Abstract
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 showed that the density and length of root hairs in the mutant were significantly reduced compared to the 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 was expressed in various tissues throughout the plant with high expression in roots and root hairs. Subcellular localization analysis confirmed that OsNOX3 was located on the plasma membrane. Staining assays showed that the content of superoxide and hydrogen peroxide were 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.
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Abbreviations
- EMS:
-
ethylmethanesulfonate
- GFP:
-
green fluorescent protein
- MS:
-
Murashige and Skoog
- ROS:
-
reactive oxygen species
- RT-PCR:
-
reverse transcription PCR
- SEM:
-
scanning electron microscope
- SSR:
-
simple sequence repeat
- STS:
-
sequence tagged site
- TM:
-
transmembrane
- WT:
-
wild type
References
Barcelo, A.R.: Xylem parenchyma cells deliver the H2O2 necessary for lignification in differentiating xylem vessels. - Planta 220: 747–756, 2005.
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 438: 1013–1016, 2005.
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. 36: 105–113, 2003.
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.
Clowes, F.: Pattern in root meristem development in angiosperms. - New Phytol. 146: 83–94, 2000.
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. 8: 88, 2017.
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. 19: 1309–1311, 2009.
Dolan, L.: Pattern in the root epidermis: an interplay of diffusible signals and cellular geometry. - Ann. Bot. 77: 547–553, 1996.
Dolan, L.: Root hair development in grasses and cereals (Poaceae). - Curr. Opin. Genet. Dev. 45: 76–81, 2017.
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 422: 442–446, 2003.
Foreman, J., Dolan, L.: Root hairs as a model system for studying plant cell growth. - Ann. Bot. 88: 1–7, 2001.
Gilroy, S., Jones, D.L.: Through form to function: root hair development and nutrient uptake. - Trends Plant Sci. 5: 56–60, 2000.
Grebe, M.: The patterning of epidermal hairs in Arabidopsis–updated. - Curr. Opin. Plant Biol. 15: 31–37, 2012.
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. 82: 39–50, 2013a.
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.
Kim, C.M., Dolan, L.: Root hair development involves asymmetric cell division in Brachypodium distachyon and symmetric division in Oryza sativa. - New Phytol. 192: 601–610, 2011.
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. 143: 1220–1230, 2007.
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 26: 1586–1597, 2014.
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.
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. 64: 5145–5155, 2013.
Marzec, M., Melzer, M., Szarejko, I.: The evolutionary context of root epidermis cell patterning in grasses (Poaceae). - Plant Signal Behav. 9: e27972, 2014.
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. 168: 407–414, 2015.
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. 104: 20996–21001, 2007.
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 28: 1966–1983, 2016.
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. 79: 729–740, 2014.
Parker, J.S., Cavell, A.C., Dolan, L., Roberts, K., Grierson, C.S.: Genetic interactions during root hair morphogenesis in Arabiopsis. - Plant Cell. 12: 1961–1974, 2000.
Row, H.C., Reeder, J.R.: Root-hair development as evidence of relationships among genera of Gramineae. - Amer. J. Bot. 44: 596–601, 1957.
Salazar-Henao, J.E., Vélez-Bermúdez, I.C., Schmidt, W.: The regulation and plasticity of root hair patterning and morphogenesis. - Development 143: 1848–1858, 2016.
Schiefelbein, J.W.: Constructing a plant cell. The genetic control of root hair development. - Plant Physiol. 124: 1525–1531, 2000.
Schiefelbein, J.W., Somerville, C.: Genetic control of root hair development in Arabidopsis thaliana. - Plant Cell 2: 235–243, 1990.
Segal, A.W.: NADPH oxidases as electrochemical generators to produce ion fluxes and turgor in fungi, plants and humans. - Open Biol. 6: 160028, 2016.
Torres, M.A., Dangl, J.L.: Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. - Curr. Opin. Plant Biol. 8: 397–403, 2005.
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. 5: 261–263, 2010.
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. 65: 4149–4157, 2014a.
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. 14: 9440–9458, 2013.
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. 78: 632–645, 2014b.
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. 156: 421–443, 2016.
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 30: 369–376, 2010.
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 19: 4022–4034, 2007.
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 29: 775–790, 2017.
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.
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.
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. 22: 127–135, 2005.
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. 66: 725–734, 2011.
Yuo, T., Toyota, M., Ichii, M., Takeda, S.: Molecular cloning of a root hairless gene rth1 in rice. - Breed. Sci. 59: 13–20, 2009.
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Acknowledgment: This work was supported by the National Natural Science Foundation of China (grant No. 31371595), the Zhejiang Provincial Natural Science Foundation of China (LY17C020002), the Natural Science Foundation of Ningbo (2017A610291, 2017A610292), and the K.C. Wong Magna Fund at Ningbo University. The first two authors contributed equally to this work.
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Wang, S.S., Zhu, X.N., Lin, J.X. et al. OsNOX3, encoding a NADPH oxidase, regulates root hair initiation and elongation in rice. Biol Plant 62, 732–740 (2018). https://doi.org/10.1007/s10535-018-0714-3
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DOI: https://doi.org/10.1007/s10535-018-0714-3