Influence of isopropylmalate synthase Os IPMS 1 on seed vigour associated with amino acid and energy metabolism in rice

He, Yongqi; Cheng, Jinping; He, Ying; Yang, Bin; Cheng, Yanhao; Yang, Can; Zhang, Hongsheng; Wang, Zhoufei

doi:10.1111/pbi.12979

Title: Influence of isopropylmalate synthase Os IPMS 1 on seed vigour associated with amino acid and energy metabolism in rice

Journal Article · Mon Jul 16 00:00:00 EDT 2018 · Plant Biotechnology Journal

DOI:https://doi.org/10.1111/pbi.12979· OSTI ID:1460467

He, Yongqi ^[1]; Cheng, Jinping ^[1]; He, Ying ^[1]; Yang, Bin ^[1]; Cheng, Yanhao ^[1]; Yang, Can ^[1]; Zhang, Hongsheng ^[1];

^[2]

The Laboratory of Seed Science and Technology State Key Laboratory of Crop Genetics and Germplasm Enhancement Jiangsu Collaborative Innovation Center for Modern Crop Production Nanjing Agricultural University Nanjing China
The Laboratory of Seed Science and Technology State Key Laboratory of Crop Genetics and Germplasm Enhancement Jiangsu Collaborative Innovation Center for Modern Crop Production Nanjing Agricultural University Nanjing China, The Laboratory of Seed Science and Technology Guangdong Key Laboratory of Plant Molecular Breeding State Key Laboratory for Conservation and Utilization of Subtropical Agro‐Bioresources South China Agricultural University Guangzhou China

Summary Seed vigour is an imperative trait for the direct seeding of rice. Isopropylmalate synthase ( IPMS ) catalyses the committed step of leucine (Leu) biosynthesis, but its effect on seed vigour remains unclear. In this study, rice Os IPMS 1 and Os IPMS 2 was cloned, and the roles of Os IPMS 1 in seed vigour were mainly investigated. Os IPMS 1 and Os IPMS 2 catalyse Leu biosynthesis, and Leu feedback inhibits their IPMS activities. Disruption of Os IPMS 1 resulted in low seed vigour under various conditions, which might be tightly associated with the reduction of amino acids in germinating seeds. Eleven amino acids that associated with stress tolerance, GA biosynthesis and tricarboxylic acid ( TCA ) cycle were significantly reduced in osipms1 mutants compared with those in wide type ( WT ) during seed germination. Transcriptome analysis indicated that a total of 1209 differentially expressed genes ( DEG s) were altered in osipms1a mutant compared with WT at the early germination stage, wherein most of the genes were involved in glycolysis/gluconeogenesis, protein processing, pyruvate, carbon, fructose and mannose metabolism. Further analysis confirmed that the regulation of Os IPMS 1 in seed vigour involved in starch hydrolysis, glycolytic activity and energy levels in germinating seeds. The effects of seed priming were tightly associated with the mRNA levels of Os IPMS 1 in priming seeds. The Os IPMS 1 might be used as a biomarker to determine the best stop time‐point of seed priming in rice. This study provides novel insights into the function of Os IPMS 1 on seed vigour and should have practical applications in seed priming of rice.

View Journal Article

Cite

Export

Save

Sponsoring Organization:: USDOE

OSTI ID:: 1460467

Alternate ID(s):: OSTI ID: 1460468

Journal Information:: Plant Biotechnology Journal, Journal Name: Plant Biotechnology Journal Vol. 17 Journal Issue: 2; ISSN 1467-7644

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

Citation Metrics:

Cited by: 45 works

Citation information provided by
Web of Science

References (64)

Dihydroxyacid dehydratase is important for gametophyte development and disruption causes increased susceptibility to salinity stress in Arabidopsis Zhang, Chun; Pang, Qiuying; Jiang, Luguang Journal of Experimental Botany, Vol. 66, Issue 3 https://doi.org/10.1093/jxb/eru449	journal	November 2014
Common QTL Affect the Rate of Tomato Seed Germination under Different Stress and Nonstress Conditions Foolad, Majid R.; Subbiah, Prakash; Zhang, Liping International Journal of Plant Genomics, Vol. 2007 https://doi.org/10.1155/2007/97386	journal	January 2007
Identification of the 2-Hydroxyglutarate and Isovaleryl-CoA Dehydrogenases as Alternative Electron Donors Linking Lysine Catabolism to the Electron Transport Chain of Arabidopsis Mitochondria Araújo, Wagner L.; Ishizaki, Kimitsune; Nunes-Nesi, Adriano The Plant Cell, Vol. 22, Issue 5 https://doi.org/10.1105/tpc.110.075630	journal	May 2010
Mapping quantitative trait loci controlling seed longevity in rice (Oryza sativa L.) Miura, K.; Lin, S.; Yano, M. Theoretical and Applied Genetics, Vol. 104, Issue 6 https://doi.org/10.1007/s00122-002-0872-x	journal	May 2002
Seed Germination and Dormancy. Bewley, J. D. The Plant Cell https://doi.org/10.1105/tpc.9.7.1055	journal	July 1997
Mapping of quantitative trait loci controlling low-temperature germinability in rice (Oryza sativa L.) Fujino, K.; Sekiguchi, H.; Sato, T. Theoretical and Applied Genetics, Vol. 108, Issue 5 https://doi.org/10.1007/s00122-003-1509-4	journal	November 2003
Abscisic acid and the control of seed dormancy and germination Nambara, Eiji; Okamoto, Masanori; Tatematsu, Kiyoshi Seed Science Research, Vol. 20, Issue 2 https://doi.org/10.1017/S0960258510000012	journal	February 2010
Two Arabidopsis Genes ( IPMS1 and IPMS2 ) Encode Isopropylmalate Synthase, the Branchpoint Step in the Biosynthesis of Leucine de Kraker, Jan-Willem; Luck, Katrin; Textor, Susanne Plant Physiology, Vol. 143, Issue 2 https://doi.org/10.1104/pp.106.085555	journal	December 2006
Inductive effect produced by a mixture of carbon source in the production of gibberellic acid by Gibberella fujikuroi Rios-Iribe, Erika Y.; Flores-Cotera, Luis B.; Chávira, Mario M. González World Journal of Microbiology and Biotechnology, Vol. 27, Issue 6 https://doi.org/10.1007/s11274-010-0603-4	journal	November 2010
Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination Holdsworth, Michael J.; Bentsink, Leónie; Soppe, Wim J. J. New Phytologist, Vol. 179, Issue 1 https://doi.org/10.1111/j.1469-8137.2008.02437.x	journal	July 2008
3-Methylcrotonyl-Coenzyme A Carboxylase Is a Component of the Mitochondrial Leucine Catabolic Pathway in Plants Anderson, Marc D.; Che, Ping; Song, Jianping Plant Physiology, Vol. 118, Issue 4 https://doi.org/10.1104/pp.118.4.1127	journal	December 1998
Identification of genes involved in rice seed priming in the early imbibition stage Cheng, J.; Wang, L.; Zeng, P. Plant Biology, Vol. 19, Issue 1 https://doi.org/10.1111/plb.12438	journal	March 2016
Quantitative trait loci analysis for rice seed vigor during the germination stage Wang, Zhou-fei; Wang, Jian-fei; Bao, Yong-mei Journal of Zhejiang University SCIENCE B, Vol. 11, Issue 12 https://doi.org/10.1631/jzus.B1000238	journal	December 2010
qLTG-9, a stable quantitative trait locus for low-temperature germination in rice (Oryza sativa L.) Li, Linfang; Liu, Xi; Xie, Kun Theoretical and Applied Genetics, Vol. 126, Issue 9 https://doi.org/10.1007/s00122-013-2137-2	journal	June 2013
Arabidopsis Seed Development and Germination Is Associated with Temporally Distinct Metabolic Switches Fait, Aaron; Angelovici, Ruthie; Less, Hadar Plant Physiology, Vol. 142, Issue 3 https://doi.org/10.1104/pp.106.086694	journal	September 2006
TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions Kim, Daehwan; Pertea, Geo; Trapnell, Cole Genome Biology, Vol. 14, Issue 4 https://doi.org/10.1186/gb-2013-14-4-r36	journal	January 2013
In-Depth Proteomic Analysis of Rice Embryo Reveals its Important Roles in Seed Germination Han, Chao; He, Dongli; Li, Ming Plant and Cell Physiology, Vol. 55, Issue 10 https://doi.org/10.1093/pcp/pcu114	journal	September 2014
Developing Rice Embryo Proteomics Reveals Essential Role for Embryonic Proteins in Regulation of Seed Germination Kim, Sun Tae; Wang, Yiming; Kang, Sun Young Journal of Proteome Research, Vol. 8, Issue 7 https://doi.org/10.1021/pr900358s	journal	July 2009
Seed priming: state of the art and new perspectives Paparella, S.; Araújo, S. S.; Rossi, G. Plant Cell Reports, Vol. 34, Issue 8 https://doi.org/10.1007/s00299-015-1784-y	journal	March 2015
Seed imbibition in Medicago truncatula Gaertn.: Expression profiles of DNA repair genes in relation to PEG-mediated stress Balestrazzi, Alma; Confalonieri, Massimo; Macovei, Anca Journal of Plant Physiology, Vol. 168, Issue 7 https://doi.org/10.1016/j.jplph.2010.10.008	journal	May 2011
Silicon improves seed germination and alleviates drought stress in lentil crops by regulating osmolytes, hydrolytic enzymes and antioxidant defense system Biju, Sajitha; Fuentes, Sigfredo; Gupta, Dorin Plant Physiology and Biochemistry, Vol. 119 https://doi.org/10.1016/j.plaphy.2017.09.001	journal	October 2017
Proteomic Analysis Reveals Proteins Involved in Seed Imbibition under Salt Stress in Rice Xu, Enshun; Chen, Mingming; He, Hui Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.02006	journal	January 2017
From Amino Acid to Glucosinolate Biosynthesis: Protein Sequence Changes in the Evolution of Methylthioalkylmalate Synthase in Arabidopsis de Kraker, Jan-Willem; Gershenzon, Jonathan The Plant Cell, Vol. 23, Issue 1 https://doi.org/10.1105/tpc.110.079269	journal	January 2011
Analysis of embryonic proteome modulation by GA and ABA from germinating rice seeds Kim, Sun Tae; Kang, Sun Young; Wang, Yiming PROTEOMICS, Vol. 8, Issue 17 https://doi.org/10.1002/pmic.200800183	journal	September 2008
The multifaceted role of aspartate-family amino acids in plant metabolism Kirma, M.; Araujo, W. L.; Fernie, A. R. Journal of Experimental Botany, Vol. 63, Issue 14 https://doi.org/10.1093/jxb/ers119	journal	April 2012
A Flux Model of Glycolysis and the Oxidative Pentosephosphate Pathway in Developing Brassica napus Embryos Schwender, Jörg; Ohlrogge, John B.; Shachar-Hill, Yair Journal of Biological Chemistry, Vol. 278, Issue 32 https://doi.org/10.1074/jbc.M303432200	journal	May 2003
Cold Stratification and Exogenous Nitrates Entail Similar Functional Proteome Adjustments during Arabidopsis Seed Dormancy Release Arc, Erwann; Chibani, Kamel; Grappin, Philippe Journal of Proteome Research, Vol. 11, Issue 11 https://doi.org/10.1021/pr3006815	journal	October 2012
Dynamic quantitative trait locus analysis of seed dormancy at three development stages in rice Cheng, Jinping; Wang, Ling; Du, Wenli Molecular Breeding, Vol. 34, Issue 2 https://doi.org/10.1007/s11032-014-0053-z	journal	February 2014
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method Livak, Kenneth J.; Schmittgen, Thomas D. Methods, Vol. 25, Issue 4 https://doi.org/10.1006/meth.2001.1262	journal	December 2001
The role of photosynthesis and amino acid metabolism in the energy status during seed development Galili, Gad; Avin-Wittenberg, Tamar; Angelovici, Ruthie Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00447	journal	September 2014
Action of gibberellic acid (GA3) on dormancy and activity of alpha-amylase in rice seeds Vieira, Antônio Rodrigues; Vieira, Maria das Graças Guimarães Carvalho; Fraga, Antônio C. Revista Brasileira de Sementes, Vol. 24, Issue 2 https://doi.org/10.1590/S0101-31222002000100008	journal	January 2002
Protein degradation – an alternative respiratory substrate for stressed plants Araújo, Wagner L.; Tohge, Takayuki; Ishizaki, Kimitsune Trends in Plant Science, Vol. 16, Issue 9 https://doi.org/10.1016/j.tplants.2011.05.008	journal	September 2011
Genetic Mapping of Anaerobic Germination-Associated QTLs Controlling Coleoptile Elongation in Rice Hsu, Sheng-Kai; Tung, Chih-Wei Rice, Vol. 8, Issue 1 https://doi.org/10.1186/s12284-015-0072-3	journal	December 2015
A seed high-lysine trait is negatively associated with the TCA cycle and slows down Arabidopsis seed germination Angelovici, Ruthie; Fait, Aaron; Fernie, Alisdair R. New Phytologist, Vol. 189, Issue 1 https://doi.org/10.1111/j.1469-8137.2010.03478.x	journal	October 2010
Proteomics reveals potential biomarkers of seed vigor in sugarbeet Catusse, Julie; Meinhard, Juliane; Job, Claudette PROTEOMICS, Vol. 11, Issue 9 https://doi.org/10.1002/pmic.201000586	journal	March 2011
Branched-Chain Amino Acid Metabolism in Arabidopsis thaliana Binder, Stefan The Arabidopsis Book, Vol. 8 https://doi.org/10.1199/tab.0137	journal	January 2010
Expression of a Brassica Isopropylmalate Synthase Gene in Arabidopsis Perturbs Both Glucosinolate and Amino Acid Metabolism Field, Ben; Furniss, Caroline; Wilkinson, Andrew Plant Molecular Biology, Vol. 60, Issue 5 https://doi.org/10.1007/s11103-005-5547-y	journal	March 2006
Genome-wide analysis of genes targeted by qLTG3-1 controlling low-temperature germinability in rice Fujino, Kenji; Matsuda, Yasuyuki Plant Molecular Biology, Vol. 72, Issue 1-2 https://doi.org/10.1007/s11103-009-9559-x	journal	October 2009
Target Site Specificity of the Tos17 Retrotransposon Shows a Preference for Insertion within Genes and against Insertion in Retrotransposon-Rich Regions of the Genome Miyao, Akio; Tanaka, Katsuyuki; Murata, Kazumasa The Plant Cell, Vol. 15, Issue 8 https://doi.org/10.1105/tpc.012559	journal	July 2003
Proteomics of seed development, desiccation tolerance, germination and vigor Wang, Wei-Qing; Liu, Shu-Jun; Song, Song-Quan Plant Physiology and Biochemistry, Vol. 86 https://doi.org/10.1016/j.plaphy.2014.11.003	journal	January 2015
Proteomics analysis reveals distinct involvement of embryo and endosperm proteins during seed germination in dormant and non-dormant rice seeds Xu, Heng-Heng; Liu, Shu-Jun; Song, Shun-Hua Plant Physiology and Biochemistry, Vol. 103 https://doi.org/10.1016/j.plaphy.2016.03.007	journal	June 2016
Gene ontology analysis for RNA-seq: accounting for selection bias Young, Matthew D.; Wakefield, Matthew J.; Smyth, Gordon K. Genome Biology, Vol. 11, Issue 2 https://doi.org/10.1186/gb-2010-11-2-r14	journal	January 2010
germinator : a software package for high-throughput scoring and curve fitting of Arabidopsis seed germination Joosen, Ronny V. L.; Kodde, Jan; Willems, Leo A. J. The Plant Journal, Vol. 62, Issue 1 https://doi.org/10.1111/j.1365-313X.2009.04116.x	journal	December 2009
The role of leucine and its metabolites in protein and energy metabolism Duan, Yehui; Li, Fengna; Li, Yinghui Amino Acids, Vol. 48, Issue 1 https://doi.org/10.1007/s00726-015-2067-1	journal	August 2015
Quantitative trait loci controlling rice seed germination under salt stress Wang, Zhoufei; Wang, Jianfei; Bao, Yongmei Euphytica, Vol. 178, Issue 3 https://doi.org/10.1007/s10681-010-0287-8	journal	November 2010
Proteome-wide characterization of sugarbeet seed vigor and its tissue specific expression Catusse, J.; Strub, J. -M.; Job, C. Proceedings of the National Academy of Sciences, Vol. 105, Issue 29 https://doi.org/10.1073/pnas.0800585105	journal	July 2008
Dynamic Quantitative Trait Loci Analysis of Seed Reserve Utilization during Three Germination Stages in Rice Cheng, Xinxin; Cheng, Jinping; Huang, Xi PLoS ONE, Vol. 8, Issue 11 https://doi.org/10.1371/journal.pone.0080002	journal	November 2013
Proteome-Wide Characterization of Seed Aging in Arabidopsis: A Comparison between Artificial and Natural Aging Protocols Rajjou, Loïc; Lovigny, Yoann; Groot, Steven P. C. Plant Physiology, Vol. 148, Issue 1 https://doi.org/10.1104/pp.108.123141	journal	July 2008
The Arabidopsis Aleurone Layer Responds to Nitric Oxide, Gibberellin, and Abscisic Acid and Is Sufficient and Necessary for Seed Dormancy Bethke, Paul C.; Libourel, Igor G. L.; Aoyama, Natsuyo Plant Physiology, Vol. 143, Issue 3 https://doi.org/10.1104/pp.106.093435	journal	January 2007
Branched-Chain Amino Acid Metabolism Harper, A. E.; Miller, R. H.; Block, K. P. Annual Review of Nutrition, Vol. 4, Issue 1 https://doi.org/10.1146/annurev.nu.04.070184.002205	journal	July 1984
Proteome changes associated with dormancy release of Dongxiang wild rice seeds Xu, Heng-Heng; Liu, Shu-Jun; Song, Shun-Hua Journal of Plant Physiology, Vol. 206 https://doi.org/10.1016/j.jplph.2016.08.016	journal	November 2016
Subdomain II of α-Isopropylmalate Synthase Is Essential for Activity: INFERRING A MECHANISM OF FEEDBACK INHIBITION Zhang, Zilong; Wu, Jian; Lin, Wei Journal of Biological Chemistry, Vol. 289, Issue 40 https://doi.org/10.1074/jbc.M114.559716	journal	August 2014
Early seedling vigour, an imperative trait for direct-seeded rice: an overview on physio-morphological parameters and molecular markers Mahender, A.; Anandan, A.; Pradhan, S. K. Planta, Vol. 241, Issue 5 https://doi.org/10.1007/s00425-015-2273-9	journal	March 2015
RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome Li, Bo; Dewey, Colin N. BMC Bioinformatics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2105-12-323	journal	August 2011
Molecular cloning of Sdr4, a regulator involved in seed dormancy and domestication of rice Sugimoto, K.; Takeuchi, Y.; Ebana, K. Proceedings of the National Academy of Sciences, Vol. 107, Issue 13 https://doi.org/10.1073/pnas.0911965107	journal	March 2010
KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases Xie, Chen; Mao, Xizeng; Huang, Jiaju Nucleic Acids Research, Vol. 39, Issue suppl_2 https://doi.org/10.1093/nar/gkr483	journal	June 2011
OsGA20ox1, a candidate gene for a major QTL controlling seedling vigor in rice Abe, Akira; Takagi, Hiroki; Fujibe, Takahiro Theoretical and Applied Genetics, Vol. 125, Issue 4 https://doi.org/10.1007/s00122-012-1857-z	journal	April 2012
Changes in Energy Metabolism and Antioxidant Defense Systems During Seed Germination of the Weed Species Ipomoea triloba L. and the Responses to Allelochemicals Pergo, Érica Marusa; Ishii-Iwamoto, Emy Luiza Journal of Chemical Ecology, Vol. 37, Issue 5 https://doi.org/10.1007/s10886-011-9945-0	journal	April 2011
Genetic dissection of methylcrotonyl CoA carboxylase indicates a complex role for mitochondrial leucine catabolism during seed development and germination: Methylcrotonyl CoA carboxylase Ding, Geng; Che, Ping; Ilarslan, Hilal The Plant Journal, Vol. 70, Issue 4 https://doi.org/10.1111/j.1365-313X.2011.04893.x	journal	February 2012
Molecular mechanisms of seed dormancy: Molecular mechanisms of seed dormancy Graeber, Kai; Nakabayashi, Kazumi; Miatton, Emma Plant, Cell & Environment, Vol. 35, Issue 10 https://doi.org/10.1111/j.1365-3040.2012.02542.x	journal	June 2012
DSDecode: A Web-Based Tool for Decoding of Sequencing Chromatograms for Genotyping of Targeted Mutations Liu, Weizhi; Xie, Xianrong; Ma, Xingliang Molecular Plant, Vol. 8, Issue 9 https://doi.org/10.1016/j.molp.2015.05.009	journal	September 2015
The aspartate-family pathway of plants: Linking production of essential amino acids with energy and stress regulation Galili, Gad Plant Signaling & Behavior, Vol. 6, Issue 2 https://doi.org/10.4161/psb.6.2.14425	journal	February 2011
Disruptions in valine degradation affect seed development and germination in Arabidopsis Gipson, Andrew B.; Morton, Kyla J.; Rhee, Rachel J. The Plant Journal, Vol. 90, Issue 6 https://doi.org/10.1111/tpj.13538	journal	April 2017
Molecular identification of a major quantitative trait locus, qLTG3-1, controlling low-temperature germinability in rice Fujino, K.; Sekiguchi, H.; Matsuda, Y. Proceedings of the National Academy of Sciences, Vol. 105, Issue 34 https://doi.org/10.1073/pnas.0805303105	journal	August 2008

Similar Records

Semi‐dominant mutation in the cysteine‐rich receptor‐like kinase gene, ALS 1 , conducts constitutive defence response in rice

Journal Article · Wed Sep 19 00:00:00 EDT 2018 · Plant Biology · OSTI ID:1460467

Du, D.; Liu, M.; Xing, Y.; +11 more

Blocking amino acid transporter Os AAP 3 improves grain yield by promoting outgrowth buds and increasing tiller number in rice

Journal Article · Sun Mar 25 00:00:00 EDT 2018 · Plant Biotechnology Journal · OSTI ID:1460467

Lu, Kai; Wu, Bowen; Wang, Jie; +5 more

SWEET 11 and 15 as key players in seed filling in rice

Journal Article · Fri Feb 02 00:00:00 EST 2018 · New Phytologist · OSTI ID:1460467

Yang, Jungil; Luo, Dangping; Yang, Bing; +2 more

Title: Influence of isopropylmalate synthase Os IPMS 1 on seed vigour associated with amino acid and energy metabolism in rice

Citation Formats

References (64)

Similar Records

Related Subjects