Coding of Non-coding RNA: Insights Into the Regulatory Functions of Pri-MicroRNA-Encoded Peptides in Plants.

Juan He,Wenping Xu,Chao Ma,Shiren Song,Lei Wang,Yue Song,Amnon Lers,Caixi Zhang,Yi Ren,Lipeng Zhang,Shiping Wang,Dinghan Guo

doi:10.3389/fpls.2021.641351

Abstract

Peptides composed of a short chain of amino acids can play significant roles in plant growth, development, and stress responses. Most of these functional peptides are derived by either processing precursor proteins or direct translation of small open reading frames present in the genome and sometimes located in the untranslated region sequence of a messenger RNA. Generally, canonical peptides serve as local signal molecules mediating short- or long-distance intercellular communication. Also, they are commonly used as ligands perceived by an associated receptor, triggering cellular signaling transduction. In recent years, increasing pieces of evidence from studies in both plants and animals have revealed that peptides are also encoded by RNAs currently defined as non-coding RNAs (ncRNAs), including long ncRNAs, circular RNAs, and primary microRNAs. Primary microRNAs (miRNAs) have been reported to encode regulatory peptides in Arabidopsis, grapevine, soybean, and Medicago, called miRNA-encoded peptides (miPEPs). Remarkably, overexpression or exogenous applications of miPEPs specifically increase the expression level of their corresponding miRNAs by enhancing the transcription of the MIRNA (MIR) genes. Here, we first outline the current knowledge regarding the coding of putative ncRNAs. Notably, we review in detail the limited studies available regarding the translation of miPEPs and their relevant regulatory mechanisms. Furthermore, we discuss the potential cellular and molecular mechanisms in which miPEPs might be involved in plants and raise problems that needed to be solved.

Highlights

For a long time, canonical phytohormones, such as auxin and cytokinin, offer the main perspective in our understanding of regulatory networks modulating plant growth, development, and stress response (Dubois et al, 2018; Kieber and Schaller, 2018)
Since systemin was first characterized in tomato, plant peptides are emerging as significant signaling molecules involved in different physiological processes (Pearce et al, 1991)
They are categorized into precursor-derived peptides and nonprecursor-derived peptides based on their biogenesis (Figure 1)

Summary

INTRODUCTION

Canonical phytohormones, such as auxin and cytokinin, offer the main perspective in our understanding of regulatory networks modulating plant growth, development, and stress response (Dubois et al, 2018; Kieber and Schaller, 2018). Known peptides usually act as ligands that bind to their receptors to activate downstream signaling cascades involved in plant innate immunity (Huffaker et al, 2006; Yamaguchi et al, 2006; Huffaker and Ryan, 2007), nutrient homeostasis (Okamoto et al, 2016), reproduction process (Kachroo et al, 2001; Okuda et al, 2009; Qu et al, 2015), stress response (Nakaminami et al, 2018; Takahashi et al, 2018), and morphogenesis (Yamaguchi et al, 2016; Qian et al, 2018). Overexpression or external application of miPEPs can positively regulate the mature miRNAs by enhancing the transcription of their associated MIR genes, which is similar to the innate immunity system in plants where the endogenous peptides can increase expression of their encoding precursor genes (Huffaker and Ryan, 2007; Huffaker et al, 2011; Couzigou et al, 2016). We review the coding of ncRNA, emphatically, focusing on the translation of pri-miRNA and their relevant biological functions and possible regulatory mechanisms

PEPTIDOME COMPLEXITY IN PLANTS

Peptides Encoded by Conventional Open Reading Frames

Regulation of root

Glycine max Stimulating nodulation

Findings

AUTHOR CONTRIBUTIONS