Abstract

The evolutionary dynamics and tissue specificity of protein-coding genes are well documented in plants. However, the evolutionary consequences of small RNAs (sRNAs) on tissue-specific functions remain poorly understood. Here, we performed integrated analysis of 195 deeply sequenced sRNA libraries of maize B73, representing more than 10 tissues, and identified a comprehensive list of 419 maize microRNA (miRNA) genes, 271 of which were newly discovered in this study. We further characterized the evolutionary dynamics and tissue specificity of miRNA genes and corresponding miRNA isoforms (isomiRs). Our analysis revealed that tissue specificity of isomiR events tends to be associated with miRNA gene abundance and suggested that the frequencies of isomiR types are affected by the local genomic regions. Moreover, genome duplication (GD) events have dramatic effect on evolutionary dynamics of maize miRNA genes, and the abundance divergence for tissue-specific miRNA genes is associated with GD events. Further study indicated that duplicate miRNA genes with tissue-specific expression patterns, such as miR2275a, a phased siRNA (phasiRNA) trigger, contribute to phenotypic traits in maize. Additionally, our study revealed the expression preference of 21- and 24-nt phasiRNAs in relation to tissue specificity. This large-scale sRNAomic study depicted evolutionary implications of tissue-specific maize sRNAs, which coordinate genome duplication, isomiR modification, phenotypic traits and phasiRNAs differentiation.

Highlights

  • Plants are multicellular eukaryotes with diverse tissues comprising various cell types, which carry out common processes essential for survival

  • We identified a total of 419 maize miRNA genes (Supplementary Table 4), consisting of 148 annotated miRNA genes in miRBase v22, as well as 271 miRNA genes newly discovered in this study

  • MiRNA genes are highly tissue specific, making it difficult to detect accurate abundance levels, unless massive amounts of tissues are available. We addressed these shortcomings by integrating 195 deeply sequenced small RNAs (sRNAs) libraries and by surveying 14 tissues in maize

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Summary

Introduction

Plants are multicellular eukaryotes with diverse tissues comprising various cell types, which carry out common processes essential for survival. Within the physical context of the tissue environment, cells exhibit unique functions that help define tissue-specific phenotypes (Edwards and Coruzzi, 1990). These common and tissue-specific processes are controlled by gene regulatory networks that alter the extent of gene expression. Evolutionary Consequences of sRNAs in Maize specificity of these processes is often described based on the expression level of protein-coding genes (PCGs) These analyses only partially capture the variety of processes that distinguish different tissues, due to the ignorance of other regulatory elements, such as small RNAs (sRNAs). The investigation of tissue-specific miRNAs and phasiRNAs will help to understand the regulatory mechanisms of tissue specific phenotypes, thereby facilitating crop improvement via genetic engineering and precision breeding

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