The Phloem-delivered RNA Pool Contains Small Noncoding RNAs and Interferes with Translation

Overview

Journal Plant Physiol

Specialty Physiology

Date 2009 Mar 6

PMID 19261735

Citations 135

Authors

Shoudong Zhang

Li Sun

Friedrich Kragler

Affiliations

Soon will be listed here.

Abstract

In plants, the vascular tissue contains the enucleated sieve tubes facilitating long-distance transport of nutrients, hormones, and proteins. In addition, several mRNAs and small interfering RNAs/microRNAs were shown to be delivered via sieve tubes whose content is embodied by the phloem sap (PS). A number of these phloem transcripts are transported from source to sink tissues and function at targeted tissues. To gain additional insights into phloem-delivered RNAs and their potential role in signaling, we isolated and characterized PS RNA molecules distinct from microRNAs/small interfering RNAs with a size ranging from 30 to 90 bases. We detected a high number of full-length and phloem-specific fragments of noncoding RNAs such as tRNAs, ribosomal RNAs, and spliceosomal RNAs in the PS of pumpkin (Cucurbita maxima). In vitro assays show that small quantities of PS RNA molecules efficiently inhibit translation in an unspecific manner. Proof of concept that PS-specific tRNA fragments may interfere with ribosomal activity was obtained with artificially produced tRNA fragments. The results are discussed in terms of a functional role for long distance delivered noncoding PS RNAs.

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References

Mok D, Mok M . CYTOKININ METABOLISM AND ACTION. Annu Rev Plant Physiol Plant Mol Biol. 2001; 52:89-118. DOI: 10.1146/annurev.arplant.52.1.89. View

Aoki K, Kragler F, Xoconostle-Cazares B, Lucas W . A subclass of plant heat shock cognate 70 chaperones carries a motif that facilitates trafficking through plasmodesmata. Proc Natl Acad Sci U S A. 2002; 99(25):16342-7. PMC: 138613. DOI: 10.1073/pnas.252427999. View

Nakazono M, Qiu F, Borsuk L, Schnable P . Laser-capture microdissection, a tool for the global analysis of gene expression in specific plant cell types: identification of genes expressed differentially in epidermal cells or vascular tissues of maize. Plant Cell. 2003; 15(3):583-96. PMC: 150015. DOI: 10.1105/tpc.008102. View

Bakowska-Zywicka K, Twardowski T . Correlation of the structure and conformational changes of selected fragments of plant small ribosomal RNA within the steps of polypeptide chain elongation. J Plant Physiol. 2006; 164(4):496-504. DOI: 10.3201/eid1204.050264. View

Lowe T, Eddy S . tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 1997; 25(5):955-64. PMC: 146525. DOI: 10.1093/nar/25.5.955. View

Taylor S, Massiah A, Lomonossoff G, Roberts L, Lord J, Hartley M . Correlation between the activities of five ribosome-inactivating proteins in depurination of tobacco ribosomes and inhibition of tobacco mosaic virus infection. Plant J. 1994; 5(6):827-35. DOI: 10.1046/j.1365-313x.1994.5060827.x. View

Lau N, Lim L, WEINSTEIN E, Bartel D . An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science. 2001; 294(5543):858-62. DOI: 10.1126/science.1065062. View

Pant B, Buhtz A, Kehr J, Scheible W . MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J. 2007; 53(5):731-8. PMC: 2268993. DOI: 10.1111/j.1365-313X.2007.03363.x. View

Piepenburg O, Pape T, PLEISS J, Wintermeyer W, Uhlenbeck O, Rodnina M . Intact aminoacyl-tRNA is required to trigger GTP hydrolysis by elongation factor Tu on the ribosome. Biochemistry. 2000; 39(7):1734-8. DOI: 10.1021/bi992331y. View

10.

Dao V, Guenther R, Malkiewicz A, Nawrot B, Sochacka E, Kraszewski A . Ribosome binding of DNA analogs of tRNA requires base modifications and supports the "extended anticodon". Proc Natl Acad Sci U S A. 1994; 91(6):2125-9. PMC: 43322. DOI: 10.1073/pnas.91.6.2125. View

11.

Akama K, Kashihara M . Plant nuclear tRNA(Met) genes are ubiquitously interrupted by introns. Plant Mol Biol. 1996; 32(3):427-34. DOI: 10.1007/BF00019094. View

12.

Yoo B, Kragler F, Varkonyi-Gasic E, Haywood V, Archer-Evans S, Lee Y . A systemic small RNA signaling system in plants. Plant Cell. 2004; 16(8):1979-2000. PMC: 519190. DOI: 10.1105/tpc.104.023614. View

13.

Ruiz-Medrano R, Xoconostle-Cazares B, Lucas W . Phloem long-distance transport of CmNACP mRNA: implications for supracellular regulation in plants. Development. 1999; 126(20):4405-19. DOI: 10.1242/dev.126.20.4405. View

14.

Lucas W, Yoo B, Kragler F . RNA as a long-distance information macromolecule in plants. Nat Rev Mol Cell Biol. 2001; 2(11):849-57. DOI: 10.1038/35099096. View

15.

Xoconostle-Cazares B, Xiang Y, Ruiz-Medrano R, Wang H, Monzer J, Yoo B . Plant paralog to viral movement protein that potentiates transport of mRNA into the phloem. Science. 1999; 283(5398):94-8. DOI: 10.1126/science.283.5398.94. View

16.

Chen H, Rosin F, Prat S, Hannapel D . Interacting transcription factors from the three-amino acid loop extension superclass regulate tuber formation. Plant Physiol. 2003; 132(3):1391-404. PMC: 167079. DOI: 10.1104/pp.103.022434. View

17.

Miyawaki K, Matsumoto-Kitano M, Kakimoto T . Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate. Plant J. 2003; 37(1):128-38. DOI: 10.1046/j.1365-313x.2003.01945.x. View

18.

Thompson D, Lu C, Green P, Parker R . tRNA cleavage is a conserved response to oxidative stress in eukaryotes. RNA. 2008; 14(10):2095-103. PMC: 2553748. DOI: 10.1261/rna.1232808. View

19.

Jochl C, Rederstorff M, Hertel J, Stadler P, Hofacker I, Schrettl M . Small ncRNA transcriptome analysis from Aspergillus fumigatus suggests a novel mechanism for regulation of protein synthesis. Nucleic Acids Res. 2008; 36(8):2677-89. PMC: 2377427. DOI: 10.1093/nar/gkn123. View

20.

Lee S, Collins K . Starvation-induced cleavage of the tRNA anticodon loop in Tetrahymena thermophila. J Biol Chem. 2005; 280(52):42744-9. DOI: 10.1074/jbc.M510356200. View