Evolutionary Comparison of Two Combinatorial Regulators of SBP-Box Genes, MiR156 and MiR529, in Plantsby Shu-Dong Zhang, Li-Zhen Ling, Quan-Fang Zhang, Jian-Di Xu, Le Cheng

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RESEARCH ARTICLE

Evolutionary Comparison of Two

Combinatorial Regulators of SBP-Box Genes,

MiR156 andMiR529, in Plants

Shu-Dong Zhang1☯, Li-Zhen Ling2☯*, Quan-Fang Zhang3, Jian-Di Xu4, Le Cheng2* 1 Germplasm Bank of Wild Species, Kunming, 650201, China, 2 BGI-Yunnan, BGI-Shenzhen, Kunming, 650106, China, 3 Bio-Tech Research Center, Shandong Academy of Agricultural Sciences, Jinan 250100,

China, 4 Shandong rice research institute, Shandong Academy of Agricultural Sciences, Jinan, 250100,

China ☯ These authors contributed equally to this work. * linglizhen@genomics.cn (L-ZL); chengle@genomics.cn (LC)

Abstract

A complete picture of the evolution of miRNA combinatorial regulation requires the synthesis of information on all miRNAs and their targets.MiR156 andmiR529 are two combinatorial regulators of squamosa promoter binding protein-like (SBP-box) genes. Previous studies have clarified the evolutionary dynamics of their targets; however, there have been no reports on the evolutionary patterns of two miRNA regulators themselves to date. In this study, we investigated the evolutionary differences between these two miRNA families in extant land plants. Our work found thatmiR529 precursor, especially of its mature miRNA sequence, has a higher evolutionary rate. Such accelerating evolution ofmiR529 has significantly effects on its structural stability, and sequence conservation against existence of itself. By contrast,miR156 evolves more rapidly in loop region of the stable secondary structure, which may contribute to its functional diversity. Moreover,miR156 andmiR529 genes have distinct rates of loss after identical duplication events.MiR529 genes have a higher average loss rate and asymmetric loss rate in duplicated gene pairs, indicating preferredmiR529 gene losses become another predominant mode of inactivation, that are implicated in the contraction of this family. On the contrary, duplicatedmiR156 genes have a low loss rate, and could serve as another new source for functional diversity. Taken together, these results provide better insight into understanding the evolutionary divergence of miR156 andmiR529 family in miRNA combinational regulation network.

Introduction

MicroRNAs (miRNAs) are small, non-coding RNA molecules that regulate gene expression by binding to target mRNA transcripts, leading to either translational repression or mRNA degradation. A growing body of evidence indicates that, in plants, a single miRNA can target and regulate multiple transcripts and conversely, the same genes can be targeted by a number of

PLOSONE | DOI:10.1371/journal.pone.0124621 April 24, 2015 1 / 12

OPEN ACCESS

Citation: Zhang S-D, Ling L-Z, Zhang Q-F, Xu J-D,

Cheng L (2015) Evolutionary Comparison of Two

Combinatorial Regulators of SBP-Box Genes,

MiR156 and MiR529, in Plants. PLoS ONE 10(4): e0124621. doi:10.1371/journal.pone.0124621

Academic Editor: Rogerio Margis, Universidade

Federal do Rio Grande do Sul, BRAZIL

Received: December 13, 2014

Accepted: March 17, 2015

Published: April 24, 2015

Copyright: © 2015 Zhang et al. This is an open access article distributed under the terms of the

Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability Statement: All relevant data are available from the miRBase database (http://www. mirbase.org/). Detailed annotation of the data used in the study are available within the paper, and accession numbers of each miRNA are available in

Table 1.

Funding: This work was supported by the National

Natural Science Foundation of China (grant no. 31200172), Promotive Research Fund for Excellent

Young and Middle-Aged Scientists of Shandong

Province (BS2013SW003), Special Fund for BGIYunnan’s High Throughput Sequencing Platform (P.

R. China, Yunnan Provincial Science and Technology different miRNAs [1–3]. With the identification of thousands of miRNAs through highthroughput sequencing, many transcription factors (TF), such as MYB, APETALA2 (AP2), and

MADS-box gene families, have been shown to be regulated by distinct miRNAs in plants [1,3].

However, we still have no idea about how the combinations of these different miRNAs work in concert to repress a target gene. In order to address this question, the basic principles that underlie the respective evolution of individual miRNA regulators and their target genes must be clarified firstly.

MiR156 andmiR529 have been demonstrated to cooperatively target squamosa promoter binding protein-like (SBP-box) genes [4]. They share a 14–16-nt-long homologous stretch in their mature sequences and have overlapping binding sites in the same target [5,6]. Our previous study showed that their targeted SBP-box genes differ greatly in their evolutionary patterns and dynamics [6]. Whether there exist evolutionary differences betweenmiR156 andmiR529 is still a mystery in plants until now. However, we found thatmiR156 andmiR529 are significantly different in three aspects. First, analysis of miRNA deep sequencing expression profile from rice has shown thatmiR156 genes are ubiquitously expressed in the root, shoot and other tissues at the seedling stage, whereasmiR529 genes are only detected in the panicle throughout development [1]. A similar phenomenon was also found in maize and Brachypodium distachyon, suggesting that ancientmiR156 andmiR529 genes have formed conserved expression patterns over long evolutionary periods [7,8]. Second, extensive genomic analysis showed that miR156 is ubiquitous throughout land plants and its regulatory circuit is extremely well conserved throughout plant evolution [9,10]. By contrast,miR529 is only present in bryophytes, lycopods, and monocots, and displays limited taxonomic distributions [11,12]. These findings indicate thatmiR529 is at least 400 million years old and may have been lost from all core eudicots and that the evolutionary forces driving the loss of this regulatory system are intriguing.