DOI: 10.1126/science.291.5503.487. SUB1, an <i>Arabidopsis</i> Ca <sup>2+</sup> -Binding Protein Involved in Cryptochrome and Phytochrome Coaction

SUB1, an Arabidopsis Ca 2+ -Binding Protein Involved in Cryptochrome and Phytochrome Coaction

10.1126/science.291.5503.487

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

Cryptochromes and phytochromes are the major photosensory receptors in plants and often regulate similar photomorphogenic responses. The molecular mechanisms underlying functional interactions of cryptochromes and phytochromes remain largely unclear. We have identified an Arabidopsis photomorphogenic mutant, sub1 , which exhibits hypersensitive responses to blue light and far-red light. Genetic analyses indicate that SUB1 functions as a component of a cryptochrome signaling pathway and as a modulator of a phytochrome signaling pathway. The SUB1 gene encodes a Ca 2+ -binding protein that suppresses light-dependent accumulation of the transcription factor HY5.

Bibliography

Guo, H., Mockler, T., Duong, H., & Lin, C. (2001). SUB1, an Arabidopsis Ca 2+ -Binding Protein Involved in Cryptochrome and Phytochrome Coaction. Science, 291(5503), 487â490.

Authors 4

Hongwei Guo (first)
Todd Mockler (additional)
Hien Duong (additional)
Chentao Lin (additional)

References 36 Referenced 109

10.1126/science.7732376
10.1126/science.284.5415.760
10.1073/pnas.95.23.13976
10.1126/science.284.5419.1539
10.1126/science.288.5467.859
Neuhaus G., Bowler C., Kern R., Chau N., Cell 73, 937 (1993). (10.1016/0092-8674(93)90272-R) / Cell by Neuhaus G. (1993)
Long J. C., Jenkins G. I., Plant Cell 10, 2077 (1998). (10.1105/tpc.10.12.2077) / Plant Cell by Long J. C. (1998)
Baum G., Long J. C., Jenkins G. I., Trewavas A. J., Proc. Natl. Acad. Sci. U.S.A. 96, 13554 (1999). (10.1073/pnas.96.23.13554) / Proc. Natl. Acad. Sci. U.S.A. by Baum G. (1999)
H. Mohr in Photomorphogenesis in Plants R. E. Kendrick G. H. M. Kronenberg Eds. (Kluwer Dordrecht Netherlands ed. 2 1994).
Fuglevand G., Jackson J. A., Jenkins G. I., Plant Cell 8, 2347 (1996). / Plant Cell by Fuglevand G. (1996)
Ahmad M., Cashmore A. R., Plant J. 11, 421 (1997). (10.1046/j.1365-313X.1997.11030421.x) / Plant J. by Ahmad M. (1997)
10.1126/science.279.5355.1360
Neff M. M., Chory J., Plant Physiol. 118, 27 (1998). (10.1104/pp.118.1.27) / Plant Physiol. by Neff M. M. (1998)
10.1242/dev.126.10.2073
Casal J. J., Photochem. Photobiol. 71, 1 (2000). (10.1562/0031-8655(2000)071<0001:PCPPII>2.0.CO;2) / Photochem. Photobiol. by Casal J. J. (2000)
10.1016/S1097-2765(00)80094-5
Mas P., Devlin P. F., Panda S., Kay S. A., Nature 408, 207 (2000). (10.1038/35041583) / Nature by Mas P. (2000)
10.1016/S0092-8674(00)00184-7
Arabidopsis mutants that showed short hypocotyls in blue light (3 μmol m −2 s −1 ) but not in red light (4 μmol m −2 s −1 ) were isolated and investigated. All the data shown here are derived from sub1-1 which was isolated from a T-DNA–tagged population of Ws background (NASC Nottingham UK). A cosegregation of sub1-1 and T-DNA was established in the F 2 and F 3 of a cross between sub1-1 and the wild type. To prepare double mutants sub1-1 was crossed to cry2-1 (12) cry1-304 (14) phyB-211 (14) and phyA-9 (from M. M. Neff and J. Chory). The T-DNA–flanking genomic regions of sub1-1 were isolated by TAIL-PCR (32) and inverse polymerase chain reaction (PCR) methods (33) and sequenced. SUB1 is located in the BAC clone BAC32A17 and mapped to 24.2 cM of chromosome 4. The GenBank accession numbers are ( SUB1 ) ( SUL1 ) and ( SUL2 ) (www.arabidopsis.org/). Sequence alignments and presentation were made using ClustalW (www.hgsc.bcm.tmc.edu/SearchLauncher/) and BoxShade (www.ch.embnet.org/software/BOX_form.html) respectively. For the results of SUB1 expression and transgenic rescue of the sub1 mutant supplementary material is available on Science Online at www.sciencemag.org/cgi/content/full/291/5503/487/DC1. The SUB1 coding region corresponding to residues 267 to 552 of the SUB1 translation product (SUB1c) was amplified by PCR expressed purified from Escherichia coli and used to raise polyclonal antibodies against SUB1. The 45 Ca 2+ overlay calcium-binding assay was as described (31 34). Light sources hypocotyl measurement genetic and transgenic analyses RNA blot immunoblot and GUS fusion protein cellular localization analyses were as described (12 14 21 22 35).
H. Guo T. Mockler H. Yang C. Lin unpublished data.
10.1073/pnas.95.5.2686
10.1046/j.1365-313X.1999.00525.x
Whitelam G. C., et al., Plant Cell 5, 757 (1993). / Plant Cell by Whitelam G. C. (1993)
Nelson M. R., Chazin W. J., Biometals 11, 297 (1998). (10.1023/A:1009253808876) / Biometals by Nelson M. R. (1998)
Yap K. L., Ames J. B., Swindells M. B., Ikura M., Proteins 37, 499 (1999). (10.1002/(SICI)1097-0134(19991115)37:3<499::AID-PROT17>3.0.CO;2-Y) / Proteins by Yap K. L. (1999)
Clough R. C., Vierstra R. D., Plant Cell Environ. 20, 713 (1997). (10.1046/j.1365-3040.1997.d01-107.x) / Plant Cell Environ. by Clough R. C. (1997)
Koornneef M., Rolff E., Spruit C. J. P., Z. Pflanzenphysiol. Bodenkd. 100, 147 (1980). (10.1016/S0044-328X(80)80208-X) / Z. Pflanzenphysiol. Bodenkd. by Koornneef M. (1980)
10.1101/gad.11.22.2983
Ang L. H., et al., Mol. Cell 1, 213 (1998). (10.1016/S1097-2765(00)80022-2) / Mol. Cell by Ang L. H. (1998)
10.1038/35013076
Keller T., et al., Plant Cell 10, 255 (1998). / Plant Cell by Keller T. (1998)
Liu Y. G., Mitsukawa N., Oosumi T., Whittier R. F., Plant J. 8, 457 (1995). (10.1046/j.1365-313X.1995.08030457.x) / Plant J. by Liu Y. G. (1995)
Mathur J., et al., Plant J. 13, 707 (1998). (10.1046/j.1365-313X.1998.00059.x) / Plant J. by Mathur J. (1998)
Lundberg S., Lehto V. P., Backman L., Biochemistry 31, 5665 (1992). (10.1021/bi00139a034) / Biochemistry by Lundberg S. (1992)
Wang Z. Y., et al., Plant Cell 9, 491 (1997). / Plant Cell by Wang Z. Y. (1997)
The authors thank S. Jacobsen for critical readings S. Luan for helpful discussions and H. Yang and S. Villa for technical support; M. M. Neff and J. Chory for phyA and phyB mutants; and P. Quail R. Vierstra and X.-W. Deng for providing antibodies. Supported in part by NIH (GM 56265 to C.L.) and USDA (99-35304-8085 to C.L.).

Dates

Type	When
Created	23 years, 1 month ago (July 27, 2002, 5:53 a.m.)
Deposited	1 year, 7 months ago (Jan. 13, 2024, 4:31 a.m.)
Indexed	2 months, 2 weeks ago (June 11, 2025, 7:22 a.m.)
Issued	24 years, 7 months ago (Jan. 19, 2001)
Published	24 years, 7 months ago (Jan. 19, 2001)
Published Print	24 years, 7 months ago (Jan. 19, 2001)

Funders 0

None

BibTeX

@article{Guo_2001, title={SUB1, an Arabidopsis Ca 2+ -Binding Protein Involved in Cryptochrome and Phytochrome Coaction}, volume={291}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.291.5503.487}, DOI={10.1126/science.291.5503.487}, number={5503}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Guo, Hongwei and Mockler, Todd and Duong, Hien and Lin, Chentao}, year={2001}, month=jan, pages={487–490} }

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