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Comparative functional genomics of the TPR gene family in Arabidopsis, rice and maize

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Abstract

The tetratricopeptide repeat (TPR) proteins found in all kingdoms of life can mediate protein-protein interactions in a variety of biological systems through binding to specific peptide ligands, such as cell cycle control, transcription, protein transport and protein folding. Although the proteins are ubiquitous, no comprehensive overview of them in Arabidopsis thaliana (At), Oryza sativa (Os), Zea mays (Zm) and Populus trichocarpa (Pt) has been available in the literature till now. Through whole genome investigation, 177 Arabidopsis, 216 rice, 211 maize and 243 poplar TPR genes were identified and categorized into 28 subfamilies and 11 groups based on their domain compositions and phylogenetic relationships, respectively. Phylogenetic analysis revealed that most genes in the same subfamilies are classified into at least two groups, implying that TPR proteins have acquired functional diversity by extensive domain shuffling and/or emerged multiple times independently during evolution. Structural analysis of ZmTPR080 showed that eight TPR motifs as two anti-parallel α-helices form an amphipathic groove capable of accepting a target protein peptide. Similar expression patterns across development stages suggested functional conservation between homologous pairs, for example, AtTPR050/ZmTPR049 may have similar functions in the regulation of flowering. Under drought stress, 26 OsTPRs showed strong alterations of their expression levels in rice leaf, while 10 and 49 ZmTPRs were significantly differentially expressed in maize leaf and cob, respectively.

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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.

Funding

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

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Author notes

  1. Kaifa Wei and Ping Han contributed equally to this work.

Authors and Affiliations

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

    Kaifa Wei

  2. School of Life Sciences, Tsinghua University, Beijing, 100084, China

    Ping Han

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  1. Kaifa Wei
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Correspondence to Kaifa Wei.

Electronic supplementary material

Table S1

The identified TPR proteins and their related information. 1 Isoelectric Point of TPRs. 2 Molecular Weight of TPRs. 3 Probability of export to mitochondria and chloroplast. 4 Predicted subcellular localization of TPRs. “C”, “M”, “S”, and “_” are represent as “chloroplast”, “mitochondrion”, “secretory pathway” and “any other location”, respectively. (PDF 461 kb)

Table S2

TPR protein information for polar (Populus trichocarpa). (PDF 105 kb)

Table S3

The Ka/Ks ratios and estimate of the absolute dates for the duplication events between the duplicated TPR gene pairs. (PDF 85 kb)

Table S4

The probe sets of AtTPR in this study. (PDF 33 kb)

Table S5

The normalized expression values (log2-based) of 161 Arabidopsis TPR genes in 63 tissues and developmental stages. (PDF 387 kb)

Table S6

The expression values of 125 OsTPR genes in 62 different tissues and development stages. (PDF 367 kb)

Table S7

List of 192 detected ZmTPR genes and their expression values in sixty distinct tissues in inbred line B73. (PDF 457 kb)

Table S8

Cis-acting elements were predicted from 1.5 kb upstream promoter region of the TPRs. (PDF 27 kb)

Table S9

OsTPR and ZmTPR expression patterns of successive stages of leaf development. (PDF 170 kb)

Table S10

The transcription levels of OsTPRs under drought stress in rice. (PDF 45 kb)

Table S11

The expression values of ZmTPRs in drought-stressed leaf and cob. MLC and MLD stand for well-watered control and drought stressed leaves, respectively, while MCC and MCD means well-watered control and drought stressed cobs, 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 represent the expression levels of up-regulated and down-regulated genes, respectively. (PDF 99 kb)

Table S12

Primers used in this study. (PDF 11 kb)

Table S13

TPR genes and their regulatory miRNAs in Arabidopsis, rice and maize. (PDF 225 kb)

Fig. S1

Circos diagram of TPR gene pairs among Arabidopsis, rice and maize genomes. Outer two circles showed the distribution of each of the TPR genes and scaled chromosomes for each species in megabase (Mb) units, respectively. Histograms below each chromosome were the value of molecular weights (MWs) of TPR genes (blue <80, yellow ≥100); the two line plots were the isoelectric points (pIs) (green <7, yellow ≥7) and the repeat numbers of each TPRs (green <3, orange ≥16). (PDF 216 kb)

Fig. S2

An ML phylogenetic tree of TPR genes in Synechocystis PCC 6803, Arabidopsis, rice, maize and poplar. The TPR genes are grouped into eleven distinct groups (A-K). The gene names marked with the same colors belong to the same subfamilies, and the branch lines in different colors represent different species. Intron numbers of each TPR genes are shown on the right side. (PDF 481 kb)

Fig. S3

The map of exon/intron arrangement of TPR genes in Arabidopsis, rice and maize. (PDF 926 kb)

Fig. S4

Genomic distribution of AtTPR, OsTPR and ZmTPR genes on chromosomes. Different subfamilies of TPR genes were marked by different colors. (PDF 447 kb)

Fig. S5

Chromosomal segments containing TPR genes from Arabidopsis, rice and maize genomes. The Arabidopsis, rice and maize genomes are abbreviated as At, Os and Zm, respectively. Regions that putatively correspond to homologous genome blocks are connected by gray lines. (PDF 417 kb)

Fig. S6

The structure features of ZmTPR080. a Sequence alignment of eight motifs of ZmTPR080 (red, conserved residues; and blue, hydrophobic residues). Secondary structure of a typical TPR motif is shown above the alignment, with gray and purple bars representing helices. b Ramachandran plot and ERRAT result of ZmTPR080 homology structure. (PDF 553 kb)

Fig. S7

Hierarchial clustering display of TPR transcripts levels detected in distinct tissues in Arabidopsis, rice and maize. (PDF 855 kb)

Fig. S8

Expression profiling of TPR genes along rice and maize leaf developmental gradients. (PDF 467 kb)

Fig. S9

Pearson’s correlation of rice and maize gene expression based on 99 orthologous gene pairs. (PDF 461 kb) (PDF 389 kb)

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Wei, K., Han, P. Comparative functional genomics of the TPR gene family in Arabidopsis, rice and maize. Mol Breeding 37, 152 (2017). https://doi.org/10.1007/s11032-017-0751-4

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