Characterization of a null allelic mutant of the rice NAL1 gene reveals its role in regulating cell division

PLoS ONE

Volumn 10, Issue 2, 2015, Pages

  Jiang, Dan ^a,b   Fang, Jingjing ^b   Lou, Lamei ^b   Zhao, Jinfeng ^b   Yuan, Shoujiang ^c   Yin, Liang ^c   Sun, Wei ^c   Peng, Lixiang ^b   Guo, Baotai ^a   Li, Xueyong ^b  

^a QINGDAO AGRICULTURAL UNIVERSITY   (China)

^b INSTITUTE OF PLANT PROTECTION   (China)

^c Shandong Rice Research Institute   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL DIVISION; CELL SIZE; CONTROLLED STUDY; CULTIVAR; EXON; GENE; GENE EXPRESSION; GRAIN YIELD; INTERNODE; LEAF DEVELOPMENT; LEAF GROWTH; LEAF MIDRIB; LEAF MORPHOLOGY; NAL1 2 GENE; NAL1 3 GENE; NAL1 GENE; NONHUMAN; NULL ALLELE; PHENOTYPE; PLANT GENETICS; PLANT LEAF; RICE; SHOOT; ALLELE; CELL CYCLE; CYTOLOGY; GENE EXPRESSION REGULATION; GENE ORDER; GENETICS; GROWTH, DEVELOPMENT AND AGING; MOLECULAR CLONING; MUTATION; ORYZA; PLANT ROOT;

SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

PLANT PROTEIN;

ALLELES; CELL CYCLE; CELL DIVISION; CLONING, MOLECULAR; GENE EXPRESSION REGULATION, PLANT; GENE ORDER; MUTATION; ORYZA; PHENOTYPE; PLANT LEAVES; PLANT PROTEINS; PLANT ROOTS;

EID: 84922611449     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0118169     Document Type: Article

References (53)

1. Lyndon RF, Cunninghame ME (1986) Control of shoot apical development via cell division. Symp Soc Exp Biol 40: 233-255. PMID: 3544304
2. Reinhardt D, Mandel T, Kuhlemeier C (2000) Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12: 507-518. PMID: 10760240
3. Fleming A, McQueen-Mason S, Mandel T, Kuhlemeier C (1997) Induction of leaf primordia by the cell wall protein expansion. Science 276: 1415-1418.
4. Bowman JL, Eshed Y, Baum SF (2002) Establishment of polarity in angiosperm lateral organs. Trends Genet 18: 134-141. PMID: 11858837
5. Gonzalez N, Vanhaeren H, Inze D (2012) Leaf size control: complex coordination of cell division and expansion. Trends Plant Sci 17: 332-340. doi: 10.1016/j.tplants.2012.02.003 PMID: 22401845
6. Narita NN, Moore S, Horiguchi G, Kubo M, Demura T, et al. (2004) Overexpression of a novel small peptide ROTUNDIFOLIA4 decreases cell proliferation and alters leaf shape in Arabidopsis thaliana. Plant J 38: 699-713. PMID: 15125775
7. Lee BH, Ko JH, Lee S, Lee Y, Pak JH, et al. (2009) The Arabidopsis GRF-INTERACTING FACTOR gene family performs an overlapping function in determining organ size as well as multiple developmental properties. Plant Physiol 151: 655-668. doi: 10.1104/pp.109.141838 PMID: 19648231
8. Eloy NB, de Freitas Lima M, Van Damme D, Vanhaeren H, Gonzalez N, et al. (2011) The APC/C subunit 10 plays an essential role in cell proliferation during leaf development. Plant J 68: 351-363. doi: 10.1111/j.1365-313X.2011.04691.x PMID: 21711400
9. Kim JH, Choi D, Kende H (2003) The AtGRF family of putative transcription factors is involved in leaf and cotyledon growth in Arabidopsis. Plant J 36: 94-104. PMID: 12974814
10. Smith LG (2001) Plant cell division: building walls in the right places. Nat Rev Mol Cell Biol 2: 33-39. PMID: 11413463
11. Errera L (1888) Über Zellformen und Siefenblasen. Botanisches Centralblatt 34: 395-399.
12. Lewis D, Bacic A, Chandler PM, Newbigin EJ (2009) Aberrant cell expansion in the elongation mutants of barley. Plant Cell Physiol 50: 554-571. doi: 10.1093/pcp/pcp015 PMID: 19181700
13. Chandler PM, Robertson M (1999) Gibberellin dose-response curves and the characterization of dwarf mutants of barley. Plant Physiol 120: 623-632. PMID: 10364415
14. Kessler S, Seiki S, Sinha N (2002) Xcl1 causes delayed oblique periclinal cell divisions in developing maize leaves, leading to cellular differentiation by lineage instead of position. Development 129: 1859-1869. PMID: 11934852
15. De Rybel B, Moller B, Yoshida S, Grabowicz I, Barbier de Reuille P, et al. (2013) A bHLH complex controls embryonic vascular tissue establishment and indeterminate growth in Arabidopsis. Dev Cell 24: 426-437. doi: 10.1016/j.devcel.2012.12.013 PMID: 23415953
16. Cho S, Yoo S, Zhang H, Lim J, Paek N (2014) Rice NARROW LEAF1 regulates leaf and adventitious root development. Plant Molecular Biology Reporter 32: 270-281.
17. Qi J, Qian Q, Bu Q, Li S, Chen Q, et al. (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 PMID: 18562767
18. Chen M, Luo J, Shao G, Wei X, Tang S, et al. (2012) Fine mapping of a major QTL for flag leaf width in rice, qFLW4, which might be caused by alternative splicing of NAL1. Plant Cell Rep 31: 863-872. doi: 10.1007/s00299-011-1207-7 PMID: 22179305
19. Takai T, Adachi S, Taguchi-Shiobara F, Sanoh-Arai Y, Iwasawa N, et al. (2013) A natural variant of NAL1, selected in high-yield rice breeding programs, pleiotropically increases photosynthesis rate. Sci Rep 3: 2149. doi: 10.1038/srep02149 PMID: 23985993
20. Fujita D, Trijatmiko KR, Tagle AG, Sapasap MV, Koide Y, et al. (2013) NAL1 allele from a rice landrace greatly increases yield in modern indica cultivars. Proc Natl Acad Sci U S A 110: 20431-20436. doi: 10.1073/pnas.1310790110 PMID: 24297875
21. Zhang GH, Li SY, Wang L, Ye WJ, Zeng DL, et al. (2014) LSCHL4 from Japonica Cultivar, which is allelic to NAL1, increases yield of indica super rice 93-11. Mol Plant 7: 1350-1364. doi: 10.1093/mp/ ssu055 PMID: 24795339
22. Yoshikawa T, Eiguchi M, Hibara K, Ito J, Nagato Y (2013) Rice slender leaf 1 gene encodes cellulose synthase-like D4 and is specifically expressed in M-phase cells to regulate cell proliferation. J Exp Bot 64: 2049-2061. doi: 10.1093/jxb/ert060 PMID: 23519729
23. Maundrell K (1990) nmt1 of fission yeast. A highly transcribed gene completely repressed by thiamine. J Biol Chem 265: 10857-10864. PMID: 2358444
24. Cebolla A, Vinardell JM, Kiss E, Olah B, Roudier F, et al. (1999) The mitotic inhibitor ccs52 is required for endoreduplication and ploidy-dependent cell enlargement in plants. EMBO J 18: 4476-4484. PMID: 10449413
25. Takada S, Takada N and Yoshida A (2013) ATML1 promotes epidermal cell differentiation in Arabidopsis shoots. Development 140: 1919-1923. doi: 10.1242/dev.094417 PMID: 23515472
26. Howell S (1998) Molecular Genetics of Plant Development. Cambridge University Press, Cambridge, UK. PMID: 25506963
27. Lyndon R (1998) The Shoot Apical Meristem: Its Growth and Development. Cambridge University Press, Cambridge, UK. PMID: 25506963
28. De Veylder L, Beeckman T, Beemster GT, Krols L, Terras F, et al. (2001) Functional analysis of cyclindependent kinase inhibitors of Arabidopsis. Plant Cell 13: 1653-1668. PMID: 11449057
29. Nelson T and Dengler N (1997) Leaf Vascular Pattern Formation. Plant Cell 9: 1121-1135. PMID: 12237378
30. Scarpella E, Rueb S, Meijer AH (2003) The RADICLELESS1 gene is required for vascular pattern formation in rice. Development 130: 645-658. PMID: 12505996
31. Fabian-Marwedel T, Umeda M, Sauter M (2002) The rice cyclin-dependent kinase-activating kinase R2 regulates S-phase progression. Plant Cell 14: 197-210. PMID: 11826308
32. Zhao SQ, Hu J, Guo LB, Qian Q, Xue HW (2010) Rice leaf inclination2, a VIN3-like protein, regulates leaf angle through modulating cell division of the collar. Cell Res 20: 935-947. doi: 10.1038/cr.2010. 109 PMID: 20644566
33. Renaudin JP, Doonan JH, Freeman D, Hashimoto J, Hirt H, et al. (1996) Plant cyclins: a unified nomenclature for plant A-, B- and D-type cyclins based on sequence organization. Plant Mol Biol 32: 1003-1018. PMID: 9002599
34. Sauter M (1997) Differential expression of a CAK (cdc2-activating kinase)-like protein kinase, cyclins and cdc2 genes from rice during the cell cycle and in response to gibberellin. Plant J 11: 181-190. PMID: 9076986
35. Colon-Carmona A, You R, Haimovitch-Gal T, Doerner P (1999) Technical advance: spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. Plant J 20: 503-508. PMID: 10607302
36. Genschik P, Criqui MC, Parmentier Y, Derevier A, Fleck J (1998) Cell cycle-dependent proteolysis in plants. Identification Of the destruction box pathway and metaphase arrest produced by the proteasome inhibitor mg132. Plant Cell 10: 2063-2076. PMID: 9836745
37. Guo J, Wang F, Song J, Sun W, Zhang XS (2010) The expression of Orysa;CycB1;1 is essential for endosperm formation and causes embryo enlargement in rice. Planta 231: 293-303. doi: 10.1007/ s00425-009-1051-y PMID: 19921249
38. Galweiler L, Guan C, Muller A, Wisman E, Mendgen K, et al. (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282: 2226-2230. PMID: 9856939
39. Friml J, Wisniewska J, Benkova E, Mendgen K, Palme K (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415: 806-809. PMID: 11845211
40. Zhao Y, Christensen SK, Fankhauser C, Cashman JR, Cohen JD, et al. (2001) A role for flavin monoox-ygenase-like enzymes in auxin biosynthesis. Science 291: 306-309. PMID: 11209081
41. Guilfoyle TJ and Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10: 453-460. PMID: 17900969
42. Bowman JL (2000) The YABBY gene family and abaxial cell fate. Curr Opin Plant Biol 3: 17-22. PMID: 10679447
43. Yamaguchi T, Nagasawa N, Kawasaki S, Matsuoka M, Nagato Y, et al. (2004) The YABBY gene DROOPING LEAF regulates carpel specification and midrib development in Oryza sativa. Plant Cell 16: 500-509. PMID: 14729915
44. Liu H, Wang S, Yu X, Yu J, He X, et al. (2005) ARL1, a LOB-domain protein required for adventitious root formation in rice. Plant J 43:47-56. PMID: 15960615
45. Liu S, Wang J, Wang L, Wang X, Xue Y, et al. (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 PMID: 19546891
46. Kitomi Y, Ito H, Hobo T, Aya K, Kitano H, et al. (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 PMID: 21481033
47. Dhondt S, Coppens F, De Winter F, Swarup K, Merks RM, et al. (2010) SHORT-ROOT and SCARECROW regulate leaf growth in Arabidopsis by stimulating S-phase progression of the cell cycle. Plant Physiol 154: 1183-1195. doi: 10.1104/pp.110.158857 PMID: 20739610
48. Rasmussen CG, Humphries JA, Smith LG (2011) Determination of symmetric and asymmetric division planes in plant cells. Annu Rev Plant Biol 62: 387-409. doi: 10.1146/annurev-arplant-042110-103802 PMID: 21391814
49. Autran D, Jonak C, Belcram K, Beemster GT, Kronenberger J, et al. (2002) Cell numbers and leaf development in Arabidopsis: a functional analysis of the STRUWWELPETER gene. EMBO J 21: 6036-6049. PMID: 12426376
50. Scanlon MJ (2003) The polar auxin transport inhibitor N-1-naphthylphthalamic acid disrupts leaf initiation, KNOX protein regulation, and formation of leaf margins in maize. Plant Physiol 133: 597-605. PMID: 14500790
51. Dai M, Hu Y, Zhao Y, Liu H, Zhou DX (2007) A WUSCHEL-LIKE HOMEOBOX gene represses a YABBY gene expression required for rice leaf development. Plant Physiol 144: 380-390. PMID: 17351053
52. Cho SH, Yoo SC, Zhang H, Pandeya D, Koh HJ, et al. (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 PMID: 23551229
53. Nagasawa N, Miyoshi M, Sano Y, Satoh H, Hirano H, et al. (2003) SUPERWOMAN1 and DROOPING LEAF genes control floral organ identity in rice. Development 130: 705-718. PMID: 12506001