Identification, cloning and characterization of sis7 and sis10 sugar-insensitive mutants of Arabidopsis

Huang, Yadong; Li, Chun Yao; Biddle, Kelly D.; Gibson, Susan I.

doi:10.1186/1471-2229-8-104

Title: Identification, cloning and characterization of sis7 and sis10 sugar-insensitive mutants of Arabidopsis

Journal Article · Tue Jan 01 00:00:00 EST 2008 · BMC Plant Biology

DOI:https://doi.org/10.1186/1471-2229-8-104· OSTI ID:1626516

Huang, Yadong ^[1]; Li, Chun Yao ^[1]; Biddle, Kelly D. ^[2]; Gibson, Susan I. ^[1]

Univ. of Minnesota, St. Paul, MN (United States). Dept. of Plant Biology
Rice Univ., Houston, TX (United States). Center for Technology in Teaching & Learning

Background: The levels of soluble sugars, such as glucose and sucrose, help regulate many plant metabolic, physiological and developmental processes. Genetic screens are helping identify some of the loci involved in plant sugar response and reveal extensive cross-talk between sugar and phytohormone response pathways. Results: A forward genetic screen was performed to identify mutants with increased resistance to the inhibitory effects of high levels of exogenous sugars on early Arabidopsis seedling development. The positional cloning and characterization of two of these sugar insensitive (sis) mutants, both of which are also involved in abscisic acid (ABA) biosynthesis or response, are reported. Plants carrying mutations in SIS7/NCED3/STO1 or SIS10/ABI3 are resistant to the inhibitory effects of high levels of exogenous Glc and Suc. Quantitative RT-PCR analyses indicate transcriptional upregulation of ABA biosynthesis genes by high concentrations of Glc in wild-type germinating seeds. Gene expression profiling revealed that a significant number of genes that are expressed at lower levels in germinating sis7-1/nced3-4/sto1-4 seeds than in wild-type seeds are implicated in auxin biosynthesis or transport, suggesting cross-talk between ABA and auxin response pathways. The degree of sugar insensitivity of different sis10/abi3 mutant seedlings shows a strong positive correlation with their level of ABA insensitivity during seed germination. Conclusion: Mutations in the SIS7/NCED3/STO1 gene, which is primarily required for ABA biosynthesis under drought conditions, confer a sugar-insensitive phenotype, indicating that a constitutive role in ABA biosynthesis is not necessary to confer sugar insensitivity. Findings presented here clearly demonstrate that mutations in ABI3 can confer a sugar-insensitive phenotype and help explain previous, mixed reports on this topic by showing that ABA and sugar insensitivity exhibit a strong positive correlation in different abi3 mutants. Expression profiling revealed a potentially novel regulation of auxin metabolism and transport in an ABA deficient mutant, sis7-1/nced3-4/sto1-4.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Univ. of Minnesota, Minneapolis, MN (United States); Consortium for Plant Biotechnology Research, Inc., St. Simons, GA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: FG02-03ER15417; FG36-02GO12026

OSTI ID:: 1626516

Journal Information:: BMC Plant Biology, Vol. 8, Issue 1; ISSN 1471-2229

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

References (59)

Positional Cloning in Arabidopsis. Why It Feels Good to Have a Genome Initiative Working for You Lukowitz, Wolfgang; Gillmor, C. Stewart; Scheible, Wolf-Rüdiger Plant Physiology, Vol. 123, Issue 3 https://doi.org/10.1104/pp.123.3.795	journal	July 2000
A gymnosperm ABI3 gene functions in a severe abscisic acid-insensitive mutant of Arabidopsis (abi3-6) to restore the wild-type phenotype and demonstrates a strong synergistic effect with sugar in the inhibition of post-germinative growth Zeng, Ying; Kermode, Allison R. Plant Molecular Biology, Vol. 56, Issue 5 https://doi.org/10.1007/s11103-004-4952-y	journal	November 2004
A Unique Short-Chain Dehydrogenase/Reductase in Arabidopsis Glucose Signaling and Abscisic Acid Biosynthesis and Functions Cheng, Wan-Hsing; Endo, Akira; Zhou, Li The Plant Cell, Vol. 14, Issue 11 https://doi.org/10.1105/tpc.006494	journal	October 2002
Impaired sucrose-induction mutants reveal the modulation of sugar-induced starch biosynthetic gene expression by abscisic acid signalling Rook, Fred; Corke, Fiona; Card, Roderick The Plant Journal, Vol. 26, Issue 4 https://doi.org/10.1046/j.1365-313x.2001.2641043.x	journal	May 2001
SUGAR-INDUCED SIGNAL TRANSDUCTION IN PLANTS Smeekens, Sjef Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 51, Issue 1 https://doi.org/10.1146/annurev.arplant.51.1.49	journal	June 2000
The photomorphogenesis-related mutant red1 is defective in CYP83B1 , a red light-induced gene encoding a cytochrome P450 required for normal auxin homeostasis Hoecker, Ute; Toledo-Ortiz, Gabriela; Bender, Judith Planta, Vol. 219, Issue 2 https://doi.org/10.1007/s00425-004-1211-z	journal	June 2004
Regulation of Abscisic Acid Biosynthesis Xiong, Liming; Zhu, Jian-Kang Plant Physiology, Vol. 133, Issue 1 https://doi.org/10.1104/pp.103.025395	journal	September 2003
Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana Alonso, J. M.; Stepanova, Anna N.; Leisse, Thomas J. Science, Vol. 301, Issue 5633, p. 653-657 https://doi.org/10.1126/science.1086391	journal	August 2003
The Arabidopsis LOS5/ABA3 Locus Encodes a Molybdenum Cofactor Sulfurase and Modulates Cold Stress- and Osmotic Stress-Responsive Gene Expression Xiong, L. THE PLANT CELL ONLINE, Vol. 13, Issue 9 https://doi.org/10.1105/tpc.13.9.2063	journal	September 2001
Glucose delays seed germination in Arabidopsis thaliana Dekkers, Bas J. W.; Schuurmans, Jolanda A. M. J.; Smeekens, Sjef C. M. Planta, Vol. 218, Issue 4 https://doi.org/10.1007/s00425-003-1154-9	journal	February 2004
Genetic interactions between ABA, ethylene and sugar signaling pathways Gazzarrini, Sonia; McCourt, Peter Current Opinion in Plant Biology, Vol. 4, Issue 5 https://doi.org/10.1016/s1369-5266(00)00190-4	journal	October 2001
The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana Koornneef, M.; Reuling, G.; Karssen, C. M. Physiologia Plantarum, Vol. 61, Issue 3 https://doi.org/10.1111/j.1399-3054.1984.tb06343.x	journal	July 1984
Arabidopsis cytochrome P450s that catalyze the first step of tryptophan-dependent indole-3-acetic acid biosynthesis Hull, Anna K.; Vij, Rekha; Celenza, John L. Proceedings of the National Academy of Sciences, Vol. 97, Issue 5 https://doi.org/10.1073/pnas.040569997	journal	February 2000
Isolation of the Arabidopsis ABI3 gene by positional cloning. Giraudat, J.; Hauge, B. M.; Valon, C. The Plant Cell, Vol. 4, Issue 10 https://doi.org/10.1105/tpc.4.10.1251	journal	October 1992
The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots Blilou, Ikram; Xu, Jian; Wildwater, Marjolein Nature, Vol. 433, Issue 7021 https://doi.org/10.1038/nature03184	journal	January 2005
Mannose Inhibits Arabidopsis Germination via a Hexokinase-Mediated Step1 Pego, Jónatas V.; Weisbeek, Peter J.; Smeekens, Sjef C. M. Plant Physiology, Vol. 119, Issue 3 https://doi.org/10.1104/pp.119.3.1017	journal	March 1999
Sugars as Signal Molecules in Plant Seed Development Wobus, U.; Weber, H. Biological Chemistry, Vol. 380, Issue 7-8 https://doi.org/10.1515/bc.1999.116	journal	January 1999
Control of plant development and gene expression by sugar signaling Gibson, Susan I. Current Opinion in Plant Biology, Vol. 8, Issue 1 https://doi.org/10.1016/j.pbi.2004.11.003	journal	February 2005
The 9- cis -epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean Qin, Xiaoqiong; Zeevaart, Jan A. D. Proceedings of the National Academy of Sciences, Vol. 96, Issue 26 https://doi.org/10.1073/pnas.96.26.15354	journal	December 1999
GeneMerge--post-genomic analysis, data mining, and hypothesis testing Castillo-Davis, C. I.; Hartl, D. L. Bioinformatics, Vol. 19, Issue 7 https://doi.org/10.1093/bioinformatics/btg114	journal	May 2003
The Arabidopsis Abscisic Acid Response Locus ABI4 Encodes an APETALA2 Domain Protein Finkelstein, Ruth R.; Li Wang, Ming; Lynch, Tim J. The Plant Cell, Vol. 10, Issue 6 https://doi.org/10.1105/tpc.10.6.1043	journal	June 1998
Regulation of ABA level and water-stress tolerance of Arabidopsis by ectopic expression of a peanut 9-cis-epoxycarotenoid dioxygenase gene Wan, Xiao-Rong; Li, Ling Biochemical and Biophysical Research Communications, Vol. 347, Issue 4 https://doi.org/10.1016/j.bbrc.2006.07.026	journal	September 2006
Genetic approaches to understanding sugar-response pathways Rook, F.; Bevan, M. W. Journal of Experimental Botany, Vol. 54, Issue 382 https://doi.org/10.1093/jxb/erg054	journal	January 2003
SUGAR SENSING AND SIGNALING IN PLANTS: Conserved and Novel Mechanisms Rolland, Filip; Baena-Gonzalez, Elena; Sheen, Jen Annual Review of Plant Biology, Vol. 57, Issue 1 https://doi.org/10.1146/annurev.arplant.57.032905.105441	journal	June 2006
Alkali treatment for rapid preparation of plant material for reliable PCR analysis Klimyuk, Victor I.; Carroll, Bernard J.; Thomas, Colwyn M. The Plant Journal, Vol. 3, Issue 3 https://doi.org/10.1111/j.1365-313x.1993.tb00169.x	journal	March 1993
Cellular and Genetic Responses of Plants to Sugar Starvation Yu, Su-May Plant Physiology, Vol. 121, Issue 3 https://doi.org/10.1104/pp.121.3.687	journal	November 1999
Three Genes That Affect Sugar Sensing (Abscisic Acid Insensitive 4, Abscisic Acid Insensitive 5, and Constitutive Triple Response 1) Are Differentially Regulated by Glucose in Arabidopsis Arroyo, Analilia; Bossi, Flavia; Finkelstein, Ruth R. Plant Physiology, Vol. 133, Issue 1 https://doi.org/10.1104/pp.103.021089	journal	September 2003
Uncoupling the Effects of Abscisic Acid on Plant Growth and Water Relations. Analysis of sto1/nced3, an Abscisic Acid-Deficient but Salt Stress-Tolerant Mutant in Arabidopsis Ruggiero, Bruno; Koiwa, Hisashi; Manabe, Yuzuki Plant Physiology, Vol. 136, Issue 2 https://doi.org/10.1104/pp.104.046169	journal	October 2004
Abscisic Acid Signaling in Seeds and Seedlings Finkelstein, Ruth R.; Gampala, Srinivas S. L.; Rock, Christopher D. The Plant Cell, Vol. 14, Issue suppl 1 https://doi.org/10.1105/tpc.010441	journal	May 2002
Crosstalk between ABA and auxin signaling pathways in roots of Arabidopsis thaliana (L.) Heynh. Rock, Christopher D.; Sun, Xin Planta, Vol. 222, Issue 1 https://doi.org/10.1007/s00425-005-1521-9	journal	May 2005
Pleiotropic control of glucose and hormone responses by PRL1, a nuclear WD protein, in Arabidopsis Nemeth, K.; Salchert, K.; Putnoky, P. Genes & Development, Vol. 12, Issue 19 https://doi.org/10.1101/gad.12.19.3059	journal	October 1998
Plant Sugar-Response Pathways. Part of a Complex Regulatory Web Gibson, Susan I. Plant Physiology, Vol. 124, Issue 4 https://doi.org/10.1104/pp.124.4.1532	journal	December 2000
Carbohydrate control of gene expression in higher plants Graham, I. A. Research in Microbiology, Vol. 147, Issue 6-7 https://doi.org/10.1016/0923-2508(96)84014-9	journal	July 1996
Carbohydrate-Modulated gene Expression in Plants Koch, K. E. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 47, Issue 1 https://doi.org/10.1146/annurev.arplant.47.1.509	journal	June 1996
Sugar Sensing and Signaling in Plants Rolland, Filip; Moore, Brandon; Sheen, Jen The Plant Cell, Vol. 14, Issue suppl 1 https://doi.org/10.1105/tpc.010455	journal	May 2002
Analysis of Arabidopsis glucose insensitive mutants, gin5 and gin6, reveals a central role of the plant hormone ABA in the regulation of plant vegetative development by sugar Arenas-Huertero, Francisco; Arroyo, Analilia; Zhou, Li Genes & Development, Vol. 14, Issue 16 https://doi.org/10.1101/gad.14.16.2085	journal	August 2000
The sugar-insensitive1 (sis1) Mutant of Arabidopsis Is Allelic to ctr1 Gibson, Susan I.; Laby, Ron J.; Kim, Donggiun Biochemical and Biophysical Research Communications, Vol. 280, Issue 1 https://doi.org/10.1006/bbrc.2000.4062	journal	January 2001
The Arabidopsis SUCROSE UNCOUPLED-6 gene is identical to ABSCISIC ACID INSENSITIVE-4: involvement of abscisic acid in sugar responses Huijser, Casper; Kortstee, Anne; Pego, Jonatas The Plant Journal, Vol. 23, Issue 5 https://doi.org/10.1046/j.1365-313x.2000.00822.x	journal	September 2000
Role of the Arabidopsis Glucose Sensor HXK1 in Nutrient, Light, and Hormonal Signaling Moore, B. Science, Vol. 300, Issue 5617 https://doi.org/10.1126/science.1080585	journal	April 2003
Glucose and ethylene signal transduction crosstalk revealed by an Arabidopsis glucose-insensitive mutant Zhou, Li; Jang, Jyan-chyun; Jones, Tamara L. Proceedings of the National Academy of Sciences, Vol. 95, Issue 17 https://doi.org/10.1073/pnas.95.17.10294	journal	August 1998
The Arabidopsis sugar-insensitive mutants sis4 and sis5 are defective in abscisic acid synthesis and response Laby, Ron J.; Kincaid, M. Sean; Kim, Donggiun The Plant Journal, Vol. 23, Issue 5 https://doi.org/10.1046/j.1365-313x.2000.00833.x	journal	September 2000
Mutations at two new Arabidopsis ABA response loci are similar to the abi3 mutations Finkelstein, Ruth R. The Plant Journal, Vol. 5, Issue 6 https://doi.org/10.1046/j.1365-313X.1994.5060765.x	journal	June 1994
A Screen for Genes That Function in Abscisic Acid Signaling in Arabidopsis thaliana Nambara, Eiji; Suzuki, Masaharu; Abrams, Suzanne Genetics, Vol. 161, Issue 3 https://doi.org/10.1093/genetics/161.3.1247	journal	July 2002
Phytohormone signalling pathways interact with sugars during seed germination and seedling development Yuan, K. Journal of Experimental Botany, Vol. 57, Issue 12 https://doi.org/10.1093/jxb/erl096	journal	August 2006
Regulation of Osmotic Stress-responsive Gene Expression by the LOS6/ABA1 Locus in Arabidopsis Xiong, Liming; Lee, Hojoung; Ishitani, Manabu Journal of Biological Chemistry, Vol. 277, Issue 10 https://doi.org/10.1074/jbc.M109275200	journal	January 2002
Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis: Regulation of drought tolerance by AtNCED3 Iuchi, Satoshi; Kobayashi, Masatomo; Taji, Teruaki The Plant Journal, Vol. 27, Issue 4 https://doi.org/10.1046/j.1365-313x.2001.01096.x	journal	August 2001
Hexokinase as a sugar sensor in higher plants. Jang, J. C.; León, P.; Zhou, L. The Plant Cell, Vol. 9, Issue 1 https://doi.org/10.1105/tpc.9.1.5	journal	January 1997
A library of Arabidopsis 35S-cDNA lines for identifying novel mutants LeClere, Sherry; Bartel, Bonnie Plant Molecular Biology, Vol. 46, Issue 6, p. 695-703 https://doi.org/10.1023/A:1011699722052	journal	January 2001
Mutations at the SPINDLY locus of Arabidopsis alter gibberellin signal transduction. Jacobsen, S. E.; Olszewski, N. E. The Plant Cell, Vol. 5, Issue 8 https://doi.org/10.1105/tpc.5.8.887	journal	August 1993
Molecular characterization of the Arabidopsis 9 -cis epoxycarotenoid dioxygenase gene family Tan, Bao-Cai; Joseph, Leina M.; Deng, Wen-Tao The Plant Journal, Vol. 35, Issue 1 https://doi.org/10.1046/j.1365-313X.2003.01786.x	journal	July 2003
Cytochrome P450 CYP79B2 from Arabidopsis Catalyzes the Conversion of Tryptophan to Indole-3-acetaldoxime, a Precursor of Indole Glucosinolates and Indole-3-acetic Acid Mikkelsen, Michael Dalgaard; Hansen, Carsten Hørslev; Wittstock, Ute Journal of Biological Chemistry, Vol. 275, Issue 43 https://doi.org/10.1074/jbc.M001667200	journal	October 2000
Characterization of an Arabidopsis Enzyme Family That Conjugates Amino Acids to Indole-3-Acetic Acid Staswick, Paul E.; Serban, Bogdan; Rowe, Martha The Plant Cell, Vol. 17, Issue 2 https://doi.org/10.1105/tpc.104.026690	journal	January 2005
TheABSCISIC ACID INSENSITIVE 3(ABI3) gene is modulated by farnesylation and is involved in auxin signaling and lateral root development inArabidopsis Brady, Siobhan Mary; Sarkar, Sara F.; Bonetta, Dario The Plant Journal, Vol. 34, Issue 1 https://doi.org/10.1046/j.1365-313X.2003.01707.x	journal	March 2003
Osmotic regulation of root system architecture: Osmotic regulation of lateral root formation Deak, Karen I.; Malamy, Jocelyn The Plant Journal, Vol. 43, Issue 1 https://doi.org/10.1111/j.1365-313X.2005.02425.x	journal	May 2005
Mechanisms of Glucose Signaling during Germination of Arabidopsis Price, John; Li, Tsai-Chi; Kang, Shin Gene Plant Physiology, Vol. 132, Issue 3 https://doi.org/10.1104/pp.103.020347	journal	July 2003
KEEP ON GOING, a RING E3 Ligase Essential for Arabidopsis Growth and Development, Is Involved in Abscisic Acid Signaling Stone, Sophia L.; Williams, Luis A.; Farmer, Lisa M. The Plant Cell, Vol. 18, Issue 12 https://doi.org/10.1105/tpc.106.046532	journal	December 2006
Functional analysis of ArabidopsisNCED6andNCED9genes indicates that ABA synthesized in the endosperm is involved in the induction of seed dormancy Lefebvre, Valérie; North, Helen; Frey, Anne The Plant Journal, Vol. 45, Issue 3 https://doi.org/10.1111/j.1365-313X.2005.02622.x	journal	February 2006
Arabidopsis Map-Based Cloning in the Post-Genome Era Jander, Georg; Norris, Susan R.; Rounsley, Steven D. Plant Physiology, Vol. 129, Issue 2 https://doi.org/10.1104/pp.003533	journal	June 2002
A small-scale procedure for the rapid isolation of plant RNAs Verwoerd, Theo C.; Dekker, Ben M. M.; Hoekema, Andre Nucleic Acids Research, Vol. 17, Issue 6 https://doi.org/10.1093/nar/17.6.2362	journal	January 1989

Cited By (7)

Capturing the phosphorylation and protein interaction landscape of the plant TOR kinase Van Leene, Jelle; Han, Chao; Gadeyne, Astrid Nature Plants, Vol. 5, Issue 3 https://doi.org/10.1038/s41477-019-0378-z	journal	March 2019
An autoregulatory feedback loop involving PAP1 and TAS4 in response to sugars in Arabidopsis Luo, Qing-Jun; Mittal, Amandeep; Jia, Fan Plant Molecular Biology, Vol. 80, Issue 1 https://doi.org/10.1007/s11103-011-9778-9	journal	May 2011
Identification of ICE1 as a negative regulator of ABA-dependent pathways in seeds and seedlings of Arabidopsis Liang, Ching-Hsing; Yang, Chien-Chih Plant Molecular Biology, Vol. 88, Issue 4-5 https://doi.org/10.1007/s11103-015-0335-9	journal	June 2015
Arabidopsis thaliana NGATHA1 transcription factor induces ABA biosynthesis by activating NCED3 gene during dehydration stress Sato, Hikaru; Takasaki, Hironori; Takahashi, Fuminori Proceedings of the National Academy of Sciences, Vol. 115, Issue 47 https://doi.org/10.1073/pnas.1811491115	journal	November 2018
Positioning of the SCRAMBLED receptor requires UDP-Glc:sterol glucosyltransferase 80B1 in Arabidopsis roots Pook, Victoria G.; Nair, Meera; Ryu, KookHui Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-05925-6	journal	July 2017
Water deficits uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs Muller, Bertrand; Pantin, Florent; Génard, Michel Journal of Experimental Botany, Vol. 62, Issue 6 https://doi.org/10.1093/jxb/erq438	journal	January 2011
Mutations in HISTONE ACETYLTRANSFERASE1 affect sugar response and gene expression in Arabidopsis Heisel, Timothy J.; Li, Chun Yao; Grey, Katia M. Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00245	journal	January 2013

Similar Records

Characterization of Sugar Insensitive (sis) Mutants of Arabidopsis

Technical Report · Mon Jun 08 00:00:00 EDT 2009 · OSTI ID:1626516

Gibson, Susan I

Three classes of abscisic acid (ABA)-insensitive mutations of Arabidopsis define genes that control overlapping subsets of ABA responses

Journal Article · Thu Nov 01 00:00:00 EST 1990 · Plant Physiology; (USA) · OSTI ID:1626516

Finkelstein, R R; Somerville, C R

Genetic analysis of the regulation of TCH gene expression, Final Report

Technical Report · Tue Oct 28 00:00:00 EDT 2008 · OSTI ID:1626516

Braam, Janet

Related Subjects

54 ENVIRONMENTAL SCIENCES
Plant Sciences

Title: Identification, cloning and characterization of sis7 and sis10 sugar-insensitive mutants of Arabidopsis

Citation Formats

References (59)

Cited By (7)

Similar Records

Related Subjects