Network analysis of noncoding RNAs in pepper provides insights into fruit ripening control

Qing Wang,Lipu Gao,Yunxiang Wang,Yunbo Luo,Benzhong Zhu,Jinhua Zuo

doi:10.1038/s41598-019-45427-1

Abstract

Pepper is an important vegetable worldwide and is a model plant for nonclimacteric fleshy fruit ripening. Drastic visual changes and internal biochemical alterations are involved in fruit coloration, flavor, texture, aroma, and palatability to animals during the pepper fruit ripening process. To explore the regulation of bell pepper fruit ripening by noncoding RNAs (ncRNAs), we examined their expression profiles; 43 microRNAs (miRNAs), 125 circular RNAs (circRNAs), 366 long noncoding RNAs (lncRNAs), and 3266 messenger RNAs (mRNAs) were differentially expressed (DE) in mature green and red ripe fruit. Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) analyses revealed that the targets of the DE ncRNAs and DE mRNAs included several kinds of transcription factors (TFs) (ERF, bHLH, WRKY, MYB, NAC, bZIP, and ARF), enzymes involved in cell wall metabolism (beta-galactosidase, beta-glucosidase, beta-amylase, chitinase, pectate lyase (PL), pectinesterase (PE) and polygalacturonase (PG)), enzymes involved in fruit color accumulation (bifunctional 15-cis-phytoene synthase, 9-cis-epoxycarotenoid dioxygenase, beta-carotene hydroxylase and carotene epsilon-monooxygenase), enzymes associated with fruit flavor and aroma (glutamate-1-semialdehyde 2,1-aminomutase, anthocyanin 5-aromatic acyltransferase, and eugenol synthase 1) and enzymes involved in the production of ethylene (ET) (ACO1/ACO4) as well as other plant hormones such as abscisic acid (ABA), auxin (IAA), and gibberellic acid (GA). Based on accumulation profiles, a network of ncRNAs and mRNAs associated with bell pepper fruit ripening was developed that provides a foundation for further developing a more refined understanding of the molecular biology of fruit ripening.

Highlights

Pepper (Capsicum annuum L.) is currently the second most important vegetable worldwide, and the major pepper production areas are located in southern European countries[1]
6527 long noncoding RNAs (lncRNAs) were found in hot pepper, and several of these lncRNAs were found during the fruit development process[26]
11999 lncRNAs were found in bell pepper fruit, of which 194 were known lncRNAs and 11805 were www.nature.com/scientificreports novel lncRNAs

Summary

Introduction

Pepper (Capsicum annuum L.) is currently the second most important vegetable worldwide, and the major pepper production areas are located in southern European countries[1]. Thousands of noncoding RNAs (ncRNAs), which play important roles in different physiological and biochemical processes, have been identified in plants[7,8,9]. Thousands of circRNAs have recently been characterized, which furthers our understanding of RNA; circRNAs reportedly play important roles in a range of biological processes in humans and animals[15,16], knowledge of the functions of circRNAs in fruit plants is limited[9,17,18]. To better understand the functions of ncRNAs in bell pepper fruit ripening, deep sequencing and bioinformatic analysis were employed, leading to the identification of 43 differentially expressed (DE) miRNAs, 125 DE circRNAs, 366 DE lncRNAs, and 3266 DE mRNAs during pepper fruit ripening. The networks of competing endogenous RNAs (ceRNAs) of miRNAs, circRNAs, lncRNAs and mRNAs were assessed using gene annotation to identify influenced pathways and processes

Methods

Results

Conclusion