Plant Growth Regulation

, Volume 85, Issue 1, pp 133–142 | Cite as

Rice gene, BBH/Lsi1, regulates the color of rice hull by reducing the absorption and deposition of silicon and accumulating excess flavonoid

  • Chengcong Yang
  • Dongdong Zeng
  • Ran Qin
  • Md. Alamin
  • Xiaoli Jin
  • Chunhai Shi
Original paper

Abstract

The color of grain hull is one of the remarkable traits which can be easily identified after heading, especially at the mature stage. In present study, a discoloration hull mutant named black–brown hull (bbh), was obtained from an indica cultivar Zhenong 34 by mutagenesis with ethyl methane sulfonate (EMS). The hull color of bbh mutant initially appeared black–brown on the 15th day and became completely black–brown on the 30th day after heading. The root of bbh was shorter than that of WT during the whole growth period. Furthermore, the total flavonoids content in the hulls and the silicon deposition in the leaves of bbh were both remarkably higher than WT. The results of map-based cloning indicated that the mutant trait of bbh was controlled by a single recessive nuclear gene, which was located on the long arm of chromosome 2 with a physical distance of 64.9 kb. The comparison of gDNA sequence between bbh and WT showed that there was a substitution from T to C (+ 2360) in the third exon of LOC_Os02g51110. BBH was an allelic gene of Lsi1, which encoded a water channel protein (aquaporin) involving in silicon uptake. The expression levels of the genes related to silicon absorption, transportation and distribution were detected to be up- or down-regulated at different stages in bbh root. Moreover, the transcripts of structural enzymatic genes involved in flavonoid biosynthesis in hulls also had apparent differences between WT and bbh mutant. Above all, the results revealed that BBH/Lsi1 was responsible to the black–brown hull by reducing the absorption and deposition of silicon and accumulating overmuch flavonoid.

Keywords

Rice (Oryza sativa L.) Black–brown hull Silicon Flavonoid Gene mapping 

Notes

Acknowledgements

This work was supported by the Science and Technology Office of Zhejiang Province (2012C12901-2, 2016C32085 and 2016C02050-6) and the National Key Research and Development of China (2017YFD0100300-5).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10725_2018_379_MOESM1_ESM.docx (16.3 mb)
Supplementary material 1 (DOCX 16727 KB)

References

  1. Azeem S, Li Z, Zheng HP, Lin WW, Arafat Y, Zhang ZX, Lin XM, Lin WX (2016) Quantitative proteomics study on Lsi1 in regulation of rice (Oryza sativa L.) cold resistance. Plant Growth Regul 78(3):307–323.  https://doi.org/10.1007/s10725-015-0094-2 CrossRefGoogle Scholar
  2. Dai WM, Zhang KQ, Duan BW, Sun CX, Zheng KL, Cai R, Zhuang JY (2005) Rapid determination of silicon content in rice (Oryza sativa). Chinese J Rice Sci 19(5):460–462Google Scholar
  3. Dallagnol LJ, Rodrigues FA, Mielli MVB, Ma JF (2014) Rice grain resistance to brown spot and yield are increased by silicon. Trop Plant Pathol 39(1):56–63.  https://doi.org/10.1590/S1982-56762014005000003 CrossRefGoogle Scholar
  4. Epstein E (1994) The anomaly of silicon in plant biology. P Natl Acad Sci USA 91(1):11–17.  https://doi.org/10.1073/pnas.91.1.11 CrossRefGoogle Scholar
  5. Epstein E (1999) Silicon. Annu Rev Plant Phys 50:641–664.  https://doi.org/10.1146/annurev.arplant.50.1.641 CrossRefGoogle Scholar
  6. Hong LL, Qian Q, Tang D, Wang KJ, Li M, Cheng ZK (2012) A mutation in the rice chalcone isomerase gene causes the golden hull and internode 1 phenotype. Planta 236(1):141–151.  https://doi.org/10.1007/s00425-012-1598-x CrossRefPubMedGoogle Scholar
  7. Isa M, Bai SQ, Yokoyama T, Ma JF, Ishibashi Y, Yuasa T, Iwaya-Inoue M (2010) Silicon enhances growth independent of silica deposition in a low-silica rice mutant, lsi1. Plant Soil 331(1–2):361–375.  https://doi.org/10.1007/s11104-009-0258-9 CrossRefGoogle Scholar
  8. Koes R, Verweij W, Quattrocchio F (2005) Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends Plant Sci 10(5):236–242.  https://doi.org/10.1016/j.tplants.2005.03.002 CrossRefPubMedGoogle Scholar
  9. Koshiba T, Murakami S, Hattori T, Mukai M, Takahashi A, Miyao A, Hirochika H, Suzuki S, Sakamoto M, Umezawa T (2013) CAD2 deficiency causes both brown midrib and gold hull and internode phenotypes in Oryza sativa L. cv. Nipponbare Plant Biotechnol-Nar 30(4):365–373.  https://doi.org/10.5511/plantbiotechnology.13.0527a CrossRefGoogle Scholar
  10. Landi S, Hausman JF, Guerriero G, Esposito S (2017) Poaceae vs. abiotic atress: focus on drought and salt stress, recent insights and perspectives. Front Plant Sci 8:1214  https://doi.org/10.3389/fpls.2017.01214 CrossRefPubMedCentralPubMedGoogle Scholar
  11. Li JY, Oulee TM, Raba R, Amundson RG, Last RL (1993) Arabidopsis flavonoid mutants are hypersensitive to UV-B Irradiation. Plant Cell 5(2):171–179.  https://doi.org/10.2307/3869583 CrossRefPubMedCentralPubMedGoogle Scholar
  12. Li F, Jin Z, Qu W, Zhao D, Ma F (2006) Cloning of a cDNA encoding the Saussurea medusa chalcone isomerase and its expression in transgenic tobacco. Plant Physiol Bioch 44(7–9):455–461.  https://doi.org/10.1016/j.plaphy.2006.08.006 CrossRefGoogle Scholar
  13. Li LJ, Zhou HP, Zhan XD, Chu ZL, Cheng SH, Cao LY (2008) Genetic mapping of a gold hull and internode gene in rice (Oryza sativa). Chinese J Rice Sci 22(4):432–434Google Scholar
  14. Li QY, Ye SH, Zhang YY, Ma XJ, Mei J, Jin QS, He ZH, Dong YJ, Zhang XM (2012) Molecular mapping of a gold hull and internode gene in Oryza sativa L. J Nucl Agric Sci 26(7):0983–0987Google Scholar
  15. Ma JF (2004) Role of silicon in enhancing the resistance of plants to biotic and abiotic stresses. Soil Sci Plant Nutr 50(1):11–18.  https://doi.org/10.1080/00380768.2004.10408447 CrossRefGoogle Scholar
  16. Ma JF, Yamaji N (2015) A cooperated system of silicon transport in plants. Trends Plant Sci 20(7):435–442.  https://doi.org/10.1016/j.tplants.2015.04.007 CrossRefPubMedGoogle Scholar
  17. Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S, Katsuhara M, Ishiguro M, Murata Y, Yano M (2006) A silicon transporter in rice. Nature 440(7084):688–691.  https://doi.org/10.1038/nature04590 CrossRefPubMedGoogle Scholar
  18. Ma JF, Tamai K, Yamaji N, Mitani N (2007) Genotypic difference in silicon uptake and expression of silicon transporter genes in rice. Plant Physiol 145(3):919–924.  https://doi.org/10.1104/pp.107.107599 CrossRefPubMedCentralPubMedGoogle Scholar
  19. Ma DY, Sun DX, Wang CY, Qin HX, Ding HN, Li YG, Guo TC (2016) Silicon application alleviates drought stress in wheat through transcriptional regulation of multiple antioxidant defense pathways. J Plant Growth Regul 35(1):1–10.  https://doi.org/10.1007/s00344-015-9500-2 CrossRefGoogle Scholar
  20. Mirecki RM, Teramura AH (1984) Effects of ultraviolet-B irradiance on soybean V. The aependence of plant-sensitivity on the photosynthetic photon flux-density during and after leaf expansion. Plant Physiol 74(3):475–480.  https://doi.org/10.1104/pp.74.3.475 CrossRefPubMedCentralPubMedGoogle Scholar
  21. Mol J, Grotewold E, Koes R (1998) How genes paint flowers and seeds. Trends Plant Sci 3(6):212–217.  https://doi.org/10.1016/S1360-1385(98)01242-4 CrossRefGoogle Scholar
  22. Morimoto M, Kumeda S, Komai K (2000) Insect antifeedant flavonoids from Gnaphalium affine D. Don. J Agric Food Chem 48(5):1888–1891.  https://doi.org/10.1021/jf990282q CrossRefPubMedGoogle Scholar
  23. Quattrocchio F, Verweij W, Kroon A, Spelt C, Mol J, Koes R (2006) PH4 of petunia is an R2R3 MYB protein that activates vacuolar acidification through interactions with basic-helix-loop-helix transcription factors of the anthocyanin pathway. Plant Cell 18(5):1274–1291.  https://doi.org/10.1105/tpc.105.034041 CrossRefPubMedCentralPubMedGoogle Scholar
  24. Richmond KE, Sussman M (2003) Got silicon? The non-essential beneficial plant nutrient. Curr Opin Plant Biol 6(3):268–272.  https://doi.org/10.1016/S1369-5266(03)00041-4 CrossRefPubMedGoogle Scholar
  25. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C-T method. Nature protocols 3(6):1101–1108.  https://doi.org/10.1038/nprot.2008.73 CrossRefPubMedGoogle Scholar
  26. Shao T, Qian Q, Tang D, Chen J, Li M, Cheng ZK, Luo Q (2012) A novel gene IBF1 is required for the inhibition of brown pigment deposition in rice hull furrows. Theor Appl Genet 125(2):381–390.  https://doi.org/10.1007/s00122-012-1840-8 CrossRefPubMedGoogle Scholar
  27. Shetty R, Frette X, Jensen B, Shetty NP, Jensen JD, Jorgensen HJ, Newman MA, Christensen LP (2011) Silicon-induced changes in antifungal phenolic acids, flavonoids, and key phenylpropanoid pathway genes during the interaction between miniature roses and the biotrophic pathogen Podosphaera pannosa. Plant physiol 157(4):2194–2205.  https://doi.org/10.1104/pp.111.185215 CrossRefPubMedCentralPubMedGoogle Scholar
  28. Shih CH, Chu H, Tang LK, Sakamoto W, Maekawa M, Chu IK, Wang M, Lo C (2008) Functional characterization of key structural genes in rice flavonoid biosynthesis. Planta 228(6):1043–1054.  https://doi.org/10.1007/s00425-008-0806-1 CrossRefPubMedGoogle Scholar
  29. Su Y, Hu SK, Zhang B, Ye WJ, Niu YF, Guo LB, Qian Q (2017) Characterization and fine mapping of a new early leaf senescence mutant es3(t) in rice. Plant Growth Regul 81(3):419–431.  https://doi.org/10.1007/s10725-016-0219-2 CrossRefGoogle Scholar
  30. Treutter D (2006) Significance of flavonoids in plant resistance: a review. Environ Chem Lett 4(3):147–157.  https://doi.org/10.1007/s10311-006-0068-8 CrossRefGoogle Scholar
  31. Winkel-Shirley B (2001) It takes a garden. How work on diverse plant species has contributed to an understanding of flavonoid metabolism. Plant Physiol 127(4):1399–1404.  https://doi.org/10.1104/Pp.010675 CrossRefPubMedCentralPubMedGoogle Scholar
  32. Yamaji N, Mitatni N, Ma JF (2008) A transporter regulating silicon distribution in rice shoots. Plant Cell 20(5):1381–1389.  https://doi.org/10.1105/tpc.108.059311 CrossRefPubMedCentralPubMedGoogle Scholar
  33. Yu HP, Qiu ZN, Xu QK, Wang ZW, Zeng DL, Hu J, Zhang GH, Zhu L, Gao ZY, Chen G, Guo LB, Qian Q, Ren DY (2017) Fine mapping of LOW TILLER 1, a gene controlling tillering and panicle branching in rice. Plant Growth Regul 83(1):93–104.  https://doi.org/10.1007/s10725-017-0286-z CrossRefGoogle Scholar
  34. Zhang KW, Qian Q, Huang ZJ, Wang YQ, Li M, Hong LL, Zeng DL, Gu MH, Chu CC, Cheng ZK (2006) GOLD HULL AND INTERNODE2 encodes a primarily multifunctional cinnamyl-alcohol dehydrogenase in rice1. Plant Physiol 140(3):972–983.  https://doi.org/10.1104/pp.105.073007 CrossRefPubMedCentralPubMedGoogle Scholar
  35. Zhang CC, Wang LJ, Zhang WX, Zhang FS (2013a) Do lignification and silicification of the cell wall precede silicon deposition in the silica cell of the rice (Oryza sativa L.) leaf epidermis? Plant Soil 372(1–2):137–149.  https://doi.org/10.1007/s11104-013-1723-z CrossRefGoogle Scholar
  36. Zhang GL, Cui YX, Ding XW, Qigen Dai QG (2013b) Stimulation of phenolic metabolism by silicon contributes to rice resistance to sheath blight. J Soil Sci Plant Nut J 176(1):118–124.  https://doi.org/10.1002/jpln.201200008 CrossRefGoogle Scholar
  37. Zhu BF, Si LZ, Wang ZX, Zhou Y, Zhu JJ, Shangguan YY, Lu DF, Fan DL, Li CY, Lin HX, Qian QA, Sang T, Zhou B, Minobe YZ, Han B (2011) Genetic control of a transition from black to straw-white seed hull in rice domestication. Plant Physiol 155(3):1301–1311.  https://doi.org/10.1104/pp.110.168500 CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Chengcong Yang
    • 1
  • Dongdong Zeng
    • 1
  • Ran Qin
    • 1
  • Md. Alamin
    • 1
  • Xiaoli Jin
    • 1
  • Chunhai Shi
    • 1
  1. 1.Department of Agronomy, College of Agriculture and BiotechnologyZhejiang UniversityHangzhouChina

Personalised recommendations