Biologia plantarum 62:732-740, 2018 | DOI: 10.1007/s10535-018-0814-3

OsNOX3, encoding a NADPH oxidase, regulates root hair initiation and elongation in rice

S. S. Wang1, X. N. Zhu1, J. X. Lin2, W. J. Zheng2, B. T. Zhang3, J. Q. Zhou1, J. Ni4, Z. C. Pan2, S. H. Zhu2, W. N. Ding2,*
1 School of Marine Sciences, Ningbo University, Ningbo, P.R. China
2 College of Science & Technology, Ningbo University, Ningbo, P.R. China
3 Cixi Institute of Biomedical Engineering, Ningbo Institute of Materials Technology and Engineering, Chinese Academy of Sciences, Ningbo, P.R. China
4 College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, P.R. China

Root hairs play important roles in plant nutrient and water acquisition. To better understand the genetic mechanism controlling root hair development in rice (Oryza sativa L.), a rice mutant with root hair defects was isolated and characterized. Cryo-scanning electron microscope (SEM) showed that the density and length of root hairs in the mutant were significantly reduced compared to wild type (WT). Map-based cloning and complementation test revealed that the mutation occurred in a NADPH oxidase gene OsNOX3 (LOC_Os01g61880). The OsNOX3 displays high sequence similarity with the previously characterized NOX genes RTH5 in maize and RHD2 in Arabidopsis, which play critical roles in root hair development. Expression pattern analysis indicated that OsNOX3 is expressed in various tissues throughout the plant with high expression in roots and root hairs. Subcellular localization analysis confirmed that OsNOX3 is located on the plasma membrane. Staining assays showed that the content of superoxide and hydrogen peroxide are significantly reduced in root hair tips of Osnox3 when compared to WT. Our results showed critical roles of OsNOX3 in regulating both root hair initiation and elongation in rice, which is similar to RTH5 but different from RHD2, confirming the difference of genetic mechanisms regulating root hair morphogenesis in monocot and dicot plants.

Keywords: gene expression; map-based cloning; Oryza sativa; SEM; subcellular localization
Subjects: NADPH oxidase; root hair iniciation; root hair elongation; gene expression; subcellular localization; rice
Species: Oryza sativa

Received: November 14, 2017; Revised: April 18, 2018; Accepted: May 15, 2018; Published: August 1, 2018Show citation

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Wang, S.S., Zhu, X.N., Lin, J.X., Zheng, W.J., Zhang, B.T., Zhou, J.Q., ... Ding, W.N. (2018). OsNOX3, encoding a NADPH oxidase, regulates root hair initiation and elongation in rice. Biologia plantarum, 62(4), 732-740. doi: 10.1007/s10535-018-0814-3.
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    References

    1. Barcelo, A.R.: Xylem parenchyma cells deliver the H2O2 necessary for lignification in differentiating xylem vessels. - Planta 747: 747-756, 2005. Go to original source...
    2. Carol, R.J., Takeda, S., Linstead, P., Durrant, M.C., Kakesova, H., Derbyshire, P., Drea, S., Zarsky, V., Dolan, L.: A RhoGDP dissociation inhibitor spatially regulates growth in root hair cells. - Nature 1013: 1013-1016, 2005. Go to original source...
    3. Chen, S.Y., Jin, W.Z, Wang, M.Y., Zhang, F., Zhou, J., Jia, Q.J., Wu, Y.R., Liu, F.Y., Wu, P.: Distribution and characterization of over 1000 T-DNA tags in rice genome. - Plant J. 105: 105-113, 2003. Go to original source...
    4. Cheng, S., Zhou, D.X., Zhao, Y.: WUSCHEL-related homeobox gene WOX11 increases rice drought resistance by controlling root hair formation and root system development. - Plant Signal. Behav. 11: e1130198, 2016. Go to original source...
    5. Clowes, F.: Pattern in root meristem development in angiosperms. - New Phytol. 83: 83-94, 2000. Go to original source...
    6. Ding, W.N., Tong, H.S., Zheng, W.J., Ye, J., Pan, Z.C., Zhang, B.T., Zhu, S.H.: Isolation, Characterization and transcriptome analysis of a cytokinin receptor mutant Osckt1 in rice. - Front. Plant Sci. 88: 88, 2017. Go to original source...
    7. Ding, W.N., Yu, Z.M., Tong, Y.L., Huang, W., Chen, H., Wu, P.: A transcription factor with a bHLH domain regulates root hair development in rice. - Cell Res. 1309: 1309-1311, 2009. Go to original source...
    8. Dolan, L.: Pattern in the root epidermis: an interplay of diffusible signals and cellular geometry. - Ann. Bot. 547: 547-553, 1996. Go to original source...
    9. Dolan, L.: Root hair development in grasses and cereals (Poaceae). - Curr. Opin. Genet. Dev. 76: 76-81, 2017. Go to original source...
    10. Foreman, J., Demidchik, V., Bothwell, J.H., Mylona, P., Miedema, H., Torres, M.A., Linstead, P., Costa, S., Brownlee, C., Jones, J.D., Davies, J.M., Dolan, L.: Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. - Nature 442: 442-446, 2003. Go to original source...
    11. Foreman, J., Dolan, L.: Root hairs as a model system for studying plant cell growth. - Ann. Bot. 1: 1-7, 2001. Go to original source...
    12. Gilroy, S., Jones, D.L.: Through form to function: root hair development and nutrient uptake. - Trends Plant Sci. 56: 56-60, 2000. Go to original source...
    13. Grebe, M.: The patterning of epidermal hairs in Arabidopsis-updated. - Curr. Opin. Plant Biol. 31: 31-37, 2012. Go to original source...
    14. Huang, J., Kim, C.M., Xuan, Y.H., Park, S.J., Piao, H.L., Je, B.I., Liu, J., Kim, T.H., Kim, B-K., Han, C-D.: OsSNDP1, a Sec14-nodulin domain containing protein, plays a critical role in root hair elongation in rice. - Plant mol. Biol. 39: 39-50, 2013a. Go to original source...
    15. Huang, J., Kim, C.M., Xuan, Y.H., Liu, J., Kim, T.H., Kim, BK., Han, C-D.: Formin homology 1 (OsFH1) regulates roothair elongation in rice (Oryza sativa). - Planta 237:1227-1239, 2013b. Go to original source...
    16. Kim, C.M., Dolan, L.: Root hair development involves asymmetric cell division in Brachypodium distachyon and symmetric division in Oryza sativa. - New Phytol. 601: 601-610, 2011. Go to original source...
    17. Kim, C.M., Park, S.H., Je, B.I., Park, S.H., Park, S.J., Piao, H.L., Eun, M.Y., Dolan, L., Han, C-D.: OsCSLD1, a cellulose synthase-like D1 gene, is required for root hair morphogenesis in rice. - Plant Physiol. 1220: 1220-1230, 2007. Go to original source...
    18. Lv, Q.D., Zhong, Y.J., Wang, Y.G., Wang, Z.Y., Zhang, L., Shi, J., Wu, Z.C., Liu, Y., Mao, C.Z., Yi, K.K., Wu, P.: SPX4 Negatively regulates phosphate signaling and homeostasis through its interaction with PHR2 in rice. - Plant Cell 1586: 1586-1597, 2014. Go to original source...
    19. Ma, N.N., Wang, Y., Qiu, S.C., Kang, Z.H., Che, S.G., Wang, G.X., Huang, J.L.: Overexpression of OsEXPA8, a rootspecific gene, improves rice growth and root system architecture by facilitating cell extension. - PLoS ONE 8: e75997, 2013. Go to original source...
    20. Marzec, M., Melzer, M., Szarejko, I.: Asymmetric growth of root epidermal cells is related to the differentiation of root hair cells in Hordeum vulgare (L.). - J. exp. Bot. 5145: 5145-5155, 2013. Go to original source...
    21. Marzec, M., Melzer, M., Szarejko, I.: The evolutionary context of root epidermis cell patterning in grasses (Poaceae). - Plant Signal Behav. 9: e27972, 2014. Go to original source...
    22. Marzec, M., Melzer, M., Szarejko, I.: Root hair development in the grasses: what we already know and what we still need to know. - Plant Physiol. 407: 407-414, 2015. Go to original source...
    23. Monshausen G.B., Bibikova T.N., Messerli M.A., Shi C., Gilroy S. Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs. - Proc. nat. Acad. Sci USA. 20996: 20996-21001, 2007. Go to original source...
    24. Nagano, M., Ishikawa, T., Fujiwara, M., Fukao, Y., Kawano, Y., Kawai-Yamada, M., Shimamoto, K. Plasma membrane microdomains are essential for Rac1-RbohB/H-mediated immunity in rice. - Plant Cell 1966: 1966-1983, 2016. Go to original source...
    25. Nestler, J., Liu, S., Wen, T.J., Paschold, A., Marcon, C., Tang, H.M., Li, D., Li, L., Meeley, R.B., Sakai, H., Bruce, W., Schnable, P.S., Hochholdinger, F.: Roothairless5, which functions in maize (Zea mays L.) root hair initiation and elongation encodes a monocot-specific NADPH oxidase. - Plant J. 729: 729-740, 2014. Go to original source...
    26. Parker, J.S., Cavell, A.C., Dolan, L., Roberts, K., Grierson, C.S.: Genetic interactions during root hair morphogenesis in Arabiopsis. - Plant Cell. 1961: 1961-1974, 2000.
    27. Row, H.C., Reeder, J.R.: Root-hair development as evidence of relationships among genera of Gramineae. - Amer. J. Bot. 596: 596-601, 1957. Go to original source...
    28. Salazar-Henao, J.E., Vélez-Bermúdez, I.C., Schmidt, W.: The regulation and plasticity of root hair patterning and morphogenesis. - Development 1848: 1848-1858, 2016.
    29. Schiefelbein, J.W.: Constructing a plant cell. The genetic control of root hair development. - Plant Physiol. 1525: 1525-1531, 2000. Go to original source...
    30. Schiefelbein, J.W., Somerville, C.: Genetic control of root hair development in Arabidopsis thaliana. - Plant Cell 235: 235-243, 1990. Go to original source...
    31. Segal, A.W.: NADPH oxidases as electrochemical generators to produce ion fluxes and turgor in fungi, plants and humans. - Open Biol. 160028: 160028, 2016.
    32. Torres, M.A., Dangl, J.L.: Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. - Curr. Opin. Plant Biol. 397: 397-403, 2005. Go to original source...
    33. Van Loock, B., Markakis, M.N., Verbelen, J-P., Vissenberg, K.: High-throughput transient transformation of Arabidopsis roots enables systematic co-localization analysis of GFPtagged proteins. - Plant Signal. Behav. 261: 261-263, 2010. Go to original source...
    34. Wang, C., Li, S., Ng, S., Zhang, B., Zhou, Y., Whelan, J., Wu, P., Shou, H.: Mutation in xyloglucan 6-xylosytransferase results in abnormal root hair development in Oryza sativa. - J. exp. Bot. 4149: 4149-4157, 2014a. Go to original source...
    35. Wang, G.F., Li, W.Q., Li, W.Y., Wu, G.L., Zhou, C.Y., Chen, K.M.: Characterization of rice NADPH oxidase genes and their expression under various environmental conditions. - Int. J. mol. Sci. 9440: 9440-9458, 2013. Go to original source...
    36. Wang, S., Xu, Y., Li, Z., Zhang, S., Lim, J.M., Lee, K.O., Li, C., Qian, Q., Jiang, A., Qi, Y.: OsMOGS is required for N-glycan formation and auxin-mediated root development in rice (Oryza sativa L.). - Plant J. 632: 632-645, 2014b. Go to original source...
    37. Wang, X., Zhang, M.M., Wang, Y.J., Gao, Y.T., Li, R., Wang, G.F., Li, W.Q., Liu, W.T., Chen, K.M.: The plasma membrane NADPH oxidase OsRbohA plays a crucial role in developmental regulation and drought-stress response in rice. - Physiol. Plant. 421: 421-443, 2016. Go to original source...
    38. Won, S.K., Choi, S.B., Kumari, S., Cho, M., Lee, S.H., Cho, H.T.: Root hair specific EXPANSIN B genes have been selected for Graminaceae root hairs. - Mol. Cells 369: 369-376, 2010. Go to original source...
    39. Wong, H.L., Pinontoan, R., Hayashi, K., Tabata, R., Yaeno, T., Hasegawa, K., Kojima, C., Yoshioka, H., Iba, K., Kawasaki, T., Shimamoto, K.: Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. - Plant Cell 4022: 4022-4034, 2007. Go to original source...
    40. Yamauchi, T., Yoshioka, M., Fukazawa, A., Mori, H., Nishizawa, N.K., Tsutsumi, N., Yoshioka, H., Nakazono, M.: An NADPH oxidase RBOH functions in rice roots during lysigenous aerenchyma formation under oxygendeficient conditions. - Plant Cell 775: 775-790, 2017. Go to original source...
    41. Yoo, S.C., Cho, S.H., Paek, N.C.: Rice WUSCHEL-related homeobox 3A (OsWOX3A) modulates auxin-transport gene expression in lateral root and root hair development. - Plant Signal. Behav. 8: e25929, 2013. Go to original source...
    42. Yoshida, S., Forno, D.A., Cock, J.H., Gomez, K.A.: Laboratory Manual for Physiological Studies of Rice, 3rd Ed. - International Rice Research Institute, Manila 1976.
    43. Yoshie, Y., Goto, K., Takai, R., Iwano, M., Takayama, S., Isogai, A., Che, F.S.: Function of the rice gp91phox homologs OsrbohA and OsrbohE genes in ROS-dependent plant immune responses. - Plant Biotechnol. 127: 127-135, 2005. Go to original source...
    44. Yu, Z.M., Kang, B., He, X.W., Lv, S.L., Bai, Y.H., Ding, W.N., Chen, M., Cho, H-T., Wu, P.: Root hair-specific EXPANSINs modulate root hair elongation in rice. - Plant J. 725: 725-734, 2011.
    45. Yuo, T., Toyota, M., Ichii, M., Takeda, S.: Molecular cloning of a root hairless gene rth1 in rice. - Breed. Sci. 13: 13-20, 2009. Go to original source...

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