Perspectives on microRNAs and Phased Small Interfering RNAs in Maize ( Zea mays L.): Functions and Big Impact on Agronomic Traits Enhancement

Abstract

Small RNA (sRNA) population in plants comprises of primarily micro RNAs (miRNAs) and small interfering RNAs (siRNAs). MiRNAs play important roles in plant growth and development. The miRNA-derived secondary siRNAs are usually known as phased siRNAs, including phasiRNAs and tasiRNAs. The miRNA and phased siRNA biogenesis mechanisms are highly conserved in plants. However, their functional conservation and diversification may differ in maize. In the past two decades, lots of miRNAs and phased siRNAs have been functionally identified for curbing important maize agronomic traits, such as those related to developmental timing, plant architecture, sex determination, reproductive development, leaf morphogenesis, root development and nutrition, kernel development and tolerance to abiotic stresses. In contrast to Arabidopsis and rice, studies on maize miRNA and phased siRNA biogenesis and functions are limited, which restricts the small RNA-based fundamental and applied studies in maize. This review updates the current status of maize miRNA and phased siRNA mechanisms and provides a survey of our knowledge on miRNA and phased siRNA functions in controlling agronomic traits. Furthermore, improvement of those traits through manipulating the expression of sRNAs or their targets is discussed.

Keywords: agronomic traits; crop improvement; maize (Zea mays L.); miRNA; phasiRNA; tasiRNA.

Figure 1

An overview showing micro RNA (miRNA) biogenesis and functioning in plants. MIRNA genes are transcribed to form primary miRNAs, from which 21 and 24 nt miRNAs are processed by DCL1 and DCL3, respectively. Their 3′ ends are methylated by HEN1. While the 21 nt species are involved in cleavage or translational inhibition of the target mRNAs, the 24 nt miRNAs are involved in DNA methylation.

Figure 2

Phased small interfering RNA (phasiRNA) and trans-acting simple interfering RNA (tasiRNA) biogenesis pathways in maize. (A) The 21 nt phasiRNA biogenesis pathway. (B) The 24 nt phasiRNA biogenesis pathway. The regulatory mechanism of 24 nt has not been fully uncovered. (C) TAS3-tasiRNA biogenesis pathway.

Figure 3

Chromosomal locations and phylogenetic analysis of known and putative components of the RNAi and miRNA pathways in maize. The protein sequences of dicer-like (DCL), argonautes (AGOs) and RNA-dependent RNA polymerase (RDR) in Arabidopsis, rice and maize AGOs were obtained from protein database (http://www.ncbi.nlm.nih.gov/protein). The neighbor-joining tree was constructed using Clustal omega [70] and iTol online software [71]. (A) The abbreviation of At represents Arabidopsis thaliana, Os for Oryza sativa, and Zm for Zea mays. Red bars indicate the chromosomal locations of ZmDCLs, yellow bars for ZmAGOs, and green bars for ZmRDRs. (B) Plants have four types of DCL proteins. There are 4 DCLs encoded in Arabidopsis genome, 4 DCL family members in rice, and 4 DCLs in maize. Of these DCL proteins, DCL3a and DCL3b are considered specific to monocots and predate the divergence of rice and maize. (C) 10, 19 and 18 AGOs are encoded by Arabidopsis, rice and maize, respectively, that can be divided phylogenetically into five subgroups in maize: AGO1, MEL1/AGO5, AGO7, AGO4, and AGO18. AGO18 subgroup has three members in maize. ZmAGO18a-c are considered specific to monocots along with OsAGO18. (D) Plants have six types of functionally distinct RDRs. While Arabidopsis has all the six types, rice lacks RDR5 and maize lacks RDR3, 4, and 5. In contrast to Arabidopsis and rice which have only single member RDR6 family, maize has a multiple member RDR6 family, which is composed of ZmRDR6a, ZmRDR6b, and ZmRDR6c.

Figure 4

Summary of functionally validated miRNAs and their targets in maize. Nine miRNAs (in red font) and three phasiRNAs (in red font) that regulate specific agronomic traits (in black font) by inducing their targets (in blue font) gene silencing. Question marks indicate that specific ZmSBP taking part in juvenile-to-adult phase transition is not known.

Figure 5

miRNAs or miRNA-phasiRNA interactions in agronomic traits. (A) Maize plant developmental timing is fine-tuned by the interaction between miR156 and miR172. However, the misslink between the two miRNAs still need to be addressed; (B) plant architectural modulation by the interaction of miR156 and miR319. Representative plants, tb1 (leaf), Cg1 (middle), and wild type (right) (all in the background of Chinese inbred line Zheng58) (Unpublished data), are shown. The potential ZmSBP gene probably connects the phenotype of apical dominance loss between maize mutants tb1 and Cg1. In this context, the connection between ZmSBPs and tb1 still need to be experimentally identified; (C) leaf shapes are being regulated by miR166 and miR390-TAS3 regulatory networks. STTMmiR166 mutants have rolling leaf phenotype (left), the wild type is ZZC01 (right). In this context, the connection between miR166 and ARF3 is still unclear.