skip to main content


This content will become publicly available on June 1, 2024

Title: The mRNA mobileome: Challenges and opportunities for deciphering signals from the noise
Organismal communication entails encoding a message that is sent over space or time to a recipient cell, where that message is decoded to activate a downstream response. Defining what qualifies as a functional signal is essential for understanding intercellular communication. In this review, we delve into what is known and unknown in the field of long-distance messenger RNA (mRNA) movement and draw inspiration from the field of information theory to provide a perspective on what defines a functional signaling molecule. Although numerous studies support the long-distance movement of hundreds to thousands of mRNAs through the plant vascular system, only a small handful of these transcripts have been associated with signaling functions. Deciphering whether mobile mRNAs generally serve a role in plant communication has been challenging, due to our current lack of understanding regarding the factors that influence mRNA mobility. Further insight into unsolved questions regarding the nature of mobile mRNAs could provide an understanding of the signaling potential of these macromolecules.  more » « less
Award ID(s):
1942437
NSF-PAR ID:
10399408
Author(s) / Creator(s):
;
Date Published:
Journal Name:
The Plant cell
ISSN:
1040-4651
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Messenger RNAs (mRNAs) function as mobile signals for cell-to-cell communication in multicellular organisms. The KNOTTED1 (KN1) homeodomain family transcription factors act non–cell autonomously to control stem cell maintenance in plants through cell-to-cell movement of their proteins and mRNAs through plasmodesmata; however, the mechanism of mRNA movement is largely unknown. We show that cell-to-cell movement of a KN1 mRNA requires ribosomal RNA–processing protein 44A (AtRRP44A), a subunit of the RNA exosome that processes or degrades diverse RNAs in eukaryotes. AtRRP44A can interact with plasmodesmata and mediates the cell-to-cell trafficking of KN1 mRNA, and genetic analysis indicates that AtRRP44A is required for the developmental functions of SHOOT MERISTEMLESS, an Arabidopsis KN1 homolog. Our findings suggest that AtRRP44A promotes mRNA trafficking through plasmodesmata to control stem cell–dependent processes in plants. 
    more » « less
  2. Abstract

    Translation is a crucial step in gene expression and plays a vital role in regulating various aspects of plant development and environmental responses. It is a dynamic and complex program that involves interactions between mRNAs, tRNAs, and the ribosome machinery, through both cis- and trans-regulation, while integrating internal and external signals. Translational control can act in a global (transcriptome-wide) or mRNA-specific manner. Recent advances in genome-wide techniques, particularly ribosome profiling and proteomics, have led to numerous exciting discoveries in both global and mRNA-specific translation. In this review, we aim to provide a ‘primer’ that introduces readers to this fascinating yet complex cellular process and provide a big picture of how essential components connect within the network. We begin with an overview of mRNA translation, followed by a discussion of the experimental approaches and recent findings in the field, focusing on unannotated translation events and translational control through cis-regulatory elements on mRNAs and trans-acting factors, as well as signaling networks through three conserved translational regulators TOR, SnRK1, and GCN2. Finally, we briefly touch on the spatial regulation of mRNAs in translational control. Here, we focus on cytosolic mRNAs, and translation in organelles and viruses is not covered in this review.

     
    more » « less
  3. Simon, Anne E. (Ed.)
    ABSTRACT Regardless of the general model of translation in eukaryotic cells, a number of studies suggested that many mRNAs encode multiple proteins. Leaky scanning, which supplies ribosomes to downstream open reading frames (ORFs) by readthrough of upstream ORFs, has great potential to translate polycistronic mRNAs. However, the mRNA elements controlling leaky scanning and their biological relevance have rarely been elucidated, with exceptions such as the Kozak sequence. Here, we have analyzed the strategy of a plant RNA virus to translate three movement proteins from a single RNA molecule through leaky scanning. The in planta and in vitro results indicate thatthe significantly shorter 5′ untranslated region (UTR) of the most upstream ORF promotes leaky scanning, potentially fine-tuning the translation efficiency of the three proteins in a single RNA molecule to optimize viral propagation. Our results suggest that the remarkably short length of the leader sequence, like the Kozak sequence, is a translational regulatory element with a biologically important role, as previous studies have shown biochemically. IMPORTANCE Potexvirus , a group of plant viruses, infect a variety of crops, including cultivated crops. It has been thought that the three transition proteins that are essential for the cell-to-cell transfer of potexviruses are translated from two subgenomic RNAs, sgRNA1 and sgRNA2. However, sgRNA2 has not been clearly detected. In this study, we have shown that sgRNA1, but not sgRNA2, is the major translation template for the three movement proteins. In addition, we determined the transcription start site of sgRNA1 in flexiviruses and found that the efficiency of leaky scanning caused by the short 5′ UTR of sgRNA1, a widely conserved feature, regulates the translation of the three movement proteins. When we tested the infection of viruses with mutations introduced into the length of the 5′ UTR, we found that the movement efficiency of the virus was affected. Our results provide important additional information on the protein translation strategy of flexiviruses, including Potexvirus , and provide a basis for research on their control as well as the need to reevaluate the short 5′ UTR as a translational regulatory element with an important role in vivo . 
    more » « less
  4. Abstract Under nitrogen starvation, most legume plants form a nitrogen-fixing symbiosis with Rhizobium bacteria. The bacteria induce the formation of a novel organ called the nodule in which rhizobia reside as intracellular symbionts and convert atmospheric nitrogen into ammonia. During this symbiosis, miRNAs are essential for coordinating the various plant processes required for nodule formation and function. miRNAs are non-coding, endogenous RNA molecules, typically 20–24 nucleotides long, that negatively regulate the expression of their target mRNAs. Some miRNAs can move systemically within plant tissues through the vascular system, which mediates, for example, communication between the stem/leaf tissues and the roots. In this review, we summarize the growing number of miRNAs that function during legume nodulation focusing on two model legumes, Lotus japonicus and Medicago truncatula, and two important legume crops, soybean (Glycine max) and common bean (Phaseolus vulgaris). This regulation impacts a variety of physiological processes including hormone signaling and spatial regulation of gene expression. The role of mobile miRNAs in regulating legume nodule number is also highlighted. 
    more » « less
  5. Abstract

    Trans-species RNA interference (RNAi) occurs naturally when small RNAs (sRNAs) silence genes in species different from their origin. This phenomenon has been observed between plants and various organisms including fungi, animals and other plant species. Understanding the mechanisms used in natural cases of trans-species RNAi, such as sRNA processing and movement, will enable more effective development of crop protection methods using host-induced gene silencing (HIGS). Recent progress has been made in understanding the mechanisms of cell-to-cell and long-distance movement of sRNAs within individual plants. This increased understanding of endogenous plant sRNA movement may be translatable to trans-species sRNA movement. Here, we review diverse cases of natural trans-species RNAi focusing on current theories regarding intercellular and long-distance sRNA movement. We also touch on trans-species sRNA evolution, highlighting its research potential and its role in improving the efficacy of HIGS.

     
    more » « less