Advertisement

Plant Molecular Biology

, Volume 82, Issue 1–2, pp 39–50 | Cite as

OsSNDP1, a Sec14-nodulin domain-containing protein, plays a critical role in root hair elongation in rice

  • Jin Huang
  • Chul Min Kim
  • Yuan-hu Xuan
  • Soon Ju Park
  • Hai Long Piao
  • Byoung Il Je
  • Jingmiao Liu
  • Tae Ho Kim
  • Bo-Kyeong Kim
  • Chang-Deok HanEmail author
Article

Abstract

Rice is cultivated in water-logged paddy lands. Thus, rice root hairs on the epidermal layers are exposed to a different redox status of nitrogen species, organic acids, and metal ions than root hairs growing in drained soil. To identify genes that play an important role in root hair growth, a forward genetics approach was used to screen for short-root-hair mutants. A short-root-hair mutant was identified and isolated by using map-based cloning and sequencing. The mutation arose from a single amino acid substitution of OsSNDP1 (Oryza sativa Sec14-nodulin domain protein), which shows high sequence homology with Arabidopsis COW1/AtSFH1 and encodes a phosphatidylinositol transfer protein (PITP). By performing complementation assays with Atsfh1 mutants, we demonstrated that OsSNDP1 is involved in growth of root hairs. Cryo-scanning electron microscopy was utilized to further characterize the effect of the Ossndp1 mutation on root hair morphology. Aberrant morphogenesis was detected in root hair elongation and maturation zones. Many root hairs were branched and showed irregular shapes due to bulged nodes. Many epidermal cells also produced dome-shaped root hairs, which indicated that root hair elongation ceased at an early stage. These studies showed that PITP-mediated phospholipid signaling and metabolism is critical for root hair elongation in rice.

Keywords

Root hair Sec14-nodulin domain-containing protein (SNDP) Phosphatidylinositol transfer protein (PITP) Rice 

Notes

Acknowledgments

This work was supported by grants from the Next-Generation BioGreen 21 Program (PJ008215 and PJ008168), the Rural Development Administration, Republic of Korea. Jingmiao Liu is supported by a scholarship from the BK21 program. We are grateful to Dr. Liam Dolan (University of Oxford, UK) for helping us with cryo-SEM work and Dr. Vytas Bankaitis (Texas A&M University, USA) for his constructive comments on our work.

Supplementary material

11103_2013_33_MOESM1_ESM.pdf (94 kb)
Five-day-old seedlings from the OsSNDP1 wild type and mutant. OsSNDP1 wild type and mutant were grown in 1/2 MS for 5 days (PDF 95 kb)
11103_2013_33_MOESM2_ESM.pdf (420 kb)
Phylogenetic analysis and protein alignment of OsSNDP1, 2, 3 and COW1/AtSFH1. a Ten OsSNDP genes can be classified into three groups. Three genes from group I, including OsSNDP1 of Os10g03400, show the highest homology with COW1/AtSFH1 of Arabidopsis. b OsSNDP1, 2, and 3 protein sequences are aligned with Arabidopsis COW1. Sec14-like domains are framed with black rectangles. Nodulin-like domains are underlined with a solid line (PDF 420  kb)
11103_2013_33_MOESM3_ESM.pdf (186 kb)
The expression levels and root-hair lengths of 7 Atsfh1 lines transformed with wild type OsSNDP1 and 6 Atsfh1 lines transformed with mutant Ossndp1 cDNA. a The expression levels of OsSNDP1 and Ossndp1 in Atsfh1 mutants were measured by qRT-PCR using ubiquitin as an internal control. b Seven-day-old Arabidopsis seedlings from each complementation line were used to measure root hair lengths. CW denotes Atsfh1 complemented with wild type OsSNDP1 cDNA while CM denotes Atsfh1 with mutant Ossndp1 cDNA (PDF 187 kb)
11103_2013_33_MOESM4_ESM.pdf (92 kb)
Gene expression analysis of OsSNDP1 using the rice array database (www.ricearry.org). Expression patterns of OsSNDP1 in suspension cells, root, shoot, anther, stigma, ovary, embryo, endosperm, and 5-day seeds were examined using the rice Affymetrix expression database. The expression data were translated into the graph (PDF 92 kb)
11103_2013_33_MOESM5_ESM.pdf (177 kb)
Hydropathy analysis of OsSNDP1 and Ossndp1 proteins. Protein sequences of OsSNDP1 and Ossndp1 were analyzed by hydropathy analysis at http://www.isb-sib.ch/ using the Kyte& Doolittle method. a Hydropathy scores were compared between OsSNDP1 and Ossndp1 proteins. b Magnified area of box in a. Window size = 7 (PDF 178 kb)
11103_2013_33_MOESM6_ESM.pdf (169 kb)
The morphology and lengths of root-hairs and Ossndp1 expression levels of F1 Arabidopsis plants (Col/CM5 and Col/CM9) obtained from crosses between Columbia (Col) and two Ossndp1 Atsfh1 lines (CM5 and CM9; see Online Resource 3). a Root hairs of Columbia and F1 plants were inspected under a microscope. Bar = 500 μm. b Root-hair lengths of five F1 seedlings from the same cross were measured. c The expression levels of Ossndp1 in F1 seedlings were measured by qRT-PCR using ubiquitin as an internal control. All the seedlings were 7-days old (PDF 169 kb)
11103_2013_33_MOESM7_ESM.pdf (79 kb)
Primer sets for map-based cloning. Primer sets such as RM7545, RM7217, RM3152, S10026C, RM1650, and S10072 were obtained from public databases. The other primer sets were designed based on public rice sequence databases. Silver stain means that PCR products were separated on polyacrylamide gels and stained by a silver staining method. Stu I means PCR products were digested with Stu I (PDF 79 kb)
11103_2013_33_MOESM8_ESM.pdf (79 kb)
Primer sets for q-RT PCR. All the primer sets were performed under the condition of 95 °C 1 min (activation), 95 °C 10 s, 55 °C 10 s, 72 °C 15 s, and 40 cycles (PDF 79 kb)

References

  1. Bohme K et al (2004) The Arabidopsis COW1 gene encodes a phosphatidylinositol transfer protein essential for root hair tip growth. Plant J 40:686–698PubMedCrossRefGoogle Scholar
  2. Bruex A et al (2012) A gene regulatory network for root epidermis cell differentiation in Arabidopsis. PLoS Genet 8:e1002446PubMedCrossRefGoogle Scholar
  3. Chin HG et al (1999) Molecular analysis of rice plants harboring an Ac/Ds transposable element-mediated gene trapping system. Plant J 19:615–623PubMedCrossRefGoogle Scholar
  4. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743PubMedCrossRefGoogle Scholar
  5. Ding W, Yu Z, Tong Y, Huang W, Chen H, Wu P (2009) A transcription factor with a bHLH domain regulates root hair development in rice. Cell Res 19:1309–1311PubMedCrossRefGoogle Scholar
  6. Dolan L, Duchett C, Grierson C, Linstead P, Schneider K, Lawson E, Dean C, Poethig S, Roberts K (1994) Clonal relationships and cell patterning in the root epidermis of Arabidopsis. Development 120:2465–2474Google Scholar
  7. Favery B et al (2001) KOJAK encodes a cellulose synthase-like protein required for root hair cell morphogenesis in Arabidopsis. Genes Dev 15:79–89PubMedCrossRefGoogle Scholar
  8. Foreman J et al (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446PubMedCrossRefGoogle Scholar
  9. Gahoonia TS, Nielsen NE, Joshi PA, Jahoor A (2001) A root hairless barley mutant for elucidating genetic of root hairs and phosphorus uptake. Plant Soil 235(2):211–219CrossRefGoogle Scholar
  10. Galway ME, Heckman JW Jr, Schiefelbein JW (1997) Growth and ultrastructure of Arabidopsis root hairs: the rhd3 mutation alters vacuole enlargement and tip growth. Planta 201:209–218PubMedCrossRefGoogle Scholar
  11. Grebe M (2012) The patterning of epidermal hairs in Arabidopsis-updated. Curr Opin Plant Biol 15:31–37PubMedCrossRefGoogle Scholar
  12. Grierson CS, Roberts K, Feldmann KA, Dolan L (1997) The COW1 locus of Arabidopsis acts after RHD2, and in parallel with RHD3 and TIP1, to determine the shape, rate of elongation, and number of root hairs produced from each site of hair formation. Plant Physiol 115:981–990PubMedCrossRefGoogle Scholar
  13. Kapranov P, Routt SM, Bankaitis VA, de Bruijn FJ, Szczyglowski K (2001) Nodule-specific regulation of phosphatidylinositol transfer protein expression in Lotus japonicus. Plant Cell 13:1369–1382PubMedGoogle Scholar
  14. Kim CM, Dolan L (2011) Root hair development involves asymmetric cell division in Brachypodium distachyon and symmetric division in Oryza sativa. New Phytol 192:601–610PubMedCrossRefGoogle Scholar
  15. Kim CM et al (2004) Rapid, large-scale generation of Ds transposant lines and analysis of the Ds insertion sites in rice. Plant J 39:252–263PubMedCrossRefGoogle Scholar
  16. Kim CM et al (2007) OsCSLD1, a cellulose synthase-like D1 gene, is required for root hair morphogenesis in rice. Plant Physiol 143:1220–1230PubMedCrossRefGoogle Scholar
  17. Kusano H et al (2008) The Arabidopsis Phosphatidylinositol Phosphate 5-Kinase PIP5K3 is a key regulator of root hair tip growth. Plant Cell 20:367–380PubMedCrossRefGoogle Scholar
  18. Leitner D et al (2010) A dynamic model of nutrient uptake by root hairs. New Phytol 185:792–802PubMedCrossRefGoogle Scholar
  19. Libault M, Brechenmacher L, Cheng J, Xu D, Stacey G (2010) Root hair systems biology. Trends Plant Sci 15:641–650PubMedCrossRefGoogle Scholar
  20. Mo P, Zhu Y, Liu X, Zhang A, Yan C, Wang D (2007) Identification of two phosphatidylinositol/phosphatidylcholine transfer protein genes that are predominately transcribed in the flowers of Arabidopsis thaliana. J Plant Physiol 164:478–486PubMedCrossRefGoogle Scholar
  21. Paungfoo-Lonhienne C et al (2010) DNA is taken up by root hairs and pollen, and stimulates root and pollen tube growth. Plant Physiol 153:799–805PubMedCrossRefGoogle Scholar
  22. Peleg-Grossman S, Golani Y, Kaye Y, Melamed-Book N, Levine A (2009) NPR1 protein regulates pathogenic and symbiotic interactions between Rhizobium and legumes and non-legumes. PLoS ONE 4:e8399PubMedCrossRefGoogle Scholar
  23. Peterman TK, Ohol YM, McReynolds LJ, Luna EJ (2004) Patellin1, a novel Sec14-like protein, localizes to the cell plate and binds phosphoinositides. Plant Physiol 136:3080–3094; discussion 3001–3082PubMedCrossRefGoogle Scholar
  24. Sha B, Phillips SE, Bankaitis VA, Luo M (1998) Crystal structure of the Saccharomyces cerevisiae phosphatidylinositol-transfer protein. Nature 391:506–510PubMedCrossRefGoogle Scholar
  25. Shimmen T, Yokota E (2004) Cytoplasmic streaming in plants. Curr Opin Cell Biol 16:68–72PubMedCrossRefGoogle Scholar
  26. Strader LC, Chen GL, Bartel B (2010) Ethylene directs auxin to control root cell expansion. Plant J 64:874–884PubMedCrossRefGoogle Scholar
  27. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCrossRefGoogle Scholar
  28. Toki S et al (2006) Early infection of scutellum tissue with Agrobacterium allows high-speed transformation of rice. Plant J 47:969–976PubMedCrossRefGoogle Scholar
  29. Vincent P et al (2005) A Sec14p-nodulin domain phosphatidylinositol transfer protein polarizes membrane growth of Arabidopsis thaliana root hairs. J Cell Biol 168:801–812PubMedCrossRefGoogle Scholar
  30. Wang X, Cnops G, Vanderhaeghen R, De Block S, Van Montagu M, Van Lijsebettens M (2001) AtCSLD3, a cellulose synthase-like gene important for root hair growth in Arabidopsis. Plant Physiol 126:575–586PubMedCrossRefGoogle Scholar
  31. Wymer CL, Bibikova TN, Gilroy S (1997) Cytoplasmic free calcium distributions during the development of root hairs of Arabidopsis thaliana. Plant J 12:427–439PubMedCrossRefGoogle Scholar
  32. Yuo T (2009) Molecular cloning of a root hairless gene. Breed Sci 59:13–20CrossRefGoogle Scholar
  33. Zheng R, Li H, Jiang R, Romheld V, Zhang F, Zhao FJ (2011) The role of root hairs in cadmium acquisition by barley. Environ Pollut 159:408–415PubMedCrossRefGoogle Scholar
  34. ZhiMing Y et al (2011) Root hair-specific expansins modulate root hair elongation in rice. Plant J 66:725–734PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Jin Huang
    • 1
  • Chul Min Kim
    • 2
  • Yuan-hu Xuan
    • 1
  • Soon Ju Park
    • 1
  • Hai Long Piao
    • 1
  • Byoung Il Je
    • 1
  • Jingmiao Liu
    • 1
  • Tae Ho Kim
    • 3
  • Bo-Kyeong Kim
    • 4
  • Chang-Deok Han
    • 1
    Email author
  1. 1.Division of Applied Life Science (BK21 Program), Plant Molecular Biology and Biotechnology Research Center (PMBBRC)Gyeongsang National UniversityJinjuKorea
  2. 2.Department of Plant SciencesUniversity of OxfordOxfordUK
  3. 3.Genomics Division, Department of Agricultural BiotechnologyNational Academy of Agricultural Science (NAAS), RDASuwonKorea
  4. 4.Rice Breeding and Cultivation Division, Department of Rice and Winter Cereal Crop (NICS)RDAIksanKorea

Personalised recommendations