Skip to main content
Log in

Rice RHC Encoding a Putative Cellulase is Essential for Normal Root Hair Elongation

  • Original Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Root hairs are tubular shaped protuberances of root epidermal cells and are found in nearly all vascular plants. Co-ordinate expression of a number of root hair morphogenesis genes involved in cytoskeleton reorganization, changes in homeostasis and distribution of ion gradients, and cell wall reassembly are required during root hair cell elongation. In this report, we have characterized a root hairspecific putative cellulase gene in rice, OsRHC. OsRHC is specifically expressed in elongating root hairs and OsRHC is targeted to the plasma membrane. The mutation of the OsRHC gene by a T-DNA knock-out and CRISPR-Cas9 system causes a severe reduction in root hair length. Bimolecular fluorescence complementation analysis demonstrated that the OsRHC protein interacts with a root hair-specific cellulose synthase protein (OsCSLD1) in the plasma membrane. Furthermore, we observed a moderate reduction of cellulose content in the osrhc mutant. Our results suggest that the plasma membrane-localized OsRHC plays a critical role in cell wall remodeling during root hair extension.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Becker JD, Takeda S, Borges F, Dolan L, Feijo JA (2014). Transcriptional profiling of Arabidopsis root hair and pollen defines an apical cell growth signature. BMC Plant Biol 14:197

    Google Scholar 

  • Bhosale R, Giri J, Pandey BK, Giehl RFH, Hartmann A, Traini R et al (2018). A mechanistic framework for auxin dependent Arabidopsis root hair elongation in response to low external phosphate. Nat Comm 9:1409

    Google Scholar 

  • Bruex A, Kainkaryam RM, Wieckowski Y, Kang YH, Bernhardt C, Xia Y, Zheng X, Wang JY, Lee MM, Benfey P, Woolf PJ, Schiefelbein J (2012). A gene regulatory network for root epidermis cell differentiation in Arabidopsis. PLoS Genetic 8:e1002446

    Book  Google Scholar 

  • Chandran AKN, Jeong HY, Jung KH, Lee C (2016). Development of functional modules based on co-expression patterns for cell-wall biosynthesis related genes in rice. J Plant Biol 59:1–15

    Article  CAS  Google Scholar 

  • Dittmer HJ (1937). A quantitative study of the roots and root hairs of a winter rye plant (Secale cereale). Am J Bot 24:417–420

    Article  Google Scholar 

  • Dolan L, Costa S. Evolution and genetics of root hair stripes in the root epidermis (2001). J Exp Bot 52:413–417

    Article  CAS  PubMed  Google Scholar 

  • Gahoonia TS, Nielsen NE (2003). Phosphorus (P) uptake and growth of a root hairless barley mutant (bald root barley, brb) and wild type in low-and high-P soils. Plant Cell Environ 26:1759–1766

    Article  CAS  Google Scholar 

  • Gahoonia TS, Nielsen NE, Joshi PA, Jahoor A (2001). A root hairless barley mutant for elucidating genetics of root hairs and phosphorus uptake. Plant and Soil 235:211–219

    Article  CAS  Google Scholar 

  • Gilroy S, Jones DL (2000). Through form to function:root hair development and nutrient uptake. Trends Plant Sci 5:56–60

    Article  CAS  PubMed  Google Scholar 

  • Giri J, Bhosale R, Huang G, Pandey B, Parker H, Zappala S. et al (2018). The rice auxin influx carrier OsAUX1 facilitates root hair elongation in response to low external phosphate. Nat Comm 9:1408

    Article  CAS  Google Scholar 

  • Grieneisen V, Xu J, Marée A, Hogeweg P, Scheres B (2007). Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature 449:1008–1013

    Article  CAS  PubMed  Google Scholar 

  • Haling RE, Brown LK, Bengough AG, Young IM, Hallett PD, White PJ, George TS (2013). Root hairs improve root penetration, rootsoil contact, and phosphorus acquisition in soils of different strength. J Exp Bot 64:3711–3721

    Article  CAS  PubMed  Google Scholar 

  • Hazen SP, Scott-Craig JS, Walton JD (2002). Cellulose synthase-like genes of rice. Plant Physiol 128:336–340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang L, Shi X, Wang W, Ryu KH, Schiefelbein J (2017). Diversification of root hair development genes in vascular plants. Plant Physiol 174:1697–1712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeon JS, Lee S, Jung KH, Jun SH, Jeong DH, Lee J, Kim C, Jang S, Yang K, Nam J, An K, Han MJ, Sung RJ, Choi HS, Yu JH, Choi JH, Cho SY, Cha SS, Kim SI, An G. T-DNA insertional mutagenesis for functional genomics in rice (2000). Plant J 22:561–570

    CAS  Google Scholar 

  • Jungk A. Root hair and the acquisition of plant nutrients from soil (2001). J Plant Nutr Soil Sci 164:121–129

    CAS  Google Scholar 

  • Kawata S, Ishihara K. Studies on the root hairs in rice plant (1959). Proc Crop Sci Soc Jpn 27:341–348

    Article  Google Scholar 

  • Kawata S, Ishihara K, Shioya T (1964). Studies on the root hairs of lowland rice plants in the upland fields. Proc Crop Sci Soc Jpn 32:250–253

    Article  Google Scholar 

  • Kim CM, Han CD, Dolan L (2017). RSL class I genes positively regulate root hair development i. Oryza sativa. New Phytol 213:314–323

    Article  CAS  PubMed  Google Scholar 

  • Kim CM, Park SH, Je BI, Park SH, Park SJ, Piao HL, Eun MY, Dolan L, Han CD (2007). OsCSLD1, a cellulose synthase-like D1 gene, is required for root hair morphogenesis in rice. Plant Physiol 143:1220–1230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim DW, Lee SH, Choi SB, Won SK, Heo YK, Cho M, Park YI, Cho HT (2006). Functional conservation of a root hair cell-specific cis-element in angiosperms with different root hair distribution patterns. Plant Cell 18:2958–2570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar M, Turner S (2015). Plant cellulose synthesis:CESA proteins crossing kingdoms. Phytochemistry 112:91–99

    Article  CAS  PubMed  Google Scholar 

  • Lane DR, Wiedemeier A, Peng L, Höfte H, Vernhettes S, Desprez T, Hocart CH, Birch RJ, Baskin TI, Burn JE, Arioli T, Betzner AS, Williamson RE (2001). Temperature-sensitive alleles of RSW2 link the KORRIGAN endo-1,4-beta-glucanase to cellulose synthesis and cytokinesis in Arabidopsis. Plant Physiol 126:278–288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee C, Zhong R, Richardson EA, Himmelsbach DS, McPhail BT, Ye ZH (2007). The PARVUS gene is expressed in cells undergoing secondary wall thickening and is essential for glucuronoxylan biosynthesis. Plant Cell Physiol 48:1659–1672

    Article  CAS  PubMed  Google Scholar 

  • Li M, Xiong G, Li R, Cui J, Tang D, Zhang B, Pauly M, Cheng Z, Zhou Y (2009). Rice cellulose synthase-like D4 is essential for normal cell-wall biosynthesis and plant growth. Plant J 60:1055–69

    Article  PubMed  Google Scholar 

  • Ma JF, Goto S, Tamai K, Ichii M (2001). Role of root hair and lateral roots in silicon uptake by rice. Plant Physiol 127:1773–1780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mangano S, Denita-Juarez SP, Choi HS, Marzol E, Hwang Y, Ranocha P, Velasquez SM, Borassi C, Barberini ML, Aptekmann AA, Muschietti JP, Nadra AD, Dunand C, Cho HT, Estevez JM (2017). Molecular link between auxin and ROS-mediated polar growth. Proc Natl Acad Sci USA 114:5289–5294

    Article  CAS  PubMed  Google Scholar 

  • Mansoori N, Timmers J, Desprez T, Kamei CL, Dees DC, Vincken JP, Visser RG, Hofte H, Vernhettes S, Trindade LM 2014;. KORRIGAN1 interacts specifically with integral components of the cellulose synthase machinery. Plos One 9:e112387

    Google Scholar 

  • Marzec M, Melzer M, Szarejko I (2015). Root hair development in the grasses:what we already know and what we still need to know. Plant Physiol 168:407–414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mølhøj M, Ulvskov P, Da Degan F (2001). Characterization of a functional soluble form of a Brassica napus membrane-anchored endo-1,4-beta-glucanase heterologously expressed in Pichia pastoris. Plant Physiol 127:674–684

    Article  PubMed  PubMed Central  Google Scholar 

  • Moon S, Chandran AKN, An G, Lee C, Jung KH (2018). Genomewide analysis of root hair-preferential genes in rice. Rice (N Y) 11(1):48

    Article  Google Scholar 

  • Muller M, Schmidt W (2004). Environmentally induced plasticity of root hair development in Arabidopsis. Plant Physiol 134:409–419.

    PubMed  Google Scholar 

  • Römling U, Galperin MY (2015). Bacterial cellulose biosynthesis:diversity of operons, subunits, products, and functions. Trends Microbiol 23:545–457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salazar-Henao JE, Vélez-Bermúdez IC, Schmidt W (2016). The regulation and plasticity of root hair patterning and morphogenesis. Development 143:1848–1858

    Article  CAS  PubMed  Google Scholar 

  • Slabaugh E, Held M, Brandizzi F (2011). Control of root hair development in Arabidopsis thaliana by an endoplasmic reticulum anchored member of the R2R3-MYB transcription factor family. Plant J 67:395–405

    Article  CAS  PubMed  Google Scholar 

  • Speth EB, Imboden L, Hauck P, He SY (2009). Subcellular localization and functional analysis of the Arabidopsis GTPase RabE. Plant Physiol 149:1824–1837

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi J, Rudsander UJ, Hedenström M, Banasiak A, Harholt J, Amelot N, Immerzeel P, Ryden P, Endo S, Ibatullin FM, Brumer H, de Campillo E, Master ER, Scheller HV, Sundberg B, Teeri TT, Mellerowicz EJ (2009). KORRIGAN1 and its aspen homolog PttCel9A1 decrease cellulose crystallinity in Arabidopsis stems. Plant Cell Physiol 50:1099–1115

    Article  CAS  PubMed  Google Scholar 

  • Updegraff DM. Semimicro determination of cellulose in biological materials (1969). Anal Biochem 32:420–424

    Article  CAS  Google Scholar 

  • Wang C, Li S, Ng S, Zhang B, Zhou Y, Whelan J, Wu P, Shou H (2014). Mutation in xyloglucan 6-xylosytransferase results in abnormal root hair development in Oryza sativa. J Exp Bot 65:4149–4157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Won SK, Lee YJ, Lee HY, Heo YK, Cho M, Cho HT (2009). Ciselement-and transcriptome-based screening of root hair-specific genes and their functional characterization in Arabidopsis. Plant Physiol 150:1459–1473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie K, Minkenberg B, Yang Y (2015). Boosting CRISPR/Cas9 multiplex editing capability with the endogenous tRNA-processing system. Proc Natl Acad Sci USA 112:3570–3575

    Article  CAS  PubMed  Google Scholar 

  • Yin L, Verhertbruggen Y, Oikawa A, Manisseri C, Knierim B, Prak L, Jensen JK, Knox JP, Auer M, Willats WG, Scheller HV (2011). The cooperative activities of CSLD2, CSLD3, and CSLD5 are required for normal Arabidopsis development. Mol Plant 4:1024–1037

    Article  CAS  PubMed  Google Scholar 

  • Yu ZM, Kang B, He XW, Lv SL, Bai YH, Ding WN, Chen M, Cho HT, Wu P (2011). Root hair-specific expansins modulate root hair elongation in rice. Plant J 66:725–734

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Chanhui Lee or Ki-Hong Jung.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Moon, S., Chandran, A.K.N., Kim, YJ. et al. Rice RHC Encoding a Putative Cellulase is Essential for Normal Root Hair Elongation. J. Plant Biol. 62, 82–91 (2019). https://doi.org/10.1007/s12374-018-0393-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-018-0393-z

Keywords

Navigation