Comparative metabolomic analysis of wild type and mads3 mutant rice anthers

Journal of Integrative Plant Biology

Volumn 56, Issue 9, 2014, Pages 849-863

  Qu, Guorun ^a   Quan, Sheng ^a,b   Mondol, Palash ^a   Xu, Jie ^a   Zhang, Dabing ^a   Shi, Jianxin ^a,b  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b Shanghai Ruifeng Agro biotechnology Co   (China)

Author keywords

Anther; Ascorbate; Cysteine cysteine; Glutathione oxidized glutathione; Oryza. sativa L; Secondary metabolism

Indexed keywords

ORYZA;

REACTIVE OXYGEN METABOLITE;

COMPARATIVE STUDY; FLOWER; GENETICS; METABOLISM; METABOLOMICS; MUTATION; RICE;

FLOWERS; METABOLOMICS; MUTATION; ORYZA SATIVA; REACTIVE OXYGEN SPECIES;

EID: 84907865587     PISSN: 16729072     EISSN: 17447909     Source Type: Journal    
DOI: 10.1111/jipb.12245     Document Type: Article

References (74)

1. Araújo WL, Tohge T, Ishizaki K, Leaver CJ, Fernie AR (2011) Protein degradation-An alternative respiratory substrate for stressed plants. Trends Plant Sci 16: 489-498
2. Ba QS, Zhang GS, Wang JS, Che HX, Liu HZ, Niu N, Ma SC, Wang JW (2013) Relationship between metabolism of reactive oxygen species and chemically induced male sterility in wheat (Triticum aestivum L.). Can J Plant Sci 93: 1-7
3. Baxter CJ, Redestig H, Schauer N, Repsilber D, Patil KR, Nielsen J, Selbig J, Liu J, Fernie AR, Sweetlove LJ (2007) The metabolic response of heterotrophic Arabidopsis cells to oxidative stress. Plant Physiol 143: 312-325
4. Beisson F, Li-Beisson Y, Pollard M (2012) Solving the puzzles of cutin and suberin polymer biosynthesis. Curr Opin Plant Biol 15: 329-337
5. Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29: 1165-1188
6. Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: A review. Ann Bot 91: 179-194
7. Borg M, Brownfield L, Twell D (2009) Male gametophyte development: A molecular perspective. J Exp Bot 60: 1465-1478
8. Borge GIA, Vogt G, Nilsson A (1999) Intermediates and products formed during fatty acid α-oxidation in cucumber (Cucumis sativus). Lipids 34: 661-673
9. Bowne JB, Erwin TA, Juttner J, Schnurbusch T, Langridge P, Bacic A, Roessner U (2012) Drought responses of leaf tissues from wheat cultivars of differing drought tolerance at the metabolite level. Mol Plant 5: 418-429
10. Chang Y, Zhao C, Zhu Z, Wu Z, Zhou J, Zhao Y, Lu X, Xu G (2012) Metabolic profiling based on LC/MS to evaluate unintended effects of transgenic rice with cry1Ac and sck genes. Plant Mol Biol 78: 477-487.
11. Chen W, Gong L, Guo Z, Wang W, Zhang H, Liu X, Yu S, Xiong L, Luo J (2013) A novel integrated method for large-scale detection, identification and quantification of widely-targeted metabolites: Application in study of rice metabolomics. Mol Plant 6: 1769-1780
12. Ciaffi M, Paolacci AR, Tanzarella OA, Porceddu E (2011) Molecular aspects of flower development in grasses. Sex Plant Reprod 24: 247-282
13. Coen ES, Meyerowitz EM (1991) The war of the whorls: Genetic interactions controlling flower development. Nature 353: 31-37
14. Couée I, Sulmon C, Gouesbet G, El Amrani A (2006) Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot 57: 449-459
15. Deng MH, Wen JF, Huo JL, Zhu HS, Dai XZ, Zhang ZQ, Zhou H, Zou XX (2012) Relationship of metabolism of reactive oxygen species with cytoplasmic male sterility in pepper (Capsicum annuum L.). Sci Hortic 134: 232-236
16. Dreni L, Osnato M, Kater MM (2013) The ins and outs of the rice AGAMOUS subfamily. Mol Plant 6: 650-664
17. Evans AM, DeHaven CD, Barrett T, Mitchell M, Milgram E (2009) Integrated, nontargeted ultrahigh performance liquid chromatography/electrospray ionization tandem mass spectrometry platform for the identification and relative quantification of the small-molecule complement of biological systems. Anal Chem 81: 6656-6667
18. Fini A, Brunetti C, Di Ferdinando M, Ferrini F, Tattini M (2011) Stress-induced flavonoid biosynthesis and the antioxidant machinery of plants. Plant Signal Behav 6: 709-711
19. Goldberg RB, Beals TP, Sanders PM (1993) Anther development: Basic principles and practical applications. Plant Cell 5: 1217-1229
20. Hall R, Beale M, Fiehn O, Hardy N, Sumner L, Bino R (2002) Plant metabolomics: The missing link in functional genomics strategies. Plant Cell 14: 1437-1440
21. Halliwell B, Rafter J, Jenner A (2005) Health promotion by flavonoids, tocopherols, tocotrienols, and other phenols: Direct or indirect effects? Antioxidant or not? Am J Clin Nutr 81: 268S-276S
22. Hartley R (1972) p-Coumaric and ferulic acid components of cell walls of ryegrass and their relationships with lignin and digestibility. J Sci Food Agric 23: 1347-1354
23. Helsper JP, Loewus FA (1982) Metabolism of L-threonic acid in Rumex x-acutus L. and Pelargonium crispum (L.) L'Hér. Plant Physiol 69: 1365-1368
24. Hirai MY, Fujiwara T, Awazuhara M, Kimura T, Noji M, Saito K (2003) Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-L-serine as a general regulator of gene expression in response to sulfur nutrition. Plant J 33: 651-663
25. Hu C, Shi J, Quan S, Cui B, Kleessen S, Nikoloski Z, Toghe T, Alexander D, Guo L, Lin H, Wang J, Cuo Xiao, Rao J, Luo Q, Zhao X, Fernie AR, Zhang D (2014) Metabolic variation between japonica and indica rice cultivars as revealed by non-targeted metabolomics. Sci Rep 4: 5067. DOI: 10.1038/srep05067
26. Hu L, Liang W, Yin C, Cui X, Zong J, Wang X, Hu J, Zhang D (2011) Rice MADS3 regulates ROS homeostasis during late anther development. Plant Cell 23: 515-5533
27. Irish VF (2010) The flowering of Arabidopsis flower development. Plant J 61: 1014-1028
28. Ishikawa T, Takahara K, Hirabayashi T, Matsumura H, Fujisawa S, Terauchi R, Uchimiya H, Kawai-Yamada M (2010) Metabolome analysis of response to oxidative stress in rice suspension cells overexpressing cell death suppressor Bax inhibitor-1. Plant Cell Physiol 51: 9-20
29. Khanday I, Yadav SR, Vijayraghavan U (2013) Rice LHS1/OsMADS1 controls floret meristem specification by coordinated regulation of transcription factors and hormone signaling pathways. Plant Physiol 161: 1970-1983
30. Koltunow AM, Truettner J, Cox KH, Wallroth M, Goldberg RB (1990) Different temporal and spatial gene expression patterns occur during anther development. Plant Cell 2: 1201-1224
31. Latendresse M (2013) Computing Gibbs Free Energy of Compounds and Reactions in MetaCyc
32. Lawton KA, Berger A, Mitchell M, Milgram KE, Evans AM, Guo L, Hanson RW, Kalhan SC, Ryals JA, Milburn MV (2008) Analysis of the adult human plasma metabolome. Pharmacogenomics 9: 383-397
33. Less H, Galili G (2008) Principal transcriptional programs regulating plant amino acid metabolism in response to abiotic stresses. Plant Physiol 147: 316-330
34. Li H, Liang W, Yin C, Zhu L, Zhang D (2011) Genetic interaction of OsMADS3, DROOPING LEAF, and OsMADS13 in specifying rice floral organ identities and meristem determinacy. Plant Physiol 156: 263-274
35. Li H, Pinot F, Sauveplane V, Werck-Reichhart D, Diehl P, Schreiber L, Franke R, Zhang P, Chen L, Gao Y (2010) Cytochrome P450 family member CYP704B2 catalyzes the ω-hydroxylation of fatty acids and is required for anther cutin biosynthesis and pollen exine formation in rice. Plant Cell 22: 173-190
36. Ma H (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol 56: 393-434
37. Matsuda F, Okazaki Y, Oikawa A, Kusano M, Nakabayashi R, Kikuchi J, Yonemaru J, Ebana K, Yano M, Saito K (2012) Dissection of genotype-phenotype associations in rice grains using metabolome quantitative trait loci analysis. Plant J 70: 624-636
38. May MJ, Vernoux T, Leaver C, Van Montagu M, Inzé D (1998) Glutathione homeostasis in plants: Implications for environmental sensing and plant development. J Exp Bot 49: 649-667
39. Miura D, Tanaka H, Wariishi H (2004) Metabolomic differential display analysis of the white-rot basidiomycete Phanerochaete chrysosporium grown under air and 100% oxygen. FEMS Microbiol Lett 234: 111-116
40. Nagasawa N, Miyoshi M, Sano Y, Satoh H, Hirano H, Sakai H, Nagato Y (2003) SUPERWOMAN1 and DROOPING LEAF genes control floral organ identity in rice. Development 130: 705-718
41. Nguyen G, Hailstones D, Wilkes M, Sutton B (2009) Drought-induced oxidative conditions in rice anthers leading to a programmed cell death and pollen abortion. J Agron Crop Sci 195: 157-164
42. Noctor G, Foyer CH (1998) Ascorbate and glutathione: Keeping active oxygen under control. Annu Rev Plant Biol 49: 249-279
43. Obata T, Matthes A, Koszior S, Lehmann M, Araújo WL, Bock R, Sweetlove LJ, Fernie AR (2011) Alteration of mitochondrial protein complexes in relation to metabolic regulation under short-term oxidative stress in Arabidopsis seedlings. Phytochemistry 72: 1081-1091
44. Ohkama-Ohtsu N, Oikawa A, Zhao P, Xiang C, Saito K, Oliver DJ (2008) A γ-Glutamyl transpeptidase-independent pathway of glutathione catabolism to glutamate via 5-oxoproline in Arabidopsis. Plant physiol 148: 1603-1613
45. Ohta T, Masutomi N, Tsutsui N, Sakairi T, Mitchell M, Milburn MV, Ryals JA, Beebe KD, Guo L (2009) Untargeted metabolomic profiling as an evaluative tool of fenofibrate-induced toxicology in Fischer 344 male rats. Toxicol Pathol 37: 521-535
46. Oliver MJ, Guo L, Alexander DC, Ryals JA, Wone BW, Cushman JC (2011) A sister group contrast using untargeted global metabolomic analysis delineates the biochemical regulation underlying desiccation tolerance in Sporobolus stapfianus. Plant Cell 23: 1231-1248
47. Paulose B, Chhikara S, Coomey J, Jung HI, Vatamaniuk O, Dhankher OP (2013) A γ-Glutamyl cyclotransferase protects Arabidopsis plants from heavy metal toxicity by recycling glutamate to maintain glutathione homeostasis. Plant Cell 25: 4580-4595
48. 2 fixation rate and carbohydrate metabolism in tomato, and decreases harmful effects of subsequent salt stress. Plant Biol 13: 105-114
49. Purdy SJ, Bussell JD, Nelson DC, Villadsen D, Smith SM (2011) A nuclear-localized protein, KOLD SENSITIV-1, affects the expression of cold-responsive genes during prolonged chilling in Arabidopsis. J Plant physiol 168: 263-269
50. Quan L, Zhang B, Shi W, Li H (2008) Hydrogen peroxide in plants: A persatile molecule of the reactive oxygen species network. J Integr Plant Biol 50: 2-18
51. Rao J, Cheng F, Hu C, Quan S, Lin H, Wang J, Chen G, Zhao X, Alexander D, Guo L, Wang G, Lai J, Zhang D, Shi J (2014) Metabolic map of mature maize kernels. Metabolomics. DOI 10.1007/s11306-11014-10624-11303
52. Riechmann JL, Krizek BA, Meyerowitz EM (1996) Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. Proc Natl Acad Sci USA 93: 4793-4798
53. Rose MT, Rose TJ, Pariasca-Tanaka J, Yoshihashi T, Neuweger H, Goesmann A, Frei M, Wissuwa M (2012) Root metabolic response of rice (Oryza sativa L.) genotypes with contrasting tolerance to zinc deficiency and bicarbonate excess. Planta 236: 959-973
54. Sanders PM, Bui AQ, Weterings K, McIntire K, Hsu YC, Lee PY, Truong MT, Beals T, Goldberg R (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex Plant Reprod 11: 297-322
55. Sappl PG, Carroll AJ, Clifton R, Lister R, Whelan J, Harvey Millar A, Singh KB (2009) The Arabidopsis glutathione transferase gene family displays complex stress regulation and co-silencing multiple genes results in altered metabolic sensitivity to oxidative stress. Plant J 58: 53-68
56. Schaller H (2003) The role of sterols in plant growth and development. Prog Lipid Res 42: 163-175
57. Scott R, Hodge R, Paul W, Draper J (1991) The molecular biology of anther differentiation. Plant Sci 80: 167-191
58. Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012: 1-26
59. Shingaki-Wells RN, Huang S, Taylor NL, Carroll AJ, Zhou W, Millar AH (2011) Differential molecular responses of rice and wheat coleoptiles to anoxia reveal novel metabolic adaptations in amino acid metabolism for tissue tolerance. Plant physiol 156: 1706-1724
60. Shulaev V, Oliver DJ (2006) Metabolic and proteomic markers for oxidative stress. New tools for reactive oxygen species research. Plant Physiol 141: 367-372
61. Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2: 755-767
62. Theißen G (2001) Development of floral organ identity: Stories from the MADS house. Curr Opin Plant Biol 4: 75-85
63. Tokimatsu T, Kotera M, Goto S, Kanehisa M (2011) KEGG and GenomeNet resources for predicting protein function from omics data including KEGG PLANT resource. In: Kihara D, ed. Protein Function Prediction for Omics Era. Springer, London. pp. 271-288
64. Voelckel C, Baldwin IT (2004) Herbivore-induced plant vaccination. Part II. Array-studies reveal the transience of herbivore-specific transcriptional imprints and a distinct imprint from stress combinations. Plant J 38: 650-663
65. Walley JW, Dehesh K (2010) Molecular mechanisms regulating rapid stress signaling networks in Arabidopsis. J Integr Plant Biol 52: 354-359
66. Wilson ZA, Yang C (2004) Plant gametogenesis: Conservation and contrasts in development. Reproduction 128: 483-492
67. Xiang C, Qu LJ, Gao YM, Shi YY (2013) Flower development and photoperiodic control of flowering in rice. Rice Sci 20: 79-87
68. Xing S, Salinas M, Huijser P (2011) New players unveiled in early anther development. Plant Signal Behav 6: 934-938
69. Yamaguchi T, Lee DY, Miyao A, Hirochika H, An G, Hirano HY (2006) Functional diversification of the two C-class MADS box genes OSMADS3 and OSMADS58 in Oryza sativa. Plant Cell 18: 15-28
70. Yao SG, Ohmori S, Kimizu M, Yoshida H (2008) Unequal genetic redundancy of rice PISTILLATA orthologs, OsMADS2 and OsMADS4, in lodicule and stamen development. Plant Cell Physiol 49: 853-857
71. Yoshida H, Nagato Y (2011) Flower development in rice. J Exp Bot 62: 4719-4730
72. Youssefian S, Nakamura M, Orudgev E, Kondo N (2001) Increased cysteine biosynthesis capacity of transgenic tobacco overexpressing an O-acetylserine (thiol) lyase modifies plant responses to oxidative stress. Plant Physiol 126: 1001-1011
73. Zhang D, Wilson ZA (2009) Stamen specification and anther development in rice. Chin Sci Bull 54: 2342-2353
74. Zhang D, Yang L (2014) Specification of tapetum and microsporocyte cells within the anther. Curr Opin Plant Biol 17: 49-55