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.
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Becraft PW, Li K, Dey N, Asuncion-Crabb Y (2002) The maize dek1 gene functions in embryonic pattern formation and cell fate specification. Development 129:5217–5225
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
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
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
Braybrook SA, Kuhlemeier C (2010) How a plant builds leaves. Plant Cell 22:1006–1018. doi:10.1105/tpc.110.073924
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
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
Clark SE, Jacobsen SE, Levin JZ, Meyerowitz EM (1996) The CLAVATA and SHOOT MERISTEMLESS loci competitively regulate meristem activity in Arabidopsis. Development 122:1567–1575
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
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
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
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
Friml J, Palme K (2002) Polar auxin transport—old questions and new concepts? Plant Mol Biol 49:273–284
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
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 282:2226–2230
Guilfoyle TJ, Hagen G (2001) Auxin response factors. J. Plant Growth Regul 10:281–291
Hedstrom L (2002) Serine protease mechanism and specificity. Chem Rev 102:4501–4524. doi:10.1021/cr000033x
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
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
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
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
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
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
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
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
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
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
Kuroda H, Maliga P (2003) The plastid clpP1 protease gene is essential for plant development. Nature 425:86–89. doi:10.1038/nature01909
Lenhard M, Jurgens G, Laux T (2002) The WUSCHEL and SHOOTMERISTEMLESS genes fulfill complementary roles in Arabidopsis shoot meristem regulation. Development 129:3195–3206
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
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
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
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
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
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
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
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
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
Poethig RS, Szymkowiak EJ (1995) Clonal analysis of leaf development in maize. Maydica 40:67–76
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
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
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
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
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
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
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
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 126:4117–4128
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
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
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
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
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
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 14:1527–1539
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
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
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
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
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
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
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
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
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.
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Sung-Hwan Cho and Soo-Cheul Yoo contributed equally to this work
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Cho, SH., Yoo, SC., Zhang, H. et al. Rice NARROW LEAF1 Regulates Leaf and Adventitious Root Development. Plant Mol Biol Rep 32, 270–281 (2014). https://doi.org/10.1007/s11105-013-0675-z
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DOI: https://doi.org/10.1007/s11105-013-0675-z