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Plant Molecular Biology Reporter

, Volume 32, Issue 1, pp 270–281 | Cite as

Rice NARROW LEAF1 Regulates Leaf and Adventitious Root Development

  • Sung-Hwan Cho
  • Soo-Cheul Yoo
  • Haitao Zhang
  • Jung-Hyun Lim
  • Nam-Chon PaekEmail author
Original Paper

Abstract

To improve our understanding of the molecular–genetic mechanisms governing leaf and root development in rice (Oryza sativa), we investigated narrow leaf1 (nal1), a pleiotropic mutant with short and narrow leaves, semi-dwarf stature, and fewer adventitious (or crown) roots. The narrow leaf5 (nal5) and nal1 mutants display similar defects in leaf and root development. Sequence analysis and complementation tests showed that nal5 is allelic to nal1. NAL1 encodes a putative trypsin-like serine/cysteine protease; the coding region of nal5 contains a missense mutation and nal1 harbors a 30-bp deletion. Quantitative real-time PCR revealed that nal1 mutants have altered expression levels of many OSHB, YABBY, and PIN-FORMED genes associated with leaf development and auxin transport. In addition, expression levels of CROWN ROOTLESS genes are markedly down-regulated in nal1. These results indicate that NAL1 functions in the regulation of both leaf and adventitious root development at the transcriptional level. Notably, exogenous auxin treatment rescued the reduced number of adventitious roots in nal1. Based on our results, we propose that NAL1 plays important roles in adventitious root development in rice.

Keywords

Adventitious root Auxin transport CROWN ROOTLESS Narrow leaf1 Narrow leaf5 Rice 

Notes

Acknowledgments

We thank the Institute of Genetic Resource in the Kyushu University, Japan for kind donation of the rice nal1 and nal5 seeds. This work was supported by a grant from the Next-Generation BioGreen 21 Program (Plant Molecular Breeding Center No. PJ008128), Rural Development Administration, Republic of Korea.

Supplementary material

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Fig. S1 (DOCX 484 kb)
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Fig. S2 (DOCX 54 kb)
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Table S1 (DOCX 23 kb)
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Table S2 (DOCX 23 kb)
11105_2013_675_MOESM5_ESM.docx (24 kb)
Table S3 (DOCX 23 kb)

References

  1. Becraft PW, Li K, Dey N, Asuncion-Crabb Y (2002) The maize dek1 gene functions in embryonic pattern formation and cell fate specification. Development 129:5217–5225PubMedGoogle Scholar
  2. Benkova E, Michniewicz M, Sauer M, Teichmann T, Seifertova D, Jurgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602. doi: 10.1016/S0092-8674(03)00924-3 PubMedCrossRefGoogle Scholar
  3. Berleth T, Mattsson J (2000) Vascular development: tracing signals along veins. Curr Opin Plant Biol 3:406–411. doi: 10.1016/S1369-5266(00)00104-7 PubMedCrossRefGoogle Scholar
  4. Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44. doi: 10.1038/nature03184 PubMedCrossRefGoogle Scholar
  5. Braybrook SA, Kuhlemeier C (2010) How a plant builds leaves. Plant Cell 22:1006–1018. doi: 10.1105/tpc.110.073924 PubMedCentralPubMedCrossRefGoogle Scholar
  6. Chen Y, Fan X, Song W, Zhang Y, Xu G (2012) Over-expression of OsPIN2 leads to increased tiller numbers, angle and shorter plant height through suppression of OsLAZY1. Plant Biotechnol J 10:139–149. doi: 10.1111/j.1467-7652.2011.00637.x PubMedCrossRefGoogle Scholar
  7. Cho SH, Yoo SC, Zhang H, Pandeya D, Koh HJ, Hwang JY, Kim GT, Paek NC (2013) The rice narrow leaf2 and narrow leaf3 loci encode WUSCHEL-related homeobox 3A (OsWOX3A) and function in leaf, spikelet, tiller and lateral root development. New Phytol 198:1071–1084. doi: 10.1111/nph.12231 PubMedCrossRefGoogle Scholar
  8. Clark SE, Jacobsen SE, Levin JZ, Meyerowitz EM (1996) The CLAVATA and SHOOT MERISTEMLESS loci competitively regulate meristem activity in Arabidopsis. Development 122:1567–1575PubMedGoogle Scholar
  9. Coudert Y, Perin C, Courtois B, Khong NG, Gantet P (2010) Genetic control of root development in rice, the model cereal. Trends Plant Sci 15:219–226. doi: 10.1016/j.tplants.2010.01.008 PubMedCrossRefGoogle Scholar
  10. De Smet I, Jurgens G (2007) Patterning the axis in plants-auxin in control. Curr Opin Genet Dev 17:337–343. doi: 10.1016/j.gde.2007.04.012 PubMedCrossRefGoogle Scholar
  11. Dengler N, Kang J (2001) Vascular patterning and leaf shape. Curr Opin Plant Biol 4:50–56. doi: 10.1016/S1369-5266(00)00135-7 PubMedCrossRefGoogle Scholar
  12. Eshed Y, Izhaki A, Baum SF, Floyd SK, Bowman JL (2004) Asymmetric leaf development and blade expansion in Arabidopsis are mediated by KANADI and YABBY activities. Development 131:2997–3006. doi: 10.1242/dev.01186 PubMedCrossRefGoogle Scholar
  13. Friml J, Palme K (2002) Polar auxin transport—old questions and new concepts? Plant Mol Biol 49:273–284PubMedCrossRefGoogle Scholar
  14. Fujino K, Matsuda Y, Ozawa K, Nishimura T, Koshiba T, Fraaije MW, Sekiguchi H (2008) NARROW LEAF 7 controls leaf shape mediated by auxin in rice. Mol Genet Genomics 279:499–507. doi: 10.1007/s00438-008-0328-3 PubMedCrossRefGoogle Scholar
  15. Galweiler L, Guan C, Muller A, Wisman E, Mendgen K, Yephremov A, Palme K (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282:2226–2230PubMedCrossRefGoogle Scholar
  16. Guilfoyle TJ, Hagen G (2001) Auxin response factors. J. Plant Growth Regul 10:281–291Google Scholar
  17. Hedstrom L (2002) Serine protease mechanism and specificity. Chem Rev 102:4501–4524. doi: 10.1021/cr000033x PubMedCrossRefGoogle Scholar
  18. Hibara K, Obara M, Hayashida E, Abe M, Ishimaru T, Satoh H, Itoh J, Nagato Y (2009) The ADAXIALIZED LEAF1 gene functions in leaf and embryonic pattern formation in rice. Dev Biol 334:345–354. doi: 10.1016/j.ydbio.2009.07.042 PubMedCrossRefGoogle Scholar
  19. Hu J, Zhu L, Zeng D, Gao Z, Guo L, Fang Y, Zhang G, Dong G, Yan M, Liu J, Qian Q (2010) Identification and characterization of NARROW AND ROLLED LEAF 1, a novel gene regulating leaf morphology and plant architecture in rice. Plant Mol Biol 73:283–292. doi: 10.1007/s11103-010-9614-7 PubMedCrossRefGoogle Scholar
  20. Husbands AY, Chitwood DH, Plavskin Y, Timmermans MC (2009) Signals and prepatterns: new insights into organ polarity in plants. Genes Dev 23:1986–1997. doi: 10.1101/gad.1819909 PubMedCrossRefGoogle Scholar
  21. Inukai Y, Sakamoto T, Ueguchi-Tanaka M, Shibata Y, Gomi K, Umemura I, Hasegawa Y, Ashikari M, Kitano H, Matsuoka M (2005) Crown rootless1, which is essential for crown root formation in rice, is a target of an AUXIN RESPONSE FACTOR in auxin signaling. Plant Cell 17:1387–1396. doi: 10.1105/tpc.105.030981 PubMedCentralPubMedCrossRefGoogle Scholar
  22. Itoh J, Hibara K, Sato Y, Nagato Y (2008) Developmental role and auxin responsiveness of Class III homeodomain leucine zipper gene family members in rice. Plant Physiol 147:1960–1975. doi: 10.1104/pp. 108.118679 PubMedCentralPubMedCrossRefGoogle Scholar
  23. Johnson KL, Degnan KA, Ross Walker J, Ingram GC (2005) AtDEK1 is essential for specification of embryonic epidermal cell fate. Plant J 44:114–127. doi: 10.1111/j.1365-313X.2005.02514.x PubMedCrossRefGoogle Scholar
  24. Kerstetter R, Vollbrecht E, Lowe B, Veit B, Yamaguchi J, Hake S (1994) Sequence analysis and expression patterns divide the maize knotted1-like homeobox genes into two classes. Plant Cell 6:1877–1887. doi: 10.1105/tpc.6.12.1877 PubMedCentralPubMedGoogle Scholar
  25. Kerstetter RA, Bollman K, Taylor RA, Bomblies K, Poethig RS (2001) KANADI regulates organ polarity in Arabidopsis. Nature 411:706–709. doi: 10.1038/35079629 PubMedCrossRefGoogle Scholar
  26. Kitomi Y, Ito H, Hobo T, Aya K, Kitano H, Inukai Y (2011) The auxin responsive AP2/ERF transcription factor CROWN ROOTLESS5 is involved in crown root initiation in rice through the induction of OsRR1, a type-A response regulator of cytokinin signaling. Plant J 67:472–484. doi: 10.1111/j.1365-313X.2011.04610.x PubMedCrossRefGoogle Scholar
  27. Kitomi Y, Ogawa A, Kitano H, Inukai Y (2008) CRL4 regulates crown root formation through auxin transport in rice. Plant Root 2:19–28. doi: 10.3117/plantroot.2.19 CrossRefGoogle Scholar
  28. Kuroda H, Maliga P (2003) The plastid clpP1 protease gene is essential for plant development. Nature 425:86–89. doi: 10.1038/nature01909 PubMedCrossRefGoogle Scholar
  29. Lenhard M, Jurgens G, Laux T (2002) The WUSCHEL and SHOOTMERISTEMLESS genes fulfill complementary roles in Arabidopsis shoot meristem regulation. Development 129:3195–3206PubMedGoogle Scholar
  30. Liu H, Wang S, Yu X, Yu J, He X, Zhang S, Shou H, Wu P (2005) ARL1, a LOB-domain protein required for adventitious root formation in rice. Plant J 43:47–56. doi: 10.1111/j.1365-313X.2005.02434.x PubMedCrossRefGoogle Scholar
  31. Liu S, Wang J, Wang L, Wang X, Xue Y, Wu P, Shou H (2009) Adventitious root formation in rice requires OsGNOM1 and is mediated by the OsPINs family. Cell Res 19:1110–1119. doi: 10.1038/cr.2009.70 PubMedCrossRefGoogle Scholar
  32. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔC T method. Methods 25:402–408. doi: 10.1006/meth.2001.1262 PubMedCrossRefGoogle Scholar
  33. Ljung K, Bhalerao RP, Sandberg G (2001) Sites and homeostatic control of auxin biosynthesis in Arabidopsis during vegetative growth. Plant J 28:465–474. doi: 10.1046/j.1365-313X.2001.01173.x PubMedCrossRefGoogle Scholar
  34. McConnell JR, Emery J, Eshed Y, Bao N, Bowman J, Barton MK (2001) Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411:709–713. doi: 10.1038/35079635 PubMedCrossRefGoogle Scholar
  35. Murtas G, Reeves PH, Fu YF, Bancroft I, Dean C, Coupland G (2003) A nuclear protease required for flowering-time regulation in Arabidopsis reduces the abundance of SMALL UBIQUITIN-RELATED MODIFIER conjugates. Plant Cell 15:2308–2319. doi: 10.1105/tpc.015487 PubMedCentralPubMedCrossRefGoogle Scholar
  36. Nakata M, Matsumoto N, Tsugeki R, Rikirsch E, Laux T, Okada K (2012) Roles of the middle domain-specific WUSCHEL-RELATED HOMEOBOX genes in early development of leaves in Arabidopsis. Plant Cell 24:519–535. doi: 10.1105/tpc.111.092858 PubMedCentralPubMedCrossRefGoogle Scholar
  37. Nishimura A, Ito M, Kamiya N, Sato Y, Matsuoka M (2002) OsPNH1 regulates leaf development and maintenance of the shoot apical meristem in rice. Plant J 30:189–201. doi: 10.1046/j.1365-313X.2002.01279.x PubMedCrossRefGoogle Scholar
  38. Peret B, Swarup K, Ferguson A, Seth M, Yang Y, Dhondt S, James N, Casimiro I, Perry P, Syed A, Yang H, Reemmer J, Venison E, Howells C, Perez-Amador MA, Yun J, Alonso J, Beemster GT, Laplaze L, Murphy A, Bennett MJ, Nielsen E, Swarup R (2012) AUX/LAX genes encode a family of auxin influx transporters that perform distinct functions during Arabidopsis development. Plant Cell 24:2874–2885. doi: 10.1105/tpc.112.097766 PubMedCentralPubMedCrossRefGoogle Scholar
  39. Poethig RS, Szymkowiak EJ (1995) Clonal analysis of leaf development in maize. Maydica 40:67–76Google Scholar
  40. Pozzi C, Rossini L, Agosti F (2001) Patterns and symmetries in leaf development. Semin Cell Dev Biol 12:363–372. doi: 10.1006/scdb.2001.0265 PubMedCrossRefGoogle Scholar
  41. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer EL, Eddy SR, Bateman A, Finn RD (2012) The Pfam protein families database. Nucleic Acids Res 40:D290–301. doi: 10.1093/nar/gkr1065 PubMedCentralPubMedCrossRefGoogle Scholar
  42. Qi J, Qian Q, Bu Q, Li S, Chen Q, Sun J, Liang W, Zhou Y, Chu C, Li X, Ren F, Palme K, Zhao B, Chen J, Chen M, Li C (2008) Mutation of the rice Narrow leaf1 gene, which encodes a novel protein, affects vein patterning and polar auxin transport. Plant Physiol 147:1947–1959. doi: 10.1104/pp. 108.118778 PubMedCentralPubMedCrossRefGoogle Scholar
  43. Rawlings ND, Barrett AJ, Bateman A (2012) MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res 40:D343–350. doi: 10.1093/nar/gkr987 PubMedCentralPubMedCrossRefGoogle Scholar
  44. Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, Bennett M, Traas J, Friml J, Kuhlemeier C (2003) Regulation of phyllotaxis by polar auxin transport. Nature 426:255–260. doi: 10.1038/nature02081 PubMedCrossRefGoogle Scholar
  45. Sarojam R, Sappl PG, Goldshmidt A, Efroni I, Floyd SK, Eshed Y, Bowman JL (2010) Differentiating Arabidopsis shoots from leaves by combined YABBY activities. Plant Cell 22:2113–2130. doi: 10.1105/tpc.110.075853 PubMedCentralPubMedCrossRefGoogle Scholar
  46. Sentoku N, Sato Y, Kurata N, Ito Y, Kitano H, Matsuoka M (1999) Regional expression of the rice KN1-type homeobox gene family during embryo, shoot, and flower development. Plant Cell 11:1651–1663. doi: 10.1105/tpc.11.9.1651 PubMedCentralPubMedGoogle Scholar
  47. Siegfried KR, Eshed Y, Baum SF, Otsuga D, Drews GN, Bowman JL (1999) Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126:4117–4128PubMedGoogle Scholar
  48. Stahle MI, Kuehlich J, Staron L, von Arnim AG, Golz JF (2009) YABBYs and the transcriptional corepressors LEUNIG and LEUNIG_HOMOLOG maintain leaf polarity and meristem activity in Arabidopsis. Plant Cell 21:3105–3118. doi: 10.1105/tpc.109.070458 PubMedCentralPubMedCrossRefGoogle Scholar
  49. Tanaka H, Watanabe M, Sasabe M, Hiroe T, Tanaka T, Tsukaya H, Ikezaki M, Machida C, Machida Y (2007) Novel receptor-like kinase ALE2 controls shoot development by specifying epidermis in Arabidopsis. Development 134:1643–1652. doi: 10.1242/dev.003533 PubMedCrossRefGoogle Scholar
  50. Teale WD, Paponov IA, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7:847–859. doi: 10.1038/nrm2020 PubMedCrossRefGoogle Scholar
  51. Tsuda K, Ito Y, Sato Y, Kurata N (2011) Positive autoregulation of a KNOX gene is essential for shoot apical meristem maintenance in rice. Plant Cell 23:4368–4381. doi: 10.1105/tpc.111.090050 PubMedCentralPubMedCrossRefGoogle Scholar
  52. van der Hoorn RA (2008) Plant proteases: from phenotypes to molecular mechanisms. Annu Rev Plant Biol 59:191–223. doi: 10.1146/annurev.arplant.59.032607.092835 PubMedCrossRefGoogle Scholar
  53. Von Groll U, Berger D, Altmann T (2002) The subtilisin-like serine protease SDD1 mediates cell-to-cell signaling during Arabidopsis stomatal development. Plant Cell 14:1527–1539CrossRefGoogle Scholar
  54. Xu M, Zhu L, Shou H, Wu P (2005) A PIN1 family gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in rice. Plant Cell Physiol 46:1674–1681. doi: 10.1093/pcp/pci183 PubMedCrossRefGoogle Scholar
  55. Yamaguchi T, Nagasawa N, Kawasaki S, Matsuoka M, Nagato Y, Hirano HY (2004) The YABBY gene DROOPING LEAF regulates carpel specification and midrib development in Oryza sativa. Plant Cell 16:500–509. doi: 10.1105/tpc.018044 PubMedCentralPubMedCrossRefGoogle Scholar
  56. Yamaguchi T, Nukazuka A, Tsukaya H (2012) Leaf adaxial–abaxial polarity specification and lamina outgrowth: evolution and development. Plant Cell Physiol 53:1180–1194. doi: 10.1093/pcp/pcs074 PubMedCrossRefGoogle Scholar
  57. Yang P, Smalle J, Lee S, Yan N, Emborg TJ, Vierstra RD (2007) Ubiquitin C-terminal hydrolases 1 and 2 affect shoot architecture in Arabidopsis. Plant J 51:441–457. doi: 10.1111/j.1365-313X.2007.03154.x PubMedCrossRefGoogle Scholar
  58. Yoo JH, Park JH, Cho SH, Yoo SC, Li J, Zhang H, Kim KS, Koh HJ, Paek NC (2011) The rice bright green leaf (bgl) locus encodes OsRopGEF10, which activates the development of small cuticular papillae on leaf surfaces. Plant Mol Biol 77:631–641. doi: 10.1007/s11103-011-9839-0 PubMedCrossRefGoogle Scholar
  59. Yoo SC, Cho SH, Sugimoto H, Li J, Kusumi K, Koh HJ, Iba K, Paek NC (2009) Rice virescent3 and stripe1 encoding the large and small subunits of ribonucleotide reductase are required for chloroplast biogenesis during early leaf development. Plant Physiol 150:388–401. doi: 10.1104/pp. 109.136648 PubMedCentralPubMedCrossRefGoogle Scholar
  60. Zazimalova E, Murphy AS, Yang H, Hoyerova K, Hosek P (2010) Auxin transporters—why so many? Cold Spring Harb Perspect Biol 2:a001552. doi: 10.1101/cshperspect.a001552 PubMedCrossRefGoogle Scholar
  61. Zhang GH, Xu Q, Zhu XD, Qian Q, Xue HW (2009) SHALLOT-LIKE1 is a KANADI transcription factor that modulates rice leaf rolling by regulating leaf abaxial cell development. Plant Cell 21:719–735. doi: 10.1105/tpc.108.061457 PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Sung-Hwan Cho
    • 1
  • Soo-Cheul Yoo
    • 1
  • Haitao Zhang
    • 1
  • Jung-Hyun Lim
    • 1
  • Nam-Chon Paek
    • 1
    • 2
    Email author
  1. 1.Department of Plant Science, Plant Genomics and Breeding Institute, and Research Institute for Agriculture and Life SciencesSeoul National UniversitySeoulRepublic of Korea
  2. 2.Institute of Green Bio Science and TechnologySeoul National UniversityPyeongchangRepublic of Korea

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