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Planta

, Volume 250, Issue 5, pp 1521–1538 | Cite as

Molecular evolution and lineage-specific expansion of the PP2C family in Zea mays

  • Kai Fan
  • Shuna Yuan
  • Jie Chen
  • Yunrui Chen
  • Zhaowei Li
  • Weiwei Lin
  • Yongqiang Zhang
  • Jianping Liu
  • Wenxiong LinEmail author
Original Article
  • 172 Downloads

Abstract

Main conclusion

97 ZmPP2Cs were clustered into 10 subfamilies with biased subfamily evolution and lineage-specific expansion. Segmental duplication after the divergence of maize and sorghum might have led to primary expansion of ZmPP2Cs.

Abstract

The protein phosphatase 2C (PP2C) enzymes control many stress responses and developmental processes in plants. In Zea mays, a comprehensive understanding of the evolution and expansion of the PP2C family is still lacking. In the current study, 97 ZmPP2Cs were identified and clustered into 10 subfamilies. Through the analysis of the PP2C family in monocots, the ZmPP2C subfamilies displayed biased subfamily molecular evolution and lineage-specific expansion, as evidenced by their differing numbers of member genes, expansion and evolutionary rates, conserved subdomains, chromosomal distributions, expression levels, responsive-regulatory elements and regulatory networks. Moreover, while segmental duplication events have caused the primary expansion of the ZmPP2Cs, the majority of their diversification occurred following the additional whole-genome duplication that took place after the divergence of maize and sorghum (Sorghum bicolor). After this event, the PP2C subfamilies showed asymmetric evolutionary rates, with the D, F2 and H subfamily likely the most closely to resemble its ancestral subfamily’s genes. These findings could provide novel insights into the molecular evolution and expansion of the PP2C family in maize, and lay the foundation for the functional analysis of these enzymes in maize and related monocots.

Keywords

Comparative genomics Expansion Functional analysis Molecular evolution Monocot Protein phosphatase 2C 

Abbreviations

ABA

Abscisic acid

GO

Gene ontology

MeJA

Methyl jasmonate

MYA

Million years ago

OG

Orthologous group

PP2C

Protein phosphatase 2C

SA

Salicylic acid

TF

Transcription factor

WGD

Whole-genome duplication

Notes

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31471567; 31671763; 31701470), China Postdoctoral Science Foundation (2017M610388; 2018T110637), China Scholarship Council (Grant 201708350002 to KF), Fujian Provincial Natural Science Foundation of China (2017J01439), Education Department of Fujian Province of China (JZ160436) and Fujian-Taiwan Joint Innovative Centre for Germplasm Resources and Cultivation of Crop (2015-75. FJ 2011 Program, China).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

425_2019_3243_MOESM1_ESM.pdf (6.2 mb)
Online resource S1 PCR primers used in this study. Online resource S2 ZmPP2C proteins identified in Z.mays. Online resource S3 PP2C proteins identified in B.distachyon, P.hallii, S.italica, S.bicolor, O.sativa and Arabidopsis. Online resource S4 Evolutionary analysis of the PP2C family in Z. mays, B. distachyon, O. sativa, S. bicolor, P. hallii, S. italica and Arabidopsis. Amino acid sequences were aligned with ClustalW, and the phylogenetic tree was generated using the FastTree method. The numbers in the clades are the bootstrap values, and each subfamily of the PP2Cs is indicated in a specific color. Online resource S5 Phylogenetic analysis of the ZmPP2C members. A neighbor-joining tree was performed with the aligned amino acid sequences using the PHYLIP package. The numbers in the clades are the bootstrap values, and each subfamily of the PP2Cs is indicated in a specific color. Online resource S6 Percentage of numbers of member genes in the PP2C subfamily and PP2C subfamily localized on each chromosome in Z. mays (a, c) and S. bicolor (b, d). Online resource S7 List of the orthologous groups of ZmPP2C through OrthoMCL clustering. Online resource S8 Sequence logos of the putative motifs in the ZmPP2C family identified by the MEME program. The height of the letter at each position represents the degree of conservation. The numbers on the x and y axes represent the sequence positions of the putative motifs and the information content measured in bits, respectively. Online resource S9 Sequence logos of the common PP2C subdomains in maize determined using the WebLogo program. The height of the letter at each position represents the degree of conservation. The numbers on the x and y axes represent the sequence positions of the corresponding PP2C subdomains and the information content measured in bits, respectively. Online resource S10 Sequence logos of some subfamily-specific PP2C subdomains in maize determined using the WebLogo program. The height of the letter at each position represents the degree of conservation. The numbers on the x and y axes represent the sequence positions of the corresponding PP2C subdomains and the information content measured in bits, respectively. Online resource S11 Comparison PP2C subdomains with the conserved motifs in the ZmPP2C family. Online resource S12 Putative motif distributions of the Arabidopsis and maize PP2C family. The PP2C subfamilies are indicated by the brackets. For the motif analysis, the putative motifs were identified using the MEME web server. The various colored boxes represent the different motifs, and the motif location along the genes can be estimated using the scale at the bottom. Online resource S13 Sequence logos of the putative motifs in the Arabidopsis and maize PP2C family identified by the MEME program. The height of the letter at each position represents the degree of conservation. The numbers on the x and y axes represent the sequence positions of the putative motifs and the information content measured in bits, respectively. Online resource S14 The structural analysis of ZmPP2C in this study. Online resource S15 Gene structure analysis of ZmPP2C and its alternatively spliced forms without PP2C domain. The gene structures were drawn using the GSDS software. The yellow box is exon, and the black line is intron. Online resource S16 Alternatively spliced transcript of ZmPP2Cs in Z.mays. Online resource S17 Expression values of some ZmPP2Cs in root, stem, leaf and flower. Online resource S18 Number of the responsive-regulatory elements in the promoter regions of ZmPP2Cs. Online resource S19 Chromosomal locations of the ZmPP2C genes across the 10 maize chromosomes. The symbols before the gene names represent their respective PP2C subfamilies. The tandem duplication event of the ZmPP2C genes is indicated with the red lines, and gray lines indicate segmental duplication events. Online resource S20 Genomic locations of the PP2C family in maize. Online resource S21 Ka/Ks analysis for the duplicated PP2Cs in S.bicolor. Online resource S22 Expression of some duplicated ZmPP2C members in different tissues. Three biological repeats about roots, stems, leaves and flowers were performed for all reactions. Online resource S23 The orthologous genes of the PP2C family in maize and five other monocots through OrthoFinder tool. Online resource S24 Phylogenetic relationship of the duplicated ZmPP2Cs and their orthologous genes in five other monocots. The unrooted tree was constructed using the FastTree method. The numbers in the clades are the bootstrap values, and each subfamily of the PP2Cs is indicated in a specific color. The red dot indicated the duplicated events. (PDF 6309 kb)

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Kai Fan
    • 1
    • 3
    • 4
  • Shuna Yuan
    • 2
  • Jie Chen
    • 1
    • 3
    • 4
  • Yunrui Chen
    • 1
    • 3
    • 4
  • Zhaowei Li
    • 3
    • 4
  • Weiwei Lin
    • 3
    • 4
  • Yongqiang Zhang
    • 3
    • 4
  • Jianping Liu
    • 3
    • 4
  • Wenxiong Lin
    • 1
    • 3
    • 4
    Email author
  1. 1.Key Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, College of Crop ScienceFujian Agriculture and Forestry UniversityFuzhouChina
  2. 2.Rubber Research Institute, Chinese Academy of Tropical Agricultural Sciences/Danzhou Investigation and Experiment Station of Tropical CropsMinistry of AgricultureDanzhouChina
  3. 3.Fujian Provincial Key Laboratory of Agroecological Processing and Safety Monitoring, College of Life SciencesFujian Agriculture and Forestry UniversityFuzhouChina
  4. 4.Key Laboratory of Crop Ecology and Molecular Physiology (Fujian Agriculture and Forestry University)Fujian Province UniversityFuzhouChina

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