Molecular Genetics and Genomics

, Volume 287, Issue 9, pp 699–709 | Cite as

Transcriptional network analysis of the tryptophan-accumulating rice mutant during grain filling

  • Dong Sub Kim
  • Kyung Jun Lee
  • Won Cheol Yim
  • Jin-Baek Kim
  • Bo-Keun Ha
  • Sang Hoon Kim
  • Si-Yong Kang
Original Paper

Abstract

In a previous study, we selected a high tryptophan (Trp)-accumulating rice (Oryza sativa L.) mutant line by in vitro mutagenesis using gamma rays. To obtain detailed information about the Trp biosynthetic pathway during the grain-filling in rice, we investigated the gene expression profiles in the wild-type (cv. Dongan) and the high-level Trp-accumulating mutant line (MRVII-33) at five different grain-filling stages using microarray analysis. The mutant line showed approximately 6.3-fold higher Trp content and 2.3-fold higher amino acids compared with the original cultivar at the final stage (stage V). The intensity of gene expression was analyzed and compared between the wild-type and mutant line at each of the five grain-filling stages using the Rice 4 × 44K oligo DNA microarray. Among the five stages, stage III showed the highest gene expression changes for both up- and down-regulated genes. Among the Trp biosynthesis-related genes, trpG showed high expression in the mutant line during stages I to IV and trpE showed higher at stage III. Gene clustering was performed based on the genes of KEGG’s amino acid metabolism, and a total of 276 genes related to amino acid metabolism were placed into three clusters. The functional annotation enrichment analysis of the genes classified into the three clusters was also conducted using ClueGO. It was found that cluster 3 uniquely included biological processes related to aromatic amino acid metabolism. These results suggest that gene analysis based on microarray data is useful for elucidating the biological mechanisms of Trp accumulation in high Trp-accumulating mutants at each of the grain-filling stages.

Keywords

Amino acid metabolism Oryza sativa Microarray Tryptophan 

Notes

Acknowledgments

This work was supported by a grant from the Korea Atomic Energy Research Institute (KAERI) and the Ministry of Education, Science, and Technology (MEST), Republic of Korea.

Supplementary material

438_2012_712_MOESM1_ESM.xls (153 kb)
Supplementary material 1 (XLS 153 kb)

References

  1. Andreson PC, Chomet PS, Griffor MC, Kriz AL (1997) Anthranilate synthase gene and its use thereof. World intellectual property organization 2497/26366Google Scholar
  2. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. The gene ontology consortium. Nat Genet 25:25–29PubMedCrossRefGoogle Scholar
  3. Baudo MM, Lyons R, Powers S, Pastori GM, Edwards KJ, Holdsworth MJ, Shewry PR (2006) Transgenesis has less impact on the transcriptome of wheat grain than conventional breeding. Plant Biotechnol J 4:369–380PubMedCrossRefGoogle Scholar
  4. Bindea G, Mlecnik B, Hackl H, Charoentong P, Tosolini M, Kirilovsky A, Fridman WH, Pages F, Trajanoski Z, Galon J (2009) ClueGo: a Cytoscape plug-into decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics 25:1091–1093PubMedCrossRefGoogle Scholar
  5. Bohlmann J, DeLuca V, Eilert U, Martin W (1995) Purification and cDNA cloning of anthranilate synthase from Ruta graveolens: modes of expression and properties of native and recombinant enzymes. Plant J 7:491–501PubMedCrossRefGoogle Scholar
  6. Brown C, Weber E, Wilson C (1970) Lipid and amino acid composition of developing oats. Crop Sci 10:488–491CrossRefGoogle Scholar
  7. Cho HJ, Brotherton JE, Song HS, Widholm JM (2000) Increasing tryptophan synthesis in a forage legume Astragalus sinicus by expressing the tobacco feedback-insensitive anthranilate synthase (ASA2) gene. Plant Physiol 123:1069–1076PubMedCrossRefGoogle Scholar
  8. Chun JB, Ha BK, Jang D-S, Song M, Lee KJ, Kim J-B, Kim SH, Kang S-Y, Lee GJ, Seo YW, Kim DS (2012) Identification of mutations in OASA1 gene from a gamma-irradiated rice mutant population. Plant Breed 131:276–281CrossRefGoogle Scholar
  9. Cohen SS (1998) A guide to the polyamines. Oxford University Press, New YorkGoogle Scholar
  10. Dexter JE, Dronzek BL (1975) Amino acid composition of maturing endosperm from hexaploid triticale and its spring rye and durum wheat parents. Can J Plant Sci 55:537–546CrossRefGoogle Scholar
  11. Druka A, Muehlbauer G, Druka I, Caldo R, Baumann U, Rostoks N, Schreiber A, Wise R, Close T, Kleinhofs A, Graner A, Schulman A, Langridge P, Sato K, Hayes P, McNicol J, Marshall D, Waugh R (2006) An atlas of gene expression from seed to seed through barley development. Funct Integr Genomics 6:202–211PubMedCrossRefGoogle Scholar
  12. Duan MJ, Sun SSM (2005) Profiling the expression of genes controlling rice grain quality. Plant Mol Physiol 59:165–178Google Scholar
  13. Feng Q, Zhang Y, Hao P, Wang S, Fu G, Huang Y, Li Y, Zhu J, Liu Y, Hu X, Jia P, Zhang Y, Zhao Q, Ying K, Yu S, Tang Y, Weng Q, Zhang L, Lu Y, Mu J, Lu Y, Zhang LS, Yu Z, Fan D, Liu X, Lu T, Li C, Wu Y, Sun T, Lei H, Li H, Hu H, Guan J, Wu M, Zhang R, Zhou B, Chen Z, Chen L, Jin Z, Wang R, Yin H, Cai Z, Ren S, Lv G, Gu W, Zhu G, Tu Y, Jia J, Zhang Y, Chen J, Kang H, Chen X, Shao C, Sun Y, Hu Q, Zhang X, Zhang W, Wang L, Ding C, Sheng H, Gu J, Chen S, Ni L, Zhu F, Chen W, Lan L, Lai Y, Chengk Z, Guk M, Jiang J, Li J, Hong G, Xue Y, Han B (2002) Sequence and analysis of rice chromosome 4. Nature 420:316–320PubMedCrossRefGoogle Scholar
  14. Firnhaber C, Puhler A, Kuster H (2005) EST sequencing and timecourse microarray hybridizations identify more than 700 Medicago truncatula genes with developmental expression regulation in flowers and pods. Planta 222:269–283PubMedCrossRefGoogle Scholar
  15. Girke T, Todd J, Ruuska S, White J, Benning C, Ohlrogge J (2000) Microarray analysis of developing Arabidopsis grains. Plant Physiol 124:1570–1581PubMedCrossRefGoogle Scholar
  16. Goff SA, Ricke D, Lan TH, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H, Hadley D, Hutchison D, Martin C, Katagiri F, Lange BM, Moughamer T, Xia Y, Budworth P, Zhong J, Miguel T, Paszkowski U, Zhang S, Colbert M, Sun WL, Chen L, Cooper B, Park S, Wood TC, Mao L, Quail P, Wing R, Dean R, Yu Y, Zharkikh A, Shen R, Sahasrabudhe S, Thomas A, Cannings R, Gutin A, Pruss D, Reid J, Tavtigian S, Mitchell J, Eldredge G, Scholl T, Miller RM, Bhatnagar S, Adey N, Rubano T, Tusneem N, Robinson R, Feldhaus J, Macalma T, Oliphant A, Briggs S (2002) A draft sequence of the rice genome (Oryza sativa L, ssp. Japonica). Science 296:92–100PubMedCrossRefGoogle Scholar
  17. Gregersen PL, Brinch-Pedersen H, Holm PB (2005) A microarraybased comparative analysis of gene expression profiles during grain development in transgenic and wild type wheat. Transgenic Res 14:887–905PubMedCrossRefGoogle Scholar
  18. Hansen M, Friis C, Bowra S, Holm PB, Vincze E (2009) A pathway-specific microarray analysis highlights the complex and co-ordinated transcriptional networks of the developing grain of field-grown barley. J Exp Bot 60:153–167PubMedCrossRefGoogle Scholar
  19. Hoseney RC, Finney KF (1967) Free amino acid composition of flours milled from wheats harvested at various stages of maturity. Crop Sci 7:3–5CrossRefGoogle Scholar
  20. Hoseney RC, Finney KF, Pomeranz Y (1966) Changes in urea dispersibility of proteins during maturation. J Sci Food Agri 17:273–276CrossRefGoogle Scholar
  21. Jang CS, Yim WC, Moon J-C, Jung JH, Lee TG, Lim SD, Cho SH, Kim W, Seo YW, Lee B-M (2008) Evolution of non-specific lipid transfer protein (nsLTP) genes in the Poaceae family: their duplication and diversity. Mol Genet Genomics 279(4):81–497Google Scholar
  22. Jennings AC, Morton RK (1963) Amino acids and protein synthesis in developing wheat endosperm. Austrlian J Biol Sci 16:384–394Google Scholar
  23. Kan YC, Wan YF, Beaudoin F, Leader DJ, Edwards K, Poole R, Wang DW, Mitchell RAC, Shewry PR (2006) Transcriptome analysis reveals differentially expressed storage protein transcripts in seeds of Aegilops and wheat. J Cereal Sci 44:75–85CrossRefGoogle Scholar
  24. Kaur-Sawhney R, Tiburcio AF, Altabella T, Galston AW (2003) Polyamines in plants: an overview. J Cell Mole Biol 2:1–12Google Scholar
  25. Kikuchi S, Satoh K, Nagata T, Kawagashira N, Doi K, Kishimoto N, Yazaki J, Ishikawa M, Yamada H, Ooka H, Hotta I, Kojima K, Namiki T, Ohneda E, Yahagi W, Suzuki K, Li CJ, Ohtsuki K, Shishiki T; Foundation of Advancement of International Science Genome Sequencing & Analysis Group, Otomo Y, Murakami K, Iida Y, Sugano S, Fujimura T, Suzuki Y, Tsunoda Y, Kurosaki T, Kodama T, Masuda H, Kobayashi M, Xie Q, Lu M, Narikawa R, Sugiyama A, Mizuno K, Yokomizo S, Niikura J, Ikeda R, Ishibiki J, Kawamata M, Yoshimura A, Miura J, Kusumegi T, Oka M, Ryu R, Ueda M, Matsubara K; RIKEN, Kawai J, Carninci P, Adachi J, Aizawa K, Arakawa T, Fukuda S, Hara A, Hashizume W, Hayatsu N, Imotani K, Ishii Y, Itoh M, Kagawa I, Kondo S, Konno H, Miyazaki A, Osato N, Ota Y, Saito R, Sasaki D, Sato K, Shibata K, Shinagawa A, Shiraki T, Yoshino M, Hayashizaki Y, Yasunishi A (2003) Collection, mapping, and annotation of over 28,000 cDNA clone from japonica rice. Science 301:376–379Google Scholar
  26. Kondou H, Ooka H, Yamada H, Satoh K, Kikuchi S, Takahara Y, Yamamoto K (2006) Microarray analysis of gene expression at initial stages of rice seed development. Breed Sci 56:235–242CrossRefGoogle Scholar
  27. Kreps JA, Ponappa T, Dong W, Town CD (1996) Molecular basis of α-methyltryptophan resistance in amt-1, a mutant of Arabidopsis thaliana with altered tryptophan metabolism. Plant Physiol 110:1159–1165PubMedCrossRefGoogle Scholar
  28. Li J, Last RL (1996) The Arabidopsis thaliana trp5 mutant has a feedback-resistant anthranilate synthase and elevated soluble tryptophan. Plant Physiol 110:51–59PubMedCrossRefGoogle Scholar
  29. Moreno-Hagelsieb G, Latimer K (2007) Choosing BLAST options for better detection of orthologs as reciprocal best hits. Bioinformatics 319–324Google Scholar
  30. Poulsen C, Bongaerts RJM, Verpoorte R (1993) Purification and characterization of anthranilate synthase from Catharanthus roseus. Eur J Biochem 212:431–440PubMedCrossRefGoogle Scholar
  31. Radchuk VV, Sreenivasulu N, Radchuk RU, Wobus U, Weschke W (2005) The methylation cycle and its possible functions in barley endosperm development. Plant Mol Physiol 59:289–307Google Scholar
  32. Romero RM, Roberts MF (1996) Anthranilate synthase from Ailanthus altissima cell suspension cultures. Phytochemstry 41:395–402CrossRefGoogle Scholar
  33. Ruuska SA, Girke T, Benning C, Ohlrogge JB (2002) Contrapuntal networks of gene expression during Arabidopsis seed filling. Plant Cell 14:1191–1206PubMedCrossRefGoogle Scholar
  34. Sasaki T, Matsumoto T, Yamamoto K, Sakata K, Baba T, Katayose Y, Wu J, Niimura Y, Cheng Z, Nagamura Y, Antonio BA, Kanamori H, Hosokawa S, Masukawa M, Arikawa K, Chiden Y, Hayashi M, Okamoto M, Ando T, Aoki H, Arita K, Hamada M, Harada C, Hijishita S, Honda M, Ichikawa Y, Idonuma A, Iijima M, Ikeda M, Ikeno M, Ito S, Ito T, Ito Y, Ito Y, Iwabuchi A, Kamiya K, Karasawa W, Katagiri S, Kikuta A, Kobayashi N, Kono I, Machita K, Maehara T, Mizuno H, Mizubayashi T, Mukai Y, Nagasaki H, Nakashima M, Nakama Y, Nakamichi Y, Nakamura M, Namiki N, Negishi M, Ohta I, Ono N, Saji S, Sakai K, Shibata M, Shimokawa T, Shomura A, Song J, Takazaki Y, Terasawa K, Tsuji K, Waki K, Yamagata H, Yamane H, Yoshiki S, Yoshihara R, Yukawa K, Zhong H, Iwama H, Endo T, Ito H, Hahn JH, Kim HI, Eun MY, Yano M, Jiang J, Gojobori T (2002) The genome sequence and structure of rice chromosome 1. Nature 420:312–316PubMedCrossRefGoogle Scholar
  35. Sato Y, Antonio B, Namiki N, Takehisa H, Minami H, Kamatsuki K, Sugimoto K, Shimizu Y, Hirochika H, Nagamura Y (2011) RiceXPro: a platform for monitoring gene expression in japonica rice grown under natural field conditions. Nucleic Acids Res 39:1141–1148CrossRefGoogle Scholar
  36. Seo J, Shneiderman B (2002) Interactively exploring hierarchical clustering results. IEEE Comput 35:80–86Google Scholar
  37. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504PubMedCrossRefGoogle Scholar
  38. Singh M, Widholm JM (1974) Measurement of the fice enzymes which convert chorismate to tryptophan in wheat plants (Triticum aestivum L.). Physiol Plant 32:362–366Google Scholar
  39. Sreenivasulu N, Altschmeid L, Radchuk V, Gubatz S, Wobus U, Weschke W (2004) Transcript profiles and deduced changes of metabolic pathways in maternal and filial tissues of developing barley grains. Plant J 37:539–553PubMedCrossRefGoogle Scholar
  40. Sreenivasulu N, Radchuk V, Strickert M, Miersch O, Weschke W, Wobus U (2006) Gene expression patterns reveal tissue-specific signalling networks controlling programmed cell death and ABA-regulated maturation in developing barley seeds. Plant J 47:310–327PubMedCrossRefGoogle Scholar
  41. Tozawa Y, Hasegawa H, Terakawa T, Wakasa K (2001) Characterization of rice anthranilate synthease α-subunit genes OASA1 and OASA2. Tryptophan accumunlation in transgenic rice expressing a feedback-insensitive mutant of OASA1. Plant Phyiol 126:1493–1506CrossRefGoogle Scholar
  42. Ufaz S, Galil G (2008) Improving the content of essential amino acids in crop plants: goals na opportunities. Plant Physiol 147:954–961PubMedCrossRefGoogle Scholar
  43. Wakasa K, Tozawa Y, Terakawa T, Hasegawa H (1999) Gene encoding α-subunit of rice anthranilate synthase and DNA relating thereto. World intellectual property organization 99/11800Google Scholar
  44. Wakasa K, Hasegawa H, Nemoto H, Matsuda F, Miyazawa H, Tozawa Y, Morino K, Komatsu A, Yamada T, Terakawa T, Miyagawa H (2006) High-level tryptophan accumulation in seeds of transgenic rice and its limited effects on agronomic traits and seed metabolite profile. J Exp Bot 57:3069–3078PubMedCrossRefGoogle Scholar
  45. Wang X, Larkins A (2001) Genetic analysis of amino acid accumulation in opaque-2 maize endosperm. Plant Physiol 125:1766–1777PubMedCrossRefGoogle Scholar
  46. Widholm JM (1972) Anthranilate synthetase from 5-methyl-tryptophan-susceptible and -resistant cultured Daucus carota cells. Biochim Biophys Acta 279:48–57PubMedCrossRefGoogle Scholar
  47. Widholm JM (1974) Control of aromatic amino acid biosynthesis in cultured plant tissues: effect of intermediates and aromatic amino acids on free levels. Physiol Plant 30:13–18CrossRefGoogle Scholar
  48. Wiggins SC, Frey KK (1958) The ration of ethanol soluble to total N in developing oat seeds. Cereal Chem 35:235–239Google Scholar
  49. Yang J, Yunying C, Zhang H, Liu L, Zhang J (2008) Involvement of polyamines in the post-anthesis development of inferior and superior spikelets in rice. Planta 228:137–149PubMedCrossRefGoogle Scholar
  50. Yu J, Hu S, Wang J, Wong GK, Li S, Liu B, Deng Y, Dai L, Zhou Y, Zhang X, Cao M, Liu J, Sun J, Tang J, Chen Y, Huang X, Lin W, Ye C, Tong W, Cong L, Geng J, Han Y, Li L, Li W, Hu G, Huang X, Li W, Li J, Liu Z, Li L, Liu J, Qi Q, Liu J, Li L, Li T, Wang X, Lu H, Wu T, Zhu M, Ni P, Han H, Dong W, Ren X, Feng X, Cui P, Li X, Wang H, Xu X, Zhai W, Xu Z, Zhang J, He S, Zhang J, Xu J, Zhang K, Zheng X, Dong J, Zeng W, Tao L, Ye J, Tan J, Ren X, Chen X, He J, Liu D, Tian W, Tian C, Xia H, Bao Q, Li G, Gao H, Cao T, Wang J, Zhao W, Li P, Chen W, Wang X, Zhang Y, Hu J, Wang J, Liu S, Yang J, Zhang G, Xiong Y, Li Z, Mao L, Zhou C, Zhu Z, Chen R, Hao B, Zheng W, Chen S, Guo W, Li G, Liu S, Tao M, Wang J, Zhu L, Yuan L, Yang H (2002) A draft sequence of the rice genome (Oryza sativa L, ssp. Indica). Science 296:79–92PubMedCrossRefGoogle Scholar
  51. Zhu T, Budworth P, Chen W, Provart N, Guimil S, Su W, Estes B, Zou G, Wang X (2003) Transcriptional control of nutrient portioning during rice grain filling. Plant Biotechnol J 1:59–70PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Dong Sub Kim
    • 1
  • Kyung Jun Lee
    • 1
    • 2
  • Won Cheol Yim
    • 2
  • Jin-Baek Kim
    • 1
  • Bo-Keun Ha
    • 1
  • Sang Hoon Kim
    • 1
  • Si-Yong Kang
    • 1
  1. 1.Radiation Research Center for Bio-technologyAdvanced Radiation Technology Institute, Korea Atomic Energy Research InstituteJeongeupKorea
  2. 2.Department of Plant BiotechnologyDongguk UniversitySeoulKorea

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