Control of rice embryo development, shoot apical meristem maintenance, and grain yield by a novel cytochrome P450

Molecular Plant

Volumn 6, Issue 6, 2013, Pages 1945-1960

  Yang, Weibing ^a   Gao, Mingjun ^a   Yin, Xin ^a   Liu, Jiyun ^b   Xu, Yonghan ^c   Zeng, Longjun ^a   Li, Qun ^a   Zhang, Shubiao ^d   Wang, Junmin ^b   Zhang, Xiaoming ^b   He, Zuhua ^a  

^a INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

^b INSTITUTE OF PLANT PROTECTION AND MICROBIOLOGY   (China)

^c ZHEJIANG A F UNIVERSITY   (China)

^d FUJIAN AGRICULTURE AND FORESTRY UNIVERSITY   (China)

Author keywords

Cytochrome P450; Embryo; Endosperm; Grain yield; Rice; Shoot apical meristem

Indexed keywords

CYTOCHROME P450;

ARTICLE; CELL PROLIFERATION; EMBRYO; ENDOPLASMIC RETICULUM; ENDOSPERM; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GRAIN YIELD; GROWTH, DEVELOPMENT AND AGING; MERISTEM; METABOLISM; MOLECULAR CLONING; MORPHOGENESIS; PLANT SEED; PRENATAL DEVELOPMENT; RICE; RICE.; SHOOT APICAL MERISTEM;

CYTOCHROME P450; EMBRYO; ENDOSPERM; GRAIN YIELD; RICE.; SHOOT APICAL MERISTEM;

CELL PROLIFERATION; CLONING, MOLECULAR; CYTOCHROME P-450 ENZYME SYSTEM; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; MERISTEM; MORPHOGENESIS; ORYZA SATIVA; SEEDS;

EID: 84891912590     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/sst107     Document Type: Article

References (71)

1. Aichinger, E., Kornet, N., Friedrich, T., and Laux, T. (2012). Plant stem cell niches. Annu. Rev. Plant Biol. 63, 615-636.
2. Anastasiou, E., Kenz, S., Gerstung, M., MacLean, D., Timmer, J., Fleck, C., and Lenhard, M. (2007). Control of plant organ size by KLUH/CYP78A5- dependent intercellular signaling. Dev. Cell. 13, 843-856.
3. Bart, R., Chern, M., Park, C.J., Bartley, L., and Ronald, P.C. (2006). A novel system for gene silencing using siRNAs in rice leaf and stem-derived protoplasts. Plant Methods. 2, 13.
4. Baud, S., Wuilleme, S., Lemoine, R., Kronenberger, J., Caboche, M., Lepiniec, L., and Rochat, C. (2005). The AtSUC5 sucrose transporter specifically expressed in the endosperm is involved in early seed development in Arabidopsis. Plant J. 43, 824-836.
5. Benkova, E., Michniewicz, M., Sauer, M., Teichmann, T., Seifertova, D., Jurgens, G., and Friml J. (2003). Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell. 115, 591-602.
6. Brand, U., Fletcher, J.C., Hobe, M., Meyerowitz, E.M., and Simon, R. (2000). Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science. 289, 617-619.
7. Breuninger, H., Rikirsch, E., Hermann, M., Ueda, M., and Laux, T. (2008). Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Dev. Cell. 14, 867-876.
8. Dresselhaus, T. (2006). Cell-cell communication during double fertilization. Curr. Opin. Plant Biol. 9, 41-47.
9. Fan, C., Xing, Y., Mao, H., Lu, T., Han, B., Xu, C., Li, X., and Zhang, Q. (2006). GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein. Theor. Appl. Genet. 112, 1164-1171.
10. Fang, W., Wang, Z., Cui, R., Li, J., and Li, Y. (2012). Maternal control of seed size by EOD3/CYP78A6 in Arabidopsis thaliana. Plant J. 70, 929-939.
11. Fincher, G.B. (1989). Molecular and cellular biology associated with endosperm mobilization in germinating cereal grains. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 305-346.
12. Fiume, E., and Fletcher, J.C. (2012). Regulation of Arabidopsis embryo and endosperm development by the polypeptide signaling molecule CLE8. Plant Cell. 24, 1000-1012.
13. Friml, J., Vieten, A., Sauer, M., Weijers, D., Schwarz, H., Hamann, T., Offringa, R., and Jurgens, G. (2003). Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature. 426, 147-153.
14. Garcia, D., Fitz Gerald, J.N., and Berger, F. (2005). Maternal control of integument cell elongation and zygotic control of endosperm growth are coordinated to determine seed size in Arabidopsis. Plant Cell. 17, 52-60.
15. Geldner, N., Anders, N., Wolters, H., Keicher, J., Kornberger, W., Muller, P., Delbarre, A., Ueda, T., Nakano, A., and Jurgens, G. (2003). The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell. 112, 219-230.
16. Guo, J., Wang, F., Song, J., Sun, W., and Zhang, X.S. (2010). The expression of Orysa;CycB1;1 is essential for endosperm formation and causes embryo enlargement in rice. Planta. 231, 293-303.
17. Hamann, T., Benkova, E., Baurle, I., Kientz, M., and Jurgens, G. (2002). The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes Dev. 16, 1610-1615.
18. Hehenberger, E., Kradolfer, D., and Köhler, C. (2012). Endosperm cellularization defines an important developmental transition for embryo development. Development. 139, 2031-2039.
19. Helliwell, C.A., Chin-Atkins, A.N., Wilson, I.W., Chapple, R., Dennis, E.S., and Chaudhury, A. (2001). The Arabidopsis AMP1 gene encodes a putative glutamate carboxypeptidase. Plant Cell. 13, 2115-2125.
20. Hirose, T., Imaizumi, N., Scofield, G.N., Furbank, R.T., and Ohsugi, R. (1997). cDNA cloning and tissue specific expression of a gene for sucrose transporter from rice (Oryza sativa L.). Plant Cell Physiol. 38, 1389-1396.
21. Hong, S.K., Aoki, T., Kitano, H., Satoh, H., and Nagato, Y. (1995). Phenotypic diversity of 188 rice embryo mutants. Dev. Genet. 16, 298-310.
22. Hong, S.K., Kitano, H., Satoh, H., and Nagato, Y. (1996). How is embryo size genetically regulated in rice? Development. 122, 2051-2058.
23. Honga, S.K., Aokia, T., Kitanob, H., Satohc, H., and Nagato, Y. (1995). Temperature-sensitive mutation, embryoless 1, affects both embryo and endosperm development in rice. Plant Sci. 108, 165-172.
24. Imaishi, H., Matsuo, S., Swai, E., and Ohkawa, H. (2000). CYP78A1 preferentially expressed in developing inflorescences of Zea mays encoded acytochrome P450-dependent lauric acid 12-monooxygenase. Biosci. Biotechnol. Biochem. 64, 1696-1701.
25. Ito, T., and Meyerowitz, E.M. (2000). Overexpression of a gene encoding a cytochrome P450, CYP78A9, induces large and seedless fruit in Arabidopsis. Plant Cell. 12, 1541-1550.
26. Itoh, J.I., Kitano, H., Matsuoka, M., and Nagato, Y. (2000). SHOOT ORGANIZATION genes regulate shoot apical meristem organization and the pattern of leaf primordium initiation in rice. Plant Cell. 12, 2161-2174.
27. Itoh, J.I., Nonomura, K., Ikeda, K., Yamaki, S., Inukai, Y., Yamagishi, H., Kitano, H., and Nagato, Y. (2005). Rice plant development: From zygote to spikelet. Plant Cell Physiol. 46, 23-47.
28. Jiao, Y., Wang, Y., Xue, D., Wang, J., Yan, M., Liu, G., Dong, G., Zeng, D., Lu, Z., Zhu, X., et al. (2010). Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat. Genet. 42, 541-544.
29. Jofuku, K.D., Omidyar, P.K., Gee, Z., and Okamuro, J.K. (2005). Control of seed mass and seed yield by the floral homeotic gene APETALA2. Proc. Natl Acad. Sci. U S A. 102, 3117-3122.
30. Jurgens, G. (2001). Apical-basal pattern formation in Arabidopsis embryogenesis. EMBO J. 20, 3609-3616.
31. Kai, K., Hashidzume, H., Yoshimura, K., Suzuki, H., Sakurai, N, Shibata, D., and Ohta, D. (2009). Metabolomics for the characterization of cytochromes P450-dependent fatty acid hydroxylation reactions in Arabidopsis. Plant Biotechnol. 26, 175-182.
32. Kaneko, M., Itoh, H., Inukai, Y., Sakamoto, T., Ueguchi-Tanaka, M., Ashikari, M., and Matsuoka, M. (2003). Where do gibberellin biosynthesis and gibberellin signaling occur in rice plants? Plant J. 35, 104-115.
33. Kawakatsu, T., Taramino, G., Itoh, J., Allen, J., Sato, Y., Hong, S.K., Yule, R., Nagasawa, N., Kojima, M., Kusaba, M., et al. (2009). PLASTOCHRON3/GOLIATH encodes a glutamate carboxypeptidase required for proper development in rice. Plant J. 58, 1028-1040.
34. Lau, S., Slane, D., Herud, O., Kong, J., and Jürgens, G. (2012). Early embryogenesis in flowering plants: Setting up the basic body pattern. Annu. Rev. Plant Biol. 63, 483-506.
35. Li, S., Liu, L., Zhuang, X., Yu, Y., Liu, X., Cui, X., Ji, L., Pan, Z., Cao, X., Mo, B., et al. (2013). MicroRNAs inhibit the translation of target mRNAs on the endoplasmic reticulum in Arabidopsis. Cell. 153, 562-574.
36. Li, Y., Fan, C., Xing, Y., Jiang, Y., Luo, L., Sun, L., Shao, D., Xu, C., Li, X., Xiao, J., et al. (2011). Natural variation in GS5 plays an important role in regulating grain size and yield in rice. Nat. Genet. 43, 1266-1269.
37. Li, Y., Zheng, L., Corke, F., Smith, C., and Bevan, M.W. (2008). Control of final seed and organ size by the DA1 gene family in Arabidopsis thaliana. Genes Dev. 22, 1331-1336.
38. Lukowitz, W., Roeder, A., Parmenter, D., and Somerville, C. (2004). A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis. Cell. 116, 109-119.
39. Luo, M., Dennis, E.S., Berger, F., Peacock, W.J., and Chaudhury, A. (2005). MINISEED3 (MINI3), a WRKY family gene, and HAIKU2 (IKU2), a leucine-rich repeat (LRR) KINASE gene, are regulators of seed size in Arabidopsis. Proc. Natl Acad. Sci. U S A. 102, 17531-17536.
40. Miura, K., Ikeda, M., Matsubara, A., Song, X.J., Ito, M., Asano, K., Matsuoka, M., Kitano, H., and Ashikari, M. (2010). OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat. Genet. 42, 545-549.
41. Miyoshi, K., Ahn, B.O., Kawakatsu, T., Ito, Y., Itoh, J., Nagato, Y., and Kurata, N. (2004). PLASTOCHRON1, a timekeeper of leaf initiation in rice, encodes cytochrome P450. Proc. Natl Acad. Sci. U S A. 101, 875-880.
42. Mizutani, M., and Ohta, D. (2010). Diversification of P450 genes during land plant evolution. Annu. Rev. Plant Biol. 61, 291-315.
43. Nagasaki, H., Itoh, J., Hayashi, K., Hibara, K., Satoh-Nagasawa, N., Nosaka, M., Mukouhata, M., Ashikari, M., Kitano, H., Matsuoka, M., et al. (2007). The small interfering RNA production pathway is required for shoot meristem initiation in rice. Proc. Natl Acad. Sci. U S A. 104, 14867-14871.
44. Nagasawa, N., Hibara, K.I., Heppard, E.P., Vander Velden, K.A., Luck, S., Beatty, M., Nagato, Y., and Sakai, H. (2013). GIANT EMBRYO, encoding CYP78A13, affects size balance between embryo and endosperm in rice. Plant J., 29, 10.1111/tpj.12223.
45. Nowack, M.K., Grini, P.E., Jakoby, M.J., Lafos, M., Koncz, C., and Schnittger, A. (2006). A positive signal from the fertilization of the egg cell sets off endosperm proliferation in angiosperm embryogenesis. Nat. Genet. 38, 63-67.
46. Ohmori, Y., Tanaka, W., Kojima, M., Sakakibara, H., and Hirano HY. (2013). WUSCHEL-RELATED HOMEOBOX4 is involved in meristem maintenance and is negatively regulated by the CLE gene FCP1 in rice. Plant Cell. 25, 229-241.
47. Pollard, M., Beisson, F., Li, Y., and Ohlrogge, J.B. (2008). Building lipid barriers: Biosynthesis of cutin and suberin. Trends Plant Sci. 13, 236-246.
48. Qi, P., Lin, Y.S., Song, X.J., Shen, J.B., Huang, W., Shan, J.X., Zhu, M.Z., Jiang, L., Gao, J.P., and Lin, H.X. (2012). The novel quantitative trait locus GL3.1 controls rice grain size and yield by regulating Cyclin-T1;3. Cell Res. 22, 1666-1680.
49. Qian, Q., Xiong, Z.M., Min, S.K., and Zhu, L.H. (1996). The RFLP of tagging of giant embryo gene. Chinese J. Rice Sci. 10, 65-70.
50. Sato, Y., Hong, S.K., Tagiri, A., Kitano, H., Yamamoto, N., Nagato, Y., and Matsuoka, M. (1996). A rice homeobox gene, OSH1, is expressed before organ differentiation in a specific region during early embryogenesis. Proc. Natl Acad. Sci. U S A. 93, 8117-8122.
51. Sazuka, T., Kamiya, N., Nishimura, T., Ohmae, K., Sato, Y., Imamura, K., Nagato, Y., Koshiba, T., Nagamura, Y., Ashikari, M., et al. (2009). A rice tryptophan deficient dwarf mutant, tdd1, contains a reduced level of indole acetic acid and develops abnormal flowers and organless embryos. Plant J. 60, 227-241.
52. Schoof, H., Lenhard, M., Haecker, A., Mayer, K.F.X., Jürgens, G., and Laux, T. (2000). The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell. 100, 635-644.
53. Schreiber, L. (2010). Transport barriers made of cutin, suberin and associated waxes. Trends Plant Sci. 15, 546-553.
54. Schruff, M.C., Spielman, M., Tiwari, S., Adams, S., Fenby, N., and Scott, R.J. (2006). The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs. Development. 133, 251-261.
55. Song, X.J., Huang, W., Shi, M., Zhu, M.Z., and Lin, H.X. (2007). A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat. Genet. 39, 623-630.
56. Sotelo-Silveira, M., Cucinotta, M., Chauvin, A.L., Chávez Montes, R.A., Colombo, L., Marsch-Martínez, N., and de Folter, S. (2013). Cytochrome P450 CYP78A9 is involved in Arabidopsis reproductive development. Plant Physiol. 162, 779-799.
57. Tanaka, H., Onouchi, H., Kondo, M., Hara-Nishimura, I., Nishimura, M., Machida, C., and Machida, Y. (2001). A subtilisin-like serine protease is required for epidermal surface formation in Arabidopsis embryos and juvenile plants. Development. 128, 4681-4689.
58. Tanaka, H., Watanabe, M., Sasabe, M., Hiroe, T., Tanaka, T., Tsukaya, H., Ikezaki, M., Machida, C., and Machida, Y. (2007). Novel receptor-like kinase ALE2 controls shoot development by specifying epidermis in Arabidopsis. Development. 134, 1643-1652.
59. Tanaka, H., Watanabe, M., Watanabe, D., Tanaka, T., Machida, C., and Machida, Y. (2002). ACR4, a putative receptor kinase gene of Arabidopsis thaliana, that is expressed in the outer cell layers of embryos and plants, is involved in proper embryogenesis. Plant Cell Physiol. 43, 419-428.
60. Tanksley, S.D., and McCouch, S.R. (1997). Seed banks and molecular maps: Unlocking genetic potential from the wild. Science. 277, 1063-1066.
61. Ueda, M., Zhang, Z., and Laux, T. (2011). Transcriptional activation of Arabidopsis axis patterning genes WOX8/9 links zygote polarity to embryo development. Dev. Cell. 20, 264-270.
62. Wang, E., Wang, J., Zhu, X., Hao, W., Wang, L., Li, Q., Zhang, L., He, W., Lu, B., Lin, H., et al. (2008a). Control of rice grain-filling and yield by a gene with a potential signature of domestication. Nat. Genet. 40, 1370-1374.
63. Wang, J.W., Schwab, R., Czech, B., Mica, E., and Weigel, D. (2008b). Dual effects of miR156-targeted SPL genes and CYP78A5/KLUH on plastochron length and organ size in Arabidopsis thaliana. Plant Cell. 20, 1231-1243.
64. Wang, S., Wu, K., Yuan, Q., Liu, X., Liu, Z., Lin, X., Zeng, R., Zhu, H., Dong, G., Qian, Q., et al. (2012). Control of grain size, shape and quality by OsSPL16 in rice. Nat. Genet. 44, 950-954.
65. Weng, J., Gu, S., Wan, X., Gao, H., Guo, T., Su, N., Lei, C., Zhang, X., Cheng, Z., Guo, X., et al. (2008). Isolation and initial characterization of GW5, a major QTL associated with rice grain width and weight. Cell Res. 18, 1199-1209.
66. Yang, W., Ren, S., Zhang, X., Gao, M., Ye, S., Qi, Y., Zheng, Y., Wang, J., Zeng, L., Li, Q., et al. (2011). BENT UPPERMOST INTERNODE1 encodes the class II formin FH5 crucial for actin organization and rice development. Plant Cell. 23, 661-680.
67. Yano, M. (2001). Genetic and molecular dissection of naturally occurring variation. Curr. Opin. Plant Biol. 4, 130-135.
68. Yephremov, A., Wisman, E., Huijser, P., Huijser, C., Wellesen, K., and Saedler, H. (1999). Characterization of the FIDDLEHEAD gene of Arabidopsis reveals a link between adhesion response and cell differentiation in the epidermis. Plant Cell. 11, 2187-2201.
69. Zhang, L.L., Shu, X.L., Wang, X.Y., Lu, H.J., Shu, Q.Y., and Wu, D.X. (2007). Characterization of indica-type giant embryo mutant rice enriched with nutritional components. Cereal Res. Commun. 35, 1459-1468.
70. Zhou, S.R., Yin, L.L., and Xue, H.W. (2013). Functional genomics based understanding of rice endosperm. Curr. Opin. Plant Biol. 16, 236-246.
71. Zondlo, S.C., and Irish, V.F. (1999). CYP78A5 encodes a cytochrome P450 that marks the shoot apical meristem boundary in Arabidopsis. Plant J. 19, 259-268.