Phenotype and transcriptome analysis reveals chloroplast development and pigment biosynthesis together influenced the leaf color formation in mutants of Anthurium andraeanum ‘Sonate’

Frontiers in Plant Science

Volumn 6, Issue MAR, 2015, Pages

  Yang, Yuxia ^a   Chen, Xingxu ^a   Xu, Bin ^a   Li, Yuxia ^a   Ma, Yuehua ^a   Wang, Guangdong ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

Anthurium andraeanum Lind; Chlorophyll; Chloroplasts; Leaf color mutants; Pigment; Transcriptome

Indexed keywords

ANTHURIUM ANDRAEANUM;

EID: 84928032612     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00139     Document Type: Article

References (69)

1. Arnon, D. L. (1949). Copper enzymes in isolated chloroplasts, polyphenol oxidase in Beta vulgaris. PlantPhsiol. 24, 1-15. doi: 10.1104/pp.24.1.1.
2. Britsch, L., and Grisebach, H. (1986). Purification and characterization of (2S)- flavanone 3-hydroxylase from Petunia hybrida. Eur. J. Biochem. 156, 569-577. doi: 10.1111/j.1432-1033.1986.tb09616.x
3. Chen, G., Bi, Y. R., and Li, N. (2005). EGY1 encodes a membrane-associated and ATP-independent metallop rotease that is required for chloroplast development. Plant J.41, 364-375. doi: 10.1111/j.1365-313X.2004.02308.x
4. Chen, W. H., Hsu, C. Y., Cheng, H. Y., Chang, H., Chen, H. H., and Ger, M. J. (2011). Downregulation of putative UDP-glucose: flavonoid 3-O- glucosyltransferase gene alters flower coloring in Phalaenopsis. Plant Cell Rep. 30, 1007-1017. doi: 10.1007/s00299-011-1006-1.
5. Cheung, A. Y., McNellis, T., and Piekos, B. (1993). Maintenance of chloroplast components during chromoplast differentiation in the tomato mutant Green Flesh. Plant Physiol. 101, 1223-1229.
6. Conesa, A., Götz, S., García-Gómez, J. M., Terón, J., Talon, M., and Robles, M. (2005). Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674-3676. doi: 10.1093/bioinformatics/bti610.
7. Duquenne, B., Eeckhaut, T., Werbrouck, S., and van Huylenbroeck, J. (2007). Effect of enzyme concentrations on protoplast isolation and protoplast culture of Spathiphyllum and Anthurium. Plant Cell Tiss Organ. Cult. 91, 165-173. doi: 10.1007/s11240-007-9226-3.
8. Eckhardt, U., Grimm, B., and Hortensteiner, S. (2004). Recent advances in chlorophyll biosynthesis and breakdown in higher plants. Plant Mol. Biol. 56, 1-14. doi: 10.1007/s11103-004-2331-3.
9. Feller, A., Machemer, K., Braun, E. L., and Grotewold, E. (2011). Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J. 66, 94-116. doi: 10.1111/j.1365-313X.2010.04459.x
10. Fitter, D. W., Martin, D. J., Copley, M. J., Scotland, R. W., and Langdale, J. A. (2002). GLK gene pairs regulate chloroplast development in diverse plant species. Plant J. 31, 713-727. doi: 10.1046/j.1365-313X.2002.01390.x
11. Fulgosi, H., Gerdes, L., and Westphal, S. (2002). Cell and chloroplast division requires ARTEMIS. Proc. Natl. Acad. Sci. U.S.A. 99, 11501-11506. doi: 10.1073/pnas.172032599.
12. Gao, H., Kadirjan-Kalbach, D., Froehlich, J. E., and Osteryoung, K. W. (2003). ARC5: a cytosolic dynamin-like protein from plants, is part of the chloro- plast division machinery. Proc. Natl. Acad. Sci. U.S.A. 100, 4328-4333. doi: 10.1073/pnas.0530206100.
13. Gao, H., Sage, T. L., and Osteryoung, K. W. (2006). FZL, an FZO-like protein in plants, is a determinant of thylakoid and chloroplast morphology. Proc. Natl. Acad. Sci. U.S.A. 103,6759-6764. doi: 10.1073/pnas.0507287103.
14. Gomez, C., Terrier, N., Torregrosa, L., Vialet, S., Foumierlevel, A., Verries, C., et al. (2009). Grapevine MATE-Type proteins act as vacuolar H+- dependent acylated anthocyanin transporters. Plant Physiol. 150, 402-415. doi: 10.1104/pp.109.135624.
15. Gong, Z. Z., Yamazaki, M., Sugiyama, M., Tanaka, Y., and Saito, K. (1997). Cloning and molecular analysis of structural genes involved in anthocyanin biosynthesis and expressed in a forma-specific manner in Perilla frutescens. Plant Mol. Biol. 35, 915-927. doi: 10.1023/A:1005959203396.
16. Goodman, C. D., Casati, P., and Walbot, V. (2004). A multidrug resistance- associated protein involved in anthocyanin transport in Zea mays. Plant Cell 16, 1812-1826. doi: 10.1105/tpc.022574.
17. Grabherr, M. G., Haas, B. J., Yassour, M., Levin, J. Z., Thompson, D. A., Amit, I., et al. (2011). Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotech. 29, 644-652. doi: 10.1038/nbt.1883.
18. Hall, L. H., Rossini, L., Cribb, L., and Langdale, J. A. (1998). GOLDEN2: a novel transcriptional regulator of cellular differentiation in the maize leaf. Plant Cell 10, 925-936. doi: 10.1105/tpc.10.6.925.
19. Han, C., Coe, E. D. Jr., and Martienssen, R. A. (1992). Molecular cloning and characterization of iojap (ij), a pattern striping gene of maize. EMBO J. 11, 4037-4046.
20. Harris, W. M., and Spurr, A. R. (1969a). Chromoplasts of tomato fruits. I. Ultrastructure of low-pigment and high-beta mutants. Carotene analyses. Am. J. Bot. 56, 369-379.
21. Harris, W. M., and Spurr, A. R. (1969b). Chromoplasts of tomato fruits. II. The red tomato. Am. J. Bot. 56, 380-389.
22. Haswell, E. S., and Meyerowitz, E. M. (2006). MscS-like proteins control plastid size and shape in Arabidopsis thaliana. Curr. Biol. 16, 1-11. doi: 10.1016/j.cub.2005.11.044.
23. Hichri, I., Barrieu, F., Bogs, J., Kappel, C., Delrot, S., and Lauvergeat, V. (2011). Recent advances in the transcriptional regulation of the flavonoid biosynthetic pathway. J. Exp. Bot. 62, 2465-2483. doi: 10.1093/jxb/erq442.
24. Hieber, A. D., Mudalige, J. R. G., and Kuehnle, A. R. (2006). Color genes in the orchid Oncidium Gower Ramsey: identification, expression, and potential genetic instability in an interspecific cross. Planta 223, 521-531. doi: 10.1007/s00425-005-0113-z
25. Holton, T. A., and Cornish, E. C. (1995). Genetics and biochemistry of anthocyanin biosynthesis. Plant Cell 7, 1071-1083. doi: 10.1105/tpc.7.7.1071.
26. Huang, X., and Madan, A. (1999). CAP3: a DNA sequence assembly program. GenomeRes. 9,868-877. doi: 10.1101/gr.9.9.868.
27. Iseli, C., Jongeneel, C. V., and Bucher, P. (1999). “ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in ESTse- quences" in Proceedings of the International Conference on Intelligent Systems for Molecular Biology (Heidelberg), 138-148.
28. Jung, K. H., Hur, J., Ryu, C. H., Choi, Y., Chung, Y. Y., Miyao, A., et al.Characterization of a rice chlorophyll-deficient mutant using the T- DNA gene-trap system. Plant Cell Physiol. 44, 463-472. doi: 10.1093/pcp/pcg064.
29. Kanehisa, M., and Goto, S. (2000). KEGG: kyoto encyclopedia of genes and genomes. NucleicAcids Res. 28, 27-30. doi: 10.1093/nar/28.1.27.
30. Kato, Y., Miura, E., Matsushima, R., and Sakamoto, W. (2007). White leaf sectors in yellow variegated2 are formed by viable cells with undifferentiated plastids. PlantPhysiol. 144, 952-960. doi: 10.1104/pp.107.099002.
31. Koes, R., Verweij, W., and Quattrocchio, F. (2005). Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends Plant Sci. 10, 236-242. doi: 10.1016/j.tplants.2005.03.002.
32. Langdale, J. A., and Kidner, C. A. (1994). Bundle sheath defective, a mutation that disrupts cellular differentiation in maize leaves. Development 120, 673-681.
33. Lewis, D. H., Arathoon, H. S., Huang, S. C., Swinny, E. E., and Funnell, K. A. . Anthocyanin and carotenoid pigments in spathe tissue from selected Zantedeschia hybrids. Acta Hortic. 624, 147-154.
34. Maple, J., and Moller, S. G. (2007). Plastid division: evolution, mechanism and complexity. Ann. Bot. 99, 565-579. doi: 10.1093/aob/mcl249.
35. Marrs, K. A., Alfenito, M. R., Lloyd, A. M., and Walbot, V. (1995). A glutathione S-transferase involved in vacuolar transfer encoded by the maize gene Bronze-2. Nature 375, 397-400. doi: 10.1038/375397a0.
36. Meyer, P., Heidmann, I., Forkmann, G., and Saedler, H. (1987). A new petunia flower colour generated by transformation of a mutant with a maize gene. Nature 330, 677-678. doi: 10.1038/330677a0.
37. Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L., and Wold, B. (2008). Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Meth. 5, 621-628. doi: 10.1038/nmeth.1226.
38. Motohashi, R., Ito, T., Kobayashi, M., Taji, T., Nagata, N., Asami, T., et al. (2003). Functional analysis of the 37kD inner envelope membrane polypeptide in chloroplast biogenesis using a Dstagged Arabidopsis pale-green mutant. Plant J. 34, 719-731. doi: 10.1046/j.1365-313X.2003.01763.x
39. Mullet, J. E. (1993). Dynamie regulation of Chloroplast transcription. PlantPhysiol. 103, 309-313. doi: 10.1104/pp.103.2.309.
40. Osteryoung, K. W., and Nunnari, J. (2003). The division of endosymbiotic organelles. Science 302, 1698-1704. doi: 10.1126/science.1082192.
41. Pan, Y., Bradley, G., Pyke, K., Ball, G., Lu, C., Fray, R., et al. (2013). Network inference analysis identifies an APRR2-Like gene linked to pigment accumulation in Tomato and Pepper fruits. Plant Physiol. 161, 1476-1485. doi: 10.1104/pp.112.212654.
42. Pelletier, M. K., and Shirley, B. W. (1996). Analysis of flavanone 3-hydroxylase in arabidopsis seedlings (Coordinate regulation with chalcone synthase and chalcone isomerase). Plant Physiol. 111, 339-345. doi: 10.1104/pp.111.1.339
43. Pourcel, L., Irani, N. G., Lu, Y., Riedl, K., Schwartz, S., and Grotewold, E. (2010). The formation of anthocyanic vacuolar inclusions in Arabidopsis thaliana and implications for the sequestration of anthocyanin pigments. Mol. Plant 3, 78-90. doi: 10.1093/mp/ssp071.
44. Pyke, K. A., and Leech, R. M. (1994). A genetic analysis of chloroplast division and expansion in Arabidopsis thaliana. PlantPhysiol. 104, 201-207.
45. Pyke, K. A., Rutherford, S. M., Robertson, E. J., and Leech, R. M. (1994). arc6, a fertile Arabidopsis mutant with only two mesophyll cell chloroplasts. Plant Physiol. 106, 1161-1177.
46. Rismani, Y. H., Haznedaroglu, B., Bibby, K., and Peccia, J. (2011). Transcriptome sequencing and annotation of the microalgae Dunaliella tertiolecta: pathway description and gene discovery for production of next-generation biofuels. BMC Genomics 12:148. doi: 10.1186/1471-2164-12-148.
47. Romualdi, C., Bortoluzzi, S., d'Alessi, F., and Danieli, G. A. (2003). IDEG6: a web tool for detection of differentially expressed genes in multiple tag sampling experiments. Physiol. Genomics 12, 159-162. doi: 10.1152/physiolge-nomics.00096.2002
48. Rossini, L., Cribb, L., Martin, D. J., and Langdale, J. A. (2001). The maize Golden2 gene defines a novel class of transcriptional regulators in plants. Plant Cell 13, 1231-1224. doi: 10.1105/tpc.13.5.1231.
49. Rosso, S. W. (1968). The ultrastructure of chromoplast development in red tomatoes. J. Ultrastruct. Res. 25, 307-322. doi: 10.1016/S0022-5320(68)80076-0.
50. Seitz, C., Vitten, M., Steinbach, P., Hartl, S., Hirsche, J., Rathje, W., et al. (2007). Redirection of anthocyanin synthesis in Osteospermum hybrida by a two-enzyme manipulation strategy. Phytochemistry 68, 824-833. doi: 10.1016/j.phytochem.2006.12.012.
51. Shimada, H., Koizumi, M., Kuroki, K., Mochizuki, M., Fujimoto, H., and Ohta, H. ARC3: a chloroplast division factor, is a chimera of prokaryotic FtsZ and part of eukaryotic phosphatidylinositol-4-phosphate 5-kinase. Plant Cell Physiol. 45, 960-967. doi: 10.1093/pcp/pch130
52. Shirley, B. W., Kubasek, W. L., Storz, G., Bruggenmann, E., Koorneef, M., Ausubel, F. M., et al. (1995). Analysis of arabidopsis mutants deficient in flavonoid biosynthesis. Plant J. 8, 659-671. doi: 10.1046/j.1365-313X.1995.08050659.x
53. Su, C. L., Chao, Y. T., Chang, Y. C. A., Chen, W. C., Chen, C. Y., Lee, A. Y., et al. (2011). De novo assembly of expressed transcripts and global analysis of the Phalaenopsis aphrodite transcriptome. Plant Cell Physiol. 52, 1501-1514. doi: 10.1093/pcp/pcr097
54. Surget-Groba, Y., and Montoya-Burgos, J. I. (2010). Optimization ofde novo tran- scriptome assembly from next-generation sequencing data. Genome Res. 20, 1432-1440. doi: 10.1371/journal.pone.0072516.
55. Tanaka, Y., Sasaki, N., and Ohmiya, A. (2008). Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. Plant J. 54, 733-749. doi: 10.1111/j.1365-313X.2008.03447.x
56. Tian, D. Q., Pan, X. Y., Yu, Y. M., Wang, W. Y., Zhang, F., Ge, Y. Y., et al. (2013). De novo characterization of the Anthurium transcriptome and analysis of its digital gene expression under cold stress. BMC Genomics 14:827. doi: 10.1186/1471-2164-14-827.
57. Tsuda, S., Fukui, Y., Nakamura, N., Katsumoto, Y., Sakakibara, K. Y., Mizu- tani, M. F., et al. (2004). Flower color modification of Petunia hybrida commercial varieties by metabolic engineering. Plant Biotech. 21, 377-386. doi: 10.5511/plantbiotechnology.21.377.
58. Vern, E. C., Paula, E. J., Kathy, E. S., Pathmanathan, U., and Kevin, M. D. Temporal and spatial expression of flavonoid biosynthetic genes in flowers of Anthurium andraeanum. Physiol. Plantarum. 122, 297-304. doi: 10.1111/j.1399-3054.2004.00402.
59. Vitha, S., Froehlich, J. E., Koksharova, O., Pyke, K. A., van Erp H., and Ostery-oung, K. W. (2003). ARC6 is a J-domain plastid division protein and an evolutionary descendant of the cyanobacterial cell division protein Ftn2. Plant Cell 15, 1918-1933. doi: 10.1105/tpc.013292.
60. Wallas, T. R., Smith, M. D., Sanehez-Nieto, S., and Schnell, D. J. (2003). The roles of toc34 and toc75 in targeting the tocl59 preprotein receptor to chloroplasts. J. Biol. Chem. 278, 44289-44297. doi: 10.1074/jbc.M307873200
61. Wang, Y., Sun, G. S., and Wang, G. D. (2011). Optimization of the method on total RNA extraction from the leaf of Anthurium andraeanum. Genomics Applied Biol. 30, 1189-1193. doi: 10.5376/gab.cn.2011.30.0029.
62. Wang, Z., Gerstein, M., and Snyder, M. (2009). RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet. 10, 57-63. doi: 10.1038/nrg2484
63. Waters, M. T., Moylan, E. C., and Langdale, J. A. (2008). GLK transcription factors regulate chloroplast development in a cell-autonomous manner. Plant J. 56, 432-444. doi: 10.1111/j.1365-313X.2008.03616.x
64. Waters, M. T., Wang, P., Korkaric, M., Capper, R. G., Saunders, N. J., and Langdale, J. A. (2009). GLK transcription factors coordinate expression of the photosynthetic apparatus in Arabidopsis. Plant Cell 21, 1109-1128. doi: 10.1105/tpc.108.065250.
65. Wu, X. L., and Prior, R. (2005). Systematic identification and characterization of anthocyanins by HPLC-ESI-MS/MS in common foods in the United States: fruits and berries. J. Agric. Food Chem. 53, 2589-2599. doi: 10.1021/jf048068b
66. Xu, B., Xin, W. J., Wang, G. D., Guo, W. M., Wen, F. D., and Jin, J. P. (2006). Characteristics of chimeras of Anthurium andraeanum from in vitro mutation. Chinese Bull. Bot. 23, 698-702.
67. Yasumura, Y., Moylan, E. C., and Langdale, J. A. (2005). A conserved transcription factor mediates nuclear control of organelle biogenesis in anciently diverged land plants. Plant Cell 17, 1894-1907.doi: 10.1105/tpc.105.033191.
68. Ye, J., Fang, L., Zheng, H., Zhang, Y., Chen, J., Zhang, Z., et al. (2006). WEGO: a web tool for plotting GO annotations. Nucleic Acids Res. 34, 293-297. doi: 10.1093/nar/gkl031
69. Zhang, X. Z. (1985). A comparison of methods for measurement of chlorophyll in plants. J. Shenyang Agri. Univ. 16, 81-85.