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Pentatricopeptide repeat proteins in maize

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Abstract

Nucleus-encoded pentatricopeptide repeat proteins (PPRs) are a superfamily of ubiquitous RNA-binding factors involved in organellar gene expression. To date, a large number of PPR genes have been identified and some of them have been functionally analyzed in higher plants, while the family in maize [Zea mays (Zm)] has long been unknown. In this study, a genome-scale analysis was conducted to identify all ZmPPR gene members, and exon/intron structure, chromosomal mapping and gene duplication events were analyzed. Then, homology modeling was used to explore structure-function relationships. Finally, publically transcriptome data and real-time PCR were used for studying gene expression. A total of 521 PPR-encoding genes were predicted to occur in the maize genome and unevenly distributed on ten chromosomes. More than 66% PPR genes rarely contain introns and similar exon/intron structural patterns were observed in the same classes/subclasses. Three-dimensional (3D) structural modeling of ZmPPR479 provided insights into the mechanism of RNA recognition. The transcript abundance of 471 genes detected in 60 different developmental stages reveled that some members exhibit tissue-specific expression. Under salt stress, five significantly differentially expressed genes were found in crown root (CR) and ten detected in primary root (PR) and seminal root (SR), respectively. For drought stress, the expressions of seven ZmPPRs showed obvious upregulation in leaf, whereas ten genes were significantly downregulated. Additionally, the expression of 25 and 145 genes were evidently increased and decreased in cob, respectively. Furthermore, the expression patterns of 18 ZmPPRs were confirmed using quantitative real-time PCR.

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Acknowledgments

We are grateful to the providers who submitted microarray and RNA-seq data to the public expression databases, which can be freely applied.

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  1. School of Biological Sciences and Biotechnology, Minnan Normal University, 36 Xian-Qian-Zhi Street, Zhangzhou, Fujian, 363000, China

    Kaifa Wei & Ping Han

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  1. Kaifa Wei
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Correspondence to Kaifa Wei.

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The project was supported by the Science and Technology Cooperation Project of Fujian Province, China (Grant No. 2015I0006)

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These authors have contributed equally to this work

Electronic supplementary material

Fig. S1

Sequence alignment of eight repeats of ZmPPR479. The secondary structure of a typical PPR motif is shown above the alignment, with green and blue bars representing helices. The sequence logo was generated using eight repeats of ZmPPR479 sequence. (PDF 404 kb)

Fig. S2

The map of exon/intron arrangement of ZmPPRs. (PDF 523 kb)

Fig. S3

Circos diagram of PPR gene pairs between maize and rice genomes. Outer two circles distribution of each of the PPR genes and scaled chromosomes for each species in megabase (Mb) units, respectively. Line plot below each chromosome Number of introns of PPR genes: green <5 introns, red ≥10 introns. Boxes represent the syntenic blocks. Colors are assigned to the syntenic regions according to the colors of the corresponding chromosomes. Innermost colored lines interconnect putative orthologous PPR gene pairs between the genomes. (PDF 273 kb)

Fig. S4

Genomic distribution of 520 ZmPPR genes on ten maize chromosomes. Different classes of ZmPPR genes have been marked by different colors. The tandem duplicated gene clusters are joined with vertical lines, and duplication genes are connected by dashed lines in green. (PDF 430 kb)

Fig. S5

Hierarchial clustering display of 471 ZmPPR transcripts detected in 60 distinct tissues at different stages in eleven organs in maize. (PDF 481 kb)

Fig. S6

Differentially expressed analysis of ZmPPRs and organelle genes along maize leaf developmental gradients. E2 enzyme was used as a internal control. Chloroplast and mitochondrial genes were highlighted with green and orange colors respectively. (PDF 538 kb)

Fig. S7

Hierarchical clustering on pairwise correlation coefficients of ZmPPRs and intracellular organelles genes [chloroplast (above) and mitochondria (below)]. (PDF 147 kb)

Fig. S8

The expression profiles of nucleus genes (ZmPPR and ZmRf genes) and intracellular organelle genes across five tissues [immature silks (IMS), mature ovary (MO), mature pollen (MP), mature silk (MS) and seedling (SL)]. (PDF 452 kb)

Fig. S9

Normalized microarray signal intensities of 64 probe sets representing 64 ZmPPRs expressed in U. maydis infected seedling leaves. (PDF 401 kb)

Fig. S10

Expression profiles of 450 ZmPPRs in three root types [primary root (PR), seminal roots (SR) and crown roots (CR)] under salt stress. Log2 based fold changes were used to create the heatmap. White box means that gene only expressed in control or was not expressed both in control and salt stress treatment, while gray box indicates that gene specifically expressed under salt treatment. (PDF 67 kb)

Table S1

The identified maize PPR proteins and their related information. 1 Isoelectric Point of ZmPPRs. 2 Molecular Weight of ZmPPRs. 3 Probability of export to mitochondria and chloroplast. 4 Predicted subcellular localization of ZmPPRs. “C”, “M”, “S”, and “_” are represent as “chloroplast”, “mitochondrion”, “secretory pathway” and “any other location”, respectively. (PDF 245 kb)

Table S2

The Ka/Ks ratios and estimate of the absolute dates for the duplication events between the duplicated ZmPPR genes. (PDF 66 kb)

Table S3

List of 471 detected PPR genes and their expression values in sixty distinct tissues representing eleven major organ systems of inbred line B73. (PDF 420 kb)

Table S4

The expression patterns of ZmPPRs and organelle genes at successive stages in leaf development. (PDF 189 kb)

Table S5

A list of ZmPPRs and their corresponding orthologous genes in Arabidopsis or rice. (PDF 153 kb)

Table S6

The probe sets of ZmPPRs on the maize 18 k GeneChip in this study. (PDF 76 kb)

Table S7

RPKM values of ZmPPRs under salt stress in crown root (CR), primary root (PR), and seminal root (SR). (PDF 130 kb)

Table S8

List of primers used in this study. (PDF 56 kb)

Table S9

List of FPKM values of ZmPPRs in maize reproductive (cob) and vegetative tissue (leaf) under both drought and well-watered conditions. MCC and MCD stand for maize ovary tissue, well watered and drought, respectively; MLC and MLD stand for maize basal leaf meristem, well watered and drought, respectively. Numbers 1 and 2 indicate the two biological replicates. The extent of differential expression is measured in terms of fold change and (−) indicates failure to calculate or undetected values. Values highlighted in red and blue stand for the fold increase and decrease in the drought-stressed tissue, respectively. (PDF 147 kb)

Table S10

Cis-acting elements were predicted from 1.5 kb upstream promoter region of ZmPPRs. (PDF 94 kb)

Table S11

List of predicted miRNA-regulated ZmPPRs. (PDF 153 kb)

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Wei, K., Han, P. Pentatricopeptide repeat proteins in maize. Mol Breeding 36, 170 (2016). https://doi.org/10.1007/s11032-016-0596-2

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