fang
  • Bin Tian
  • Xiaoqin Zhang
  • Dali Zeng
  • Longbiao Guo
  • Jiang Hu
  • Dawei Xue
Brief communication

Abstract

Cadmium (Cd) is a non-essential toxic metal that is primarily released into the environment from artificial sources in recent decades. To investigate the genetics of Cd toxicity tolerance at the seedling stage in rice, a QTL analysis was carried out under cadmium stress conditions with two toxicity-linked traits—leaf rolling (LR) and the green leaf ratio (GLR). Using 127 rice lines of doubled haploid (DH) population derived from a cross between a japonica JX17 and indica ZYQ8, two QTLs for LR (qLR-1 and qLR-9) and one QTL for GLR (qGLR-3) were detected. Among them, the phenotypic variation of qLR-1 and qGLR-3 were 19.27 and 16.09, values which are useful for marker-assistant selection in breeding elite rice cultivars that have the capacity to tolerate Cd. The results further demonstrate that visual measurements of both LR and GLR in seedlings are effective methods for screening tolerant rice germplasm in cadmium stress scenarios.

Keywords

Rice QTL Cadmium Leaf rolling Green leaf ration 

Notes

Acknowledgements

This work was supported by Hangzhou Scientific and Technological Program (20170432B03), the National Key Technology Research and Development Program (2015BAD01B02) and the National Natural Science Foundation of China (31661143006). This work was also supported in part by the National GMO New Variety Breeding Program of PRC (2016ZX08011-001), National Science Foundation of China (31671666).

References

  1. 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):284–291CrossRefPubMedPubMedCentralGoogle Scholar
  2. Agrawal GK, Rakwal R, Iwahashi H (2002) Isolation of novel rice (Oryza sativa L.) multiple stress responsive MAP kinase gene, OsMSRMK2, whose mRNA accumulates rapidly in response to environmental cues. Biochem Biophys Res Commun 294(5):1009–1016CrossRefPubMedGoogle Scholar
  3. Agrawal GK, Agrawal SK, Shibato J, Iwahashi H, Rakwal R (2003) Novel rice MAP kinases OsMSRMK3 and OsWJUMK1 involved in encountering diverse environmental stresses and developmental regulation. Biochem Biophys Res Commun 300(3):775–783CrossRefPubMedGoogle Scholar
  4. Anjum SA, Tanveer M, Hussain S, Bao M, Wang L, Khan I, Ullah E, Tung SA, Samad RA, Shahzad B (2015) Cadmium toxicity in maize (Zea mays L.): consequences on antioxidative systems, reactive oxygen species and cadmium accumulation. Environ Sci Pollut Res Int 22(21):17022–17030CrossRefPubMedGoogle Scholar
  5. 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):715–723CrossRefGoogle Scholar
  6. Das N, Bhattacharya S, Bhattacharyya S, Maiti MK (2017) Identification of alternatively spliced transcripts of rice phytochelatin synthase 2 gene OsPCS2, involved in mitigation of cadmium and arsenic stresses. Plant Mol Biol 94(1–2):167–183CrossRefPubMedGoogle Scholar
  7. Fang Y, Wu W, Zhang X, Jiang H, Lu W, Pan J, Hu J, Guo L, Zeng D, Xue D (2015) Identification of quantitative trait loci associated with tolerance to low potassium and related ions concentrations at seedling stage in rice (Oryza sativa L.). Plant Growth Regul 77:157–166CrossRefGoogle Scholar
  8. Guo LB, Qian Q, Zeng DL, Dong GJ, Teng S, Zhu LH (2004) Genetic dissection for leaf correlative traits of rice (Oryza sativa L.) under drought stress. Yi Chuan Xue Bao 31(3):275–280PubMedGoogle Scholar
  9. Gupta U, Gupta S (1998) Trace element toxicity relationships to crop production and livestock and human health: implications for management. Commun Soil Sci Plant Anal 29(11–14):1491–1522CrossRefGoogle Scholar
  10. He S, Yang X, He Z, Baligar VC (2017) Morphological and physiological responses of plants to cadmium toxicity: a review. Pedosphere 27:421–438CrossRefGoogle Scholar
  11. Hsiao TC, Turner NC (1984) Influence of osmotic adjustment on leaf rolling and tissue death in rice (Oryza sativa L.). Plant Physiol 75(2):338–341CrossRefPubMedPubMedCentralGoogle Scholar
  12. Hsu YT, Kao CH (2007) Toxicity in leaves of rice exposed to cadmium is due to hydrogen peroxide accumulation. Plant Soil 298(1–2):231–241CrossRefGoogle Scholar
  13. Huang DR, Fan YY, Hu BL, Xiao YQ, Chen DZ, Zhuang JY (2017) Assessment and genetic analysis of heavy metal content in rice grain using an Oryza sativa × O. rufipogon backcross inbred line population. J Sci Food Agric 7:17704Google Scholar
  14. Inoue H, Takahashi M, Kobayashi T, Suzuki M, Nakanishi H, Mori S, Nishizawa NK (2008) Identification and localisation of the rice nicotianamine aminotransferase gene OsNAAT1 expression suggests the site of phytosiderophore synthesis in rice. Plant Mol Biol 66(1–2):193–203CrossRefPubMedGoogle Scholar
  15. Ishikawa S, Abe T, Kuramata M, Yamaguchi M, Ando T, Yamamoto T, Yano M (2010) A major quantitative trait locus for increasing cadmium-specific concentration in rice grain is located on the short arm of chromosome 7. J Exp Bot 61(3):923–934CrossRefPubMedGoogle Scholar
  16. Ishikawa S, Ishimaru Y, Igura M, Kuramata M, Abe T, Senoura T, Hase Y, Arao T, Nishizawa NK, Nakanishi H (2012) Ion-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice. Proc Natl Acad Sci USA 109(47):19166–19171CrossRefPubMedPubMedCentralGoogle Scholar
  17. Ishimaru Y, Kakei Y, Shimo H, Bashir K, Sato Y, Sato Y, Uozumi N, Nakanishi H, Nishizawa NK (2011) A rice phenolic efflux transporter is essential for solubilizing precipitated apoplasmic iron in the plant stele. J Biol Chem 286(28):24649–24655CrossRefPubMedPubMedCentralGoogle Scholar
  18. Kashiwagi T, Shindoh K, Hirotsu N, Ishimaru K (2009) Evidence for separate translocation pathways in determining cadmium accumulation in grain and aerial plant parts in rice. BMC Plant Biol 9:8CrossRefPubMedPubMedCentralGoogle Scholar
  19. Koike S, Inoue H, Mizuno D, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2004) OsYSL2 is a rice metal-nicotianamine transporter that is regulated by iron and expressed in the phloem. Plant J 39(3):415–424CrossRefPubMedGoogle Scholar
  20. Kuramata M, Masuya S, Takahashi Y, Kitagawa E, Inoue C, Ishikawa S, Youssefian S, Kusano T (2009) Novel cysteine-rich peptides from Digitaria ciliaris and Oryza sativa enhance tolerance to cadmium by limiting its cellular accumulation. Plant Cell Physiol 50(1):106–117CrossRefPubMedGoogle Scholar
  21. Lang Y, Zhang Z, Gu X, Yang J, Zhu Q (2004) Physiological and ecological effects of crimpy leaf character in rice (Oryza sativa L.) II. Photosynthetic character, dry mass production and yield forming. Acta Agronomica Sin 30(9):883–887Google Scholar
  22. Larsson EH, Bornman JF, Asp H (1998) Influence of UV-B radiation and Cd2+ on chlorophyll fluorescence, growth and nutrient content in Brassica napus. J Exp Bot 49(323):1031–1039CrossRefGoogle Scholar
  23. Lee S, Kim YY, Lee Y, An G (2007) Rice P1B-type heavy-metal ATPase, OsHMA9, Is a metal efflux protein. Plant Physiol 145(3):831–842CrossRefPubMedPubMedCentralGoogle Scholar
  24. Lim SD, Hwang JG, Han AR, Park YC, Lee C, Ok YS, Jang CS (2014) Positive regulation of rice RING E3 ligase OsHIR1 in arsenic and cadmium uptakes. Plant Mol Biol 85(4–5):365–379CrossRefPubMedGoogle Scholar
  25. McCouch SR, Cho YG, Yano M, Paul E, Blinstrub M, Morishima H, Kinoshita T (1997) Report on QTL nomenclature. Rice Genet Newslett 14:11–13Google Scholar
  26. Mishra SS, Panda D (2017) Leaf traits and antioxidant defense for drought tolerance during early growth stage in some popular traditional rice landraces from Koraput, India. Rice Sci 24(4):207–217CrossRefGoogle Scholar
  27. Miyadate H, Adachi S, Hiraizumi A, Tezuka K, Nakazawa N, Kawamoto T, Katou K, Kodama I, Sakurai K, Takahashi H, Satoh NN, Watanabe A, Fujimura T, Akagi H (2011) OsHMA3, a P1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytol 189(1):190–199CrossRefPubMedGoogle Scholar
  28. 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):75–80CrossRefPubMedGoogle Scholar
  29. Mukhopadhyay A, Vij S, Tyagi AK (2004) Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco. Proc Natl Acad Sci USA 101(16):6309–6314CrossRefPubMedPubMedCentralGoogle Scholar
  30. 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):464–469CrossRefGoogle Scholar
  31. Norton GJ, Deacon CM, Xiong LZ, Huang SY, Meharg AA, Price AH (2010) Genetic mapping of the rice ionome in leaves and grain: identification of QTLs for 17 elements including arsenic, cadmium, iron and selenium. Plant Soil 329(1):139–153CrossRefGoogle Scholar
  32. Oda K, Otani M, Uraguchi S, Akihiro T, Fujiwara T (2011) Rice ABCG43 is Cd inducible and confers Cd tolerance on yeast. Biosci Biotechnol Biochem 75(6):1211–1213CrossRefPubMedGoogle Scholar
  33. Ouzounidou G, Moustakas M, Eleftheriou EP (1997) Physiological and ultrastructural effects of cadmium on wheat, (Triticum aestivum L.) leaves. Arch Environ Contam Toxicol 32(2):154–160CrossRefPubMedGoogle Scholar
  34. Qin P, Hu J, Chen W, Zhang G, Li J, Fan S, Bin T, Chen X, Wang Y, Li S, Ma B (2016) SmallOrgan 1 plays an essential role in cell proliferation, cell expansion and cadmium uptake in rice. PeerJ PrePrints.  https://doi.org/10.7287/peerj.preprints.2593v1 Google Scholar
  35. Ramegowda Y, Venkategowda R, Jagadish P, Govind G, Hanumanthareddy RR, Makarla U, Guligowda S (2013) Expression of a rice Zn transporter, OsZIP1, increases Zn concentration in tobacco and finger millet transgenic plants. Plant Biotechnol Rep 7(3):309–319CrossRefGoogle Scholar
  36. Sebastian A, Prasad MNV (2014) Cadmium minimization in rice. A review. Agron Sustain Dev 34(1):155–173CrossRefGoogle Scholar
  37. Shim D, Hwang JU, Lee J, Lee S, Choi Y, An G, Martinoia E, Lee Y (2009) Orthologs of the class A4 heat shock transcription factor HsfA4a confer cadmium tolerance in wheat and rice. Plant Cell 21(12):4031–4043CrossRefPubMedPubMedCentralGoogle Scholar
  38. Shimo H, Ishimaru Y, An G, Yamakawa T, Nakanishi H, Nishizawa NK (2011) Low cadmium (LCD), a novel gene related to cadmium tolerance and accumulation in rice. J Exp Bot 62(15):5727–5734CrossRefPubMedPubMedCentralGoogle Scholar
  39. Srividhya A, Vemireddy LR, Sridhar S, Jayaprada M, Ramanarao PV, Hariprasad AS, Reddy HK, Anuradha G, Siddiq E (2011) Molecular mapping of QTLs for yield and its components under two water supply conditions in rice (Oryza sativa L.). J Crop Sci Biotechnol 14(1):45–56CrossRefGoogle Scholar
  40. 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):4843–4850CrossRefPubMedPubMedCentralGoogle Scholar
  41. 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):1948–1957CrossRefPubMedGoogle Scholar
  42. Talukdar PR, Rathi S, Pathak K, Chetia SK, Sarma RN (2017) Population structure and marker-trait association in indigenous aromatic rice. Rice Sci 24(3):145–154CrossRefGoogle Scholar
  43. Tan M, Cheng D, Yang Y, Zhang G, Qin M, Chen Y, Jiang M (2017) Co-expression network analysis of the transcriptomes of rice roots exposed to various cadmium stresses reveals universal cadmium-responsive genes. BMC Plant Biol 17(1):194CrossRefPubMedPubMedCentralGoogle Scholar
  44. Turner NC (1997) Further progress in crop water relations. Adv Agron 58(8):293–338Google Scholar
  45. 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):644–653CrossRefPubMedGoogle Scholar
  46. Uraguchi S, Kamiya T, Sakamoto T, Kassai K, Sato Y, Nagamura Y, Yoshida A, Kyozuka J, Ishikawa S, Fujiwara T (2011) Low-affinity cation transporter (OsLCT1) regulates cadmium transport into rice grains. Proc Natl Acad Sci USA 108(52):20959–20964CrossRefPubMedPubMedCentralGoogle Scholar
  47. Vivitha P, Raveendran M, Vijayalakshmi D (2017) Introgression of QTLs controlling spikelet fertility maintains membrane integrity and grain yield in improved white Ponni derived progenies exposed to heat stress. Rice Sci 24(1):32–40CrossRefGoogle Scholar
  48. Wang F, Wang M, Liu Z, Shi Y, Han T, Ye Y, Gong N, Sun J, Zhu C (2015) Different responses of low grain-Cd-accumulating and high grain-Cd-accumulating rice cultivars to Cd stress. Plant Physiol Biochem 96:261–269CrossRefPubMedGoogle Scholar
  49. Wang C, Guo W, Shan Y, Wei P, David WO (2016) Reduction of Cd in rice through expression of OXS3-like gene fragments. Mol Plant 9(2):301–304CrossRefPubMedGoogle Scholar
  50. Xu Y, Shen L, McCouch S, Zhu L (1998) Extension of the rice DH population genetic map with microsatellite markers. Chin Sci Bull 42:149–152Google Scholar
  51. 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(3):587–596CrossRefGoogle Scholar
  52. Xue D, Jiang H, Deng X, Zhang X, Wang H, Xu X,. Hu J, Zeng D, Guo L, Qian Q (2014) Comparative proteomic analysis provides new insights into cadmium accumulation in rice grain under cadmium stress. J Hazard Mater 280:269–278CrossRefPubMedGoogle Scholar
  53. Yan YF, Lestari P, Lee KJ, Kim MY, Lee SH, Lee BW (2013) Identification of quantitative trait loci for cadmium accumulation and distribution in rice (Oryza sativa). Genome 56(4):227–232CrossRefPubMedGoogle Scholar
  54. Yang Y, Xiong J, Chen R, Fu G, Chen T, Tao L (2016) Excessive nitrate enhances cadmium (Cd) uptake by up-regulating the expression of OsIRT1, in rice (Oryza sativa). Environ Exp Bot 122:141–149CrossRefGoogle Scholar
  55. Yeh CM, Hsiao LJ, Huang HJ (2004) Cadmium activates a mitogen-activated protein kinase gene and MBP kinases in rice. Plant Cell Physiol 45(9):1306–1312CrossRefPubMedGoogle Scholar
  56. Yoshida S, Forna DA, Cock JH (1976) Laboratory manual for physiological studies of rice. International Rice Research Institute, Los Banos, pp 62–63Google Scholar
  57. Yu C, Sun C, Shen C, Wang S, Liu F, Liu Y, Chen Y, Li C, Qian Q, Aryal B, Geisler M, Jiang de A, Qi Y (2015) The auxin transporter, OsAUX1, is involved in primary root and root hair elongation and in Cd stress responses in rice (Oryza sativa L.). Plant J 83(5):818–830CrossRefPubMedGoogle Scholar
  58. Yuan L, Yang S, Liu B, Zhang M, Wu K (2012) Molecular characterization of a rice metal tolerance protein, OsMTP1. Plant Cell Rep 31(1):67–79CrossRefPubMedGoogle Scholar
  59. Yue B, Xue WY, Luo LJ, Xing YZ (2006) QTL analysis for flag leaf characteristics and their relationships with yield and yield traits in rice. Yi Chuan Xue Bao 33(9):824–832PubMedGoogle Scholar
  60. Zhang X, Zhang G, Guo L, Wang H, Zeng D, Dong G, Qian Q, Xue D (2011) Identification of quantitative trait loci for Cd and Zn concentrations of brown rice grown in Cd-polluted soils. Euphytica 180:173–179CrossRefGoogle Scholar
  61. 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):2292–2298CrossRefPubMedGoogle Scholar
  62. Zhao FJ, Ma Y, Zhu YG, Tang Z, McGrath SP (2015) Soil contamination in China: current status and mitigation strategies. Environ Sci Technol 49(2):750–759CrossRefPubMedGoogle Scholar
  63. Zhao Y, Zhang SJ, Wen N, Zhang C, Wang J, Liu Z (2017) Modeling uptake of cadmium from solution outside of root to cell wall of shoot in rice seedling. Plant Growth Regul 82(1):11–20CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.College of Life and Environmental SciencesHangzhou Normal UniversityHangzhouChina
  2. 2.State Key Laboratory of Rice BiologyChina National Rice Research InstituteHangzhouChina

Personalised recommendations