DHH1/DDX6-like RNA Helicases Maintain Ephemeral Half-lives of Stress-response MRNAs

Overview

Journal Nat Plants

Specialties Biology
Genetics

Date 2020 Jun 3

PMID 32483330

Citations 36

Authors

Thanin Chantarachot

Reed S Sorenson

Maureen Hummel

Haiyan Ke

Alek T Kettenburg

Daniel Chen

Karen Aiyetiwa

Katayoon Dehesh

Thomas Eulgem

Leslie E Sieburth

Julia Bailey-Serres

Affiliations

Soon will be listed here.

Abstract

Gene transcription is counterbalanced by messenger RNA decay processes that regulate transcript quality and quantity. We show here that the evolutionarily conserved DHH1/DDX6-like RNA hellicases of Arabidopsis thaliana control the ephemerality of a subset of cellular mRNAs. These RNA helicases co-localize with key markers of processing bodies and stress granules and contribute to their subcellular dynamics. They function to limit the precocious accumulation and ribosome association of stress-responsive mRNAs involved in auto-immunity and growth inhibition under non-stress conditions. Given the conservation of this RNA helicase subfamily, they may control basal levels of conditionally regulated mRNAs in diverse eukaryotes, accelerating responses without penalty.

Citing Articles

Stress sensing and response through biomolecular condensates in plants.

Peng J, Yu Y, Fang X Plant Commun. 2024; 6(2):101225.

PMID: 39702967 PMC: 11897469. DOI: 10.1016/j.xplc.2024.101225.

AtPRMT3-RPS2B promotes ribosome biogenesis and coordinates growth and cold adaptation trade-off.

Wang Z, Zhang X, Liu C, Duncan S, Hang R, Sun J Nat Commun. 2024; 15(1):8693.

PMID: 39375381 PMC: 11488217. DOI: 10.1038/s41467-024-52945-8.

Prion-like Proteins in Plants: Key Regulators of Development and Environmental Adaptation via Phase Separation.

Wu P, Li Y Plants (Basel). 2024; 13(18).

PMID: 39339640 PMC: 11435361. DOI: 10.3390/plants13182666.

mA modification plays an integral role in mRNA stability and translation during pattern-triggered immunity.

Chen T, Greene G, Motley J, Mwimba M, Luo G, Xu G Proc Natl Acad Sci U S A. 2024; 121(33):e2411100121.

PMID: 39116132 PMC: 11331096. DOI: 10.1073/pnas.2411100121.

A double-stranded RNA binding protein enhances drought resistance via protein phase separation in rice.

Wang H, Ye T, Guo Z, Yao Y, Tu H, Wang P Nat Commun. 2024; 15(1):2514.

PMID: 38514621 PMC: 10957929. DOI: 10.1038/s41467-024-46754-2.

References

Chantarachot T, Bailey-Serres J . Polysomes, Stress Granules, and Processing Bodies: A Dynamic Triumvirate Controlling Cytoplasmic mRNA Fate and Function. Plant Physiol. 2017; 176(1):254-269. PMC: 5761823. DOI: 10.1104/pp.17.01468. View

Sheth U, Parker R . Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science. 2003; 300(5620):805-8. PMC: 1876714. DOI: 10.1126/science.1082320. View

Hubstenberger A, Courel M, Benard M, Souquere S, Ernoult-Lange M, Chouaib R . P-Body Purification Reveals the Condensation of Repressed mRNA Regulons. Mol Cell. 2017; 68(1):144-157.e5. DOI: 10.1016/j.molcel.2017.09.003. View

Sorenson R, Bailey-Serres J . Selective mRNA sequestration by OLIGOURIDYLATE-BINDING PROTEIN 1 contributes to translational control during hypoxia in Arabidopsis. Proc Natl Acad Sci U S A. 2014; 111(6):2373-8. PMC: 3926019. DOI: 10.1073/pnas.1314851111. View

Zhang W, Murphy C, Sieburth L . Conserved RNaseII domain protein functions in cytoplasmic mRNA decay and suppresses Arabidopsis decapping mutant phenotypes. Proc Natl Acad Sci U S A. 2010; 107(36):15981-5. PMC: 2936607. DOI: 10.1073/pnas.1007060107. View

Sorenson R, Deshotel M, Johnson K, Adler F, Sieburth L . mRNA decay landscape arises from specialized RNA decay substrates, decapping-mediated feedback, and redundancy. Proc Natl Acad Sci U S A. 2018; 115(7):E1485-E1494. PMC: 5816150. DOI: 10.1073/pnas.1712312115. View

Siwaszek A, Ukleja M, Dziembowski A . Proteins involved in the degradation of cytoplasmic mRNA in the major eukaryotic model systems. RNA Biol. 2014; 11(9):1122-36. PMC: 4615280. DOI: 10.4161/rna.34406. View

Kim C, Kushima M, Okada Y, TOMOYOSHI T . [Tunica albuginea cyst associated with hydrocele testis: report of a case]. Hinyokika Kiyo. 1991; 37(9):1065-8. View

Goeres D, Van Norman J, Zhang W, Fauver N, Spencer M, Sieburth L . Components of the Arabidopsis mRNA decapping complex are required for early seedling development. Plant Cell. 2007; 19(5):1549-64. PMC: 1913740. DOI: 10.1105/tpc.106.047621. View

10.

Xu J, Chua N . Arabidopsis decapping 5 is required for mRNA decapping, P-body formation, and translational repression during postembryonic development. Plant Cell. 2009; 21(10):3270-9. PMC: 2782270. DOI: 10.1105/tpc.109.070078. View

11.

Perea-Resa C, Hernandez-Verdeja T, Lopez-Cobollo R, Castellano M, Salinas J . LSM proteins provide accurate splicing and decay of selected transcripts to ensure normal Arabidopsis development. Plant Cell. 2012; 24(12):4930-47. PMC: 3556967. DOI: 10.1105/tpc.112.103697. View

12.

Sanders E . Association of the Golgi complex with the plasma membrane of amphibian embryonic cells. Protoplasma. 1973; 76(1):115-22. DOI: 10.1007/BF01279678. View

13.

Martinez de Alba A, Moreno A, Gabriel M, Mallory A, Christ A, Bounon R . In plants, decapping prevents RDR6-dependent production of small interfering RNAs from endogenous mRNAs. Nucleic Acids Res. 2015; 43(5):2902-13. PMC: 4357720. DOI: 10.1093/nar/gkv119. View

14.

Xu J, Chua N . Dehydration stress activates Arabidopsis MPK6 to signal DCP1 phosphorylation. EMBO J. 2012; 31(8):1975-84. PMC: 3343339. DOI: 10.1038/emboj.2012.56. View

15.

Soma F, Mogami J, Yoshida T, Abekura M, Takahashi F, Kidokoro S . ABA-unresponsive SnRK2 protein kinases regulate mRNA decay under osmotic stress in plants. Nat Plants. 2017; 3:16204. DOI: 10.1038/nplants.2016.204. View

16.

Perea-Resa C, Carrasco-Lopez C, Catala R, Tureckova V, Novak O, Zhang W . The LSM1-7 Complex Differentially Regulates Arabidopsis Tolerance to Abiotic Stress Conditions by Promoting Selective mRNA Decapping. Plant Cell. 2016; 28(2):505-20. PMC: 4790874. DOI: 10.1105/tpc.15.00867. View

17.

Gloggnitzer J, Akimcheva S, Srinivasan A, Kusenda B, Riehs N, Stampfl H . Nonsense-mediated mRNA decay modulates immune receptor levels to regulate plant antibacterial defense. Cell Host Microbe. 2014; 16(3):376-90. DOI: 10.1016/j.chom.2014.08.010. View

18.

Kami D, Kitani T, Nakamura A, Wakui N, Mizutani R, Ohue M . The DEAD-box RNA-binding protein DDX6 regulates parental RNA decay for cellular reprogramming to pluripotency. PLoS One. 2018; 13(10):e0203708. PMC: 6166933. DOI: 10.1371/journal.pone.0203708. View

19.

Boag P, Atalay A, Robida S, Reinke V, Blackwell T . Protection of specific maternal messenger RNAs by the P body protein CGH-1 (Dhh1/RCK) during Caenorhabditis elegans oogenesis. J Cell Biol. 2008; 182(3):543-57. PMC: 2500139. DOI: 10.1083/jcb.200801183. View

20.

Kamenska A, Simpson C, Vindry C, Broomhead H, Benard M, Ernoult-Lange M . The DDX6-4E-T interaction mediates translational repression and P-body assembly. Nucleic Acids Res. 2016; 44(13):6318-34. PMC: 5291280. DOI: 10.1093/nar/gkw565. View