The spliceosome assembly factor GEMIN2 attenuates the effects of temperature on alternative splicing and circadian rhythms

被引:79
作者
Gustavo Schlaen, Ruben [1 ]
Mancini, Estefania [1 ]
Elena Sanchez, Sabrina [1 ]
Perez-Santangelo, Soledad [1 ]
Rugnone, Matias L. [1 ]
Simpson, Craig G. [2 ]
Brown, John W. S. [2 ,3 ]
Zhang, Xu [4 ]
Chernomoretz, Ariel [1 ]
Yanovsky, Marcelo J. [1 ]
机构
[1] Consejo Nacl Invest Cient & Tecn, Inst Invest Bioquim Buenos Aires, Fdn Inst Leloir, RA-1405 Buenos Aires, DF, Argentina
[2] James Hutton Inst, Cell & Mol Sci, Dundee DD2 5DA, Scotland
[3] Univ Dundee, James Hutton Inst, Plant Sci, Dundee DD2 5DA, Scotland
[4] Univ Illinois, Dept Med, Sect Hematol Oncol, Chicago, IL 60612 USA
关键词
spliceosome assembly; alternative splicing; circadian rhythms; Arabidopsis; GEMIN2; CLOCK; REVEALS; COMPLEX; GENES; EXPRESSION; RESPONSES; DEFECTS; PROTEIN; SYSTEM; CORE;
D O I
10.1073/pnas.1504541112
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
The mechanisms by which poikilothermic organisms ensure that biological processes are robust to temperature changes are largely unknown. Temperature compensation, the ability of circadian rhythms to maintain a relatively constant period over the broad range of temperatures resulting from seasonal fluctuations in environmental conditions, is a defining property of circadian networks. Temperature affects the alternative splicing (AS) of several clock genes in fungi, plants, and flies, but the splicing factors that modulate these effects to ensure clock accuracy throughout the year remain to be identified. Here we show that GEMIN2, a spliceosomal small nuclear ribonucleoprotein assembly factor conserved from yeast to humans, modulates low temperature effects on a large subset of pre-mRNA splicing events. In particular, GEMIN2 controls the AS of several clock genes and attenuates the effects of temperature on the circadian period in Arabidopsis thaliana. We conclude that GEMIN2 is a key component of a posttranscriptional regulatory mechanism that ensures the appropriate acclimation of plants to daily and seasonal changes in temperature conditions.
引用
收藏
页码:9382 / 9387
页数:6
相关论文
共 42 条
[1]   Genome-wide Insertional mutagenesis of Arabidopsis thaliana [J].
Alonso, JM ;
Stepanova, AN ;
Leisse, TJ ;
Kim, CJ ;
Chen, HM ;
Shinn, P ;
Stevenson, DK ;
Zimmerman, J ;
Barajas, P ;
Cheuk, R ;
Gadrinab, C ;
Heller, C ;
Jeske, A ;
Koesema, E ;
Meyers, CC ;
Parker, H ;
Prednis, L ;
Ansari, Y ;
Choy, N ;
Deen, H ;
Geralt, M ;
Hazari, N ;
Hom, E ;
Karnes, M ;
Mulholland, C ;
Ndubaku, R ;
Schmidt, I ;
Guzman, P ;
Aguilar-Henonin, L ;
Schmid, M ;
Weigel, D ;
Carter, DE ;
Marchand, T ;
Risseeuw, E ;
Brogden, D ;
Zeko, A ;
Crosby, WL ;
Berry, CC ;
Ecker, JR .
SCIENCE, 2003, 301 (5633) :653-657
[2]   Circadian regulation of gene expression: at the crossroads of transcriptional and post-transcriptional regulatory networks [J].
Beckwith, Esteban J. ;
Yanovsky, Marcelo J. .
CURRENT OPINION IN GENETICS & DEVELOPMENT, 2014, 27 :35-42
[3]   Widespread intron retention in mammals functionally tunes transcriptomes [J].
Braunschweig, Ulrich ;
Barbosa-Morais, Nuno L. ;
Pan, Qun ;
Nachman, Emil N. ;
Alipanahi, Babak ;
Gonatopoulos-Pournatzis, Thomas ;
Frey, Brendan ;
Irimia, Manuel ;
Blencowe, Benjamin J. .
GENOME RESEARCH, 2014, 24 (11) :1774-1786
[4]   A comparison of the low temperature transcriptomes and CBF regulons of three plant species that differ in freezing tolerance: Solanum commersonii, Solanum tuberosum, and Arabidopsis thaliana [J].
Carvallo, Marcela A. ;
Pino, Maria-Teresa ;
Jeknic, Zoran ;
Zou, Cheng ;
Doherty, Colleen J. ;
Shiu, Shin-Han ;
Chen, Tony H. H. ;
Thomashow, Michael F. .
JOURNAL OF EXPERIMENTAL BOTANY, 2011, 62 (11) :3807-3819
[5]   Environmental Stresses Modulate Abundance and Timing of Alternatively Spliced Circadian Transcripts in Arabidopsis [J].
Filichkin, Sergei A. ;
Cumbie, Jason S. ;
Dharmawardhana, Palitha ;
Jaiswal, Pankaj ;
Chang, Jeff H. ;
Palusa, Saiprasad G. ;
Reddy, A. S. N. ;
Megraw, Molly ;
Mockler, Todd C. .
MOLECULAR PLANT, 2015, 8 (02) :207-227
[6]   Genome-wide mapping of alternative splicing in Arabidopsis thaliana [J].
Filichkin, Sergei A. ;
Priest, Henry D. ;
Givan, Scott A. ;
Shen, Rongkun ;
Bryant, Douglas W. ;
Fox, Samuel E. ;
Wong, Weng-Keen ;
Mockler, Todd C. .
GENOME RESEARCH, 2010, 20 (01) :45-58
[7]   The SMN-SIP1 complex has an essential role in spliceosomal snRNP biogenesis [J].
Fischer, U ;
Liu, Q ;
Dreyfuss, G .
CELL, 1997, 90 (06) :1023-1029
[8]   Structure and expression of a plant U1 snRNP 70K gene: Alternative splicing of U1 snRNP 70K Pre-mRNAs produces two different transcripts [J].
Golovkin, M ;
Reddy, ASN .
PLANT CELL, 1996, 8 (08) :1421-1435
[9]   Network balance via CRY signalling controls the Arabidopsis circadian clock over ambient temperatures [J].
Gould, Peter D. ;
Ugarte, Nicolas ;
Domijan, Mirela ;
Costa, Maria ;
Foreman, Julia ;
MacGregor, Dana ;
Rose, Ken ;
Griffiths, Jayne ;
Millar, Andrew J. ;
Finkenstaedt, Baerbel ;
Penfield, Steven ;
Rand, David A. ;
Halliday, Karen J. ;
Hall, Anthony J. W. .
MOLECULAR SYSTEMS BIOLOGY, 2013, 9
[10]   Structural Basis of Assembly Chaperone-Mediated snRNP Formation [J].
Grimm, Clemens ;
Chari, Ashwin ;
Pelz, Jann-Patrick ;
Kuper, Jochen ;
Kisker, Caroline ;
Diederichs, Kay ;
Stark, Holger ;
Schindelin, Hermann ;
Fischer, Utz .
MOLECULAR CELL, 2013, 49 (04) :692-703